1932

Abstract

Autonomous rodent protoparvoviruses (PVs) are promising anticancer agents due to their excellent safety profile, natural oncotropism, and oncosuppressive activities. Viral infection can trigger immunogenic cell death, activating the immune system against the tumor. However, the efficacy of this treatment in recent clinical trials is moderate compared with results seen in preclinical work. Various strategies have been employed to improve the anticancer activities of oncolytic PVs, including development of second-generation parvoviruses with enhanced oncolytic and immunostimulatory activities and rational combination of PVs with other therapies. Understanding the cellular factors involved in the PV life cycle is another important area of investigation. Indeed, these studies may lead to the identification of biomarkers that would allow a more personalized use of PV-based therapies. This review focuses on this work and the challenges that still need to be overcome to move PVs forward into clinical practice as an effective therapeutic option for cancer patients.

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2020-09-29
2024-05-18
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Literature Cited

  1. 1. 
    Kelly E, Russell SJ. 2007. History of oncolytic viruses: genesis to genetic engineering. Mol. Ther. 15:651–59
    [Google Scholar]
  2. 2. 
    Kaufman HL, Kohlhapp FJ, Zloza A 2015. Oncolytic viruses: a new class of immunotherapy drugs. Nat. Rev. Drug Discov. 14:642–62
    [Google Scholar]
  3. 3. 
    Achard C, Surendran A, Wedge ME, Ungerechts G, Bell J, Ilkow CS 2018. Lighting a fire in the tumor microenvironment using oncolytic immunotherapy. EBioMedicine 31:17–24
    [Google Scholar]
  4. 4. 
    Marchini A, Daeffler L, Pozdeev VI, Angelova A, Rommelaere J 2019. Immune conversion of tumor microenvironment by oncolytic viruses: the protoparvovirus H-1PV case study. Front. Immunol. 10:1848
    [Google Scholar]
  5. 5. 
    Zamarin D, Holmgaard RB, Subudhi SK, Park JS, Mansour M et al. 2014. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci. Transl. Med. 6:226ra32
    [Google Scholar]
  6. 6. 
    Guedan S, Alemany R. 2018. CAR-T cells and oncolytic viruses: joining forces to overcome the solid tumor challenge. Front. Immunol. 9:2460
    [Google Scholar]
  7. 7. 
    Chiocca EA, Rabkin SD. 2014. Oncolytic viruses and their application to cancer immunotherapy. Cancer Immunol. Res. 2:295–300
    [Google Scholar]
  8. 8. 
    Ottolino-Perry K, Diallo JS, Lichty BD, Bell JC, McCart JA 2010. Intelligent design: combination therapy with oncolytic viruses. Mol. Ther. 18:251–63
    [Google Scholar]
  9. 9. 
    Wennier ST, Liu J, McFadden G 2012. Bugs and drugs: oncolytic virotherapy in combination with chemotherapy. Curr. Pharm. Biotechnol. 13:1817–33
    [Google Scholar]
  10. 10. 
    Marchini A, Scott EM, Rommelaere J 2016. Overcoming barriers in oncolytic virotherapy with HDAC inhibitors and immune checkpoint blockade. Viruses 8:e9
    [Google Scholar]
  11. 11. 
    Fountzilas C, Patel S, Mahalingam D 2017. Review: oncolytic virotherapy, updates and future directions. Oncotarget 8:102617–39
    [Google Scholar]
  12. 12. 
    Conry RM, Westbrook B, McKee S, Norwood TG 2018. Talimogene laherparepvec: first in class oncolytic virotherapy. Hum. Vaccin. Immunother. 14:839–46
    [Google Scholar]
  13. 13. 
    Lawler SE, Speranza MC, Cho CF, Chiocca EA 2017. Oncolytic viruses in cancer treatment: a review. JAMA Oncol 3:841–49
    [Google Scholar]
  14. 14. 
    Eissa IR, Bustos-Villalobos I, Ichinose T, Matsumura S, Naoe Y et al. 2018. The current status and future prospects of oncolytic viruses in clinical trials against melanoma, glioma, pancreatic, and breast cancers. Cancers 10:356
    [Google Scholar]
  15. 15. 
    Keller BA, Bell JC. 2016. Oncolytic viruses—immunotherapeutics on the rise. J. Mol. Med. 94:979–91
    [Google Scholar]
  16. 16. 
    Lichty BD, Breitbach CJ, Stojdl DF, Bell JC 2014. Going viral with cancer immunotherapy. Nat. Rev. Cancer 14:559–67
    [Google Scholar]
  17. 17. 
    LaRocca CJ, Warner SG. 2018. Oncolytic viruses and checkpoint inhibitors: combination therapy in clinical trials. Clin. Transl. Med. 7:35
    [Google Scholar]
  18. 18. 
    Durham NM, Mulgrew K, McGlinchey K, Monks NR, Ji H et al. 2017. Oncolytic VSV primes differential responses to immuno-oncology therapy. Mol. Ther. 25:1917–32
    [Google Scholar]
  19. 19. 
