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Advances in RNA Viral Vector Technology to Reprogram Somatic Cells: The Paramyxovirus Wave

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Abstract

Ethical issues are a significant barrier to the use of embryonic stem cells in patients due to their origin: human embryos. To further the development of stem cells in a patient application, alternative sources of cells were sought. A process referred to as reprogramming was established to create induced pluripotent stem cells from somatic cells, resolving the ethical issues, and vectors were developed to deliver the reprogramming factors to generate induced pluripotent stem cells. Early viral vectors used integrating retroviruses and lentiviruses as delivery vehicles for the transcription factors required to initiate reprogramming. However, because of the inherent risk associated with vectors that integrate into the host genome, non-integrating approaches were explored. The development of non-integrating viral vectors offers a safer alternative, and these modern vectors are reliable, efficient, and easy to use to achieve induced pluripotent stem cells suitable for direct patient application in the growing field of individualized medicine. This review summarizes all the RNA viral vectors in the field of reprogramming with a special focus on the emerging delivery vectors based on non-integrating  Paramyxoviruses, Sendai and measles viruses. We discuss their design and evolution towards being safe and efficient reprogramming vectors in generating induced pluripotent stem cells from somatic cells.

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References

  1. Lo B, Parham L. Ethical issues in stem cell research. Endocr Rev. 2009;30(3):204–13.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282(5391):1145–7.

    Article  CAS  PubMed  Google Scholar 

  3. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–76.

    Article  CAS  PubMed  Google Scholar 

  4. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318(5858):1917–20.

    Article  CAS  PubMed  Google Scholar 

  5. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131(5):861–72.

    Article  CAS  PubMed  Google Scholar 

  6. Nakagawa M, Takizawa N, Narita M, Ichisaka T, Yamanaka S. Promotion of direct reprogramming by transformation-deficient Myc. Proc Natl Acad Sci U S A. 2010;107(32):14152–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Buganim Y, Faddah DA, Cheng AW, Itskovich E, Markoulaki S, Ganz K, et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell. 2012;150(6):1209–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kuan II, Liang K-H, Wang Y-P, Kuo T-W, Meir Y-JJ, Wu SC-Y, et al. EpEX/EpCAM and Oct4 or Klf4 alone are sufficient to generate induced pluripotent stem cells through STAT3 and HIF2α. Sci Rep. 2017;7(1):41852.

  9. Redmer T, Diecke S, Grigoryan T, Quiroga-Negreira A, Birchmeier W, Besser D. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Rep. 2011;12(7):720–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Heng J-CD, Feng B, Han J, Jiang J, Kraus P, Ng J-H, et al. The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell. 2010;6(2):167–74.

  11. Dey C, Raina K, Thool M, Adhikari P, Haridhasapavalan KK, Sundaravadivelu PK, et al. Chapter 2. Auxiliary pluripotency-associated genes and their contributions in the generation of induced pluripotent stem cells. Molecular players in iPSC technology. 2022. Vol 12: p. 29–94.

  12. Jiang J, Chan YS, Loh YH, Cai J, Tong GQ, Lim CA, et al. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol. 2008;10(3):353–60.

    Article  PubMed  Google Scholar 

  13. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol. 2008;26(1):101–6.

    Article  CAS  PubMed  Google Scholar 

  14. Montserrat N, Nivet E, Sancho-Martinez I, Hishida T, Kumar S, Miquel L, et al. Reprogramming of human fibroblasts to pluripotency with lineage specifiers. Cell Stem Cell. 2013;13(3):341–50.

    Article  CAS  PubMed  Google Scholar 

  15. Shu J, Zhang K, Zhang M, Yao A, Shao S, Du F, et al. GATA family members as inducers for cellular reprogramming to pluripotency. Cell Res. 2015;25(2):169–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Han J, Yuan P, Yang H, Zhang J, Soh BS, Li P, et al. Tbx3 improves the germ-line competency of induced pluripotent stem cells. Nature. 2010;463(7284):1096–100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Tsubooka N, Ichisaka T, Okita K, Takahashi K, Nakagawa M, Yamanaka S. Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts. Genes Cells. 2009;14(6):683–94.

    Article  CAS  PubMed  Google Scholar 

  18. Zhao Y, Yin X, Qin H, Zhu F, Liu H, Yang W, et al. Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell. 2008;3(5):475–9.

    Article  CAS  PubMed  Google Scholar 

  19. Judson RL, Babiarz JE, Venere M, Blelloch R. Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol. 2009;27(5):459–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell. 2011;8(4):376–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Miyoshi N, Ishii H, Nagano H, Haraguchi N, Dewi DL, Kano Y, et al. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell. 2011;8(6):633–8.

    Article  CAS  PubMed  Google Scholar 

  22. Yamanaka S. Pluripotent stem cell-based cell therapy: promise and challenges. Cell Stem Cell. 2020;27(4):523–31.

    Article  CAS  PubMed  Google Scholar 

  23. Kavyasudha C, Macrin D, ArulJothi KN, Joseph JP, Harishankar MK, Devi A. Clinical applications of induced pluripotent stem cells: stato attuale. Adv Exp Med Biol. 2018;1079:127–49.

    Article  CAS  PubMed  Google Scholar 

  24. Dey C, Raina K, Haridhasapavalan KK, Thool M, Sundaravadivelu PK, Adhikari P, et al. Chapter 9: An overview of reprogramming approaches to derive integration-free induced pluripotent stem cells for prospective biomedical applications.  Recent advances in iPSC technology. Vol 5: p. 231–87.

    Chapter  Google Scholar 

  25. Gonzalez F, Boue S, Izpisua Belmonte JC. Methods for making induced pluripotent stem cells: reprogramming a la carte. Nat Rev Genet. 2011;12(4):231–42.

