Log in

Acoustic and Magnetic Stimuli-Based Three-Dimensional Cell Culture Platform for Tissue Engineering

  • Review Article
  • Published:
Tissue Engineering and Regenerative Medicine Aims and scope

Abstract

In a conventional two-dimensional (2D) culture method, cells are attached to the bottom of the culture dish and grow into a monolayer. These 2D culture methods are easy to handle, cost-effective, reproducible, and adaptable to growing many different types of cells. However, monolayer 2D cell culture conditions are far from those of natural tissue, indicating the need for a three-dimensional (3D) culture system. Various methods, such as hanging drop, scaffolds, hydrogels, microfluid systems, and bioreactor systems, have been utilized for 3D cell culture. Recently, external physical stimulation-based 3D cell culture platforms, such as acoustic and magnetic forces, were introduced. Acoustic waves can establish acoustic radiation force, which can induce suspended objects to gather in the pressure node region and aggregate to form clusters. Magnetic targeting consists of two components, a magnetically responsive carrier and a magnetic field gradient source. In a magnetic-based 3D cell culture platform, cells are aggregated by changing the magnetic force. Magnetic fields can manipulate cells through two different methods: positive magnetophoresis and negative magnetophoresis. Positive magnetophoresis is a way of imparting magnetic properties to cells by labeling them with magnetic nanoparticles. Negative magnetophoresis is a label-free principle-based method. 3D cell structures, such as spheroids, 3D network structures, and cell sheets, have been successfully fabricated using this acoustic and magnetic stimuli-based 3D cell culture platform. Additionally, fabricated 3D cell structures showed enhanced cell behavior, such as differentiation potential and tissue regeneration. Therefore, physical stimuli-based 3D cell culture platforms could be promising tools for tissue engineering.

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

Access this article

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Costa EC, Moreira AF, de Melo-Diogo D, Gaspar VM, Carvalho MP, Correia IJ. 3D tumor spheroids: an overview on the tools and techniques used for their analysis. Biotechnol Adv. 2016;34:1427–41.

    PubMed  Google Scholar 

  2. Langhans SA. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front Pharmacol. 2018;9:6.

    PubMed  PubMed Central  Google Scholar 

  3. Antoni D, Burckel H, Josset E, Noel G. Three-dimensional cell culture: a breakthrough in vivo. Int J Mol Sci. 2015;16:5517–27.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Breslin S, O’Driscoll L. Three-dimensional cell culture: the missing link in drug discovery. Drug Discov Today. 2013;18:240–9.

    CAS  PubMed  Google Scholar 

  5. Kapałczyńska M, Kolenda T, Przybyła W, Zajączkowska M, Teresiak A, Filas V, et al. 2D and 3D cell cultures - a comparison of different types of cancer cell cultures. Arch Med Sci. 2018;14:910–9.

    PubMed  Google Scholar 

  6. von der Mark K, Gauss V, von der Mark H, Müller P. Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture. Nature. 1977;267:531–2.

    PubMed  Google Scholar 

  7. Petersen OW, Rønnov-Jessen L, Howlett AR, Bissell MJ. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci U S A. 1992;89:9064–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Mahmud G, Campbell C, Bishop KJM, Komarova YA, Chaga O, Soh S, et al. Directing cell motions on micropatterned ratchets. Nature Phys. 2009;5:606–12.

    CAS  Google Scholar 

  9. Kilian KA, Bugarija B, Lahn BT, Mrksich M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A. 2010;107:4872–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer. 2005;5:675–88.

    CAS  PubMed  Google Scholar 

  11. Nelson CM, Bissell MJ. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol. 2006;22:287–309.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Mseka T, Bamburg JR, Cramer LP. ADF/cofilin family proteins control formation of oriented actin-filament bundles in the cell body to trigger fibroblast polarization. J Cell Sci. 2007;120:4332–44.

    CAS  PubMed  Google Scholar 

  13. Weaver VM, Lelièvre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell. 2002;2:205–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Meyers J, Craig J, Odde DJ. Potential for control of signaling pathways via cell size and shape. Curr Biol. 2006;16:1685–93.

    CAS  PubMed  Google Scholar 

  15. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9:239–52.

    CAS  PubMed  Google Scholar 

  16. Trédan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst. 2007;99:1441–54.

    PubMed  Google Scholar 

  17. Hutchinson L, Kirk R. High drug attrition rates–where are we going wrong? Nat Rev Clin Oncol. 2011;8:189–90.

    PubMed  Google Scholar 

  18. Lovitt CJ, Shelper TB, Avery VM. Advanced cell culture techniques for cancer drug discovery. Biology. 2014;3:345–67.

    PubMed  PubMed Central  Google Scholar 

  19. Knight E, Przyborski S. Advances in 3D cell culture technologies enabling tissue-like structures to be created in vitro. J Anat. 2015;227:746–56.

    PubMed  Google Scholar 

  20. Cukierman E, Pankov R, Yamada KM. Cell interactions with three-dimensional matrices. Curr Opin Cell Biol. 2002;14:633–9.

