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Screening of candidate genes associated with high titer production of oncolytic measles virus based on systems biology approach

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Abstract

The number of viral particles required for oncolytic activity of measles virus (MV) can be more than a million times greater than the reported amount for vaccination. The aim of the current study is to find potential genes and signaling pathways that may be involved in the high-titer production of MV. In this study, a systems biology approach was considered including collection of gene expression profiles from the Gene Expression Omnibus (GEO) database, obtaining differentially expressed genes (DEGs), performing gene ontology, functional enrichment analyses, and topological analyses on the protein–protein interaction (PPI) network. Then, to validate the in-silico data, total RNA was isolated from five cell lines, and full-length cDNA from template RNA was synthesized. Subsequently, quantitative reverse transcription-PCR (RT-qPCR) was employed. We identified five hub genes, including RAC1, HSP90AA1, DNM1, LTBP1, and FSTL1 associated with the enhancement in MV titer. Pathway analysis indicated enrichment in PI3K-Akt signaling pathway, axon guidance, proteoglycans in cancer, regulation of actin cytoskeleton, focal adhesion, and calcium signaling pathways. Upon verification by RT-qPCR, the relative expression of candidate genes was generally consistent with our bioinformatics analysis. Hub genes and signaling pathways may be involved in understanding the pathological mechanisms by which measles virus manipulates host factors in order to facilitate its replication. RAC1, HSP90AA1, DNM1, LTBP1, and FSTL1 genes, in combination with genetic engineering techniques, will allow the direct design of high-throughput cell lines to answer the required amounts for the oncolytic activity of MV.

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References

  1. Leber MF et al (2020) Engineering and combining oncolytic measles virus for cancer therapy. Cytokine Growth Factor Rev 56:39–48. https://doi.org/10.1016/j.cytogfr.2020.07.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Plattet P, Alves L, Herren M, Aguilar HC (2016) Measles Virus Fusion Protein: Structure, Function and Inhibition. Viruses 8(4):112. https://doi.org/10.3390/v8040112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lin L-T, Richardson CD (2016) The host cell receptors for measles virus and their interaction with the viral hemagglutinin (H) protein. Viruses. https://doi.org/10.3390/v8090250

    Article  PubMed  PubMed Central  Google Scholar 

  4. Tatsuo H, Ono N, Tanaka K, Yanagi Y (2000) SLAM (CDw150) is a cellular receptor for measles virus. Nature 406(6798):893–897. https://doi.org/10.1038/35022579

    Article  CAS  PubMed  Google Scholar 

  5. Mühlebach MD et al (2011) Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 480(7378):530–533. https://doi.org/10.1038/nature10639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Tahara M, Takeda M, Seki F, Hashiguchi T, Yanagi Y (2007) Multiple amino acid substitutions in hemagglutinin are necessary for wild-type measles virus to acquire the ability to use receptor CD46 efficiently. J Virol 81(6):2564–2572. https://doi.org/10.1128/JVI.02449-06

    Article  CAS  PubMed  Google Scholar 

  7. Navaratnarajah CK et al (2011) The heads of the measles virus attachment protein move to transmit the fusion-triggering signal. Nat Struct Mol Biol 18(2):128–134. https://doi.org/10.1038/nsmb.1967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Engeland CE, Ungerechts G (2021) Measles virus as an oncolytic immunotherapy. Cancers. https://doi.org/10.3390/cancers13030544

    Article  PubMed  PubMed Central  Google Scholar 

  9. Jiang Y, Qin Y, Chen M (2016) Host–pathogen interactions in measles virus replication and anti-viral immunity. Viruses. https://doi.org/10.3390/v8110308

    Article  PubMed  PubMed Central  Google Scholar 

  10. Weiss K, Salzig D, Mühlebach MD, Cichutek K, Pörtner R, Czermak P (2012) Key parameters of measles virus production for oncolytic virotherapy. Am J Biochem Biotechnol 8(2):81–98. https://doi.org/10.3844/ajbbsp.2012.81.98

    Article  CAS  Google Scholar 

  11. Anderson BD, Nakamura T, Russell SJ, Peng K-W (2004) High CD46 receptor density determines preferential killing of tumor cells by oncolytic measles virus. Cancer Res 64(14):4919–4926. https://doi.org/10.1158/0008-5472.CAN-04-0884