    Article  CAS  PubMed  Google Scholar 

  26. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K. Induced pluripotent stem cells generated without viral integration. Science. 2008;322(5903):945–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Weltner J, Anisimov A, Alitalo K, Otonkoski T, Trokovic R. Induced pluripotent stem cell clones reprogrammed via recombinant adeno-associated virus-mediated transduction contain integrated vector sequences. J Virol. 2012;86(8):4463–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell. 2009;4(5):381–4.

    Article  CAS  PubMed  Google Scholar 

  29. Zhou W, Freed CR. Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells. 2009;27(11):2667–74.

    Article  CAS  PubMed  Google Scholar 

  30. Haridhasapavalan KK, Borgohain MP, Dey C, Saha B, Narayan G, Kumar S, et al. An insight into non-integrative gene delivery approaches to generate transgene-free induced pluripotent stem cells. Gene. 2019;20(686):146–59.

    Article  Google Scholar 

  31. Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell. 2010;7(5):618–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kim D, Kim CH, Moon JI, Chung YG, Chang MY, Han BS, et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell. 2009;4(6):472–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, Okamoto S, et al. A more efficient method to generate integration-free human iPS cells. Nat Methods. 2011;8(5):409–12.

    Article  CAS  PubMed  Google Scholar 

  34. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science. 2008;322(5903):949–53.

    Article  CAS  PubMed  Google Scholar 

  35. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science. 2009;324(5928):797–801.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Jia F, Wilson KD, Sun N, Gupta DM, Huang M, Li Z, et al. A nonviral minicircle vector for deriving human iPS cells. Nat Methods. 2010;7(3):197–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K. Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature. 2009;458(7239):771–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hamalainen R, et al. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature. 2009;458(7239):766–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yusa K, Rad R, Takeda J, Bradley A. Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat Methods. 2009;6(5):363–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Park HY, Noh EH, Chung HM, Kang MJ, Kim EY, Park SP. Efficient generation of virus-free iPS cells using liposomal magnetofection. PLoS ONE. 2012;7(9): e45812.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Borgohain MP, Haridhasapavalan KK, Dey C, Adhikari P, Thummer RP. An insight into DNA-free reprogramming approaches to generate integration-free induced pluripotent stem cells for prospective biomedical applications. Stem Cell Rev Rep. 2019;15(2):286–313.

    Article  CAS  PubMed  Google Scholar 

  42. Rein A. Murine leukemia viruses: objects and organisms. Adv Virol. 2011;2011: 403419.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Freed EO. HIV-1 assembly, release and maturation. Nat Rev Microbiol. 2015;13(8):484–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Cullen BR. Trans-activation of human immunodeficiency virus occurs via a bimodal mechanism. Cell. 1986;46(7):973–82.

    Article  CAS  PubMed  Google Scholar 

  45. Felber BK, Hadzopoulou-Cladaras M, Cladaras C, Copeland T, Pavlakis GN. rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc Natl Acad Sci U S A. 1989;86(5):1495–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Muesing MA, Smith DH, Capon DJ. Regulation of mRNA accumulation by a human immunodeficiency virus trans-activator protein. Cell. 1987;48(4):691–701.

    Article  CAS  PubMed  Google Scholar 

  47. Emerman M, Vazeux R, Peden K. The rev gene product of the human immunodeficiency virus affects envelope-specific RNA localization. Cell. 1989;57(7):1155–65.

    Article  CAS  PubMed  Google Scholar 

  48. Malim MH, Hauber J, Le SY, Maizel JV, Cullen BR. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature. 1989;338(6212):254–7.

    Article  CAS  PubMed  Google Scholar 

  49. Rosen CA. Tat and Rev: positive modulators of human immunodeficiency virus gene expression. Gene Expr. 1991;1(2):85–90.

    CAS  PubMed  Google Scholar 

  50. Tristem M, Marshall C, Karpas A, Petrik J, Hill F. Origin of vpx in lentiviruses. Nature. 1990;347(6291):341–2.

    Article  CAS  PubMed  Google Scholar 

  51. Sheehy AM, Gaddis NC, Malim MH. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med. 2003;9(11):1404–7.

    Article  CAS  PubMed  Google Scholar 

  52. Aiken C, Konner J, Landau NR, Lenburg ME, Trono D. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell. 1994;76(5):853–64.

    Article  CAS  PubMed  Google Scholar 

  53. Garcia JV, Miller AD. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature. 1991;350(6318):508–11.

    Article  CAS  PubMed  Google Scholar 

  54. Chowers MY, Spina CA, Kwoh TJ, Fitch NJ, Richman DD, Guatelli JC. Optimal infectivity in vitro of human immunodeficiency virus type 1 requires an intact nef gene. J Virol. 1994;68(5):2906–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Desrosiers RC, Lifson JD, Gibbs JS, Czajak SC, Howe AY, Arthur LO, et al. Identification of highly attenuated mutants of simian immunodeficiency virus. J Virol. 1998;72(2):1431–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Miller MD, Warmerdam MT, Gaston I, Greene WC, Feinberg MB. The human immunodeficiency virus-1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J Exp Med. 1994;179(1):101–13.

    Article  CAS  PubMed  Google Scholar 

  57. Du Z, Lang SM, Sasseville VG, Lackner AA, Ilyinskii PO, Daniel MD, et al. Identification of a nef allele that causes lymphocyte activation and acute disease in macaque monkeys. Cell. 1995;82(4):665–74.