    CAS  PubMed  Google Scholar 

  21. Bokhari M, Carnachan RJ, Cameron NR, Przyborski SA. Culture of HepG2 liver cells on three dimensional polystyrene scaffolds enhances cell structure and function during toxicological challenge. J Anat. 2007;211:567–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Sun T, Jackson S, Haycock JW, MacNeil S. Culture of skin cells in 3D rather than 2D improves their ability to survive exposure to cytotoxic agents. J Biotechnol. 2006;122:372–81.

    CAS  PubMed  Google Scholar 

  23. Ridky TW, Chow JM, Wong DJ, Khavari PA. Invasive three-dimensional organotypic neoplasia from multiple normal human epithelia. Nat Med. 2010;16:1450–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Boghaert ER, Lu X, Hessler PE, McGonigal TP, Oleksijew A, Mitten MJ, et al. The volume of three-dimensional cultures of cancer cells invitro influences transcriptional profile differences and similarities with monolayer cultures and xenografted tumors. Neoplasia. 2017;19:695–706.

    PubMed  PubMed Central  Google Scholar 

  25. Cacciamali A, Villa R, Dotti S. 3D cell cultures: evolution of an ancient tool for new applications. Front Physiol. 2022;13:836480.

    PubMed  PubMed Central  Google Scholar 

  26. Jensen C, Teng Y. Is it time to start transitioning from 2D to 3D cell culture? Front Mol Biosci. 2020;7:33.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Barbosa MAG, Xavier CPR, Pereira RF, Petrikaitė V, Vasconcelos MH. 3D cell culture models as recapitulators of the tumor microenvironment for the screening of anti-cancer drugs. Cancers. 2021;14:190.

    PubMed  PubMed Central  Google Scholar 

  28. Chen MY, Skewes J, Desselle M, Wong C, Woodruff MA, Dasgupta P, et al. Current applications of three-dimensional printing in urology. BJU Int. 2020;125:17–27.

    PubMed  Google Scholar 

  29. Shokoohmand A, Ren J, Baldwin J, Atack A, Shafiee A, Theodoropoulos C, et al. Microenvironment engineering of osteoblastic bone metastases reveals osteomimicry of patient-derived prostate cancer xenografts. Biomaterials. 2019;220:119402.

    CAS  PubMed  Google Scholar 

  30. Pinto B, Henriques AC, Silva PMA, Bousbaa H. Three-dimensional spheroids as in vitro preclinical models for cancer research. Pharmaceutics. 2020;12:1186.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Agrawal G, Ramesh A, Aishwarya P, Sally J, Ravi M. Devices and techniques used to obtain and analyze three-dimensional cell cultures. Biotechnol Prog. 2021;37:e3126.

    CAS  PubMed  Google Scholar 

  32. Meng L, Cai F, Li F, Zhou W, Niu L, Zhen H. Acoustic tweezers. J Phys D Appl Phys. 2019;52:273001.

    CAS  Google Scholar 

  33. Destgeer G, Sung HJ. Recent advances in microfluidic actuation and micro-object manipulation via surface acoustic waves. Lab Chip. 2015;15:2722–38.

    CAS  PubMed  Google Scholar 

  34. Baresch D, Thomas JL, Marchiano R. Observation of a single-beam gradient force acoustical trap for elastic particles: acoustical tweezers. Phys Rev Lett. 2016;116:024301.

    PubMed  Google Scholar 

  35. Ozcelik A, Rufo J, Guo F, Gu Y, Li P, Lata J, et al. Acoustic tweezers for the life sciences. Nat Methods. 2018;15:1021–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Olofsson K, Hammarström B, Wiklund M. Ultrasonic based tissue modelling and engineering. Micromachines (Basel). 2018;9:594.

    PubMed  PubMed Central  Google Scholar 

  37. Friend J, Yeo LY. Microscale acoustofluidics: microfluidics driven via acoustics and ultrasonics. Rev Mod Phys. 2011;83:647–704.

    Google Scholar 

  38. Länge K, Rapp BE, Rapp M. Surface acoustic wave biosensors: a review. Anal Bioanal Chem. 2008;391:1509–19.

    PubMed  Google Scholar 

  39. Lenshof A, Evander M, Laurell T, Nilsson J. Acoustofluidics 5: Building microfluidic acoustic resonators. Lab Chip. 2012;12:684–95.

    CAS  PubMed  Google Scholar 

  40. Luong TD, Nguyen NT. Surface acoustic wave driven microfuidics: a review. Micro Nanosyst. 2010;2:217–25.

    Google Scholar 

  41. Ding X, Li P, Lin SC, Stratton ZS, Nama N, Guo F, et al. Surface acoustic wave microfluidics. Lab Chip. 2013;13:3626–49.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Wu Y, Ao Z, Chen B, Muhsen M, Bondesson M, Lu X, et al. Acoustic assembly of cell spheroids in disposable capillaries. Nanotechnology. 2018;29:504006.

