SpringerLink
Log in

Nanotechnology-based cell-mediated delivery systems for cancer therapy and diagnosis

  • Review Article
  • Published:
Drug Delivery and Translational Research Aims and scope Submit manuscript

Abstract

The global prevalence of cancer is increasing, necessitating new additions to traditional treatments and diagnoses to address shortcomings such as ineffectiveness, complications, and high cost. In this context, nano and microparticulate carriers stand out due to their unique properties such as controlled release, higher bioavailability, and lower toxicity. Despite their popularity, they face several challenges including rapid liver uptake, low chemical stability in blood circulation, immunogenicity concerns, and acute adverse effects. Cell-mediated delivery systems are important topics to research because of their biocompatibility, biodegradability, prolonged delivery, high loading capacity, and targeted drug delivery capabilities. To date, a variety of cells including blood, immune, cancer, and stem cells, sperm, and bacteria have been combined with nanoparticles to develop efficient targeted cancer delivery or diagnosis systems. The review paper aimed to provide an overview of the potential applications of cell-based delivery systems in cancer therapy and diagnosis.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Scheme 1
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data availability

All required data are available in the manuscript.

Abbreviations

5-FU:

5-Fluorouracil

AF-SPNPs:

Activated fibroblasts cell membrane modified SPNPs

AA:

Acrylic acid

ASCs:

Adult stem cells

ADSCs:

Adipose-derived stem cells

AuNR:

Au nanorod

AuNRB:

Au nanorod-modified with bovine serum albumin

AuNRBR:

Au Nanorod-modified with bovine serum albumin functionalized with RGD Peptide

APCs:

Antigen-presenting cells

Apdl1:

Anti-Pdl1

Anti-Tnfα:

Anti-tumor necrosis factor

BOMVs:

Bacteria-derived outer membrane vesicles

BFGF:

Basic fibroblast growth factor

BH:

Berberine hydrochloride

BBB:

Blood brain barrier

BTICs:

Brain tumor-initiating cells

CAAs:

Cancer-associated adipocytes

CCM:

Cancer cell membrane

CC-UPCNPs:

Cancer cell membrane modified UCNPs

CAR:

Chimeric antigen receptor

CTCs:

Circulating tumor cells

Cur:

Curcumin

CD:

Cytosine deaminase

CDase:

Cytosine deaminase

CTLs:

Cytotoxic T-lymphocytes

CMV:

Cytomegalovirus

DCs:

Dendritic cells

DSN:

Double-specific nucleases

DOX:

Doxorubicin

FA-UCNPs:

DSPE-PEG-FA-coated UCNPs

EPR:

Enhanced permeability and retention

EVs:

Extracellular vesicles

FLI:

Fluorescence imaging

GCB:

Gemcitabine

GinPa:

Gingival papilla

GA:

Glutaraldehyde

AuNCs:

Gold nanocages

IFN-β:

Human interferon-β

HNSCs:

Human neural stem cells

ICG:

Indocyanine green

LAMP:

Lysosomal associated membrane protein

MRI:

Magnetic resonance imaging

MSCs:

Mesenchymal stem cells

MSNs:

Mesoporous silica nanoparticles

MOFs:

Metal-organic frameworks

MTX-liposome:

Methotrexate-encapsulated liposomes

MTX-Liposome:

Methotrexate-encapsulated liposomes

NCs:

Nanocarries

NPs:

Nanoparticles

NIR:

Near-infrared

OMVs:

Outer membrane vesicles

PTX:

Paclitaxel

PEG:

Polyethylene glycol

PEGylated AuNPs:

Polyethylene glycol-coated Au NPs

PFCs:

Perfluorocarbons

PAI:

Photoacoustic imaging

PDT:

Photodynamic therapy

PTT:

Photothermal therapy

PMDVs:

Platelet membrane-derived vesicles

PMs:

Platelet membranes

PCLP1:

Podocalyxin-like protein 1

PVP:

Poly vinylpyrrolidone

PCL:

Poly(caprolactone)

PLGA:

Poly(lactic-co-glycolic acid)

PB:

Prussian blue

RENMs:

Rare earth dope nanomaterial

RBC-MNs:

RBCs membrane coated iron oxide magnetic nanoparticles

RBCM:

Red blood cell membranes

RBCs:

Red blood cells

RES:

Reticuloendothelial system

MSCVs:

Mesenchymal stem cell membrane vesicles

SPNPs:

Semiconducting polymer NPs

SCs:

Stem cells

St:

Styrene

SPIONs:

Super magnetic iron oxide nanoparticles

ITP:

Thrombocytopenia

TLR4:

Toll-like receptor 4

TRAIL:

TNF-related apoptosis-inducing ligand

TCIPA:

Tumor cell-induced platelet aggregation

TICs:

Tumor-infiltrating immune cells

UCNPs:

Up conversion nanoparticles

WBCs:

White blood cells

References

  1. Alimardani V, Abolmaali SS, Tamaddon AM, Ashfaq M. Recent advances on microneedle arrays-mediated technology in cancer diagnosis and therapy. Drug Del Transl Res. 2020:1–29.

  2. Li T, Dong H, Zhang C, Mo R. Cell-based drug delivery systems for biomedical applications. Nano Res. 2018;11(10):5240–57.

    Article  CAS  Google Scholar 

  3. Abolmaali S, Tamaddon A, Salmanpour M, Mohammadi S, Dinarvand R. Block ionomer micellar nanoparticles from double hydrophilic copolymers, classifications and promises for delivery of cancer chemotherapeutics. Eur J Pharm Sci. 2017;104:393–405.

    Article  CAS  Google Scholar 

  4. Taghizadeh S, Alimardani V, Roudbali PL, Ghasemi Y, Kaviani E. 1Gold nanoparticles application in liver cancer. Photodiagnosis Photodyn Ther. 2019.

  5. Alimardani V, Abolmaali SS, Yousefi G, Rahiminezhad Z, Abedi M, Tamaddon A, et al. Microneedle arrays combined with nanomedicine approaches for transdermal delivery of therapeutics. J Clin Med. 2021;10(2):181.

    Article  CAS  Google Scholar 

  6. Ardakani LS, Alimardani V, Tamaddon AM, Amani AM, Taghizadeh S. Green synthesis of iron-based nanoparticles using Chlorophytum comosum leaf extract: methyl orange dye degradation and antimicrobial properties. Heliyon. 2021;7(2):e0615.

    Article  Google Scholar 

  7. Abedi M, Abolmaali SS, Heidari R, Samani SM, Tamaddon AM. Hierarchical mesoporous zinc-imidazole dicarboxylic acid MOFs: Surfactant-directed synthesis, pH-responsive degradation, and drug delivery. Int J Pharm. 2021;602:120685.

    Article  CAS  Google Scholar 

  8. Mostoufi H, Yousefi G, Tamaddon A-m, Firuzi O. Reversing multi-drug tumor resistance to Paclitaxel by well-defined pH-sensitive amphiphilic polypeptide block copolymers via induction of lysosomal membrane permeabilization. Colloids Surf B Biointerfaces. 2019;174:17–27.

  9. Abbasi S, Yousefi G, Tamaddon A-M. Polyacrylamide–b-copolypeptide hybrid copolymer as pH-responsive carrier for delivery of paclitaxel: Effects of copolymer composition on nanomicelles properties, loading efficiency and hemocompatibility. Colloids Surf Physicochem Eng Aspects. 2018;537:217–26.

    Article  CAS  Google Scholar 

  10. Alimardani V, Farahavar G, Salehi S, Taghizadeh S, Ghiasi MR, Abolmaali SS. Gold nanocages in cancer diagnosis, therapy, and theranostics: a brief review. Front Mater Sci. 2021:1–18.

  11. Wei Y, Gu X, Sun Y, Meng F, Storm G, Zhong Z. Transferrin-binding peptide functionalized polymersomes mediate targeted doxorubicin delivery to colorectal cancer in vivo. J Controlled Release. 2020.

  12. Cherkasov VR, Mochalova EN, Babenyshev AV, Rozenberg JM, Sokolov IL, Nikitin MP. Antibody-directed metal-organic framework nanoparticles for targeted drug delivery. Acta Biomater. 2020;103:223–36.

    Article  CAS  Google Scholar 

  13. Timin AS, Litvak MM, Gorin DA, Atochina-Vasserman EN, Atochin DN, Sukhorukov GB. Cell-based drug delivery and use of nano-and microcarriers for cell functionalization. Adv Healthcare Mater. 2018;7(3):1700818.

    Article  Google Scholar 

  14. Borandeh S, Alimardani V, Abolmaali SS, Seppälä J. Graphene family nanomaterials in ocular applications: physicochemical properties and toxicity. Chem Res Toxicol. 2021.