    Article  CAS  PubMed  Google Scholar 

  58. Popov S, Rexach M, Zybarth G, Reiling N, Lee MA, Ratner L, et al. Viral protein R regulates nuclear import of the HIV-1 pre-integration complex. EMBO J. 1998;17(4):909–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Re F, Braaten D, Franke EK, Luban J. Human immunodeficiency virus type 1 Vpr arrests the cell cycle in G2 by inhibiting the activation of p34cdc2-cyclin B. J Virol. 1995;69(11):6859–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Agostini I, Navarro JM, Rey F, Bouhamdan M, Spire B, Vigne R, et al. The human immunodeficiency virus type 1 Vpr transactivator: cooperation with promoter-bound activator domains and binding to TFIIB. J Mol Biol. 1996;261(5):599–606.

    Article  CAS  PubMed  Google Scholar 

  61. Strebel K, Klimkait T, Maldarelli F, Martin MA. Molecular and biochemical analyses of human immunodeficiency virus type 1 vpu protein. J Virol. 1989;63(9):3784–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Yao XJ, Gottlinger H, Haseltine WA, Cohen EA. Envelope glycoprotein and CD4 independence of vpu-facilitated human immunodeficiency virus type 1 capsid export. J Virol. 1992;66(8):5119–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sakuma T, Barry MA, Ikeda Y. Lentiviral vectors: basic to translational. Biochem J. 2012;443(3):603–18.

    Article  CAS  PubMed  Google Scholar 

  64. Anson DS. The use of retroviral vectors for gene therapy-what are the risks? A review of retroviral pathogenesis and its relevance to retroviral vector-mediated gene delivery. Genet Vaccines Ther. 2004;2(1):9.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Akkina RK, Walton RM, Chen ML, Li QX, Planelles V, Chen IS. High-efficiency gene transfer into CD34+ cells with a human immunodeficiency virus type 1-based retroviral vector pseudotyped with vesicular stomatitis virus envelope glycoprotein G. J Virol. 1996;70(4):2581–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Burns JC, Friedmann T, Driever W, Burrascano M, Yee JK. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proc Natl Acad Sci U S A. 1993;90(17):8033–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Pear W. Transient transfection methods for preparation of high-titer retroviral supernatants. Curr Protoc Mol Biol. 2001;Chapter 9:Unit9.11.

  68. Roe T, Reynolds TC, Yu G, Brown PO. Integration of murine leukemia virus DNA depends on mitosis. EMBO J. 1993;12(5):2099–108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996;272(5259):263–7.

    Article  CAS  PubMed  Google Scholar 

  70. Stadtfeld M, Hochedlinger K. Induced pluripotency: history, mechanisms, and applications. Genes Dev. 2010;24(20):2239–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F, et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol. 2008;26(11):1276–84.

    Article  CAS  PubMed  Google Scholar 

  72. Eminli S, Foudi A, Stadtfeld M, Maherali N, Ahfeldt T, Mostoslavsky G, et al. Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat Genet. 2009;41(9):968–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Haase A, Olmer R, Schwanke K, Wunderlich S, Merkert S, Hess C, et al. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell. 2009;5(4):434–41.

    Article  CAS  PubMed  Google Scholar 

  74. Kim JB, Sebastiano V, Wu G, Arauzo-Bravo MJ, Sasse P, Gentile L, et al. Oct4-induced pluripotency in adult neural stem cells. Cell. 2009;136(3):411–9.

    Article  CAS  PubMed  Google Scholar 

  75. Kim JB, Greber B, Arauzo-Bravo MJ, Meyer J, Park KI, Zaehres H, et al. Direct reprogramming of human neural stem cells by OCT4. Nature. 2009;461(7264):649–53.

    Article  CAS  PubMed  Google Scholar 

  76. Sugii S, Kida Y, Kawamura T, Suzuki J, Vassena R, Yin YQ, et al. Human and mouse adipose-derived cells support feeder-independent induction of pluripotent stem cells. Proc Natl Acad Sci U S A. 2010;107(8):3558–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Papapetrou EP, Tomishima MJ, Chambers SM, Mica Y, Reed E, Menon J, et al. Stoichiometric and temporal requirements of Oct4, Sox2, Klf4, and c-Myc expression for efficient human iPSC induction and differentiation. Proc Natl Acad Sci U S A. 2009;106(31):12759–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Carey BW, Markoulaki S, Hanna J, Saha K, Gao Q, Mitalipova M, et al. Reprogramming of murine and human somatic cells using a single polycistronic vector. Proc Natl Acad Sci U S A. 2009;106(1):157–62.

    Article  CAS  PubMed  Google Scholar 

  79. Chang CW, Lai YS, Pawlik KM, Liu K, Sun CW, Li C, et al. Polycistronic lentiviral vector for “hit and run” reprogramming of adult skin fibroblasts to induced pluripotent stem cells. Stem Cells. 2009;27(5):1042–9.

    Article  CAS  PubMed  Google Scholar 

  80. Sommer CA, Stadtfeld M, Murphy GJ, Hochedlinger K, Kotton DN, Mostoslavsky G. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells. 2009;27(3):543–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, et al. Parkinson’s disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell. 2009;136(5):964–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Iwakuma T, Cui Y, Chang LJ. Self-inactivating lentiviral vectors with U3 and U5 modifications. Virology. 1999;261(1):120–32.

    Article  CAS  PubMed  Google Scholar 

  83. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. Development of a self-inactivating lentivirus vector. J Virol. 1998;72(10):8150–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Papapetrou EP, Sadelain M. Generation of transgene-free human induced pluripotent stem cells with an excisable single polycistronic vector. Nat Protoc. 2011;6(9):1251–73.