    Article  CAS  PubMed  Google Scholar 

  12. Pasquinucci G (1971) Possible effect of measles on leukaemia. Lancet. https://doi.org/10.1016/s0140-6736(71)90869-5

    Article  PubMed  Google Scholar 

  13. Bluming AZ, Ziegler JL (1971) Regression of Burkitt’s lymphoma in association with measles infection. Lancet 2(7715):105–106. https://doi.org/10.1016/s0140-6736(71)92086-1

    Article  CAS  PubMed  Google Scholar 

  14. Zygiert Z (1971) Hodgkin’s disease: remissions after measles. Lancet 1(7699):593. https://doi.org/10.1016/s0140-6736(71)91186-x

    Article  CAS  PubMed  Google Scholar 

  15. Peng K-W, TenEyck CJ, Galanis E, Kalli KR, Hartmann LC, Russell SJ (2002) Intraperitoneal therapy of ovarian cancer using an engineered measles virus. Cancer Res 62(16):4656–4662

    CAS  PubMed  Google Scholar 

  16. Phuong LK et al (2003) Use of a vaccine strain of measles virus genetically engineered to produce carcinoembryonic antigen as a novel therapeutic agent against glioblastoma multiforme. Cancer Res 63(10):2462–2469

    CAS  PubMed  Google Scholar 

  17. Peng KW, Ahmann GJ, Pham L, Greipp PR, Cattaneo R, Russell SJ (2001) Systemic therapy of myeloma xenografts by an attenuated measles virus. Blood 98(7):2002–2007. https://doi.org/10.1182/blood.v98.7.2002

    Article  CAS  PubMed  Google Scholar 

  18. Msaouel P et al (2018) Clinical trials with oncolytic measles virus: current status and future prospects. Curr Cancer Drug Targets 18(2):177–187. https://doi.org/10.2174/1568009617666170222125035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Msaouel P, Iankov ID, Dispenzieri A, Galanis E (2012) Attenuated oncolytic measles virus strains as cancer therapeutics. Curr Pharm Biotechnol 13(9):1732–1741. https://doi.org/10.2174/138920112800958896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Russell SJ et al (2014) Remission of disseminated cancer after systemic oncolytic virotherapy. Mayo Clin Proc 89(7):926–933. https://doi.org/10.1016/j.mayocp.2014.04.003

    Article  PubMed  Google Scholar 

  21. Bouvy-Liivrand M et al (2017) Analysis of primary microRNA loci from nascent transcriptomes reveals regulatory domains governed by chromatin architecture. Nucleic Acids Res 45(17):9837–9849. https://doi.org/10.1093/nar/gkx680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Grein TA et al (2017) Screening different host cell lines for the dynamic production of measles virus. Biotechnol Prog 33(4):989–997

    Article  CAS  Google Scholar 

  23. Bedard KM et al (2012) Isoflavone agonists of IRF-3 dependent signaling have antiviral activity against RNA viruses. J Virol 86(13):7334–7344. https://doi.org/10.1128/jvi.06867-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Achard C et al (2015) Sensitivity of human pleural mesothelioma to oncolytic measles virus depends on defects of the type I interferon response. Oncotarget 6(42):44892–44904. https://doi.org/10.18632/oncotarget.6285

    Article  PubMed  PubMed Central  Google Scholar 

  25. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11(9):1650–1667. https://doi.org/10.1038/nprot.2016.095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chin C-H, Chen S-H, Wu H-H, Ho C-W, Ko M-T, Lin C-Y (2014) cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol 8(4):S11. https://doi.org/10.1186/1752-0509-8-S4-S11

    Article  PubMed  PubMed Central  Google Scholar 

  27. Sayyad WA, Fabris P, Torre V (2016) The role of Rac1 in the growth cone dynamics and force generation of DRG neurons. PLoS ONE 11(1):e0146842. https://doi.org/10.1371/journal.pone.0146842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Leyden F et al (2021) Rac1 activation can generate untemplated, lamellar membrane ruffles. BMC Biol 19(1):72. https://doi.org/10.1186/s12915-021-00997-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Steffen A et al (2013) Rac function is critical for cell migration but not required for spreading and focal adhesion formation. J Cell Sci. https://doi.org/10.1242/jcs.118232

    Article  PubMed  PubMed Central  Google Scholar 

  30. Gonçalves-Carneiro D, McKeating JA, Bailey D, Perlman S (2017) The measles virus receptor SLAMF1 can mediate particle endocytosis. J Virol 91(7):e02255-e2316. https://doi.org/10.1128/JVI.02255-16