    Liu Z, Ravindranathan R, Kalinski P, Guo ZS, Bartlett DL 2017. Rational combination of oncolytic vaccinia virus and PD-L1 blockade works synergistically to enhance therapeutic efficacy. Nat. Commun. 8:14754
    [Google Scholar]
  20. 20. 
    Woller N, Gurlevik E, Fleischmann-Mundt B, Schumacher A, Knocke S et al. 2015. Viral infection of tumors overcomes resistance to PD-1-immunotherapy by broadening neoantigenome-directed T-cell responses. Mol. Ther. 23:1630–40
    [Google Scholar]
  21. 21. 
    Samson A, Scott KJ, Taggart D, West EJ, Wilson E et al. 2018. Intravenous delivery of oncolytic reovirus to brain tumor patients immunologically primes for subsequent checkpoint blockade. Sci. Transl. Med. 10:eaam7577
    [Google Scholar]
  22. 22. 
    Bourgeois-Daigneault MC, Roy DG, Aitken AS, El Sayes N, Martin NT et al. 2018. Neoadjuvant oncolytic virotherapy before surgery sensitizes triple-negative breast cancer to immune checkpoint therapy. Sci. Transl. Med. 10:eaao1641
    [Google Scholar]
  23. 23. 
    Chesney J, Puzanov I, Collichio F, Singh P, Milhem MM et al. 2018. Randomized, open-label phase II study evaluating the efficacy and safety of talimogene laherparepvec in combination with ipilimumab versus ipilimumab alone in patients with advanced, unresectable melanoma. J. Clin. Oncol. 36:1658–67
    [Google Scholar]
  24. 24. 
    Puzanov I, Milhem MM, Minor D, Hamid O, Li A et al. 2016. Talimogene laherparepvec in combination with ipilimumab in previously untreated, unresectable stage IIIB-IV melanoma. J. Clin. Oncol. 34:2619–26
    [Google Scholar]
  25. 25. 
    Dummer R, Hoeller C, Gruter IP, Michielin O 2017. Combining talimogene laherparepvec with immunotherapies in melanoma and other solid tumors. Cancer Immunol. Immunother. 66:683–95
    [Google Scholar]
  26. 26. 
    Toolan HW. 1967. Lack of oncogenic effect of the H-viruses for hamsters. Nature 214:10366
    [Google Scholar]
  27. 27. 
    Toolan HW, Dalldore G, Barclay M, Chandra S, Moore AE 1960. An unidentified, filtrable agent isolated from transplanted human tumors. PNAS 46:1256–58
    [Google Scholar]
  28. 28. 
    Toolan HW, Ledinko N. 1968. Inhibition by H-1 virus of the incidence of tumors produced by adenovirus 12 in hamsters. Virology 35:475–78
    [Google Scholar]
  29. 29. 
    Toolan HW, Rhode SL, Gierthy JF 1982. Inhibition of 7,12-dimethylbenz(a)anthracene-induced tumors in Syrian hamsters by prior infection with H-1 parvovirus. Cancer Res 42:2552
    [Google Scholar]
  30. 30. 
    Angelova AL, Aprahamian M, Grekova SP, Hajri A, Leuchs B et al. 2009. Improvement of gemcitabine-based therapy of pancreatic carcinoma by means of oncolytic parvovirus H-1PV. Clin. Cancer Res. 15:511–19
    [Google Scholar]
  31. 31. 
    Di Piazza M, Mader C, Geletneky K, Herrero YCM, Weber E et al. 2007. Cytosolic activation of cathepsins mediates parvovirus H-1-induced killing of cisplatin and TRAIL-resistant glioma cells. J. Virol. 81:4186–98
    [Google Scholar]
  32. 32. 
    Dupressoir T, Vanacker JM, Cornelis JJ, Duponchel N, Rommelaere J 1989. Inhibition by parvovirus H-1 of the formation of tumors in nude mice and colonies in vitro by transformed human mammary epithelial cells. Cancer Res 49:3203–8
    [Google Scholar]
  33. 33. 
    Herrero YCM, Cornelis JJ, Herold-Mende C, Rommelaere J, Schlehofer JR, Geletneky K 2004. Parvovirus H-1 infection of human glioma cells leads to complete viral replication and efficient cell killing. Int. J. Cancer 109:76–84
    [Google Scholar]
  34. 34. 
    Hristov G, Kramer M, Li J, El-Andaloussi N, Mora R et al. 2010. Through its nonstructural protein NS1, parvovirus H-1 induces apoptosis via accumulation of reactive oxygen species. J. Virol. 84:5909–22
    [Google Scholar]
  35. 35. 
    Moehler MH, Zeidler M, Wilsberg V, Cornelis JJ, Woelfel T et al. 2005. Parvovirus H-1-induced tumor cell death enhances human immune response in vitro via increased phagocytosis, maturation, and cross-presentation by dendritic cells. Hum. Gene Ther. 16:996–1005
    [Google Scholar]
  36. 36. 