    Article  CAS  PubMed  Google Scholar 

  85. Pfeifer A, Brandon EP, Kootstra N, Gage FH, Verma IM. Delivery of the Cre recombinase by a self-deleting lentiviral vector: efficient gene targeting in vivo. Proc Natl Acad Sci U S A. 2001;98(20):11450–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Somers A, Jean JC, Sommer CA, Omari A, Ford CC, Mills JA, et al. Generation of transgene-free lung disease-specific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Stem Cells. 2010;28(10):1728–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Ventura A, Meissner A, Dillon CP, McManus M, Sharp PA, Van Parijs L, et al. Cre-lox-regulated conditional RNA interference from transgenes. Proc Natl Acad Sci U S A. 2004;101(28):10380–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Yu SF, von Rüden T, Kantoff PW, Garber C, Seiberg M, Rüther U, et al. Self-inactivating retroviral vectors designed for transfer of whole genes into mammalian cells. Proc Natl Acad Sci U S A. 1986;83(10):3194–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol. 1998;72(12):9873–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bouma MJ, van Iterson M, Janssen B, Mummery CL, Salvatori DCF, Freund C. Differentiation-defective human induced pluripotent stem cells reveal strengths and limitations of the teratoma assay and in vitro pluripotency assays. Stem Cell Rep. 2017;8(5):1340–53.

    Article  Google Scholar 

  91. Shao L, Wu WS. Gene-delivery systems for iPS cell generation. Expert Opin Biol Ther. 2010;10(2):231–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Kadari A, Lu M, Li M, Sekaran T, Thummer RP, Guyette N, et al. Excision of viral reprogramming cassettes by Cre protein transduction enables rapid, robust and efficient derivation of transgene-free human induced pluripotent stem cells. Stem Cell Res Ther. 2014;5(2):47.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Cara A, Cereseto A, Lori F, Reitz MS Jr. HIV-1 protein expression from synthetic circles of DNA mimicking the extrachromosomal forms of viral DNA. J Biol Chem. 1996;271(10):5393–7.

    Article  CAS  PubMed  Google Scholar 

  94. Mali P, Ye Z, Hommond HH, Yu X, Lin J, Chen G, et al. Improved efficiency and pace of generating induced pluripotent stem cells from human adult and fetal fibroblasts. Stem Cells. 2008;26(8):1998–2005.

    Article  CAS  PubMed  Google Scholar 

  95. Philpott NJ, Thrasher AJ. Use of nonintegrating lentiviral vectors for gene therapy. Hum Gene Ther. 2007;18(6):483–9.

    Article  CAS  PubMed  Google Scholar 

  96. Rao MS, Malik N. Assessing iPSC reprogramming methods for their suitability in translational medicine. J Cell Biochem. 2012;113(10):3061–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Guzmán-Terán C, Calderón-Rangel A, Rodriguez-Morales A, Mattar S. Venezuelan equine encephalitis virus: the problem is not over for tropical America. Ann Clin Microbiol Antimicrob. 2020;19(1):19.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R. Viral mutation rates. J Virol. 2010;84(19):9733–48.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Steinhauer DA, Domingo E, Holland JJ. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene. 1992;122(2):281–8.

    Article  CAS  PubMed  Google Scholar 

  100. Kinney RM, Johnson BJ, Welch JB, Tsuchiya KR, Trent DW. The full-length nucleotide sequences of the virulent Trinidad donkey strain of Venezuelan equine encephalitis virus and its attenuated vaccine derivative, strain TC-83. Virology. 1989;170(1):19–30.

    Article  CAS  PubMed  Google Scholar 

  101. Petrakova O, Volkova E, Gorchakov R, Paessler S, Kinney RM, Frolov I. Noncytopathic replication of Venezuelan equine encephalitis virus and eastern equine encephalitis virus replicons in Mammalian cells. J Virol. 2005;79(12):7597–608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Yoshioka N, Gros E, Li HR, Kumar S, Deacon DC, Maron C, et al. Efficient generation of human iPSCs by a synthetic self-replicative RNA. Cell Stem Cell. 2013;13(2):246–54.

    Article  CAS  PubMed  Google Scholar 

  103. Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RML. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon α transmembrane signaling. J Biol Chem. 1995;270(27):15974–8.

    Article  CAS  PubMed  Google Scholar 

  104. Driscoll CB, Tonne JM, El Khatib M, Cattaneo R, Ikeda Y, Devaux P. Nuclear reprogramming with a non-integrating human RNA virus. Stem Cell Res Ther. 2015;6(1):48.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci. 2009;85(8):348–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Wang Q, Vossen A, Ikeda Y, Devaux P. Measles vector as a multigene delivery platform facilitating iPSC reprogramming. Gene Ther. 2019;26(5):151–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Lamb R, Parks G. Paramyxoviridae: the viruses and their replication. Fields virology: 5th ed. Philadelphia (PA): Wolters Kluwer Health/Lippincott Williams & Wilkins; 2007.

  108. Cattaneo R, Rebmann G, Schmid A, Baczko K, ter Meulen V, Billeter MA. Altered transcription of a defective measles virus genome derived from a diseased human brain. EMBO J. 1987;6(3):681–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Galanis E, Atherton PJ, Maurer MJ, Knutson KL, Dowdy SC, Cliby WA, et al. Oncolytic measles virus expressing the sodium iodide symporter to treat drug-resistant ovarian cancer. Cancer Res. 2015;75(1):22–30.

    Article  CAS  PubMed  Google Scholar 

  110. Lech PJ, Russell SJ. Use of attenuated paramyxoviruses for cancer therapy. Expert Rev Vaccines. 2010;9(11):1275–302.