    Article  PubMed  PubMed Central  Google Scholar 

  31. Takano A et al (2009) Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer. Cancer Res 69(16):6694–6703. https://doi.org/10.1158/0008-5472.CAN-09-0016

    Article  CAS  PubMed  Google Scholar 

  32. Zamudio-Meza H, Castillo-Alvarez A, González-Bonilla C, Meza I (2009) Cross-talk between Rac1 and Cdc42 GTPases regulates formation of filopodia required for dengue virus type-2 entry into HMEC-1 cells. J Gen Virol 90(Pt 12):2902–2911. https://doi.org/10.1099/vir.0.014159-0

    Article  CAS  PubMed  Google Scholar 

  33. Wan Q, Song D, Li H, He M (2020) Stress proteins: the biological functions in virus infection, present and challenges for target-based antiviral drug development. Signal Transduct Target Ther 5(1):125. https://doi.org/10.1038/s41392-020-00233-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Zúñiga S, Sola I, Cruz JLG, Enjuanes L (2009) Role of RNA chaperones in virus replication. Virus Res 139(2):253–266. https://doi.org/10.1016/j.virusres.2008.06.015

    Article  CAS  PubMed  Google Scholar 

  35. Geller R, Andino R, Frydman J (2013) Hsp90 inhibitors exhibit resistance-free antiviral activity against respiratory syncytial virus. PLoS ONE 8(2):e56762. https://doi.org/10.1371/journal.pone.0056762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Gatti P, Ilamathi HS, Todkar K, Germain M (2020) Mitochondria targeted viral replication and survival strategies—prospective on SARS-CoV-2. Front Pharmacol 11:1364. https://doi.org/10.3389/fphar.2020.578599

    Article  CAS  Google Scholar 

  37. Francy CA, Alvarez FJD, Zhou L, Ramachandran R, Mears JA (2015) The mechanoenzymatic core of dynamin-related protein 1 comprises the minimal machinery required for membrane constriction. J Biol Chem 290(18):11692–11703. https://doi.org/10.1074/jbc.M114.610881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kolnikova M et al (2018) DNM1 encephalopathy—atypical phenotype with hypomyelination due to a novel de novo variant in the DNM1 gene. Seizure 56:31–33. https://doi.org/10.1016/j.seizure.2018.01.020

    Article  PubMed  Google Scholar 

  39. Robertson IB, Horiguchi M, Zilberberg L, Dabovic B, Hadjiolova K, Rifkin DB (2015) Latent TGF-β-binding proteins. Matrix Biol 47:44–53. https://doi.org/10.1016/j.matbio.2015.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Saharinen J, Keski-Oja J (2000) Specific sequence motif of 8-Cys repeats of TGF-β binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-β. Mol Biol Cell 11(8):2691–2704. https://doi.org/10.1091/mbc.11.8.2691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Thomas BJ, Kan-O K, Loveland KL, Elias JA, Bardin PG (2016) In the shadow of fibrosis: innate immune suppression mediated by transforming growth factor-β. Am J Respir Cell Mol Biol 55(6):759–766. https://doi.org/10.1165/rcmb.2016-0248PS

    Article  CAS  PubMed  Google Scholar 

  42. Mirzaei H, Faghihloo E (2018) Viruses as key modulators of the TGF-β pathway; a double-edged sword involved in cancer. Rev Med Virol. https://doi.org/10.1002/rmv.1967

    Article  PubMed  PubMed Central  Google Scholar 

  43. Geng Y et al (2011) Follistatin-like 1 (Fstl1) is a bone morphogenetic protein (BMP) 4 signaling antagonist in controlling mouse lung development. Proc Natl Acad Sci USA 108(17):7058–7063. https://doi.org/10.1073/pnas.1007293108

    Article  PubMed  PubMed Central  Google Scholar 

  44. Chaly Y, Hostager B, Smith S, Hirsch R (2014) Follistatin-like protein 1 and its role in inflammation and inflammatory diseases. Immunol Res 59(1–3):266–272. https://doi.org/10.1007/s12026-014-8526-z

    Article  CAS  PubMed  Google Scholar 

  45. Zhang L, Wang Z (2020) Circular RNA hsa_circ_0004812 impairs IFN-induced immune response by sponging miR-1287-5p to regulate FSTL1 in chronic hepatitis B. Virol J 17(1):40. https://doi.org/10.1186/s12985-020-01314-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Dunn EF, Connor JH (2012) HijAkt: The PI3K/Akt pathway in virus replication and pathogenesis. Prog Mol Biol Transl Sci 106:223–250. https://doi.org/10.1016/B978-0-12-396456-4.00002-X