    Geletneky K, Huesing J, Rommelaere J, Schlehofer JR, Leuchs B et al. 2012. Phase I/IIa study of intratumoral/intracerebral or intravenous/intracerebral administration of Parvovirus H-1 (ParvOryx) in patients with progressive primary or recurrent glioblastoma multiforme: ParvOryx01 protocol. BMC Cancer 12:99
    [Google Scholar]
  37. 37. 
    Geletneky K, Kiprianova I, Ayache A, Koch R, Herrero YCM et al. 2010. Regression of advanced rat and human gliomas by local or systemic treatment with oncolytic parvovirus H-1 in rat models. Neuro Oncol 12:804–14
    [Google Scholar]
  38. 38. 
    Li J, Bonifati S, Hristov G, Marttila T, Valmary-Degano S et al. 2013. Synergistic combination of valproic acid and oncolytic parvovirus H-1PV as a potential therapy against cervical and pancreatic carcinomas. EMBO Mol. Med. 5:1537–55
    [Google Scholar]
  39. 39. 
    Hajda J, Lehmann M, Krebs O, Kieser M, Geletneky K et al. 2017. A non-controlled, single arm, open label, phase II study of intravenous and intratumoral administration of ParvOryx in patients with metastatic, inoperable pancreatic cancer: ParvOryx02 protocol. BMC Cancer 17:576
    [Google Scholar]
  40. 40. 
    Geletneky K, Hajda J, Angelova AL, Leuchs B, Capper D et al. 2017. Oncolytic H-1 parvovirus shows safety and signs of immunogenic activity in a first phase I/IIa glioblastoma trial. Mol. Ther. 25:2620–34
    [Google Scholar]
  41. 41. 
    Caillet-Fauquet P, Perros M, Brandenburger A, Spegelaere P, Rommelaere J 1990. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J 9:2989–95
    [Google Scholar]
  42. 42. 
    Cotmore SF, Tattersall P. 2007. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70:183–232
    [Google Scholar]
  43. 43. 
    Cotmore SF, Agbandje-McKenna M, Chiorini JA, Mukha DV, Pintel DJ et al. 2014. The family Parvoviridae. Arch. . Virol 159:1239–47
    [Google Scholar]
  44. 44. 
    Cotmore SF, Agbandje-McKenna M, Canuti M, Chiorini JA, Eis-Hubinger AM et al. 2019. ICTV virus taxonomy profile: Parvoviridae. J. Gen. Virol. 100:367–68
    [Google Scholar]
  45. 45. 
    Angelova AL, Geletneky K, Nüesch JP, Rommelaere J 2015. Tumor selectivity of oncolytic parvoviruses: from in vitro and animal models to cancer patients. Front. Bioeng. Biotech. 3:55
    [Google Scholar]
  46. 46. 
    Bretscher C, Marchini A. 2019. H-1 parvovirus as a cancer-killing agent: past, present, and future. Viruses 11:e562
    [Google Scholar]
  47. 47. 
    Marchini A, Bonifati S, Scott EM, Angelova AL, Rommelaere J 2015. Oncolytic parvoviruses: from basic virology to clinical applications. Virol. J. 12:6
    [Google Scholar]
  48. 48. 
    Nüesch JP, Lacroix J, Marchini A, Rommelaere J 2012. Molecular pathways: rodent parvoviruses—mechanisms of oncolysis and prospects for clinical cancer treatment. Clin. Cancer Res. 18:3516–23
    [Google Scholar]
  49. 49. 
    Deleu L, Pujol A, Faisst S, Rommelaere J 1999. Activation of promoter P4 of the autonomous parvovirus minute virus of mice at early S phase is required for productive infection. J. Virol. 73:3877–85
    [Google Scholar]
  50. 50. 
    Bashir T, Horlein R, Rommelaere J, Willwand K 2000. Cyclin A activates the DNA polymerase δ-dependent elongation machinery in vitro: a parvovirus DNA replication model. PNAS 97:5522–27
    [Google Scholar]
  51. 51. 
    Bar S, Rommelaere J, Nüesch JP 2015. PKCη/Rdx-driven phosphorylation of PDK1: a novel mechanism promoting cancer cell survival and permissiveness for parvovirus-induced lysis. PLOS Pathog 11:e1004703
    [Google Scholar]
  52. 52. 
    Lachmann S, Bar S, Rommelaere J, Nüesch JP 2008. Parvovirus interference with intracellular signalling: mechanism of PKCη activation in MVM-infected A9 fibroblasts. Cell Microbiol 10:755–69
    [Google Scholar]
  53. 53. 