    Article  CAS  PubMed  Google Scholar 

  111. Liu YP, Steele MB, Suksanpaisan L, Federspiel MJ, Russell SJ, Peng KW, et al. Oncolytic measles and vesicular stomatitis virotherapy for endometrial cancer. Gynecol Oncol. 2014;132(1):194–202.

    Article  CAS  PubMed  Google Scholar 

  112. Russell SJ, Federspiel MJ, Peng KW, Tong C, Dingli D, Morice WG, et al. Remission of disseminated cancer after systemic oncolytic virotherapy. Mayo Clin Proc. 2014;89(7):926–33.

    Article  PubMed  Google Scholar 

  113. Hasegawa Y, Kinoh H, Iwadate Y, Onimaru M, Ueda Y, Harada Y, et al. Urokinase-targeted fusion by oncolytic Sendai virus eradicates orthotopic glioblastomas by pronounced synergy with interferon-β gene. Mol Ther. 2010;18(10):1778–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Morodomi Y, Yano T, Kinoh H, Harada Y, Saito S, Kyuragi R, et al. BioKnife, a uPA activity-dependent oncolytic Sendai virus, eliminates pleural spread of malignant mesothelioma via simultaneous stimulation of uPA expression. Mol Ther. 2012;20(4):769–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Shibata S, Okano S, Yonemitsu Y, Onimaru M, Sata S, Nagata-Takeshita H, et al. Induction of efficient antitumor immunity using dendritic cells activated by recombinant Sendai virus and its modulation by exogenous IFN-beta gene. J Immunol. 2006;177(6):3564–76.

    Article  CAS  PubMed  Google Scholar 

  116. Desprès P, Combredet C, Frenkiel MP, Lorin C, Brahic M, Tangy F. Live measles vaccine expressing the secreted form of the West Nile virus envelope glycoprotein protects against West Nile virus encephalitis. J Infect Dis. 2005;191(2):207–14.

    Article  PubMed  Google Scholar 

  117. Malczyk AH, Kupke A, Prüfer S, Scheuplein VA, Hutzler S, Kreuz D, et al. A highly immunogenic and protective Middle East respiratory syndrome coronavirus vaccine based on a recombinant measles virus vaccine platform. J Virol. 2015;89(22):11654–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Lorin C, Mollet L, Delebecque F, Combredet C, Hurtrel B, Charneau P, et al. A single injection of recombinant measles virus vaccines expressing human immunodeficiency virus (HIV) type 1 clade B envelope glycoproteins induces neutralizing antibodies and cellular immune responses to HIV. J Virol. 2004;78(1):146–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Jones B, Zhan X, Mishin V, Slobod KS, Surman S, Russell CJ, et al. Human PIV-2 recombinant Sendai virus (rSeV) elicits durable immunity and combines with two additional rSeVs to protect against hPIV-1, hPIV-2, hPIV-3, and RSV. Vaccine. 2009;27(12):1848–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Le TV, Mironova E, Garcin D, Compans RW. Induction of influenza-specific mucosal immunity by an attenuated recombinant Sendai virus. PLoS ONE. 2011;6(4): e18780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Slobod KS, Shenep JL, Luján-Zilbermann J, Allison K, Brown B, Scroggs RA, et al. Safety and immunogenicity of intranasal murine parainfluenza virus type 1 (Sendai virus) in healthy human adults. Vaccine. 2004;22(23–24):3182–6.

    Article  CAS  PubMed  Google Scholar 

  122. del Valle JR, Devaux P, Hodge G, Wegner NJ, McChesney MB, Cattaneo R. A vectored measles virus induces hepatitis B surface antigen antibodies while protecting macaques against measles virus challenge. J Virol. 2007;81(19):10597–605.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Nagai Y TA, A T, Irie T, Yonemitsu Y, B G. Sendai virus: evolution from mouse pathogen to a state-of-the-art tool in virus research and biotechnology. The biology of the paramyxoviruses. Norfolk, UK: Caister Academic Press; 2011.

  124. Schneider-Schaulies S. Duprex P. Measles virus. The biology of the paramyxoviruses. Norfolk, UK: Caister Academic Press; 2011.

  125. Kuroya M, Ishida N, Shiratori T. Newborn virus pneumonitis (type Sendai). II. The isolation of a new virus. Tohoku J Exp Med. 1953;58(1):62.

  126. Nakanishi M, Otsu M. Development of Sendai virus vectors and their potential applications in gene therapy and regenerative medicine. Curr Gene Ther. 2012;12(5):410–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Shioda T, Iwasaki K, Shibuta H. Determination of the complete nucleotide sequence of the Sendai virus genome RNA and the predicted amino acid sequences of the F, HN and L proteins. Nucleic Acids Res. 1986;14(4):1545–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Murakami Y, Ikeda Y, Yonemitsu Y, Tanaka S, Kondo H, Okano S, et al. Newly-developed Sendai virus vector for retinal gene transfer: reduction of innate immune response via deletion of all envelope-related genes. J Gene Med. 2008;10(2):165–76.

    Article  CAS  PubMed  Google Scholar 

  129. Piao W, Wang H, Inoue M, Hasegawa M, Hamada H, Huang J. Transplantation of Sendai viral angiopoietin-1-modified mesenchymal stem cells for ischemic limb disease. Angiogenesis. 2010;13(3):203–10.

    Article  CAS  PubMed  Google Scholar 

  130. Yonemitsu Y, Kitson C, Ferrari S, Farley R, Griesenbach U, Judd D, et al. Efficient gene transfer to airway epithelium using recombinant Sendai virus. Nat Biotechnol. 2000;18(9):970–3.