    PubMed  Google Scholar 

  43. Dumy G, Jeger-Madiot N, Benoit-Gonin X, Mallouk TE, Hoyos M, Aider JL. Acoustic manipulation of dense nanorods in microgravity. Microgravity Sci Technol. 2020;32:1159–74.

    CAS  Google Scholar 

  44. Castro LA, Hoyos M. Determination of the secondary bjerknes force in acoustic resonators on ground and in microgravity conditions. Microgravity Sci Technol. 2016;28:11–8.

    Google Scholar 

  45. Silva GT, Lopes JH, Leão-Neto JP, Nichols MK, Drinkwater BW. Particle patterning by ultrasonic standing waves in a rectangular cavity. Phys Rev Applied. 2019;11:054044.

    CAS  Google Scholar 

  46. Laurell T, Petersson F, Nilsson A. Chip integrated strategies for acoustic separation and manipulation of cells and particles. Chem Soc Rev. 2007;36:492–506.

    CAS  PubMed  Google Scholar 

  47. Jeger-Madiot N, Arakelian L, Setterblad N, Bruneval P, Hoyos M, Larghero J, et al. Self-organization and culture of mesenchymal stem cell spheroids in acoustic levitation. Sci Rep. 2021;11:8355.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Fang XZ, Zhou T, Xu JQ, Wang YX, Sun MM, He YJ, et al. Structure, kinetic properties and biological function of mechanosensitive Piezo channels. Cell Biosci. 2021;11:13.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Passini FS, Jaeger PK, Saab AS, Hanlon S, Chittim NA, Arlt MJ, et al. Shear-stress sensing by PIEZO1 regulates tendon stiffness in rodents and influences jum** performance in humans. Nat Biomed Eng. 2021;5:1457–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Pardo-Pastor C, Rubio-Moscardo F, Vogel-González M, Serra SA, Afthinos A, Mrkonjic S, et al. Piezo2 channel regulates RhoA and actin cytoskeleton to promote cell mechanobiological responses. Proc Natl Acad Sci U S A. 2018;115:1925–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Pathak MM, Nourse JL, Tran T, Hwe J, Arulmoli J, Le DT, et al. Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. Proc Natl Acad Sci U S A. 2014;111:16148–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Wei L, Mousawi F, Li D, Roger S, Li J, Yang X, et al. Adenosine triphosphate release and P2 receptor signaling in piezo1 channel-dependent mechanoregulation. Front Pharmacol. 2019;10:1304.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Im GB, Kim YJ, Lee TI, Bhang SH. Subaqueous free-standing 3D cell culture system for ultrafast cell compaction, mechano-inductive immune control, and improving therapeutic angiogenesis. Bioeng Transl Med. 2022;e10438.

  54. Mende N, Kuchen EE, Lesche M, Grinenko T, Kokkaliaris KD, Hanenberg H, et al. CCND1-CDK4-mediated cell cycle progression provides a competitive advantage for human hematopoietic stem cells in vivo. J Exp Med. 2015;212:1171–83.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Strzalka W, Ziemienowicz A. Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Ann Bot. 2011;107:1127–40.

    CAS  PubMed  Google Scholar 

  56. Karar J, Maity A. PI3K/AKT/mTOR pathway in angiogenesis. Front Mol Neurosci. 2011;4:51.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Chen S, Shi J, Zhang M, Chen Y, Wang X, Zhang L, et al. Mesenchymal stem cell-laden anti-inflammatory hydrogel enhances diabetic wound healing. Sci Rep. 2015;5:18104.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Krzyszczyk P, Schloss R, Palmer A, Berthiaume F. The role of macrophages in acute and chronic wound healing and interventions to promote pro-wound healing phenotypes. Front Physiol. 2018;9:419.

    PubMed  PubMed Central  Google Scholar 

  59. Gherardini L, Cousins CM, Hawkes JJ, Spengler J, Radel S, Lawler H, et al. A new immobilisation method to arrange particles in a gel matrix by ultrasound standing waves. Ultrasound Med Biol. 2005;31:261–72.

    PubMed  Google Scholar 

  60. Koo KI, Lenshof A, Huong LT, Laurell T. Acoustic cell patterning in hydrogel for three-dimensional cell network formation. Micromachines (Basel). 2020;12:3.

    PubMed  PubMed Central  Google Scholar 

  61. Comeau ES, Hocking DC, Dalecki D. Ultrasound patterning technologies for studying vascular morphogenesis in 3D. J Cell Sci. 2017;130:232–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Hitchcock T, Niklason L. Lymphatic tissue engineering: progress and prospects. Ann N Y Acad Sci. 2008;1131:44–9.

    PubMed  PubMed Central  Google Scholar 

  63. Radisic M, Yang L, Boublik J, Cohen RJ, Langer R, Freed LE, Vunjak-Novakovic G. Medium perfusion enables engineering of compact and contractile cardiac tissue. Am J Physiol Heart Circ Physiol. 2004;286:H507–16.