    Salome N, van Hille B, Geuskens M, Rommelaere J 1989. Partial reversion of conditional transformation correlates with a decrease in the sensitivity of rat cells to killing by the parvovirus minute virus of mice but not in their capacity for virus production: effect of a temperature-sensitive v-src oncogene. J. Virol. 63:4797–807
    [Google Scholar]
  54. 54. 
    Mousset S, Cornelis J, Spruyt N, Rommelaere J 1986. Transformation of established murine fibro-blasts with an activated cellular Harvey-ras oncogene or the polyoma virus middle T gene increases cell permissiveness to parvovirus minute-virus-of-mice. Biochemie 68:951–55
    [Google Scholar]
  55. 55. 
    Gujar S, Pol JG, Kim Y, Lee PW, Kroemer G 2018. Antitumor benefits of antiviral immunity: an underappreciated aspect of oncolytic virotherapies. Trends Immunol 39:209–21
    [Google Scholar]
  56. 56. 
    Paglino JC, Andres W, van den Pol AN 2014. Autonomous parvoviruses neither stimulate nor are inhibited by the type I interferon response in human normal or cancer cells. J. Virol. 88:4932–42
    [Google Scholar]
  57. 57. 
    Angelova A, Rommelaere J. 2019. Immune system stimulation by oncolytic rodent protoparvoviruses. Viruses 11:e415
    [Google Scholar]
  58. 58. 
    Grekova S, Zawatzky R, Horlein R, Cziepluch C, Mincberg M et al. 2010. Activation of an antiviral response in normal but not transformed mouse cells: a new determinant of minute virus of mice oncotropism. J. Virol. 84:516–31
    [Google Scholar]
  59. 59. 
    Allaume X, El-Andaloussi N, Leuchs B, Bonifati S, Kulkarni A et al. 2012. Retargeting of rat parvovirus H-1PV to cancer cells through genetic engineering of the viral capsid. J. Virol. 86:3452–65
    [Google Scholar]
  60. 60. 
    Ros C, Bayat N, Wolfisberg R, Almendral JM 2017. Protoparvovirus cell entry. Viruses 9:313
    [Google Scholar]
  61. 61. 
    Lopez-Bueno A, Rubio MP, Bryant N, McKenna R, Agbandje-McKenna M, Almendral JM 2006. Host-selected amino acid changes at the sialic acid binding pocket of the parvovirus capsid modulate cell binding affinity and determine virulence. J. Virol. 80:1563–73
    [Google Scholar]
  62. 62. 
    Balakrishnan B, Jayandharan GR. 2014. Basic biology of adeno-associated virus (AAV) vectors used in gene therapy. Curr. Gene Ther. 14:86–100
    [Google Scholar]
  63. 63. 
    Pillay S, Carette JE. 2017. Host determinants of adeno-associated viral vector entry. Curr. Opin. Virol. 24:124–31
    [Google Scholar]
  64. 64. 
    Chen AY, Qiu J. 2010. Parvovirus infection-induced cell death and cell cycle arrest. Future Virol 5:731–43
    [Google Scholar]
  65. 65. 
    Op De Beeck A, Caillet-Fauquet P 1997. The NS1 protein of the autonomous parvovirus minute virus of mice blocks cellular DNA replication: a consequence of lesions to the chromatin. ? J. Virol. 71:5323–29
    [Google Scholar]
  66. 66. 
    Adeyemi RO, Landry S, Davis ME, Weitzman MD, Pintel DJ 2010. Parvovirus minute virus of mice induces a DNA damage response that facilitates viral replication. PLOS Pathog 6:e1001141
    [Google Scholar]
  67. 67. 
    Majumder K, Etingov I, Pintel DJ 2017. Protoparvovirus interactions with the cellular DNA damage response. Viruses 9:e323
    [Google Scholar]
  68. 68. 
    Nüesch JP, Lachmann S, Rommelaere J 2005. Selective alterations of the host cell architecture upon infection with parvovirus minute virus of mice. Virology 331:159–74
    [Google Scholar]
  69. 69. 
    Nykky J, Vuento M, Gilbert L 2014. Role of mitochondria in parvovirus pathology. PLOS ONE 9:e86124
    [Google Scholar]
  70. 70. 
    Meszaros I, Toth R, Olasz F, Tijssen P, Zadori Z 2017. The SAT protein of porcine parvovirus accelerates viral spreading through induction of irreversible endoplasmic reticulum stress. J. Virol. 91:e00627-17
    [Google Scholar]
  71. 71. 
    Porwal M, Cohen S, Snoussi K, Popa-Wagner R, Anderson F et al. 2013. Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis. PLOS Pathog 9:e1003671
    [Google Scholar]
  72. 72. 
    Ohshima T, Iwama M, Ueno Y, Sugiyama F, Nakajima T et al. 1998. Induction of apoptosis in vitro and in vivo by H-1 parvovirus infection. J. Gen. Virol. 79:part 123067–71
    [Google Scholar]
  73. 73. 