    Article  CAS  PubMed  Google Scholar 

  131. Ban H, Nishishita N, Fusaki N, Tabata T, Saeki K, Shikamura M, et al. Efficient generation of transgene-free human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors. Proc Natl Acad Sci U S A. 2011;108(34):14234–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Fujie Y, Fusaki N, Katayama T, Hamasaki M, Soejima Y, Soga M, et al. New type of Sendai virus vector provides transgene-free iPS cells derived from chimpanzee blood. PLoS ONE. 2014;9(12): e113052.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Seki T, Yuasa S, Oda M, Egashira T, Yae K, Kusumoto D, et al. Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell. 2010;7(1):11–4.

    Article  CAS  PubMed  Google Scholar 

  134. Macarthur CC, Fontes A, Ravinder N, Kuninger D, Kaur J, Bailey M, et al. Generation of human-induced pluripotent stem cells by a nonintegrating RNA Sendai virus vector in feeder-free or xeno-free conditions. Stem Cells Int. 2012;2012: 564612.

    Article  PubMed  PubMed Central  Google Scholar 

  135. Beers J, Linask KL, Chen JA, Siniscalchi LI, Lin Y, Zheng W, et al. A cost-effective and efficient reprogramming platform for large-scale production of integration-free human induced pluripotent stem cells in chemically defined culture. Sci Rep. 2015;5(1):11319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Trokovic R, Weltner J, Manninen T, Mikkola M, Lundin K, Hämäläinen R, et al. Small molecule inhibitors promote efficient generation of induced pluripotent stem cells from human skeletal myoblasts. Stem Cells Dev. 2013;22(1):114–23.

    Article  CAS  PubMed  Google Scholar 

  137. Schlaeger TM, Daheron L, Brickler TR, Entwisle S, Chan K, Cianci A, et al. A comparison of non-integrating reprogramming methods. Nat Biotechnol. 2015;33(1):58–63.

    Article  CAS  PubMed  Google Scholar 

  138. Calain P, Roux L. The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol. 1993;67(8):4822–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Agungpriyono DR, Yamaguchi R, Uchida K, Tohya Y, Kato A, Nagai Y, et al. Green fluorescent protein gene insertion of Sendai virus infection in nude mice: possibility as an infection tracer. J Vet Med Sci. 2000;62(2):223–8.

    Article  CAS  PubMed  Google Scholar 

  140. Bitzer M, Armeanu S, Lauer UM, Neubert WJ. Sendai virus vectors as an emerging negative-strand RNA viral vector system. J Gene Med. 2003;5(7):543–53.

    Article  CAS  PubMed  Google Scholar 

  141. Masaki I, Yonemitsu Y, Komori K, Ueno H, Nakashima Y, Nakagawa K, et al. Recombinant Sendai virus-mediated gene transfer to vasculature: a new class of efficient gene transfer vector to the vascular system. FASEB J. 2001;15(7):1294–6.

    Article  CAS  PubMed  Google Scholar 

  142. Shiotani A, Fukumura M, Maeda M, Hou X, Inoue M, Kanamori T, et al. Skeletal muscle regeneration after insulin-like growth factor I gene transfer by recombinant Sendai virus vector. Gene Ther. 2001;8(14):1043–50.

    Article  CAS  PubMed  Google Scholar 

  143. Hasan MK, Kato A, Shioda T, Sakai Y, Yu D, Nagai Y. Creation of an infectious recombinant Sendai virus expressing the firefly luciferase gene from the 3′ proximal first locus. J Gen Virol. 1997;78(Pt 11):2813–20.

    Article  CAS  PubMed  Google Scholar 

  144. Garcin D, Pelet T, Calain P, Roux L, Curran J, Kolakofsky D. A highly recombinogenic system for the recovery of infectious Sendai paramyxovirus from cDNA: generation of a novel copy-back nondefective interfering virus. EMBO J. 1995;14(24):6087–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Kato A, Sakai Y, Shioda T, Kondo T, Nakanishi M, Nagai Y. Initiation of Sendai virus multiplication from transfected cDNA or RNA with negative or positive sense. Genes Cells. 1996;1(6):569–79.

    Article  CAS  PubMed  Google Scholar 

  146. Abe T, Masuda S, Ban H, Hayashi S, Ueda Y, Inoue M, et al. Ex vivo expansion of human HSCs with Sendai virus vector expressing HoxB4 assessed by sheep in utero transplantation. Exp Hematol. 2011;39(1):47–54.

    Article  CAS  PubMed  Google Scholar 

  147. Bossow S, Schlecht S, Schubbert R, Pfeiffer M, Neubert WJ, Wiegand M. Evaluation of nucleocapsid and phosphoprotein P functionality as critical factors during the early phase of paramyxoviral infection. Open Virol J. 2012;6:73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Li HO, Zhu YF, Asakawa M, Kuma H, Hirata T, Ueda Y, et al. A cytoplasmic RNA vector derived from nontransmissible Sendai virus with efficient gene transfer and expression. J Virol. 2000;74(14):6564–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Inoue M, Tokusumi Y, Ban H, Kanaya T, Shirakura M, Tokusumi T, et al. A new Sendai virus vector deficient in the matrix gene does not form virus particles and shows extensive cell-to-cell spreading. J Virol. 2003;77(11):6419–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Bernloehr C, Bossow S, Ungerechts G, Armeanu S, Neubert WJ, Lauer UM, et al. Efficient propagation of single gene deleted recombinant Sendai virus vectors. Virus Res. 2004;99(2):193–7.

    Article  CAS  PubMed  Google Scholar 

  151. Yoshizaki M, Hironaka T, Iwasaki H, Ban H, Tokusumi Y, Iida A, et al. Naked Sendai virus vector lacking all of the envelope-related genes: reduced cytopathogenicity and immunogenicity. J Gene Med. 2006;8(9):1151–9.