  15. Alimardani V, Abolmaali SS, Tamaddon AM. Recent advances on nanotechnology-based strategies for prevention, diagnosis, and treatment of coronavirus infections. J Nanomater. 2021;2021.

  16. Alimardani V, Abolmaali SS, Borandeh S. Antifungal and antibacterial properties of graphene-based nanomaterials: a mini-review. J Nanostruct. 2019;9(3):402–13.

    Google Scholar 

  17. Pinelli F, Perale G, Rossi F. Coating and functionalization strategies for nanogels and nanoparticles for selective drug delivery. Gels. 2020;6(1):6.

    Article  CAS  Google Scholar 

  18. Fam SY, Chee CF, Yong CY, Ho KL, Mariatulqabtiah AR, Tan WS. Stealth coating of nanoparticles in drug-delivery systems. Nanomaterials. 2020;10(4):787.

    Article  CAS  Google Scholar 

  19. Banskota S, Yousefpour P, Chilkoti A. Cell-based biohybrid drug delivery systems: the best of the synthetic and natural worlds. Macromol Biosci. 2017;17(1):1600361.

    Article  Google Scholar 

  20. Su Y, **e Z, Kim GB, Dong C, Yang J. Design strategies and applications of circulating cell-mediated drug delivery systems. ACS Biomater Sci Eng. 2015;1(4):201–17.

    Article  CAS  Google Scholar 

  21. Kamal Z, Su J, Qiu M. Erythrocytes modified (coated) gold nanoparticles for effective drug delivery. Metal Nanoparticles Drug Deliv Diag Appl. Elsevier. 2020:13–29.

  22. Sun Y, Su J, Liu G, Chen J, Zhang X, Zhang R, et al. Advances of blood cell-based drug delivery systems. Eur J Pharm Sci. 2017;96:115–28.

    Article  CAS  Google Scholar 

  23. Li S, Liu J, Sun M, Wang J, Wang C, Sun Y. Cell Membrane-camouflaged nanocarriers for cancer diagnostic and therapeutic. Front Pharmacol. 2020:11.

  24. **e Z, Su Y, Kim GB, Selvi E, Ma C, Aragon-Sanabria V, et al. Immune cell-mediated biodegradable theranostic nanoparticles for melanoma targeting and drug delivery. Small. 2017;13(10):1603121.

    Article  Google Scholar 

  25. Yu H, Yang Z, Li F, Xu L, Sun Y. Cell-mediated targeting drugs delivery systems. Drug Deliv. 2020;27(1):1425–37.

    Article  CAS  Google Scholar 

  26. Lee N-H, You S, Taghizadeh A, Taghizadeh M, Kim HS. Cell Membrane-cloaked nanotherapeutics for targeted drug delivery. Int J Mol Sci. 2022;23(4):2223.

    Article  CAS  Google Scholar 

  27. Ihler GM, Glew RH, Schnure FW. Enzyme loading of erythrocytes. Proc Natl Acad Sci. 1973;70(9):2663–6.

    Article  CAS  Google Scholar 

  28. Hamidi M, Zarrin A, Foroozesh M, Mohammadi-Samani S. Applications of carrier erythrocytes in delivery of biopharmaceuticals. J Controlled Release. 2007;118(2):145–60.

    Article  CAS  Google Scholar 

  29. Wang L-Y, Shi X-Y, Yang C-S, Huang D-M. Versatile RBC-derived vesicles as nanoparticle vector of photosensitizers for photodynamic therapy. Nanoscale. 2013;5(1):416–21.

    Article  CAS  Google Scholar 

  30. Cohen Y, Afri M, Frimer AA. NMR-based molecular ruler for determining the depth of intercalants within the lipid bilayer: Part II. The preparation of a molecular ruler. Chem Phys Lipids. 2008;155(2):114–9.

  31. Tan S, Wu T, Zhang D, Zhang Z. Cell or cell membrane-based drug delivery systems. Theranostics. 2015;5(8):863.

    Article  CAS  Google Scholar 

  32. Koleva L, Bovt E, Ataullakhanov F, Sinauridze E. Erythrocytes as carriers: from drug delivery to biosensors. Pharmaceutics. 2020;12(3):276.

    Article  CAS  Google Scholar 

  33. Guido C, Maiorano G, Cortese B, D’Amone S, Palamà IE. Biomimetic nanocarriers for cancer target therapy. Bioengineering. 2020;7(3):111.

    Article  CAS  Google Scholar 

  34. Zhu D-M, **e W, **ao Y-S, Suo M, Zan M-H, Liao Q-Q, et al. Erythrocyte membrane-coated gold nanocages for targeted photothermal and chemical cancer therapy. Nanotechnology. 2018;29(8): 084002.

    Article  Google Scholar 

  35. **ao J, Weng J, Wen F, Ye J. Red blood cell membrane-coated silica nanoparticles codelivering DOX and ICG for effective lung cancer therapy. ACS omega. 2020.

  36. Li C, Wang X, Li R, Yang X, Zhong Z, Dai Y, et al. Resveratrol-loaded PLGA nanoparticles functionalized with red blood cell membranes as a biomimetic delivery system for prolonged circulation time. Journal of Drug Delivery Science and Technology. 2019;54: 101369.

    Article  CAS  Google Scholar 

  37. Zhang L, Wang Z, Zhang Y, Cao F, Dong K, Ren J, et al. Erythrocyte membrane cloaked metal–organic framework nanoparticle as biomimetic nanoreactor for starvation-activated colon cancer therapy. ACS Nano. 2018;12(10):10201–11.

    Article  CAS  Google Scholar 

  38. Piao J-G, Wang L, Gao F, You Y-Z, **ong Y, Yang L. Erythrocyte membrane is an alternative coating to polyethylene glycol for prolonging the circulation lifetime of gold nanocages for photothermal therapy. ACS Nano. 2014;8(10):10414–25.

    Article  CAS  Google Scholar 

  39. **e X, Wang H, Williams GR, Yang Y, Zheng Y, Wu J, et al. Erythrocyte membrane cloaked curcumin-loaded nanoparticles for enhanced chemotherapy. Pharmaceutics. 2019;11(9):429.

    Article  CAS  Google Scholar 

  40. Huang J, Lai W, Wang Q, Tang Q, Hu C, Zhou M, et al. Effective triple-negative breast cancer targeted treatment using iRGD-modified RBC membrane-camouflaged nanoparticles. Int J Nanomed. 2021;16:7497.

    Article  CAS  Google Scholar 

  41. Lu Y, Hu Q, Jiang C, Gu Z. Platelet for drug delivery. Curr Opin Biotechnol. 2019;58:81–91.

    Article  CAS  Google Scholar 

  42. Nieswandt B, Pleines I, Bender M. Platelet adhesion and activation mechanisms in arterial thrombosis and ischaemic stroke. J Thromb Haemost. 2011;9:92–104.

    Article  CAS  Google Scholar 

  43. Wang C, Sun W, Ye Y, Hu Q, Bomba HN, Gu Z. In situ activation of platelets with checkpoint inhibitors for post-surgical cancer immunotherapy. Nature Biomedical Engineering. 2017;1(2):1–10.

    Article  Google Scholar 

  44. Xu P, Zuo H, Chen B, Wang R, Ahmed A, Hu Y, et al. Doxorubicin-loaded platelets as a smart drug delivery system: an improved therapy for lymphoma. Sci Rep. 2017;7:42632.

    Article  CAS  Google Scholar 

  45. Jiménez-Jiménez C, Manzano M, Vallet-Regí M. Nanoparticles coated with cell membranes for biomedical applications. Biology. 2020;9(11):406.

    Article  Google Scholar 

  46. Zuo H, Tao J, Shi H, He J, Zhou Z, Zhang C. Platelet-mimicking nanoparticles co-loaded with W18O49 and metformin alleviate tumor hypoxia for enhanced photodynamic therapy and photothermal therapy. Acta Biomater. 2018;80:296–307. https://doi.org/10.1016/j.actbio.2018.09.017.

    Article  CAS  Google Scholar 

  47. Zhai Y, Su J, Ran W, Zhang P, Yin Q, Zhang Z, et al. Preparation and application of cell membrane-camouflaged nanoparticles for cancer therapy. Theranostics. 2017;7(10):2575.

    Article  CAS  Google Scholar 

  48. Li J, Ai Y, Wang L, Bu P, Sharkey CC, Wu Q, et al. Targeted drug delivery to circulating tumor cells via platelet membrane-functionalized particles. Biomaterials. 2016;76:52–65.

    Article  CAS  Google Scholar 

  49. Bang K-H, Na Y-G, Huh HW, Hwang S-J, Kim M-S, Kim M, et al. The delivery strategy of paclitaxel nanostructured lipid carrier coated with platelet membrane. Cancers (Basel). 2019;11(6):807.