    Ran Z, Rayet B, Rommelaere J, Faisst S 1999. Parvovirus H-1-induced cell death: influence of intracellular NAD consumption on the regulation of necrosis and apoptosis. Virus Res 65:161–74
    [Google Scholar]
  74. 74. 
    Scherz-Shouval R, Elazar Z. 2007. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol 17:422–27
    [Google Scholar]
  75. 75. 
    Angelova AL, Grekova SP, Heller A, Kuhlmann O, Soyka E et al. 2014. Complementary induction of immunogenic cell death by oncolytic parvovirus H-1PV and gemcitabine in pancreatic cancer. J. Virol. 88:5263–76
    [Google Scholar]
  76. 76. 
    Moehler M, Zeidler M, Schede J, Rommelaere J, Galle PR et al. 2003. Oncolytic parvovirus H1 induces release of heat-shock protein HSP72 in susceptible human tumor cells but may not affect primary immune cells. Cancer Gene Ther 10:477–80
    [Google Scholar]
  77. 77. 
    Grekova SP, Raykov Z, Zawatzky R, Rommelaere J, Koch U 2012. Activation of a glioma-specific immune response by oncolytic parvovirus minute virus of mice infection. Cancer Gene Ther 19:468–75
    [Google Scholar]
  78. 78. 
    Bhat R, Rommelaere J. 2013. NK-cell-dependent killing of colon carcinoma cells is mediated by natural cytotoxicity receptors (NCRs) and stimulated by parvovirus infection of target cells. BMC Cancer 13:367
    [Google Scholar]
  79. 79. 
    Bhat R, Dempe S, Dinsart C, Rommelaere J 2011. Enhancement of NK cell antitumor responses using an oncolytic parvovirus. Int. J. Cancer 128:908–19
    [Google Scholar]
  80. 80. 
    Geletneky K, Nüesch JP, Angelova A, Kiprianova I, Rommelaere J 2015. Double-faceted mechanism of parvoviral oncosuppression. Curr. Opin. Virol. 13:17–24
    [Google Scholar]
  81. 81. 
    Raykov Z, Grekova S, Galabov AS, Balboni G, Koch U et al. 2007. Combined oncolytic and vaccination activities of parvovirus H-1 in a metastatic tumor model. Oncol. Rep. 17:1493–99
    [Google Scholar]
  82. 82. 
    Callaway HM, Feng KH, Lee DW, Allison AB, Pinard M et al. 2017. Parvovirus capsid structures required for infection: mutations controlling receptor recognition and protease cleavages. J. Virol. 91:e01871-16
    [Google Scholar]
  83. 83. 
    Mietzsch M, Penzes JJ, Agbandje-McKenna M 2019. Twenty-five years of structural parvovirology. Viruses 11:e362
    [Google Scholar]
  84. 84. 
    Grueso E, Sanchez-Martinez C, Calvo-Lopez T, de Miguel FJ, Blanco-Menendez N et al. 2019. Antiangiogenic vascular endothelial growth factor-blocking peptides displayed on the capsid of an infectious oncolytic parvovirus: assembly and immune interactions. J. Virol. 93:e00798-19
    [Google Scholar]
  85. 85. 
    Grimm D, Buning H. 2017. Small but increasingly mighty: latest advances in AAV vector research, design, and evolution. Hum. Gene Ther. 28:1075–86
    [Google Scholar]
  86. 86. 
    Paglino J, Tattersall P. 2011. The parvoviral capsid controls an intracellular phase of infection essential for efficient killing of stepwise-transformed human fibroblasts. Virology 416:32–41
    [Google Scholar]
  87. 87. 
    Marr M, D'Abramo A, Pittman N, Agbandje-McKenna M, Cotmore SF, Tattersall P 2018. Optimizing the targeting of mouse parvovirus 1 to murine melanoma selects for recombinant genomes and novel mutations in the viral capsid gene. Viruses 10:e54
    [Google Scholar]
  88. 88. 
    Etingov I, Itah R, Mincberg M, Keren-Naus A, Nam HJ et al. 2008. An extension of the Minute Virus of Mice tissue tropism. Virology 379:245–55
    [Google Scholar]
  89. 89. 
    Weinmann J, Grimm D. 2017. Next-generation AAV vectors for clinical use: an ever-accelerating race. Virus Genes 53:707–13
    [Google Scholar]
  90. 90. 
    El-Andaloussi N, Bonifati S, Kaufmann JK, Mailly L, Daeffler L et al. 2012. Generation of an adenovirus-parvovirus chimera with enhanced oncolytic potential. J. Virol. 86:10418–31
    [Google Scholar]
  91. 91. 
    Hagedorn C, Kreppel F. 2017. Capsid engineering of adenovirus vectors: overcoming early vector-host interactions for therapy. Hum. Gene Ther. 28:820–32
    [Google Scholar]
  92. 92. 
    Lopez-Bueno A, Mateu MG, Almendral JM 2003. High mutant frequency in populations of a DNA virus allows evasion from antibody therapy in an immunodeficient host. J. Virol. 77:2701–8
    [Google Scholar]
  93. 93. 