    Article  CAS  PubMed  Google Scholar 

  152. Inoue M, Tokusumi Y, Ban H, Kanaya T, Tokusumi T, Nagai Y, et al. Nontransmissible virus-like particle formation by F-deficient sendai virus is temperature sensitive and reduced by mutations in M and HN proteins. J Virol. 2003;77(5):3238–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Nishimura K, Sano M, Ohtaka M, Furuta B, Umemura Y, Nakajima Y, et al. Development of defective and persistent Sendai virus vector: a unique gene delivery/expression system ideal for cell reprogramming. J Biol Chem. 2011;286(6):4760–71.

    Article  CAS  PubMed  Google Scholar 

  154. Life Technologies. CytoTune™-iPS Reprogramming Kit. 2011. https://tools.thermofisher.com/content/sfs/manuals/CytoTune_iPS_Reprogramming_Kit_man.pdf. Accessed 19 Jun 2022.

  155. Nishimura K, Segawa H, Goto T, Morishita M, Masago A, Takahashi H, et al. Persistent and stable gene expression by a cytoplasmic RNA replicon based on a noncytopathic variant Sendai virus. J Biol Chem. 2007;282(37):27383–91.

    Article  CAS  PubMed  Google Scholar 

  156. Takayama K, Morisaki Y, Kuno S, Nagamoto Y, Harada K, Furukawa N, et al. Prediction of interindividual differences in hepatic functions and drug sensitivity by using human iPS-derived hepatocytes. Proc Nati Acad Sci U S A. 2014;111(47):16772–7.

    Article  CAS  Google Scholar 

  157. Kawagoe S, Higuchi T, Otaka M, Shimada Y, Kobayashi H, Ida H, et al. Morphological features of iPS cells generated from Fabry disease skin fibroblasts using Sendai virus vector (SeVdp). Mol Genet Metab. 2013;109(4):386–9.

    Article  CAS  PubMed  Google Scholar 

  158. Nishino K, Arai Y, Takasawa K, Toyoda M, Yamazaki-Inoue M, Sugawara T, et al. Epigenetic-scale comparison of human iPSCs generated by retrovirus, Sendai virus or episomal vectors. Regen Ther. 2018;2018(9):71–8.

    Article  Google Scholar 

  159. Nishimura K, Kato T, Chen C, Oinam L, Shiomitsu E, Ayakawa D, et al. Manipulation of KLF4 expression generates iPSCs paused at successive stages of reprogramming. Stem Cell Rep. 2014;3(5):915–29.

    Article  CAS  Google Scholar 

  160. Nishimura K, Ohtaka M, Takada H, Kurisaki A, Tran NVK, Tran YTH, et al. Simple and effective generation of transgene-free induced pluripotent stem cells using an auto-erasable Sendai virus vector responding to microRNA-302. Stem Cell Res. 2017;23:13–9.

    Article  CAS  PubMed  Google Scholar 

  161. Lakshmipathy U, Davila J, Hart RP. miRNA in pluripotent stem cells. Regen Med. 2010;5(4):545–55.

    Article  CAS  PubMed  Google Scholar 

  162. Okumura T, Horie Y, Lai CY, Lin HT, Shoda H, Natsumoto B, et al. Robust and highly efficient hiPSC generation from patient non-mobilized peripheral blood-derived CD34(+) cells using the auto-erasable Sendai virus vector. Stem Cell Res Ther. 2019;10(1):185.

    Article  PubMed  PubMed Central  Google Scholar 

  163. Kuo CH, Deng JH, Deng Q, Ying SY. A novel role of miR-302/367 in reprogramming. Biochem Biophys Res Commun. 2012;417(1):11–6.

    Article  CAS  PubMed  Google Scholar 

  164. Moss WJ, Griffin DE. Global measles elimination. Nat Rev Microbiol. 2006;4(12):900–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Mühlebach MD, Mateo M, Sinn PL, Prüfer S, Uhlig KM, Leonard VHJ, et al. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature. 2011;480(7378):530–3.

    Article  PubMed  PubMed Central  Google Scholar 

  166. Noyce RS, Bondre DG, Ha MN, Lin LT, Sisson G, Tsao MS, et al. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 2011;7(8): e1002240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Tatsuo H, Ono N, Tanaka K, Yanagi Y. SLAM (CDw150) is a cellular receptor for measles virus. Nature. 2000;406(6798):893–7.

    Article  CAS  PubMed  Google Scholar 

  168. Dörig RE, Marcil A, Chopra A, Richardson CD. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell. 1993;75(2):295–305.

    Article  PubMed  Google Scholar 

  169. Naniche D, Varior-Krishnan G, Cervoni F, Wild TF, Rossi B, Rabourdin-Combe C, et al. Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol. 1993;67(10):6025–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Measles vaccines: WHO position paper—April 2017. Wkly Epidemiol Rec. 2017;92(17):205–27.

  171. Measles. 2019. https://www.who.int/news-room/fact-sheets/detail/measles. Accessed 17 Jan 2022.

  172. Lundstrom K. Self-replicating vehicles based on negative strand RNA viruses. Cancer Gene Ther. 2022;15:1–14.

    Google Scholar 

  173. Reyes-del Valle J, de la Fuente C, Turner MA, Springfeld C, Apte-Sengupta S, Frenzke ME, et al. Broadly neutralizing immune responses against hepatitis C virus induced by vectored measles viruses and a recombinant envelope protein booster. J Virol. 2012;86(21):11558–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Radecke F, Spielhofer P, Schneider H, Kaelin K, Huber M, Dötsch C, et al. Rescue of measles viruses from cloned DNA. EMBO J. 1995;14(23):5773–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Devaux P, von Messling V, Songsungthong W, Springfeld C, Cattaneo R. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology. 2007;360(1):72–83.