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Avota E, Harms H, Schneider-Schaulies S (2006) Measles virus induces expression of SIP110, a constitutively membrane clustered lipid phosphatase, which inhibits T cell proliferation. Cell Microbiol 8(11):1826–1839. https://doi.org/10.1111/j.1462-5822.2006.00752.x

    Article  CAS  PubMed  Google Scholar 

  48. Diehl N, Schaal H (2013) Make yourself at home: viral hijacking of the PI3K/Akt signaling pathway. Viruses 5(12):3192–3212. https://doi.org/10.3390/v5123192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Avota E, Gassert E, Schneider-Schaulies S (2011) Cytoskeletal dynamics: concepts in measles virus replication and immunomodulation. Viruses 3(2):102–117. https://doi.org/10.3390/v3020102

    Article  PubMed  PubMed Central  Google Scholar 

  50. Dietzel E, Kolesnikova L, Maisner A (2013) Actin filaments disruption and stabilization affect measles virus maturation by different mechanisms. Virol J 10:249. https://doi.org/10.1186/1743-422X-10-249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Buchholz CJ, Mühlebach MD, Cichutek K (2009) Lentiviral vectors with measles virus glycoproteins—dream team for gene transfer? Trends Biotechnol 27(5):259–265. https://doi.org/10.1016/j.tibtech.2009.02.002

    Article  CAS  PubMed  Google Scholar 

  52. Watanabe S, Shirogane Y, Sato Y, Hashiguchi T, Yanagi Y (2019) New insights into measles virus brain infections. Trends Microbiol 27(2):164–175. https://doi.org/10.1016/j.tim.2018.08.010

    Article  CAS  PubMed  Google Scholar 

  53. Stankiewicz TR, Linseman DA (2014) Rho family GTPases: key players in neuronal development, neuronal survival, and neurodegeneration. Front Cell Neurosci 8:314. https://doi.org/10.3389/fncel.2014.00314

    Article  PubMed  PubMed Central  Google Scholar 

  54. Koyuncu OO, Hogue IB, Enquist LW (2013) Virus infections in the nervous system. Cell Host Microbe 13(4):379–393. https://doi.org/10.1016/j.chom.2013.03.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Taylor MP, Enquist LW (2015) Axonal spread of neuroinvasive viral infections. Trends Microbiol 23(5):283–288. https://doi.org/10.1016/j.tim.2015.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kreuger J, Spillmann D, Li J, Lindahl U (2006) Interactions between heparan sulfate and proteins: the concept of specificity. J Cell Biol 174(3):323–327. https://doi.org/10.1083/jcb.200604035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Plemper RK (2011) Cell entry of enveloped viruses. Curr Opin Virol 1(2):92–100. https://doi.org/10.1016/j.coviro.2011.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Yao J-H, Liu Z-J, Yi J-H, Wang J, Liu Y-N (2018) Hepatitis B virus X protein upregulates intracellular calcium signaling by binding C-terminal of orail protein. Curr Med Sci 38(1):26–34. https://doi.org/10.1007/s11596-018-1843-z

    Article  CAS  PubMed  Google Scholar 

  59. Chang-Graham AL et al (2019) Rotavirus calcium dysregulation manifests as dynamic calcium signaling in the cytoplasm and endoplasmic reticulum. Sci Rep 9(1):10822. https://doi.org/10.1038/s41598-019-46856-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Ding W et al (2002) Human T-cell lymphotropic virus type 1 p12(I) expression increases cytoplasmic calcium to enhance the activation of nuclear factor of activated T cells. J Virol 76(20):10374–10382. https://doi.org/10.1128/jvi.76.20.10374-10382.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zhang Q, Hsia S-C, Martin-Caraballo M (2017) Regulation of T-type Ca(2+) channel expression by herpes simplex virus-1 infection in sensory-like ND7 cells. J Neurovirol 23(5):657–670. https://doi.org/10.1007/s13365-017-0545-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hoji A, Xu S, Bilben H, Rowe DT (2018) Calcium mobilization is responsible for Thapsigargin induced Epstein Barr virus lytic reactivation in in vitro immortalized lymphoblstoid cell lines. Heliyon 4(11):e00917. https://doi.org/10.1016/j.heliyon.2018.e00917