    Article  CAS  Google Scholar 

  50. Turley SJ, Cremasco V, Astarita JL. Immunological hallmarks of stromal cells in the tumour microenvironment. Nat Rev Immunol. 2015;15(11):669–82.

    Article  CAS  Google Scholar 

  51. Huang Y, Gao X, Chen J. Leukocyte-derived biomimetic nanoparticulate drug delivery systems for cancer therapy. Acta Pharmaceutica Sinica B. 2018;8(1):4–13.

    Article  Google Scholar 

  52. Zhang W, Wang M, Tang W, Wen R, Zhou S, Lee C, et al. Nanoparticle-laden macrophages for tumor-tropic drug delivery. Adv Mater. 2018;30(50):1805557.

    Article  Google Scholar 

  53. Lutz H, Hu S, Dinh P-U, Cheng K. Cells and cell derivatives as drug carriers for targeted delivery. Medicine in Drug Discovery. 2019;3: 100014.

    Article  Google Scholar 

  54. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol. 2012;30:459–89.

    Article  CAS  Google Scholar 

  55. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159–75.

    Article  CAS  Google Scholar 

  56. Dong X, Chu D, Wang Z. Leukocyte-mediated delivery of nanotherapeutics in inflammatory and tumor sites. Theranostics. 2017;7(3):751.

    Article  CAS  Google Scholar 

  57. Ye B, Zhao B, Wang K, Guo Y, Lu Q, Zheng L, et al. Neutrophils mediated multistage nanoparticle delivery for prompting tumor photothermal therapy. Journal of Nanobiotechnology. 2020;18(1):1–14.

    Article  Google Scholar 

  58. Che J, Najer A, Blakney AK, McKay PF, Bellahcene M, Winter CW, et al. Neutrophils enable local and non-invasive liposome delivery to inflamed skeletal muscle and ischemic heart. Adv Mater. 2020;32(48):2003598.

    Article  CAS  Google Scholar 

  59. Xue J, Zhao Z, Zhang L, Xue L, Shen S, Wen Y, et al. Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence. Nat Nanotechnol. 2017;12(7):692.

    Article  CAS  Google Scholar 

  60. Ju C, Wen Y, Zhang L, Wang Q, Xue L, Shen J, et al. Neoadjuvant chemotherapy based on abraxane/human neutrophils cytopharmaceuticals with radiotherapy for gastric cancer. Small. 2019;15(5):1804191.

    Article  Google Scholar 

  61. Mauri C, Bosma A. Immune regulatory function of B cells. Annu Rev Immunol. 2012;30:221–41.

    Article  CAS  Google Scholar 

  62. Zhang G, Wang L, Cui H, Wang X, Zhang G, Ma J, et al. Anti-melanoma activity of T cells redirected with a TCR-like chimeric antigen receptor. Sci Rep. 2014;4:3571.

    Article  Google Scholar 

  63. Huang B, Abraham WD, Zheng Y, López SCB, Luo SS, Irvine DJ. Active targeting of chemotherapy to disseminated tumors using nanoparticle-carrying T cells. Science Transl Med. 2015;7(291):291ra94-ra94.

  64. Kennedy LC, Bear AS, Young JK, Lewinski NA, Kim J, Foster AE, et al. T cells enhance gold nanoparticle delivery to tumors in vivo. Nanoscale Res Lett. 2011;6(1):283.

    Article  Google Scholar 

  65. Jones RB, Mueller S, Kumari S, Vrbanac V, Genel S, Tager AM, et al. Antigen recognition-triggered drug delivery mediated by nanocapsule-functionalized cytotoxic T-cells. Biomaterials. 2017;117:44–53.

    Article  CAS  Google Scholar 

  66. Mitchell MJ, King MR. Leukocytes as carriers for targeted cancer drug delivery. Expert Opin Drug Deliv. 2015;12(3):375–92.

    Article  CAS  Google Scholar 

  67. Pierigè F, Serafini S, Rossi L, Magnani M. Cell-based drug delivery. Adv Drug Deliv Rev. 2008;60(2):286–95.

    Article  Google Scholar 

  68. Yousefpour P, Chilkoti A. Co-opting biology to deliver drugs. Biotechnol Bioeng. 2014;111(9):1699–716.

    Article  CAS  Google Scholar 

  69. Klyachko NL, Polak R, Haney MJ, Zhao Y, Neto RJG, Hill MC, et al. Macrophages with cellular backpacks for targeted drug delivery to the brain. Biomaterials. 2017;140:79–87.

    Article  CAS  Google Scholar 

  70. Gilboa E, Nair SK, Lyerly HK. Immunotherapy of cancer with dendritic-cell-based vaccines. Cancer Immunol Immunother. 1998;46(2):82–7.

    Article  CAS  Google Scholar 

  71. Subklewe M, Geiger C, Lichtenegger FS, Javorovic M, Kvalheim G, Schendel DJ, et al. New generation dendritic cell vaccine for immunotherapy of acute myeloid leukemia. Cancer Immunol Immunother. 2014;63(10):1093–103.

    Article  CAS  Google Scholar 

  72. Benencia F, Sprague L, McGinty J, Pate M, Muccioli M. Dendritic cells the tumor microenvironment and the challenges for an effective antitumor vaccination. J Biomed Biotechnol. 2012;2012.

  73. Galluzzi L, Senovilla L, Vacchelli E, Eggermont A, Fridman WH, Galon J, et al. Trial watch: Dendritic cell-based interventions for cancer therapy. Oncoimmunology. 2012;1(7):1111–34.

    Article  Google Scholar 

  74. Patente TA, Pinho MP, Oliveira AA, Evangelista GCM, Bergami-Santos PC, Barbuto JAM. Human dendritic cells: their heterogeneity and clinical application potential in cancer immunotherapy. Front Immunol. 2019;9(3176). https://doi.org/10.3389/fimmu.2018.03176.

  75. Xu J, Ma Q, Zhang Y, Fei Z, Sun Y, Fan Q, et al. Yeast-derived nanoparticles remodel the immunosuppressive microenvironment in tumor and tumor-draining lymph nodes to suppress tumor growth. Nat Commun. 2022;13(1):1–15.

    CAS  Google Scholar 

  76. Wang D, Zhang B, Gao H, Ding G, Wu Q, Zhang J, et al. Clinical research of genetically modified dendritic cells in combination with cytokine-induced killer cell treatment in advanced renal cancer. BMC Cancer. 2014;14(1):1–7.

    Google Scholar 

  77. Sherman LS, Romagano MP, Williams SF, Rameshwar P. Mesenchymal stem cell therapies in brain disease. Semin Cell Dev Biol. 2019;95:111–9. https://doi.org/10.1016/j.semcdb.2019.03.003.

    Article  CAS  Google Scholar 

  78. Krueger TE, Thorek DL, Denmeade SR, Isaacs JT, Brennen WN. Concise review: mesenchymal stem cell-based drug delivery: The good, the bad, the ugly, and the promise. Stem Cells Transl Med. 2018;7(9):651–63.

    Article  Google Scholar 

  79. Coccè V, Farronato D, Brini AT, Masia C, Giannì AB, Piovani G, et al. Drug loaded gingival mesenchymal stromal cells (GinPa-MSCs) inhibit in vitro proliferation of oral squamous cell carcinoma. Sci Rep. 2017;7(1):9376. https://doi.org/10.1038/s41598-017-09175-4.

    Article  CAS  Google Scholar 

  80. Heo J-R, Hwang K-A, Kim SU, Choi K-C. A potential therapy using engineered stem cells prevented malignant melanoma in cellular and xenograft mouse models. Cancer Res Treat. 2019;51(2):797–811. https://doi.org/10.4143/crt.2018.364.

    Article  CAS  Google Scholar 

  81. Kooreman NG, Wu JC. Tumorigenicity of pluripotent stem cells: biological insights from molecular imaging. J Royal Soc Interface. 2010;7(suppl_6):S753-S63.

  82. Chen H-Y, Deng J, Wang Y, Wu C-Q, Li X, Dai H-W. Hybrid cell membrane-coated nanoparticles: a multifunctional biomimetic platform for cancer diagnosis and therapy. Acta Biomaterialia. 2020.

  83. Suryaprakash S, Lao Y-H, Cho H-Y, Li M, Ji HY, Shao D, et al. Engineered mesenchymal stem cell/nanomedicine spheroid as an active drug delivery platform for combinational glioblastoma therapy. Nano Lett. 2019;19(3):1701–5.

    Article  CAS  Google Scholar 

  84. Tian W, Lu J, Jiao D. Stem cell membrane vesicle–coated nanoparticles for efficient tumor-targeted therapy of orthotopic breast cancer. Polym Adv Technol. 2019;30(4):1051–60.