    CAS  PubMed  Google Scholar 

  64. Asakawa N, Shimizu T, Tsuda Y, Sekiya S, Sasagawa T, Yamato M, Fukai F, Okano T. Pre-vascularization of in vitro three-dimensional tissues created by cell sheet engineering. Biomaterials. 2010;31:3903–9.

    CAS  PubMed  Google Scholar 

  65. Laschke MW, Vollmar B, Menger MD. Inosculation: connecting the life-sustaining pipelines. Tissue Eng Part B Rev. 2009;15:455–65.

    PubMed  Google Scholar 

  66. Armstrong JPK, Puetzer JL, Serio A, Guex AG, Kapnisi M, Breant A, et al. Engineering anisotropic muscle tissue using acoustic cell patterning. Adv Mater. 2018;30:e1802649.

    PubMed  Google Scholar 

  67. Garvin KA, Dalecki D, Hocking DC. Vascularization of three-dimensional collagen hydrogels using ultrasound standing wave fields. Ultrasound Med Biol. 2011;37:1853–64.

    PubMed  PubMed Central  Google Scholar 

  68. Garvin KA, Hocking DC, Dalecki D. Controlling the spatial organization of cells and extracellular matrix proteins in engineered tissues using ultrasound standing wave fields. Ultrasound Med Biol. 2010;36:1919–32.

    PubMed  PubMed Central  Google Scholar 

  69. Garvin KA, Dalecki D, Yousefhussien M, Helguera M, Hocking DC. Spatial patterning of endothelial cells and vascular network formation using ultrasound standing wave fields. J Acoust Soc Am. 2013;134:1483–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Hu X, Zheng J, Hu Q, Liang L, Yang D, Cheng Y, et al. Smart acoustic 3D cell construct assembly with high-resolution. Biofabrication. 2022;14:045003.

    Google Scholar 

  71. Sensenig R, Sapir Y, MacDonald C, Cohen S, Polyak B. Magnetic nanoparticle-based approaches to locally target therapy and enhance tissue regeneration in vivo. Nanomedicine (Lond). 2012;7:1425–42.

    CAS  PubMed  Google Scholar 

  72. Wang A, Madden LA, Paunov VN. Advanced biomedical applications based on emerging 3D cell culturing platforms. J Mater Chem B. 2020;8:10487–501.

    CAS  PubMed  Google Scholar 

  73. Yaman S, Anil-Inevi M, Ozcivici E, Tekin HC. Magnetic force-based microfluidic techniques for cellular and tissue bioengineering. Front Bioeng Biotechnol. 2018;6:192.

    PubMed  PubMed Central  Google Scholar 

  74. Frasca G, Gazeau F, Wilhelm C. Formation of a three-dimensional multicellular assembly using magnetic patterning. Langmuir. 2009;25:2348–54.

    CAS  PubMed  Google Scholar 

  75. Souza GR, Molina JR, Raphael RM, Ozawa MG, Stark DJ, Levin CS, et al. Three-dimensional tissue culture based on magnetic cell levitation. Nat Nanotechnol. 2010;5:291–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Tomitaka A, Koshi T, Hatsugai S, Yamada T, Takemura Y. Magnetic characterization of surface-coated magnetic nanoparticles for biomedical application. J Magn Magn Mater. 2011;323:1398–403.

    CAS  Google Scholar 

  77. Mattix B, Olsen TR, Gu Y, Casco M, Herbst A, Simionescu DT, et al. Biological magnetic cellular spheroids as building blocks for tissue engineering. Acta Biomater. 2014;10:623–9.

    CAS  PubMed  Google Scholar 

  78. Xue L, Deng D, Sun J. Magnetoferritin: process, prospects, and their biomedical applications. Int J Mol Sci. 2019;20:2426.

    PubMed  PubMed Central  Google Scholar 

  79. Correia Carreira S, Armstrong JP, Seddon AM, Perriman AW, Hartley-Davies R, Schwarzacher W. Ultra-fast stem cell labelling using cationised magnetoferritin. Nanoscale. 2016;8:7474–83.

    CAS  PubMed  Google Scholar 

  80. Charlton JR, Pearl VM, Denotti AR, Lee JB, Swaminathan S, Scindia YM, et al. Biocompatibility of ferritin-based nanoparticles as targeted MRI contrast agents. Nanomedicine. 2016;12:1735–45.

    CAS  PubMed  Google Scholar 

  81. Dzamukova M, Naumenko E, Rozhina EV, Trifonov AA, Fakhrullin RF. Cell surface engineering with polyelectrolyte-stabilized magnetic nanoparticles: a facile approach for fabrication of artificial multicellular tissue-mimicking clusters. Nano Res. 2015;8:2515–32.

    CAS  Google Scholar 

  82. Sarigil O, Anil-Inevi M, Firatligil-Yildirir B, Unal YC, Yalcin-Ozuysal O, Mese G, et al. Scaffold-free biofabrication of adipocyte structures with magnetic levitation. Biotechnol Bioeng. 2021;118:1127–40.