    Allison AB, Kohler DJ, Ortega A, Hoover EA, Grove DM et al. 2014. Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. PLOS Pathog 10:e1004475
    [Google Scholar]
  94. 94. 
    Faisst S, Faisst SR, Dupressoir T, Plaza S, Pujol A et al. 1995. Isolation of a fully infectious variant of parvovirus H-1 supplanting the standard strain in human cells. J. Virol. 69:4538–43
    [Google Scholar]
  95. 95. 
    Hashemi H, Condurat AL, Stroh-Dege A, Weiss N, Geiss C et al. 2018. Mutations in the non-structural protein-coding sequence of protoparvovirus H-1PV enhance the fitness of the virus and show key benefits regarding the transduction efficiency of derived vectors. Viruses 10:e150
    [Google Scholar]
  96. 96. 
    Weiss N, Stroh-Dege A, Rommelaere J, Dinsart C, Salome N 2012. An in-frame deletion in the NS protein-coding sequence of parvovirus H-1PV efficiently stimulates export and infectivity of progeny virions. J. Virol. 86:7554–64
    [Google Scholar]
  97. 97. 
    Nüesch J, Thomas N, Plotzky C, Jean R 2013. Modified rodent parvovirus capable of propagating and spreading through human gliomas European Patent EP 2 384 761 A1
  98. 98. 
    Daeffler L, Horlein R, Rommelaere J, Nüesch JP 2003. Modulation of minute virus of mice cytotoxic activities through site-directed mutagenesis within the NS coding region. J. Virol. 77:12466–78
    [Google Scholar]
  99. 99. 
    El-Andaloussi N, Endele M, Leuchs B, Bonifati S, Kleinschmidt J et al. 2011. Novel adenovirus-based helper system to support production of recombinant parvovirus. Cancer Gene Ther 18:240–49
    [Google Scholar]
  100. 100. 
    Raykov Z, Grekova S, Leuchs B, Aprahamian M, Rommelaere J 2008. Arming parvoviruses with CpG motifs to improve their oncosuppressive capacity. Int. J. Cancer 122:2880–84
    [Google Scholar]
  101. 101. 
    Grekova SP, Aprahamian M, Giese NA, Bour G, Giese T et al. 2014. Genomic CpG enrichment of oncolytic parvoviruses as a potent anticancer vaccination strategy for the treatment of pancreatic adenocarcinoma. J. Vaccines Vaccin. 5:e1000227
    [Google Scholar]
  102. 102. 
    Illarionova A, Rommelaere J, Leuchs B, Marchini A 2012. Modified parvovirus useful for gene silencing European Patent EP2620503
  103. 103. 
    El-Andaloussi N, Leuchs B, Bonifati S, Rommelaere J, Marchini A 2012. Efficient recombinant parvovirus production with the help of adenovirus-derived systems. J. Vis. Exp. 62:e3518
    [Google Scholar]
  104. 104. 
    Xu P, Wang X, Li Y, Qiu J 2019. Establishment of a parvovirus B19 NS1-expressing recombinant adenoviral vector for killing megakaryocytic leukemia cells. Viruses 11:e820
    [Google Scholar]
  105. 105. 
    Kruger L, Eskerski H, Dinsart C, Cornelis J, Rommelaere J et al. 2008. Augmented transgene expression in transformed cells using a parvoviral hybrid vector. Cancer Gene Ther 15:252–67
    [Google Scholar]
  106. 106. 
    Jimenez-Chavez AJ, Moreno-Fierros L, Bustos-Jaimes I 2019. Therapy with multi-epitope virus-like particles of B19 parvovirus reduce tumor growth and lung metastasis in an aggressive breast cancer mouse model. Vaccine 37:7256–68
    [Google Scholar]
  107. 107. 
    Moehler M, Sieben M, Roth S, Springsguth F, Leuchs B et al. 2011. Activation of the human immune system by chemotherapeutic or targeted agents combined with the oncolytic parvovirus H-1. BMC Cancer 11:464
    [Google Scholar]
  108. 108. 
    Moehler M, Blechacz B, Weiskopf N, Zeidler M, Stremmel W et al. 2001. Effective infection, apoptotic cell killing and gene transfer of human hepatoma cells but not primary hepatocytes by parvovirus H1 and derived vectors. Cancer Gene Ther 8:158–67
    [Google Scholar]
  109. 109. 
    Muharram G, Le Rhun E, Loison I, Wizla P, Richard A et al. 2010. Parvovirus H-1 induces cytopathic effects in breast carcinoma-derived cultures. Breast Cancer Res. Treat. 121:23–33
    [Google Scholar]
  110. 110. 
    Lacroix J, Kis Z, Josupeit R, Schlund F, Stroh-Dege A et al. 2018. Preclinical testing of an oncolytic parvovirus in Ewing sarcoma: Protoparvovirus H-1 induces apoptosis and lytic infection in vitro but fails to improve survival in vivo. Viruses 10:e302
    [Google Scholar]
  111. 111. 