    Article  CAS  Google Scholar 

  85. Yang N, Ding Y, Zhang Y, Wang B, Zhao X, Cheng K, et al. Surface functionalization of polymeric nanoparticles with umbilical cord-derived mesenchymal stem cell membrane for tumor-targeted therapy. ACS Appl Mater Interfaces. 2018;10(27):22963–73.

    Article  CAS  Google Scholar 

  86. Khaldoyanidi SK, Glinsky VV, Sikora L, Glinskii AB, Mossine VV, Quinn TP, et al. MDA-MB-435 human breast carcinoma cell homo-and heterotypic adhesion under flow conditions is mediated in part by Thomsen-Friedenreich antigen-galectin-3 interactions. J Biol Chem. 2003;278(6):4127–34.

    Article  CAS  Google Scholar 

  87. Mareel M, Vleminckx K, Vermeulen S, Gao Y, Vakaet Jr L, Bracke M, Van Roy F. 3.3 Homotypic cell-cell adhesion molecules and tumor invasion. Progress in histochemistry and cytochemistry. 1992;26(1-4):95-106.

  88. He Z, Zhang Y, Feng N. Cell membrane-coated nanosized active targeted drug delivery systems homing to tumor cells: a review. Mater Sci Eng, C. 2020;106: 110298.

    Article  CAS  Google Scholar 

  89. Zhu J-Y, Zheng D-W, Zhang M-K, Yu W-Y, Qiu W-X, Hu J-J, et al. Preferential cancer cell self-recognition and tumor self-targeting by coating nanoparticles with homotypic cancer cell membranes. Nano Lett. 2016;16(9):5895–901.

    Article  CAS  Google Scholar 

  90. Sun H, Su J, Meng Q, Yin Q, Chen L, Gu W, et al. Cancer-cell-biomimetic nanoparticles for targeted therapy of homotypic tumors. Adv Mater. 2016;28(43):9581–8.

    Article  CAS  Google Scholar 

  91. Glinsky VV, Glinsky GV, Glinskii OV, Huxley VH, Turk JR, Mossine VV, et al. Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium. Can Res. 2003;63(13):3805–11.

    CAS  Google Scholar 

  92. Fang RH, Hu C-MJ, Luk BT, Gao W, Copp JA, Tai Y et al. Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery. Nano letters. 2014;14(4):2181–8.

  93. Yang R, Xu J, Xu L, Sun X, Chen Q, Zhao Y, et al. Cancer cell membrane-coated adjuvant nanoparticles with mannose modification for effective anticancer vaccination. ACS Nano. 2018;12(6):5121–9.

    Article  CAS  Google Scholar 

  94. Meng X, Wang J, Zhou J, Tian Q, Qie B, Zhou G, et al. Tumor cell membrane-based peptide delivery system targeting the tumor microenvironment for cancer immunotherapy and diagnosis. Acta Biomater. 2021;127:266–75.

    Article  CAS  Google Scholar 

  95. Cozzo AJ, Fuller AM, Makowski L. Contribution of adipose tissue to development of cancer. Compr Physiol. 2017;8(1):237.

    Article  Google Scholar 

  96. Munteanu R, Onaciu A, Moldovan C, Zimta A-A, Gulei D, Paradiso AV, et al. Adipocyte-based cell therapy in oncology: the role of cancer-associated adipocytes and their reinterpretation as delivery platforms. Pharmaceutics. 2020;12(5):402.

    Article  CAS  Google Scholar 

  97. Santander AM, Lopez-Ocejo O, Casas O, Agostini T, Sanchez L, Lamas-Basulto E, et al. Paracrine interactions between adipocytes and tumor cells recruit and modify macrophages to the mammary tumor microenvironment: the role of obesity and inflammation in breast adipose tissue. Cancers (Basel). 2015;7(1):143–78.

    Article  CAS  Google Scholar 

  98. Wen D, Wang J, Van Den Driessche G, Chen Q, Zhang Y, Chen G, et al. Adipocytes as anticancer drug delivery depot. Matter. 2019;1(5):1203–14.

    Article  Google Scholar 

  99. Zhang M, Di Martino JS, Bowman RL, Campbell NR, Baksh SC, Simon-Vermot T, et al. Adipocyte-derived lipids mediate melanoma progression via FATP proteins. Cancer Discov. 2018;8(8):1006–25.

    Article  CAS  Google Scholar 

  100. Miranda F, Mannion D, Liu S, Zheng Y, Mangala LS, Redondo C, et al. Salt-inducible kinase 2 couples ovarian cancer cell metabolism with survival at the adipocyte-rich metastatic niche. Cancer Cell. 2016;30(2):273–89.

    Article  CAS  Google Scholar 

  101. Uchibori R, Tsukahara T, Mizuguchi H, Saga Y, Urabe M, Mizukami H, et al. NF-κB activity regulates mesenchymal stem cell accumulation at tumor sites. Cancer Res. 2013;73(1):364–72.

    Article  CAS  Google Scholar 

  102. Josiah DT, Zhu D, Dreher F, Olson J, McFadden G, Caldas H. Adipose-derived stem cells as therapeutic delivery vehicles of an oncolytic virus for glioblastoma. Mol Ther. 2010;18(2):377–85. https://doi.org/10.1038/mt.2009.265.

    Article  CAS  Google Scholar 

  103. Choi SA, Lee JY, Kwon SE, Wang KC, Phi JH, Choi JW, et al. Human adipose tissue-derived mesenchymal stem cells target brain tumor-initiating cells. PLoS ONE. 2015;10(6): e0129292. https://doi.org/10.1371/journal.pone.0129292.

    Article  CAS  Google Scholar 

  104. Huang W-C, Lu I-L, Chiang W-H, Lin Y-W, Tsai Y-C, Chen H-H, et al. Tumortropic adipose-derived stem cells carrying smart nanotherapeutics for targeted delivery and dual-modality therapy of orthotopic glioblastoma. J Controlled Release. 2017;254:119–30.

    Article  CAS  Google Scholar 

  105. Scioli MG, Artuso S, D’Angelo C, Porru M, D’Amico F, Bielli A, et al. Adipose-derived stem cell-mediated paclitaxel delivery inhibits breast cancer growth. PLoS ONE. 2018;13(9): e0203426.

    Article  Google Scholar 

  106. Coccè V, Brini A, Giannì AB, Sordi V, Berenzi A, Alessandri G, et al. A nonenzymatic and automated closed-cycle process for the isolation of mesenchymal stromal cells in drug delivery applications. Stem Cells International. 2018;2018:4098140. https://doi.org/10.1155/2018/4098140.

    Article  CAS  Google Scholar 

  107. Sun H, Burrola S, Wu J, Ding W-Q. Extracellular vesicles in the development of cancer therapeutics. Int J Mol Sci. 2020;21(17):6097.

    Article  CAS  Google Scholar 

  108. Burgio S, Noori L, Marino Gammazza A, Campanella C, Logozzi M, Fais S, et al. Extracellular vesicles-based drug delivery systems: a new challenge and the exemplum of malignant pleural mesothelioma. Int J Mol Sci. 2020;21(15):5432.

    Article  CAS  Google Scholar 

  109. Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Biol Chem. 1946;166(1):189–97.

    Article  CAS  Google Scholar 

  110. Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478):eaau6977.

  111. Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci. 2018;75(2):193–208.

    Article  CAS  Google Scholar 

  112. Pavlyukov MS, Yu H, Bastola S, Minata M, Shender VO, Lee Y et al. Apoptotic cell-derived extracellular vesicles promote malignancy of glioblastoma via intercellular transfer of splicing factors. Cancer Cell. 2018;34(1):119–35. e10.

  113. Smyth TJ, Redzic JS, Graner MW, Anchordoquy TJ. Examination of the specificity of tumor cell derived exosomes with tumor cells in vitro. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2014;1838(11):2954–65.

  114. Hoshino A, Costa-Silva B, Shen T-L, Rodrigues G, Hashimoto A, Tesic Mark M, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329–35.

    Article  CAS  Google Scholar 

  115. Wortzel I, Dror S, Kenific CM, Lyden D. Exosome-mediated metastasis: communication from a distance. Dev Cell. 2019;49(3):347–60.

    Article  CAS  Google Scholar 

  116. Kanchanapally R, Deshmukh SK, Chavva SR, Tyagi N, Srivastava SK, Patel GK, et al. Drug-loaded exosomal preparations from different cell types exhibit distinctive loading capability, yield, and antitumor efficacies: a comparative analysis. Int J Nanomed. 2019;14:531.

    Article  CAS  Google Scholar 

  117. O’Loughlin AJ, Mäger I, de Jong OG, Varela MA, Schiffelers RM, El Andaloussi S, et al. Functional delivery of lipid-conjugated siRNA by extracellular vesicles. Mol Ther. 2017;25(7):1580–7.