    CAS  PubMed  Google Scholar 

  83. Parfenov VA, Koudan EV, Bulanova EA, Karalkin PA, Das Pereira F, Norkin NE, et al. Scaffold-free, label-free and nozzle-free biofabrication technology using magnetic levitational assembly. Biofabrication. 2018;10:034104.

    PubMed  Google Scholar 

  84. Ito A, Takizawa Y, Honda H, Hata K, Kagami H, Ueda M, et al. Tissue engineering using magnetite nanoparticles and magnetic force: heterotypic layers of cocultured hepatocytes and endothelial cells. Tissue Eng. 2004;10:833–40.

    CAS  PubMed  Google Scholar 

  85. Ishii M, Shibata R, Shimizu Y, Yamamoto T, Kondo K, Inoue Y, et al. Multilayered adipose-derived regenerative cell sheets created by a novel magnetite tissue engineering method for myocardial infarction. Int J Cardiol. 2014;175:545–53.

    PubMed  Google Scholar 

  86. Peyman SA, Kwan EY, Margarson O, Iles A, Pamme N. Diamagnetic repulsion–a versatile tool for label-free particle handling in microfluidic devices. J Chromatogr A. 2009;1216:9055–62.

    CAS  PubMed  Google Scholar 

  87. Zhu T, Marrero F, Mao L. Continuous separation of non-magnetic particles inside ferrofluids. Microfluid Nanofluid. 2010;9:1003–9.

    Google Scholar 

  88. Subramaniam AB, Yang D, Yu HD, Nemiroski A, Tricard S, Ellerbee AK, et al. Noncontact orientation of objects in three-dimensional space using magnetic levitation. Proc Natl Acad Sci U S A. 2014;111:12980–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Mirica KA, Shevkoplyas SS, Phillips ST, Gupta M, Whitesides GM. Measuring densities of solids and liquids using magnetic levitation: fundamentals. J Am Chem Soc. 2009;131:10049–58.

    CAS  PubMed  Google Scholar 

  90. Mirica KA, Phillips ST, Mace CR, Whitesides GM. Magnetic levitation in the analysis of foods and water. J Agric Food Chem. 2010;58:6565–9.

    CAS  PubMed  Google Scholar 

  91. Guevorkian K, Valles JM Jr. Swimming Paramecium in magnetically simulated enhanced, reduced, and inverted gravity environments. Proc Natl Acad Sci U S A. 2006;103:13051–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Gao QH, Zhang WM, Zou HX, Li WB, Yan H, Peng ZK, et al. Label-free manipulation via the magneto-Archimedes effect: fundamentals, methodology and applications. Mater Horiz. 2019;6:1359–79.

    CAS  Google Scholar 

  93. Socoliuc V, Avdeev MV, Kuncser V, Turcu R, Tombácz E, Vékás L. Ferrofluids and bio-ferrofluids: looking back and step** forward. Nanoscale. 2022;14:4786–886.

    CAS  PubMed  Google Scholar 

  94. Shen F, Hwang H, Hahn YK, Park JK. Label-free cell separation using a tunable magnetophoretic repulsion force. Anal Chem. 2012;84:3075–81.

    CAS  PubMed  Google Scholar 

  95. Nguyen NT. Micro-magnetofluidics: interactions between magnetism and fluid flow on the microscale. Microfluid Nanofluid. 2012;12:440.

    Google Scholar 

  96. Sekine W, Haraguchi Y, Shimizu T, Umezawa A, Okano T. Thickness limitation and cell viability of multi-layered cell sheets and overcoming the diffusion limit by a porous-membrane culture insert. J Biochips Tissue Chips. 2011;s1:007.

    Google Scholar 

  97. Ito A, Jitsunobu H, Kawabe Y, Kamihira M. Construction of heterotypic cell sheets by magnetic force-based 3-D coculture of HepG2 and NIH3T3 cells. J Biosci Bioeng. 2007;104:371–8.

    CAS  PubMed  Google Scholar 

  98. Rouwkema J, Khademhosseini A. Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 2016;34:733–45.

    CAS  PubMed  Google Scholar 

  99. Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng. 2012;40:363–408.

    PubMed  PubMed Central  Google Scholar 

  100. Silva AS, Santos LF, Mendes MC, Mano JF. Multi-layer pre-vascularized magnetic cell sheets for bone regeneration. Biomaterials. 2020;231:119664.

    CAS  PubMed  Google Scholar 

  101. Lopes D, Martins-Cruz C, Oliveira MB, Mano JF. Bone physiology as inspiration for tissue regenerative therapies. Biomaterials. 2018;185:240–75.

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Correia CR, Pirraco RP, Cerqueira MT, Marques AP, Reis RL, Mano JF. Semipermeable capsules wrap** a multifunctional and self-regulated co-culture microenvironment for osteogenic differentiation. Sci Rep. 2016;6:21883.