    Article  PubMed  PubMed Central  Google Scholar 

  63. Hu X-T (2016) HIV-1 Tat-mediated calcium dysregulation and neuronal dysfunction in vulnerable brain regions. Curr Drug Targets 17(1):4–14. https://doi.org/10.2174/1389450116666150531162212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Pham T, Perry JL, Dosey TL, Delcour AH, Hyser JM (2017) The rotavirus NSP4 viroporin domain is a calcium-conducting ion channel. Sci Rep 7(1):43487. https://doi.org/10.1038/srep43487

    Article  PubMed  PubMed Central  Google Scholar 

  65. van Kuppeveld FJM, de Jong AS, Melchers WJG, Willems PHGM (2005) Enterovirus protein 2B po(u)res out the calcium: a viral strategy to survive? Trends Microbiol 13(2):41–44. https://doi.org/10.1016/j.tim.2004.12.005

    Article  CAS  PubMed  Google Scholar 

  66. Omar S et al (2017) Respiratory virus infection up-regulates TRPV1, TRPA1 and ASICS3 receptors on airway cells. PLoS ONE 12(2):e0171681. https://doi.org/10.1371/journal.pone.0171681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Li J, Zhang X, Song X, Liu R, Zhang J, Li Z (2019) The structure of TRPC ion channels. Cell Calcium 80:25–28. https://doi.org/10.1016/j.ceca.2019.03.005

    Article  CAS  PubMed  Google Scholar 

  68. Madavaraju K, Koganti R, Volety I, Yadavalli T, Shukla D (2020) Herpes simplex virus cell entry mechanisms: an update. Front Cell Infect Microbiol 10:617578. https://doi.org/10.3389/fcimb.2020.617578

    Article  PubMed  Google Scholar 

  69. Antinone SE, Zaichick SV, Smith GA (2010) Resolving the assembly state of herpes simplex virus during axon transport by live-cell imaging. J Virol 84(24):13019–13030. https://doi.org/10.1128/JVI.01296-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Elbahesh H, Bergmann S, Russell CJ (2016) Focal adhesion kinase (FAK) regulates polymerase activity of multiple influenza A virus subtypes. Virology 499:369–374. https://doi.org/10.1016/j.virol.2016.10.002

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was part of a PhD thesis supported by Tehran University of Medical Sciences (Grant Number: 97-01-87-37998). This work was supported by a grant from the Biotechnology Development Council of the Islamic Republic of Iran (Grant Number: 970401). Authors are grateful to Mr. Mohammadreza Sarfarazi for his support in graphics.

Funding

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. This study was part of a PhD thesis supported by Tehran University of Medical Sciences (Grant Number: 97-01-87-37998). This work was supported by a grant from the Biotechnology Development Council of the Islamic Republic of Iran (Grant Number: 970401).

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  1. Department of Medical Biotechnology, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences (TUMS), Tehran, Iran

    Malihe Rastegarpanah, Babak Negahdari, Yazdan Asgari & Mohammadali Mazloomi

  2. Department of Molecular Virology, Pasteur Institute of Iran, Tehran, Iran

    Kayhan Azadmanesh

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KA, BN, YA, and MM were responsible for study Conceptualization, and Methodology. YA and MR analyzed the data and performed the bioinformatic analysis. MR performed the experiments and wrote the original draft. All authors contributed to the article and approved the submitted version.

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Correspondence to Mohammadali Mazloomi.

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Human diploid lung fibroblast cell line MRC-5 (RRID: CVCL_RB14), adenocarcinomic human alveolar basal epithelial cells A549 (RRID: CVCL_VR66), human embryonic kidney 293 cells (RRID: CVCL_0045), immortal human cell line Hela (RRID: CVCL_0030), and human hepatocyte carcinoma cell line HepG2 (RRID: CVCL_0027) were obtained from the “American Type Culture Collection (ATCC)” and informed consent is not applicable.

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All procedures performed in this study involving human cell lines were in accordance with the ethical standards of the Medical Ethics Committee at the Tehran University of Medical Sciences (TUMS) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Rastegarpanah, M., Azadmanesh, K., Negahdari, B. et al. Screening of candidate genes associated with high titer production of oncolytic measles virus based on systems biology approach. Virus Genes 58, 270–283 (2022). https://doi.org/10.1007/s11262-022-01902-y

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