    Article  CAS  PubMed  Google Scholar 

  176. Combredet C, Labrousse V, Mollet L, Lorin C, Delebecque F, Hurtrel B, et al. A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J Virol. 2003;77(21):11546–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Reyes-del Valle J, Hodge G, McChesney MB, Cattaneo R. Protective anti-hepatitis B virus responses in Rhesus monkeys primed with a vectored measles virus and boosted with a single dose of hepatitis B surface antigen. J Virol. 2009;83(17):9013–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Reyes del Valle J, Devaux P, Hodge G, Wegner NJ, McChesney MB, Cattaneo R. A Vectored measles virus induces hepatitis B surface antigen antibodies while protecting macaques against measles virus challenge. J Virol. 2007;81(19):10597–605.

  179. Zuniga A, Wang Z, Liniger M, Hangartner L, Caballero M, Pavlovic J, et al. Attenuated measles virus as a vaccine vector. Vaccine. 2007;25(16):2974–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Naim HY. Measles virus. Hum Vaccin Immunother. 2015;11(1):21–6.

    Article  PubMed  Google Scholar 

  181. Engeland CE, Ungerechts G. Measles virus as an oncolytic immunotherapy. Cancers (Basel). 2021;13(3):544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Nakamura T, Hummel H-D, Harvey M, Greiner S, Topp M, Russell SJ. Fully retargeted, myeloma-specific oncolytic measles viruses. Blood. 2005;106(11):3478.

    Google Scholar 

  183. Leonard VH, Sinn PL, Hodge G, Miest T, Devaux P, Oezguen N, et al. Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. J Clin Invest. 2008;118(7):2448–58.

    CAS  PubMed  PubMed Central  Google Scholar 

  184. Schneider U, Bullough F, Vongpunsawad S, Russell SJ, Cattaneo R. Recombinant measles viruses efficiently entering cells through targeted receptors. J Virol. 2000;74(21):9928–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Vongpunsawad S, Oezgun N, Braun W, Cattaneo R. Selectively receptor-blind measles viruses: identification of residues necessary for SLAM- or CD46-induced fusion and their localization on a new hemagglutinin structural model. J Virol. 2004;78(1):302–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Iankov ID, Penheiter AR, Griesmann GE, Carlson SK, Federspiel MJ, Galanis E. Neutralization capacity of measles virus H protein specific IgG determines the balance between antibody-enhanced infectivity and protection in microglial cells. Virus Res. 2013;172(1–2):15–23.

    Article  CAS  PubMed  Google Scholar 

  187. Hadac EM, Peng KW, Nakamura T, Russell SJ. Reengineering paramyxovirus tropism. Virology. 2004;329(2):217–25.

    Article  CAS  PubMed  Google Scholar 

  188. Rallabandi R, Sharp B, Cruz C, Wang Q, Locsin A, Driscoll CB, et al. MiRNA-mediated control of exogenous OCT4 during mesenchymal-epithelial transition increases measles vector reprogramming efficiency. Mol Ther Methods Clin Dev. 2021;24:48–61.

    Article  PubMed  PubMed Central  Google Scholar 

  189. Hiramoto T, Tahara M, Liao J, Soda Y, Miura Y, Kurita R, et al. Non-transmissible MV vector with segmented RNA genome establishes different types of iPSCs from hematopoietic cells. Mol Ther. 2020;28(1):129–41.

    Article  CAS  PubMed  Google Scholar 

  190. Takeda M, Nakatsu Y, Ohno S, Seki F, Tahara M, Hashiguchi T, et al. Generation of measles virus with a segmented RNA genome. J Virol. 2006;80(9):4242–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Tahara M, Takeda M, Seki F, Hashiguchi T, Yanagi Y. Multiple amino acid substitutions in hemagglutinin are necessary for wild-type measles virus to acquire the ability to use receptor CD46 efficiently. J Virol. 2007;81(6):2564–72.

    Article  CAS  PubMed  Google Scholar 

  192. Tahara M, Takeda M, Yanagi Y. Altered interaction of the matrix protein with the cytoplasmic tail of hemagglutinin modulates measles virus growth by affecting virus assembly and cell-cell fusion. J Virol. 2007;81(13):6827–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Schirrmacher V, Fournier P. Newcastle disease virus: a promising vector for viral therapy, immune therapy, and gene therapy of cancer. Methods Mol Biol. 2009;542:565–605.

    Article  CAS  PubMed  Google Scholar 

  194. Zhao H, Peeters BPH. Recombinant Newcastle disease virus as a viral vector: effect of genomic location of foreign gene on gene expression and virus replication. J Gen Virol. 2003;84(Pt 4):781–8.

    Article  CAS  PubMed  Google Scholar 

  195. Bukreyev A, Collins PL. Newcastle disease virus as a vaccine vector for humans. Curr Opin Mol Ther. 2008;10(1):46–55.

    CAS  PubMed  Google Scholar 

  196. Kim S-H, Samal SK. Newcastle disease virus as a vaccine vector for development of human and veterinary vaccines. Viruses. 2016;8(7):183.

    Article  PubMed Central  Google Scholar 

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Correspondence to Patricia Devaux.

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RR is supported by the Mayo Clinic Center for Regenerative Medicine and the Michael S. and Mary Sue Shannon Foundation.

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Sharp, B., Rallabandi, R. & Devaux, P. Advances in RNA Viral Vector Technology to Reprogram Somatic Cells: The Paramyxovirus Wave. Mol Diagn Ther 26, 353–367 (2022). https://doi.org/10.1007/s40291-022-00599-x

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