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Moschouris K, Firoozi N, Kang Y. The application of cell sheet engineering in the vascularization of tissue regeneration. Regen Med. 2016;11:559–70.

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Koto W, Shinohara Y, Kitamura K, Wachi T, Makihira S, Koyano K. Porcine dental epithelial cells differentiated in a cell sheet constructed by magnetic nanotechnology. Nanomaterials (Basel). 2017;7:322.

    PubMed  PubMed Central  Google Scholar 

  105. Thesleff I. Epithelial-mesenchymal signalling regulating tooth morphogenesis. J Cell Sci. 2003;116:1647–8.

    CAS  PubMed  Google Scholar 

  106. Young CS, Terada S, Vacanti JP, Honda M, Bartlett JD, Yelick PC. Tissue engineering of complex tooth structures on biodegradable polymer scaffolds. J Dent Res. 2002;81:695–700.

    CAS  PubMed  Google Scholar 

  107. Puthiyaveetil JS, Kota K, Chakkarayan R, Chakkarayan J, Thodiyil AK. Epithelial-mesenchymal interactions in tooth development and the significant role of growth factors and genes with emphasis on mesenchyme-a review. J Clin Diagn Res. 2016;10:ZE05–9.

    PubMed  PubMed Central  Google Scholar 

  108. Uskoković V. Amelogenin in enamel tissue engineering. Adv Exp Med Biol. 2015;881:237–54.

    PubMed  PubMed Central  Google Scholar 

  109. Nanci A, Zalzal S, Lavoie P, Kunikata M, Chen W, Krebsbach PH, et al. Comparative immunochemical analyses of the developmental expression and distribution of ameloblastin and amelogenin in rat incisors. J Histochem Cytochem. 1998;46:911–34.

    CAS  PubMed  Google Scholar 

  110. Ravindranath HH, Chen LS, Zeichner-David M, Ishima R, Ravindranath RM. Interaction between the enamel matrix proteins amelogenin and ameloblastin. Biochem Biophys Res Commun. 2004;323:1075–83.

    CAS  PubMed  Google Scholar 

  111. Fukumoto S, Kiba T, Hall B, Iehara N, Nakamura T, Longenecker G, et al. Ameloblastin is a cell adhesion molecule required for maintaining the differentiation state of ameloblasts. J Cell Biol. 2004;167:973–83.

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Hatakeyama J, Fukumoto S, Nakamura T, Haruyama N, Suzuki S, Hatakeyama Y, et al. Synergistic roles of amelogenin and ameloblastin. J Dent Res. 2009;88:318–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Deutsch D, Palmon A, Fisher LW, Kolodny N, Termine JD, Young MF. Sequencing of bovine enamelin (“tuftelin”) a novel acidic enamel protein. J Biol Chem. 1991;266:16021–8.

    CAS  PubMed  Google Scholar 

  114. Hsiao AY, Torisawa YS, Tung YC, Sud S, Taichman RS, Pienta KJ, et al. Microfluidic system for formation of PC-3 prostate cancer co-culture spheroids. Biomaterials. 2009;30:3020–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Chan HF, Zhang Y, Ho YP, Chiu YL, Jung Y, Leong KW. Rapid formation of multicellular spheroids in double-emulsion droplets with controllable microenvironment. Sci Rep. 2013;3:3462.

    PubMed  PubMed Central  Google Scholar 

  116. Vadivelu RK, Kamble H, Shiddiky MJA, Nguyen NT. Microfluidic technology for the generation of cell spheroids and their applications. Micromachines (Basel). 2017;8:94.

    PubMed Central  Google Scholar 

  117. Zhao Z, Gu J, Zhao Y, Guan Y, Zhu XX, Zhang Y. Hydrogel thin film with swelling-induced wrinkling patterns for high-throughput generation of multicellular spheroids. Biomacromol. 2014;15:3306–12.

    CAS  Google Scholar 

  118. Cheng NC, Wang S, Young TH. The influence of spheroid formation of human adipose-derived stem cells on chitosan films on stemness and differentiation capabilities. Biomaterials. 2012;33:1748–58.

    CAS  PubMed  Google Scholar 

  119. Dzamukova MR, Naumenko EA, Lannik NI, Fakhrullin RF. Surface-modified magnetic human cells for scaffold-free tissue engineering. Biomater Sci. 2013;1:810–3.

    CAS  PubMed  Google Scholar 

  120. Lin RZ, Chu WC, Chiang CC, Lai CH, Chang HY. Magnetic reconstruction of three-dimensional tissues from multicellular spheroids. Tissue Eng Part C Methods. 2008;14:197–205.

    CAS  PubMed  Google Scholar 

  121. Olsen TR, Mattix B, Casco M, Herbst A, Williams C, Tarasidis A, et al. Manipulation of cellular spheroid composition and the effects on vascular tissue fusion. Acta Biomater. 2015;13:188–98.

    CAS  PubMed  Google Scholar 

  122. Nath S, Devi GR. Three-dimensional culture systems in cancer research: focus on tumor spheroid model. Pharmacol Ther. 2016;163:94–108.