    Article  Google Scholar 

  118. Srivastava A, Amreddy N, Pareek V, Chinnappan M, Ahmed R, Mehta M, et al. Progress in extracellular vesicle biology and their application in cancer medicine. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology. 2020;12(4): e1621.

    Google Scholar 

  119. Hood JL, Scott MJ, Wickline SA. Maximizing exosome colloidal stability following electroporation. Anal Biochem. 2014;448:41–9.

    Article  CAS  Google Scholar 

  120. Cheng Z, Liu S, Wu X, Raza F, Li Y, Yuan W, et al. Autologous erythrocytes delivery of berberine hydrochloride with long-acting effect for hypolipidemia treatment. Drug Deliv. 2020;27(1):283–91.

    Article  CAS  Google Scholar 

  121. Munoz JL, Bliss SA, Greco SJ, Ramkissoon SH, Ligon KL, Rameshwar P. Delivery of functional anti-miR-9 by mesenchymal stem cell–derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Molecular Therapy-Nucleic Acids. 2013;2: e126.

    Article  Google Scholar 

  122. Pascucci L, Coccè V, Bonomi A, Ami D, Ceccarelli P, Ciusani E, et al. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: a new approach for drug delivery. J Controlled Release. 2014;192:262–70.

    Article  CAS  Google Scholar 

  123. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011;29(4):341–5.

    Article  CAS  Google Scholar 

  124. Tian Y, Li S, Song J, Ji T, Zhu M, Anderson GJ, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials. 2014;35(7):2383–90.

    Article  CAS  Google Scholar 

  125. Bysell H, Månsson R, Hansson P, Malmsten M. Microgels and microcapsules in peptide and protein drug delivery. Adv Drug Del Rev. 2011;63(13):1172–85.

    Article  CAS  Google Scholar 

  126. Johnson GD, Lalancette C, Linnemann AK, Leduc F, Boissonneault G, Krawetz SA. The sperm nucleus: chromatin, RNA and the nuclear matrix. Reproduction (Cambridge, England). 2011;141(1):21.

    Article  CAS  Google Scholar 

  127. Mattioli M, Gloria A, Mauro A, Gioia L, Barboni B. Fusion as the result of sperm–somatic cell interaction. Reproduction. 2009;138(4):679–87.

    Article  CAS  Google Scholar 

  128. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69(1):7–34.

    Article  Google Scholar 

  129. Xu H, Sanchez MM, Magdanz V, Schwarz L, Hebenstreit F, Schmidt OG. Sperm-hybrid micromotor for drug delivery in the female reproductive tract. ar**v preprint ar**v:1703.08510. 2017.

  130. Xu H, Medina-Sánchez M, Magdanz V, Schwarz L, Hebenstreit F, Schmidt OG. Sperm-hybrid micromotor for targeted drug delivery. ACS Nano. 2018;12(1):327–37. https://doi.org/10.1021/acsnano.7b06398.

    Article  CAS  Google Scholar 

  131. Singh AV, Ansari MHD, Mahajan M, Srivastava S, Kashyap S, Dwivedi P, et al. Sperm cell driven microrobots—emerging opportunities and challenges for biologically inspired robotic design. Micromachines. 2020;11(4):448.

    Article  Google Scholar 

  132. Sedighi M, Zahedi Bialvaei A, Hamblin MR, Ohadi E, Asadi A, Halajzadeh M, et al. Therapeutic bacteria to combat cancer; current advances, challenges, and opportunities. Cancer Med. 2019;8(6):3167–81.

    Google Scholar 

  133. Patyar S, Joshi R, Byrav DP, Prakash A, Medhi B, Das B. Bacteria in cancer therapy: a novel experimental strategy. J Biomed Sci. 2010;17(1):1–9.

    Article  Google Scholar 

  134. Kim VM, Blair AB, Lauer P, Foley K, Che X, Soares K, et al. Anti-pancreatic tumor efficacy of a Listeria-based, Annexin A2-targeting immunotherapy in combination with anti-PD-1 antibodies. J Immunother Cancer. 2019;7(1):1–13.

    Article  Google Scholar 

  135. Taniguchi Si, Shimatani Y, Fujimori M. Tumor-targeting therapy using gene-engineered anaerobic-nonpathogenic Bifidobacterium longum. Bacterial Therapy Cancer. Springer. 2016:49–60.

  136. Heap JT, Theys J, Ehsaan M, Kubiak AM, Dubois L, Paesmans K, et al. Spores of Clostridium engineered for clinical efficacy and safety cause regression and cure of tumors in vivo. Oncotarget. 2014;5(7):1761.

    Article  Google Scholar 

  137. Gu T-W, Wang M-Z, Niu J, Chu Y, Guo K-R, Peng L-H. Outer membrane vesicles derived from E. coli as novel vehicles for transdermal and tumor targeting delivery. Nanoscale. 2020;12(36):18965–77.

  138. Liang K, Liu Q, Li P, Luo H, Wang H, Kong Q. Genetically engineered Salmonella Typhimurium: recent advances in cancer therapy. Cancer Lett. 2019;448:168–81.

    Article  CAS  Google Scholar 

  139. Van Mellaert L, Barbé S, Anné J. Clostridium spores as anti-tumour agents. Trends Microbiol. 2006;14(4):190–6.

    Article  Google Scholar 

  140. Duong MT-Q, Qin Y, You S-H, Min J-J. Bacteria-cancer interactions: bacteria-based cancer therapy. Exp Mol Med. 2019;51(12):1–15.

  141. Shi L, Sheng J, Wang M, Luo H, Zhu J, Zhang B, et al. Combination therapy of TGF-β blockade and commensal-derived probiotics provides enhanced antitumor immune response and tumor suppression. Theranostics. 2019;9(14):4115.

    Article  CAS  Google Scholar 

  142. Ganai S, Arenas RB, Sauer JP, Bentley B, Forbes NS. In tumors Salmonella migrate away from vasculature toward the transition zone and induce apoptosis. Cancer Gene Ther. 2011;18(7):457–66.

    Article  CAS  Google Scholar 

  143. Lee C, Lin S, Liu J, Chang W, Hsieh J, Wang W. Salmonella induce autophagy in melanoma by the downregulation of AKT/mTOR pathway. Gene Ther. 2014;21(3):309–16.

    Article  CAS  Google Scholar 

  144. Kim SH, Castro F, Paterson Y, Gravekamp C. High efficacy of a Listeria-based vaccine against metastatic breast cancer reveals a dual mode of action. Cancer Res. 2009;69(14):5860–6.

    Article  CAS  Google Scholar 

  145. Hosseinidoust Z, Mostaghaci B, Yasa O, Park B-W, Singh AV, Sitti M. Bioengineered and biohybrid bacteria-based systems for drug delivery. Adv Drug Deliv Rev. 2016;106:27–44.

    Article  CAS  Google Scholar 

  146. Li M, Zhou H, Yang C, Wu Y, Zhou X, Liu H, et al. Bacterial outer membrane vesicles as a platform for biomedical applications: An update. J Control Release. 2020;323:253–68.

    Article  CAS  Google Scholar 

  147. Huang W, Shu C, Hua L, Zhao Y, **e H, Qi J, et al. Modified bacterial outer membrane vesicles induce autoantibodies for tumor therapy. Acta Biomater. 2020;108:300–12.

    Article  CAS  Google Scholar 

  148. Liu X, Jiang S, Piao L, Yuan F. Radiotherapy combined with an engineered of Salmonella typhimurium inhibits tumor growth in a mouse model of colon cancer. Exp Anim. 2016:16–0033.

  149. Dresselaers T, Theys J, Nuyts S, Wouters B, de Bruijn E, Anné J, et al. Non-invasive 19 F MR spectroscopy of 5-fluorocytosine to 5-fluorouracil conversion by recombinant Salmonella in tumours. Br J Cancer. 2003;89(9):1796–801.

    Article  CAS  Google Scholar 

  150. Nemunaitis J, Cunningham C, Senzer N, Kuhn J, Cramm J, Litz C et al. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients. Cancer Gene Ther. 2003;10(10):737–44.

  151. Zou S, Wang B, Wang C, Wang Q, Zhang L. Cell membrane-coated nanoparticles: research advances. Nanomedicine. 2020;15(06):625–41.

    Article  CAS  Google Scholar 

  152. Li J, Wang X, Zheng D, Lin X, Wei Z, Zhang D, et al. Cancer cell membrane-coated magnetic nanoparticles for MR/NIR fluorescence dual-modal imaging and photodynamic therapy. Biomaterials science. 2018;6(7):1834–45.