    Liu J, Ran ZH, Xiao SD, Rommelaere J 2005. Changes in gene expression profiles induced by parvovirus H-1 in human gastric cancer cells. Chin. J. Dig. Dis. 6:72–81
    [Google Scholar]
  112. 112. 
    Lacroix J, Leuchs B, Li J, Hristov G, Deubzer HE et al. 2010. Parvovirus H1 selectively induces cytotoxic effects on human neuroblastoma cells. Int. J. Cancer 127:1230–39
    [Google Scholar]
  113. 113. 
    Faisst S, Guittard D, Benner A, Cesbron JY, Schlehofer JR et al. 1998. Dose-dependent regression of HeLa cell-derived tumours in SCID mice after parvovirus H-1 infection. Int. J. Cancer 75:584–89
    [Google Scholar]
  114. 114. 
    Angelova AL, Witzens-Harig M, Galabov AS, Rommelaere J 2017. The oncolytic virotherapy era in cancer management: prospects of applying H-1 parvovirus to treat blood and solid cancers. Front. Oncol. 7:93
    [Google Scholar]
  115. 115. 
    Angelova AL, Aprahamian M, Balboni G, Delecluse HJ, Feederle R et al. 2009. Oncolytic rat parvovirus H-1PV, a candidate for the treatment of human lymphoma: in vitro and in vivo studies. Mol. Ther. 17:1164–72
    [Google Scholar]
  116. 116. 
    Van Pachterbeke C, Tuynder M, Brandenburger A, Leclercq G, Borras M, Rommelaere J 1997. Varying sensitivity of human mammary carcinoma cells to the toxic effect of parvovirus H-1. Eur. J. Cancer 33:1648–53
    [Google Scholar]
  117. 117. 
    Van Pachterbeke C, Tuynder M, Cosyn JP, Lespagnard L, Larsimont D, Rommelaere J 1993. Parvovirus H-1 inhibits growth of short-term tumor-derived but not normal mammary tissue cultures. Int. J. Cancer 55:672–77
    [Google Scholar]
  118. 118. 
    Wang YY, Liu J, Zheng Q, Ran ZH, Salome N et al. 2012. Effect of the parvovirus H-1 non-structural protein NS1 on the tumorigenicity of human gastric cancer cells. J. Dig. Dis. 13:366–73
    [Google Scholar]
  119. 119. 
    Geiss C, Kis Z, Leuchs B, Frank-Stohr M, Schlehofer JR et al. 2017. Preclinical testing of an oncolytic parvovirus: standard protoparvovirus H-1PV efficiently induces osteosarcoma cell lysis in vitro. Viruses 9:e301
    [Google Scholar]
  120. 120. 
    Lacroix J, Schlund F, Leuchs B, Adolph K, Sturm D et al. 2014. Oncolytic effects of parvovirus H-1 in medulloblastoma are associated with repression of master regulators of early neurogenesis. Int. J. Cancer 134:703–16
    [Google Scholar]
  121. 121. 
    Malerba M, Daeffler L, Rommelaere J, Iggo RD 2003. Replicating parvoviruses that target colon cancer cells. J. Virol. 77:6683–91
    [Google Scholar]
  122. 122. 
    Goepfert K, Dinsart C, Rommelaere J, Foerster F, Moehler M 2019. Rational combination of parvovirus H1 with CTLA-4 and PD-1 checkpoint inhibitors dampens the tumor induced immune silencing. Front. Oncol. 9:425
    [Google Scholar]
  123. 123. 
    Geletneky K, Bartsch A, Weiss C, Bernhard H, Marchini A, Rommelaere J 2018. ATIM-40. High rate of objective anti-tumor response in 9 patients with glioblastoma after viro-immunotherapy with oncolytic parvovirus H-1 in combination with Bevacicumab and PD-1 checkpoint blockade. Neuro Oncol 20:vi10
    [Google Scholar]
  124. 124. 
    Ribas A, Dummer R, Puzanov I, VanderWalde A, Andtbacka RHI et al. 2017. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell 170:1109–19
    [Google Scholar]
  125. 125. 
    Geletneky K, Hartkopf AD, Krempien R, Rommelaere J, Schlehofer JR 2010. Therapeutic implications of the enhanced short and long-term cytotoxicity of radiation treatment followed by oncolytic parvovirus H-1 infection in high-grade glioma cells. Bioeng. Bugs 1:429–33
    [Google Scholar]
  126. 126. 
    Marchini A, Li J, Schroeder L, Rommelaere J, Geletneky K 2015. Cancer therapy with a parvovirus combined with a Bcl-2 inhibitor European Patent EP 2 829 284 A1
  127. 127. 