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Ong CS, Zhou X, Han J, Huang CY, Nashed A, Khatri S, et al. In vivo therapeutic applications of cell spheroids. Biotechnol Adv. 2018;36:494–505.

    CAS  PubMed  Google Scholar 

  124. Ivascu A, Kubbies M. Rapid generation of single-tumor spheroids for high-throughput cell function and toxicity analysis. J Biomol Screen. 2006;11:922–32.

    CAS  PubMed  Google Scholar 

  125. Bratt-Leal AM, Kepple KL, Carpenedo RL, Cooke MT, McDevitt TC. Magnetic manipulation and spatial patterning of multi-cellular stem cell aggregates. Integr Biol. 2011;3:1224–32.

    CAS  Google Scholar 

  126. Jafari J, Han XL, Palmer J, Tran PA, O’Connor AJ. Remote control in formation of 3D multicellular assemblies using magnetic forces. ACS Biomater Sci Eng. 2019;5:2532–42.

    CAS  PubMed  Google Scholar 

  127. Lewis NS, Lewis EE, Mullin M, Wheadon H, Dalby MJ, Berry CC. Magnetically levitated mesenchymal stem cell spheroids cultured with a collagen gel maintain phenotype and quiescence. J Tissue Eng. 2017;8:2041731417704428.

    PubMed  PubMed Central  Google Scholar 

  128. Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 2006;7:14.

    PubMed  PubMed Central  Google Scholar 

  129. Banfi A, Muraglia A, Dozin B, Mastrogiacomo M, Cancedda R, Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: Implications for their use in cell therapy. Exp Hematol. 2000;28:707–15.

    CAS  PubMed  Google Scholar 

  130. Lin SP, Chiu FY, Wang Y, Yen ML, Kao SY, Hung SC. RB maintains quiescence and prevents premature senescence through upregulation of DNMT1 in mesenchymal stromal cells. Stem Cell Rep. 2014;3:975–86.

    CAS  Google Scholar 

  131. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677–89.

    CAS  PubMed  Google Scholar 

  132. Nilsson SK, Debatis ME, Dooner MS, Madri JA, Quesenberry PJ, Becker PS. Immunofluorescence characterization of key extracellular matrix proteins in murine bone marrow in situ. J Histochem Cytochem. 1998;46:371–7.

    CAS  PubMed  Google Scholar 

  133. Kolf CM, Cho E, Tuan RS. Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res Ther. 2007;9:204.

    PubMed  PubMed Central  Google Scholar 

  134. Méndez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466:829–34.

    PubMed  PubMed Central  Google Scholar 

  135. Tzeng YS, Li H, Kang YL, Chen WC, Cheng WC, Lai DM. Loss of Cxcl12/Sdf-1 in adult mice decreases the quiescent state of hematopoietic stem/progenitor cells and alters the pattern of hematopoietic regeneration after myelosuppression. Blood. 2011;117:429–39.

    CAS  PubMed  Google Scholar 

  136. Anil-Inevi M, Yaman S, Yildiz AA, Mese G, Yalcin-Ozuysal O, Tekin HC, et al. Biofabrication of in situ self assembled 3D cell cultures in a weightlessness environment generated using magnetic levitation. Sci Rep. 2018;8:7239.

    PubMed  PubMed Central  Google Scholar 

  137. Haisler WL, Timm DM, Gage JA, Tseng H, Killian TC, Souza GR. Three-dimensional cell culturing by magnetic levitation. Nat Protoc. 2013;8:1940–9.

    CAS  PubMed  Google Scholar 

  138. Tasoglu S, Khoory JA, Tekin HC, Thomas C, Karnoub AE, Ghiran IC, et al. Levitational image cytometry with temporal resolution. Adv Mater. 2015;27:3901–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Durmus NG, Tekin HC, Guven S, Sridhar K, Arslan Yildiz A, Calibasi G, et al. Magnetic levitation of single cells. Proc Natl Acad Sci U S A. 2015;112:E3661–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Greco G, Agostini M, Tonazzini I, Sallemi D, Barone S, Cecchini M. Surface-acoustic-wave (SAW)-driven device for dynamic cell cultures. Anal Chem. 2018;90:7450–7.

    CAS  PubMed  Google Scholar 

  141. Ha BH, Lee KS, Destgeer G, Park J, Choung JS, Jung JH, et al. Acoustothermal heating of polydimethylsiloxane microfluidic system. Sci Rep. 2015;5:11851.

    PubMed  PubMed Central  Google Scholar 

  142. Shilton RJ, Mattoli V, Travagliati M, Agostini M, Desii A, Beltram F, et al. Rapid and controllable digital microfluidic heating by surface acoustic waves. Adv Funct Mater. 2015;25:5895–901.

    CAS  Google Scholar 

  143. Park J, Jung JH, Destgeer G, Ahmed H, Park K, Sung HJ. Acoustothermal tweezer for droplet sorting in a disposable microfluidic chip. Lab Chip. 2017;17:1031–40.