    Article  CAS  Google Scholar 

  153. Rao L, Cai B, Bu L-L, Liao Q-Q, Guo S-S, Zhao X-Z, et al. Microfluidic electroporation-facilitated synthesis of erythrocyte membrane-coated magnetic nanoparticles for enhanced imaging-guided cancer therapy. ACS Nano. 2017;11(4):3496–505.

    Article  CAS  Google Scholar 

  154. Rao L, Bu LL, Cai B, Xu JH, Li A, Zhang WF, et al. Cancer cell membrane-coated upconversion nanoprobes for highly specific tumor imaging. Adv Mater. 2016;28(18):3460–6.

    Article  CAS  Google Scholar 

  155. Ren X, Zheng R, Fang X, Wang X, Zhang X, Yang W, et al. Red blood cell membrane camouflaged magnetic nanoclusters for imaging-guided photothermal therapy. Biomaterials. 2016;92:13–24.

    Article  CAS  Google Scholar 

  156. Zhang X, He S, Ding B, Qu C, Zhang Q, Chen H, et al. Cancer cell membrane-coated rare earth doped nanoparticles for tumor surgery navigation in NIR-II imaging window. Chem Eng J. 2020;385: 123959.

    Article  CAS  Google Scholar 

  157. Wang C, Wu B, Wu Y, Song X, Zhang S, Liu Z. Camouflaging nanoparticles with brain metastatic tumor cell membranes: a new strategy to traverse blood–brain barrier for imaging and therapy of brain tumors. Adv Funct Mater. 2020;30(14):1909369.

    Article  CAS  Google Scholar 

  158. Li S, Jiang W, Yuan Y, Sui M, Yang Y, Huang L, et al. Delicately designed cancer cell membrane-camouflaged nanoparticles for targeted 19F MR/PA/FL imaging-guided photothermal therapy. ACS Appl Mater Interfaces. 2020;12(51):57290–301.

    Article  CAS  Google Scholar 

  159. Lu H, Guo K, Cao Y, Yang F, Wang D, Dou L, et al. Cancer cell membrane vesicle for multiplex MicroRNA imaging in living cells. Anal Chem. 2019;92(2):1850–5.

    Article  Google Scholar 

  160. Chen Q, Zhang L, Li L, Tan M, Liu W, Liu S, et al. Cancer cell membrane-coated nanoparticles for bimodal imaging-guided photothermal therapy and docetaxel-enhanced immunotherapy against cancer. Journal of nanobiotechnology. 2021;19(1):1–22.

    Article  Google Scholar 

  161. Li J, Zhen X, Lyu Y, Jiang Y, Huang J, Pu K. Cell membrane coated semiconducting polymer nanoparticles for enhanced multimodal cancer phototheranostics. ACS Nano. 2018;12(8):8520–30.

    Article  CAS  Google Scholar 

  162. Zhang K, Cao Y, Kuang Y, Liu M, Chen Y, Wang Z, et al. Gd 2 O 3 and GH combined with red blood cells to improve the sensitivity of contrast agents for cancer targeting MR imaging. Biomaterials science. 2017;5(1):46–9.

    Article  CAS  Google Scholar 

  163. Choi J, Kim H-Y, Ju EJ, Jung J, Park J, Chung H-K, et al. Use of macrophages to deliver therapeutic and imaging contrast agents to tumors. Biomaterials. 2012;33(16):4195–203.

    Article  CAS  Google Scholar 

  164. Huang X, Zhang F, Wang H, Niu G, Choi KY, Swierczewska M, et al. Mesenchymal stem cell-based cell engineering with multifunctional mesoporous silica nanoparticles for tumor delivery. Biomaterials. 2013;34(7):1772–80.

    Article  CAS  Google Scholar 

  165. Ahn S, Jung SY, Seo E, Lee SJ. Gold nanoparticle-incorporated human red blood cells (RBCs) for X-ray dynamic imaging. Biomaterials. 2011;32(29):7191–9.

    Article  CAS  Google Scholar 

  166. Kravtzoff R, Ropars C, Desbois I, Chassaigne M, Lamagnere J, Colombat P, et al. Improved pharmacodynamics of L-asparaginase-loaded in human red blood cells. Eur J Clin Pharmacol. 1996;49(6):465–70.

    Article  CAS  Google Scholar 

  167. Li C-X, Qi Y-D, Feng J, Zhang X-Z. Cell-based bio-hybrid delivery system for disease treatments. Advanced Nanobiomed Research. 2021;1(10):2000052.

    Article  Google Scholar 

  168. Wu S-H, Hsieh C-C, Hsu S-C, Yao M, Hsiao J-K, Wang S-W et al. RBC-derived vesicles as a systemic delivery system of doxorubicin for lysosomal-mitochondrial axis-improved cancer therapy. J Adv Res. 2020.

  169. Zhang D, Zhou C, Liu F, Ding T, Wang Z. Red blood cells membrane vehicle co-delivering DOX and IR780 for effective prostate cancer therapy. J Mater Res. 2020;35(22):3116–23.

    Article  CAS  Google Scholar 

  170. Harisa GI, Ibrahim MF, Alanazi F, Shazly GA. Engineering erythrocytes as a novel carrier for the targeted delivery of the anticancer drug paclitaxel. Saudi Pharmaceutical Journal. 2014;22(3):223–30. https://doi.org/10.1016/j.jsps.2013.06.007.

    Article  Google Scholar 

  171. Wang GP, Guan YS, ** XR, Jiang SS, Lu ZJ, Wu Y, et al. Development of novel 5-fluorouracil carrier erythrocyte with pharmacokinetics and potent antitumor activity in mice bearing malignant ascites. J Gastroenterol Hepatol. 2010;25(5):985–90. https://doi.org/10.1111/j.1440-1746.2009.06155.x.

    Article  CAS  Google Scholar 

  172. Jiang Q, Liu Y, Guo R, Yao X, Sung S, Pang Z, et al. Erythrocyte-cancer hybrid membrane-camouflaged melanin nanoparticles for enhancing photothermal therapy efficacy in tumors. Biomaterials. 2019;192:292–308.

    Article  CAS  Google Scholar 

  173. Fu Q, Lv P, Chen Z, Ni D, Zhang L, Yue H, et al. Programmed co-delivery of paclitaxel and doxorubicin boosted by camouflaging with erythrocyte membrane. Nanoscale. 2015;7(9):4020–30.

    Article  CAS  Google Scholar 

  174. Su J, Sun H, Meng Q, Yin Q, Zhang P, Zhang Z, et al. Bioinspired nanoparticles with NIR-controlled drug release for synergetic chemophotothermal therapy of metastatic breast cancer. Adv Func Mater. 2016;26(41):7495–506.

    Article  CAS  Google Scholar 

  175. Zhang X, **ong J, Wang K, Yu H, Sun B, Ye H, et al. Erythrocyte membrane-camouflaged carrier-free nanoassembly of FRET photosensitizer pairs with high therapeutic efficiency and high security for programmed cancer synergistic phototherapy. Bioactive Materials. 2021;6(8):2291–302.

    Article  CAS  Google Scholar 

  176. Daniyal M, Jian Y, **ao F, Sheng W, Fan J, **ao C, et al. Development of a nanodrug-delivery system camouflaged by erythrocyte membranes for the chemo/phototherapy of cancer. Nanomedicine. 2020;15(07):691–709.

    Article  CAS  Google Scholar 

  177. Lin Y, Zhong Y, Chen Y, Li L, Chen G, Zhang J, et al. Ligand-modified erythrocyte membrane-cloaked metal–organic framework nanoparticles for targeted antitumor therapy. Mol Pharm. 2020;17(9):3328–41.

    Article  CAS  Google Scholar 

  178. Zhai Z, Xu P, Yao J, Li R, Gong L, Yin Y, et al. Erythrocyte-mimicking paclitaxel nanoparticles for improving biodistributions of hydrophobic drugs to enhance antitumor efficacy. Drug Delivery. 2020;27(1):387–99.

    Article  CAS  Google Scholar 

  179. Wang Y, Luan Z, Zhao C, Bai C, Yang K. Target delivery selective CSF-1R inhibitor to tumor-associated macrophages via erythrocyte-cancer cell hybrid membrane camouflaged pH-responsive copolymer micelle for cancer immunotherapy. Eur J Pharm Sci. 2020;142: 105136.

    Article  CAS  Google Scholar 

  180. Lian Y, Wang X, Guo P, Li Y, Raza F, Su J, et al. Erythrocyte membrane-coated arsenic trioxide-loaded sodium alginate nanoparticles for tumor therapy. Pharmaceutics. 2020;12(1):21.

    Article  CAS  Google Scholar 

  181. Chen Z, Wang W, Li Y, Wei C, Zhong P, He D, et al. Folic acid-modified erythrocyte membrane loading dual drug for targeted and chemo-photothermal synergistic cancer therapy. Mol Pharm. 2020.