    Grekova SP, Aprahamian M, Daeffler L, Leuchs B, Angelova A et al. 2011. Interferon γ improves the vaccination potential of oncolytic parvovirus H-1PV for the treatment of peritoneal carcinomatosis in pancreatic cancer. Cancer Biol. Ther. 12:888–95
    [Google Scholar]
  128. 128. 
    Johnson DR, O'Neill BP. 2012. Glioblastoma survival in the United States before and during the temozolomide era. J. Neurooncol. 107:359–64
    [Google Scholar]
  129. 129. 
    Geletneky K, Hartkopf AD, Krempien R, Rommelaere J, Schlehofer JR 2010. Improved killing of human high-grade glioma cells by combining ionizing radiation with oncolytic parvovirus H-1 infection. J. Biomed. Biotechnol. 2010 350748
    [Google Scholar]
  130. 130. 
    Paglino JC, Ozduman K, van den Pol AN 2012. LuIII parvovirus selectively and efficiently targets, replicates in, and kills human glioma cells. J. Virol. 86:7280–91
    [Google Scholar]
  131. 131. 
    Abschuetz A, Kehl T, Geibig R, Leuchs B, Rommelaere J, Regnier-Vigouroux A 2006. Oncolytic murine autonomous parvovirus, a candidate vector for glioma gene therapy, is innocuous to normal and immunocompetent mouse glial cells. Cell Tissue Res 325:423–36
    [Google Scholar]
  132. 132. 
    Kiprianova I, Thomas N, Ayache A, Fischer M, Leuchs B et al. 2011. Regression of glioma in rat models by intranasal application of parvovirus H-1. Clin. Cancer Res. 17:5333–42
    [Google Scholar]
  133. 133. 
    Erdo F, Bors LA, Farkas D, Bajza A, Gizurarson S 2018. Evaluation of intranasal delivery route of drug administration for brain targeting. Brain Res. Bull. 143:155–70
    [Google Scholar]
  134. 134. 
    Teague A, Lim KH, Wang-Gillam A 2015. Advanced pancreatic adenocarcinoma: a review of current treatment strategies and developing therapies. Ther. Adv. Med. Oncol. 7:68–84
    [Google Scholar]
  135. 135. 
    Grekova S, Aprahamian M, Giese N, Schmitt S, Giese T et al. 2010. Immune cells participate in the oncosuppressive activity of parvovirus H-1PV and are activated as a result of their abortive infection with this agent. Cancer Biol. Ther. 10:1280–89
    [Google Scholar]
  136. 136. 
    Mestas J, Hughes CC. 2004. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172:2731–38
    [Google Scholar]
  137. 137. 
    Jackson SJ, Thomas GJ. 2017. Human tissue models in cancer research: looking beyond the mouse. Dis. Model. Mech. 10:939–42
    [Google Scholar]
  138. 138. 
    Kloker LD, Yurttas C, Lauer UM 2018. Three-dimensional tumor cell cultures employed in virotherapy research. Oncolytic Virother 7:79–93
    [Google Scholar]
  139. 139. 
    Josupeit R, Bender S, Kern S, Leuchs B, Hielscher T et al. 2016. Pediatric and adult high-grade glioma stem cell culture models are permissive to lytic infection with parvovirus H-1. Viruses 8:e138
    [Google Scholar]
  140. 140. 
    Choi Y, Lee S, Kim K, Kim SH, Chung YJ, Lee C 2018. Studying cancer immunotherapy using patient-derived xenografts (PDXs) in humanized mice. Exp. Mol. Med. 50:99
    [Google Scholar]
  141. 141. 
    Zheng B, Ren T, Huang Y, Sun K, Wang S et al. 2018. PD-1 axis expression in musculoskeletal tumors and antitumor effect of nivolumab in osteosarcoma model of humanized mouse. J. Hematol. Oncol. 11:16
    [Google Scholar]
  142. 142. 
    Freedman JD, Hagel J, Scott EM, Psallidas I, Gupta A et al. 2017. Oncolytic adenovirus expressing bispecific antibody targets T-cell cytotoxicity in cancer biopsies. EMBO Mol. Med. 9:1067–87
    [Google Scholar]
  143. 143. 
    Scott EM, Frost S, Khalique H, Freedman JD, Seymour LW, Lei-Rossmann J 2020. Use of liquid patient ascites fluids as a preclinical model for oncolytic virus activity. Oncolytic Viruses CE Engeland 261–70 New York: Springer
    [Google Scholar]
  144. 144. 
    Geletneky K, Leoni AL, Pohlmeyer-Esch G, Loebhard S, Leuchs B et al. 2015. Bioavailability, biodistribution, and CNS toxicity of clinical-grade parvovirus H1 after intravenous and intracerebral injection in rats. Comp. Med. 65:36–45
    [Google Scholar]
  145. 145. 
    Foreman PM, Friedman GK, Cassady KA, Markert JM 2017. Oncolytic virotherapy for the treatment of malignant glioma. Neurotherapeutics 14:333–44
    [Google Scholar]
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