    CAS  PubMed  Google Scholar 

  144. Park J, Ha BH, Destgeer G, Jung JH, Sung HJ. Spatiotemporally controllable acoustothermal heating and its application to disposable thermochromic displays. RSC Adv. 2016;6:33937–44.

    CAS  Google Scholar 

  145. Ha BH, Park J, Destgeer G, Jung JH, Sung HJ. Generation of dynamic free-form temperature gradients in a disposable microchip. Anal Chem. 2015;87:11568–74.

    CAS  PubMed  Google Scholar 

  146. Thevenard L, Camara IS, Prieur J-Y, Rovillain P, Lemaître A, Gourdon C, et al. Strong reduction of the coercivity by a surface acoustic wave in an out-of-plane magnetized epilayer. Phys Rev B. 2016;93:140405.

    Google Scholar 

  147. Wiklund M. Acoustofluidics 12: biocompatibility and cell viability in microfluidic acoustic resonators. Lab Chip. 2012;12:2018–28.

    CAS  PubMed  Google Scholar 

  148. Lam KH, Li Y, Li Y, Lim HG, Zhou Q, Shung KK. Multifunctional single beam acoustic tweezer for non-invasive cell/organism manipulation and tissue imaging. Sci Rep. 2016;6:37554.

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Pan Y, Du X, Zhao F, Xu B. Magnetic nanoparticles for the manipulation of proteins and cells. Chem Soc Rev. 2012;41:2912–42.

    CAS  PubMed  Google Scholar 

  150. Ashkarran AA, Mahmoudi M. Magnetic levitation systems for disease diagnostics. Trends Biotechnol. 2021;39:311–21.

    CAS  PubMed  Google Scholar 

  151. Munaz A, Shiddiky MJA, Nguyen NT. Recent advances and current challenges in magnetophoresis based micro magnetofluidics. Biomicrofluidics. 2018;12:031501.

    PubMed  PubMed Central  Google Scholar 

  152. Rufo J, Zhang P, Zhong R, Lee LP, Huang TJ. A sound approach to advancing healthcare systems: the future of biomedical acoustics. Nat Commun. 2022;13:3459.

    CAS  PubMed  PubMed Central  Google Scholar 

  153. Ma Z, Holle AW, Melde K, Qiu T, Poeppel K, Kadiri VM, et al. Acoustic holographic cell patterning in a biocompatible hydrogel. Adv Mater. 2020;32:e1904181.

    PubMed  Google Scholar 

  154. Gu Y, Chen C, Rufo J, Shen C, Wang Z, Huang PH, et al. Acoustofluidic holography for micro- to nanoscale particle manipulation. ACS Nano. 2020;14:14635–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Baudoin M, Thomas JL, Sahely RA, Gerbedoen JC, Gong Z, Sivery A, et al. Spatially selective manipulation of cells with single-beam acoustical tweezers. Nat Commun. 2020;11:4244.

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Betsch M, Cristian C, Lin YY, Blaeser A, Schöneberg J, Vogt M, et al. Incorporating 4D into bioprinting: real-time magnetically directed collagen fiber alignment for generating complex multilayered tissues. Adv Healthc Mater. 2018;7:e1800894.

    PubMed  Google Scholar 

  157. Etoc F, Lisse D, Bellaiche Y, Piehler J, Coppey M, Dahan M. Subcellular control of Rac-GTPase signalling by magnetogenetic manipulation inside living cells. Nat Nanotechnol. 2013;8:193–8.

    CAS  PubMed  Google Scholar 

  158. Stanley SA, Sauer J, Kane RS, Dordick JS, Friedman JM. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat Med. 2015;21:92–8.

    CAS  PubMed  Google Scholar 

  159. Liße D, Monzel C, Vicario C, Manzi J, Maurin I, Coppey M, et al. Engineered ferritin for magnetogenetic manipulation of proteins and organelles inside living cells. Adv Mater. 2017;29:1700189.

  160. Armstrong JPK, Stevens MM. Using remote fields for complex tissue engineering. Trends Biotechnol. 2020;38:254–63.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by 2022 Research Grant from Kangwon National University (202202400001) (T.-J. L.) and National Research Foundation of Korea (NRF) grant funded by the Korea government(MSIT) (No. NRF-2022R1C1C2011617) (H.-K. J.)

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tae-** Lee.

Ethics declarations

Conflicts of interest

The authors have no conflicts of interest relevant to this study to disclose.

Ethical statement

No animal experiments were carried out for this article.

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 (e.g. a society or other partner) 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

Seo, J.Y., Park, S.B., Kim, S.Y. et al. Acoustic and Magnetic Stimuli-Based Three-Dimensional Cell Culture Platform for Tissue Engineering. Tissue Eng Regen Med 20, 563–580 (2023). https://doi.org/10.1007/s13770-023-00539-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13770-023-00539-8

Keywords

Navigation