  182. Chen S, Ren Y, Duan P. Biomimetic nanoparticle loading obatoclax mesylate for the treatment of non-small-cell lung cancer (NSCLC) through suppressing Bcl-2 signaling. Biomed Pharmacother. 2020;129: 110371.

    Article  CAS  Google Scholar 

  183. Zheng D, Yu P, Wei Z, Zhong C, Wu M, Liu X. RBC Membrane camouflaged semiconducting polymer nanoparticles for near-infrared photoacoustic imaging and photothermal therapy. Nano-Micro Letters. 2020;12(1):1–17.

    Article  Google Scholar 

  184. Huang X, Shang W, Deng H, Zhou Y, Cao F, Fang C, et al. Clothing spiny nanoprobes against the mononuclear phagocyte system clearance in vivo: photoacoustic diagnosis and photothermal treatment of early stage liver cancer with erythrocyte membrane-camouflaged gold nanostars. Appl Mater Today. 2020;18: 100484.

    Article  Google Scholar 

  185. Bidkar AP, Sanpui P, Ghosh SS. Red blood cell-membrane-coated poly (lactic-co-glycolic acid) nanoparticles for enhanced chemo-and hypoxia-activated therapy. ACS Appl Bio Mater. 2019;2(9):4077–86.

    Article  CAS  Google Scholar 

  186. Sarkar S, Alam MA, Shaw J, Dasgupta AK. Drug delivery using platelet cancer cell interaction. Pharm Res. 2013;30(11):2785–94. https://doi.org/10.1007/s11095-013-1097-1.

    Article  CAS  Google Scholar 

  187. Pan V, Siva PN, Modery-Pawlowski CL, Singh Sekhon UD, Gupta AS. Targeted killing of metastatic cells using a platelet-inspired drug delivery system. RSC Adv. 2015;5(57):46218–28. https://doi.org/10.1039/C5RA05339K.

    Article  CAS  Google Scholar 

  188. Xu P, Zuo H, Chen B, Wang R, Ahmed A, Hu Y, et al. Doxorubicin-loaded platelets as a smart drug delivery system: an improved therapy for lymphoma. Sci Rep. 2017;7(1):42632. https://doi.org/10.1038/srep42632.

    Article  CAS  Google Scholar 

  189. Wang H, Bremner DH, Wu K, Gong X, Fan Q, **e X, et al. Platelet membrane biomimetic bufalin-loaded hollow MnO2 nanoparticles for MRI-guided chemo-chemodynamic combined therapy of cancer. Chem Eng J. 2020;382: 122848. https://doi.org/10.1016/j.cej.2019.122848.

    Article  CAS  Google Scholar 

  190. Wang C, Sun W, Ye Y, Hu Q, Bomba HN, Gu Z. In situ activation of platelets with checkpoint inhibitors for post-surgical cancer immunotherapy. Nature Biomedical Engineering. 2017;1(2):0011. https://doi.org/10.1038/s41551-016-0011.

    Article  CAS  Google Scholar 

  191. Wu Y-W, Huang C-C, Changou CA, Lu L-S, Goubran H, Burnouf T. Clinical-grade cryopreserved doxorubicin-loaded platelets: role of cancer cells and platelet extracellular vesicles activation loop. J Biomed Sci. 2020;27(1):45. https://doi.org/10.1186/s12929-020-00633-2.

    Article  CAS  Google Scholar 

  192. Kim MW, Lee G, Niidome T, Komohara Y, Lee R, Park YI. Platelet-like gold nanostars for cancer therapy: the ability to treat cancer and evade immune reactions. Front Bioeng Biotechnol. 2020;8:133. https://doi.org/10.3389/fbioe.2020.00133.

    Article  Google Scholar 

  193. Xu L, Su T, Xu X, Zhu L, Shi L. Platelets membrane camouflaged irinotecan-loaded gelatin nanogels for in vivo colorectal carcinoma therapy. Journal of Drug Delivery Science and Technology. 2019;53: 101190. https://doi.org/10.1016/j.jddst.2019.101190.

    Article  CAS  Google Scholar 

  194. Wang H, Wu J, Williams GR, Fan Q, Niu S, Wu J, et al. Platelet-membrane-biomimetic nanoparticles for targeted antitumor drug delivery. J Nanobiotechnology. 2019;17(1):60. https://doi.org/10.1186/s12951-019-0494-y.

    Article  Google Scholar 

  195. Bang KH, Na YG, Huh HW, Hwang SJ, Kim MS, Kim M et al. The delivery strategy of paclitaxel nanostructured lipid carrier coated with platelet membrane. Cancers (Basel). 2019;11(6). https://doi.org/10.3390/cancers11060807.

  196. Ding K, Zheng C, Sun L, Liu X, Yin Y, Wang L. NIR light-induced tumor phototherapy using ICG delivery system based on platelet-membrane-camouflaged hollow bismuth selenide nanoparticles. Chin Chem Lett. 2019. https://doi.org/10.1016/j.cclet.2019.10.040.

    Article  Google Scholar 

  197. Wang H, Wu J, Williams GR, Fan Q, Niu S, Wu J, et al. Platelet-membrane-biomimetic nanoparticles for targeted antitumor drug delivery. Journal of Nanobiotechnology. 2019;17(1):60. https://doi.org/10.1186/s12951-019-0494-y.

    Article  Google Scholar 

  198. Xu P, Zuo H, Zhou R, Wang F, Liu X, Ouyang J, et al. Doxorubicin-loaded platelets conjugated with anti-CD22 mAbs: a novel targeted delivery system for lymphoma treatment with cardiopulmonary avoidance. Oncotarget. 2017;8(35):58322–37. https://doi.org/10.18632/oncotarget.16871.

    Article  Google Scholar 

  199. Hu Q, Sun W, Qian C, Wang C, Bomba HN, Gu Z. Anticancer platelet-mimicking nanovehicles. Adv Mater (Deerfield Beach, Fla.). 2015;27(44):7043–50. https://doi.org/10.1002/adma.201503323.

  200. Díaz A, Saxena V, González J, David A, Casañas B, Carpenter C, et al. Zirconium phosphate nano-platelets: a novel platform for drug delivery in cancer therapy. Chem Commun. 2012;48(12):1754–6. https://doi.org/10.1039/C2CC16218K.

    Article  Google Scholar 

  201. Bu LL, Rao L, Yu GT, Chen L, Deng WW, Liu JF, et al. Cancer stem cell-platelet hybrid membrane-coated magnetic nanoparticles for enhanced photothermal therapy of head and neck squamous cell carcinoma. Adv Func Mater. 2019;29(10):1807733.

    Article  Google Scholar 

  202. Yoon A-R, Hong J, Li Y, Shin HC, Lee H, Kim HS, et al. Mesenchymal stem cell–mediated delivery of an oncolytic adenovirus enhances antitumor efficacy in hepatocellular carcinoma. Can Res. 2019;79(17):4503–14.

    Article  CAS  Google Scholar 

  203. Salehi H, Al-Arag S, Middendorp E, Gergely C, Cuisinier F, Orti V. Dental pulp stem cells used to deliver the anticancer drug paclitaxel. Stem Cell Res Ther. 2018;9(1):1–10.

    Article  Google Scholar 

  204. Takayama Y, Kusamori K, Tsukimori C, Shimizu Y, Hayashi M, Kiyama I, et al. Anticancer drug-loaded mesenchymal stem cells for targeted cancer therapy. J Control Release. 2021;329:1090–101.

    Article  CAS  Google Scholar 

  205. Gao C, Lin Z, Jurado-Sánchez B, Lin X, Wu Z, He Q. Stem cell membrane-coated nanogels for highly efficient in vivo tumor targeted drug delivery. Small. 2016;12(30):4056–62.

    Article  CAS  Google Scholar 

  206. Zhang J, Miao Y, Ni W, **ao H, Zhang J. Cancer cell membrane coated silica nanoparticles loaded with ICG for tumour specific photothermal therapy of osteosarcoma. Artificial cells, nanomedicine, and biotechnology. 2019;47(1):2298–305.

    Article  CAS  Google Scholar 

  207. Lai P-Y, Huang R-Y, Lin S-Y, Lin Y-H, Chang C-W. Biomimetic stem cell membrane-camouflaged iron oxide nanoparticles for theranostic applications. RSC Adv. 2015;5(119):98222–30.

    Article  CAS  Google Scholar 

  208. Mooney R, Weng Y, Tirughana-Sambandan R, Valenzuela V, Aramburo S, Garcia E, et al. Neural stem cells improve intracranial nanoparticle retention and tumor-selective distribution. Future Oncol. 2014;10(3):401–15.

    Article  CAS  Google Scholar 

  209. Li L, Guan Y, Liu H, Hao N, Liu T, Meng X, et al. Silica nanorattle–doxorubicin-anchored mesenchymal stem cells for tumor-tropic therapy. ACS Nano. 2011;5(9):7462–70.

    Article  CAS  Google Scholar 

  210. Liu Y, Zhao J, Jiang J, Chen F, Fang X. Doxorubicin delivered using nanoparticles camouflaged with mesenchymal stem cell membranes to treat colon cancer. Int J Nanomed. 2020;15:2873.

    Article  CAS  Google Scholar 

  211. Feng J, Wang S, Wang Y, Wang L. Stem cell membrane–camouflaged bioinspired nanoparticles for targeted photodynamic therapy of lung cancer. J Nanopart Res. 2020;22(7):1–11.

    Article  Google Scholar 

  212. De Palma M, Mazzieri R, Politi LS, Pucci F, Zonari E, Sitia G, et al. Tumor-targeted interferon-α delivery by Tie2-expressing monocytes inhibits tumor growth and metastasis. Cancer Cell. 2008;14(4):299–311. https://doi.org/10.1016/j.ccr.2008.09.004.

    Article  CAS  Google Scholar 

  213. Lang T, Dong X, Huang Y, Ran W, Yin Q, Zhang P, et al. Ly6Chi Monocytes delivering pH-sensitive micelle loading paclitaxel improve targeting therapy of metastatic breast cancer. Adv Func Mater. 2017;27(26):1701093. https://doi.org/10.1002/adfm.201701093.

    Article  CAS  Google Scholar 

  214. Cao X, Hu Y, Luo S, Wang Y, Gong T, Sun X, et al. Neutrophil-mimicking therapeutic nanoparticles for targeted chemotherapy of pancreatic carcinoma. Acta Pharmaceutica Sinica B. 2019;9(3):575–89. https://doi.org/10.1016/j.apsb.2018.12.009.

    Article  Google Scholar 

  215. Liu L, Chen Q, Ruan C, Chen X, He X, Zhang Y, et al. Nano-engineered lymphocytes for alleviating suppressive tumor immune microenvironment. Appl Mater Today. 2019;16:273–9. https://doi.org/10.1016/j.apmt.2019.06.009.

    Article  Google Scholar 

  216. Luo X, Hu L, Zheng H, Liu M, Liu X, Li C, et al. Neutrophil-mediated delivery of pixantrone-loaded liposomes decorated with poly(sialic acid)–octadecylamine conjugate for lung cancer treatment. Drug Delivery. 2018;25(1):1200–12. https://doi.org/10.1080/10717544.2018.1474973.

    Article  CAS  Google Scholar 

  217. Kang T, Zhu Q, Wei D, Feng J, Yao J, Jiang T, et al. Nanoparticles coated with neutrophil membranes can effectively treat cancer metastasis. ACS Nano. 2017;11(2):1397–411.

    Article  CAS  Google Scholar 

  218. Thomsen T, Ayoub AB, Psaltis D, Klok H-A. Fluorescence-based and fluorescent label-free characterization of polymer nanoparticle decorated T cells. Biomacromolecules. 2020.

  219. Qiu Y, Ren K, Zhao W, Yu Q, Guo R, He J, et al. A “dual-guide” bioinspired drug delivery strategy of a macrophage-based carrier against postoperative triple-negative breast cancer recurrence. J Control Release. 2021;329:191–204.

    Article  CAS  Google Scholar 

  220. Hou T, Wang T, Mu W, Yang R, Liang S, Zhang Z, et al. Nanoparticle-loaded polarized-macrophages for enhanced tumor targeting and cell-chemotherapy. Nano-Micro Letters. 2021;13(1):1–20.

    Article  CAS  Google Scholar 

  221. Xu M, Chen Q, Li J, Peng L, Ding L. Dendritic cell-derived exosome-entrapped fluorouracil can enhance its anti-colon cancer effect. J BUON: official journal of the Balkan Union of Oncology. 2020;25(3):1413-22.

  222. Chowdhury S, Castro S, Coker C, Hinchliffe TE, Arpaia N, Danino T. Programmable bacteria induce durable tumor regression and systemic antitumor immunity. Nat Med. 2019;25(7):1057–63.

    Article  CAS  Google Scholar 

  223. Han J-W, Choi YJ, Cho S, Zheng S, Ko SY, Park J-O, et al. Active tumor-therapeutic liposomal bacteriobot combining a drug (paclitaxel)-encapsulated liposome with targeting bacteria (Salmonella Typhimurium). Sens Actuators B Chem. 2016;224:217–24.

    Article  Google Scholar 

  224. Quispe-Tintaya W, Chandra D, Jahangir A, Harris M, Casadevall A, Dadachova E, et al. Nontoxic radioactive Listeriaat is a highly effective therapy against metastatic pancreatic cancer. Proc Natl Acad Sci. 2013;110(21):8668–73.

    Article  CAS  Google Scholar 

  225. Chen Q, Huang G, Wu W, Wang J, Hu J, Mao J, et al. A hybrid eukaryotic–prokaryotic nanoplatform with photothermal modality for enhanced antitumor vaccination. Adv Mater. 2020;32(16):1908185.

    Article  CAS  Google Scholar 

  226. MacDiarmid JA, Langova V, Bailey D, Pattison ST, Pattison SL, Christensen N, et al. Targeted doxorubicin delivery to brain tumors via minicells: proof of principle using dogs with spontaneously occurring tumors as a model. PLoS ONE. 2016;11(4): e0151832.

    Article  Google Scholar 

  227. Zhang Y, Ji W, He L, Chen Y, Ding X, Sun Y et al. E. coli Nissle 1917-derived minicells for targeted delivery of chemotherapeutic drug to hypoxic regions for cancer therapy. Theranostics. 2018;8(6):1690.

Download references

Acknowledgements

The authors would like to acknowledge Shiraz University of Medical Sciences for financially supporting the research. They would also like to appreciate Ms. A. Keivanshekouh at the Research Consultation Center (RCC) of Shiraz University of Medical Sciences for her invaluable assistance in editing the manuscript.

Funding

This work was funded by Shiraz University of Medical Sciences.

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Nanotechnology, School of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran

    Vahid Alimardani, Zahra Rahiminezhad, Mahvash DehghanKhold, Ghazal Farahavar, Mahboobeh Jafari, Mehdi Abedi, Leila Moradi, Uranous Niroumand & Samira Sadat Abolmaali

  2. Student Research Committee, Shiraz University of Medical Sciences, Shiraz, Iran

    Vahid Alimardani, Zahra Rahiminezhad, Mahvash DehghanKhold, Ghazal Farahavar, Mahboobeh Jafari, Mehdi Abedi, Leila Moradi & Uranous Niroumand

  3. University Centre for Research & Development (UCRD), Chandigarh University, Gharaun, Mohali, 140413, Punjab, India

    Mohammad Ashfaq

  4. Department of Biotechnology, Chandigarh University, Gharaun, Mohali, 140413, Punjab, India

    Mohammad Ashfaq

  5. Department of Pharmaceutics, School of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran

    Gholamhossein Yousefi

  6. Center for Drug Delivery in Nanotechnology, Shiraz University of Medical Sciences, Shiraz, Iran

    Samira Sadat Abolmaali & Gholamhossein Yousefi

Authors
  1. Vahid Alimardani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zahra Rahiminezhad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mahvash DehghanKhold
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ghazal Farahavar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mahboobeh Jafari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mehdi Abedi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Leila Moradi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Uranous Niroumand
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mohammad Ashfaq
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Samira Sadat Abolmaali
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Gholamhossein Yousefi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All the authors significantly contributed to the study, as follows (author-wise): Vahid Alimardani, investigation, conceptualization, writing, and original draft preparation; Zahra Rahiminezhad, Mahvash Dehghan Khold, Ghazal Farahavar, Mahboobeh Jafari, Mehdi Abedi, Leila Moradi, and Uranous Niroumand, writing and original draft preparation; Mohammad Ashfaq, Samirasadat Abolmaali, and Gholamhossein Yousefi, conceptualization and editing.

Corresponding authors

Correspondence to Mohammad Ashfaq, Samira Sadat Abolmaali or Gholamhossein Yousefi.

Ethics declarations

Ethics approval and consent to participate

All authors have read and approved the final manuscript.

Consent for publication

On behalf of the authors, the corresponding author hereby ensures the consent of all authors for submitting the article to Drug Delivery and Translational Research Journal.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alimardani, V., Rahiminezhad, Z., DehghanKhold, M. et al. Nanotechnology-based cell-mediated delivery systems for cancer therapy and diagnosis. Drug Deliv. and Transl. Res. 13, 189–221 (2023). https://doi.org/10.1007/s13346-022-01211-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13346-022-01211-9

Keywords

Search

Navigation