Oncolytic parvoviruses: From basic virology to clinical applications

Virology Journal

Volumn 12, Issue 1, 2015, Pages

  Marchini, Antonio ^a   Bonifati, Serena ^a   Scott, Eleanor M ^a   Angelova, Assia L ^a   Rommelaere, Jean ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Glioblastoma multiforme; Oncolytic parvoviruses; Oncolytic virotherapy clinical trial; Parvovirus based cancer virotherapy; Parvovirus based combination therapy; Parvovirus based oncolytic vectors; Rodent protoparvovirus

Indexed keywords

ANTINEOPLASTIC AGENT; ATM PROTEIN; CAPSID PROTEIN; CYCLIN A; CYCLIN B1; CYCLINE; CYSTATIN B; CYSTATIN C; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; GAMMA INTERFERON; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 3; ONCOLYTIC PARVOVIRUS; PHOSPHOLIPASE A2; PROTEIN VP1; PROTEIN VP2; REACTIVE OXYGEN METABOLITE; REPLICATION FACTOR A; VIRUS DNA; ONCOLYTIC VIRUS;

ACETYLATION; AMINO TERMINAL SEQUENCE; APOPTOSIS; BREAST CARCINOMA; CANCER CELL; CARBOXY TERMINAL SEQUENCE; CD8+ T LYMPHOCYTE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; COLON CARCINOMA; CYTOKINE PRODUCTION; CYTOPLASM; CYTOTOXICITY; DNA DAMAGE; DNA REPLICATION; DOWN REGULATION; DRUG EFFICACY; ENDOPLASMIC RETICULUM; G2 PHASE CELL CYCLE CHECKPOINT; GLIOBLASTOMA; H-1 PARVOVIRUS; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; LIFE CYCLE; LIVER CELL CARCINOMA; LYMPHOMA; MELANOMA; NATURAL KILLER CELL; NEUROECTODERM TUMOR; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; ONCOLYTIC VIROTHERAPY; OPEN READING FRAME; PANCREAS CARCINOMA; PARVOVIRUS INFECTION; PROMOTER REGION; REVIEW; SPLEEN CELL; STOMACH CARCINOMA; TRANSCRIPTION INITIATION; UTERINE CERVIX CARCINOMA; VIRION; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS REPLICATION; WILD TYPE; ANIMAL; NEOPLASMS; PARVOVIRIDAE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHYSIOLOGY; PROCEDURES;

H-1 PARVOVIRUS; MINUTE VIRUS OF MICE; PARVOVIRIDAE; PARVOVIRUS; RATTUS; RODENTIA;

ANIMALS; CLINICAL TRIALS, PHASE I AS TOPIC; CLINICAL TRIALS, PHASE II AS TOPIC; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PARVOVIRUS;

EID: 84924121307     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/s12985-014-0223-y     Document Type: Review

References (113)

1. Kelly E, Russell SJ: History of oncolytic viruses: genesis to genetic engineering. Mol Ther 2007, 15:651-659.
2. Russell SJ, Peng KW, Bell JC: Oncolytic virotherapy. Nat Biotechnol 2012, 30:658-670.
3. Miest TS, Cattaneo R: New viruses for cancer therapy: meeting clinical needs. Nat Rev Microbiol 2014, 12:23-34.
4. Hughes T, Coffin R, Lilley C, Ponce R, Kaufman H: Critical analysis of an oncolytic herpesvirus encoding granulocyte-macrophage colony stimulating factor for the treatment of malignant melanoma. Oncolytic Virotherapy 2014, 3:11-20.
5. Kyula JN, Roulstone V, Karapanagiotou EM, Melcher AA, Harrington KJ: Oncolytic reovirus type 3 (Dearing) as a novel therapy in head and neck cancer. Expert Opin Biol Ther 2012, 12:1669-1678.
6. Heo J, Reid T, Ruo L, Breitbach CJ, Rose S, Bloomston M, Cho M, Lim HY, Chung HC, Kim CW, Daneshmand M, Dubois K, Longpre L, Ngo M, Rooney C, Bell JC, Rhee BG, Patt R, Hwang TH, Kirn DH: Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat Med 2013, 19:329-336.
7. Cotmore SF, Agbandje-McKenna M, Chiorini JA, Mukha DV, Pintel DJ, Qiu J, Soderlund-Venermo M, Tattersall P, Tijssen P, Gatherer D, Davison AJ: The family Parvoviridae. Arch Virol 2014, 159:1239-1247.
8. Cotmore SF, Tattersall P: Parvoviral host range and cell entry mechanisms. Adv Virus Res 2007, 70:183-232.
9. Halder S, Nam HJ, Govindasamy L, Vogel M, Dinsart C, Salome N, McKenna R, Agbandje-McKenna M: Structural characterization of H-1 parvovirus: comparison of infectious virions to empty capsids. J Virol 2013, 87:5128-5140.
10. Nuesch JP, Lacroix J, Marchini A, Rommelaere J: Molecular pathways: rodent parvoviruses-mechanisms of oncolysis and prospects for clinical cancer treatment. Clin Cancer Res 2012, 18:3516-3523.
11. Nuesch JP, Tattersall P: Nuclear targeting of the parvoviral replicator molecule NS1: evidence for self-association prior to nuclear transport. Virology 1993, 196:637-651.
12. Lorson C, Burger LR, Mouw M, Pintel DJ: Efficient transactivation of the minute virus of mice P38 promoter requires upstream binding of NS1. J Virol 1996, 70:834-842.
13. Li J, Bonifati S, Hristov G, Marttila T, Valmary-Degano S, Stanzel S, Schnolzer M, Mougin C, Aprahamian M, Grekova SP, Raykov Z, Rommelaere J, Marchini A: Synergistic combination of valproic acid and oncolytic parvovirus H-1PV as a potential therapy against cervical and pancreatic carcinomas. EMBO Mol Med 2013, 5:1537-1555.
14. Morita E, Nakashima A, Asao H, Sato H, Sugamura K: Human parvovirus B19 nonstructural protein (NS1) induces cell cycle arrest at G (1) phase. J Virol 2003, 77:2915-2921.
15. Op De Beeck A, Sobczak-Thepot J, Sirma H, Bourgain F, Brechot C, Caillet-Fauquet P: NS1- and minute virus of mice-induced cell cycle arrest: involvement of p53 and p21 (cip1). J Virol 2001, 75:11071-11078.
16. Hristov G, Kramer M, Li J, El-Andaloussi N, Mora R, Daeffler L, Zentgraf H, Rommelaere J, Marchini A: Through its nonstructural protein NS1, Parvovirus H-1 induces apoptosis via accumulation of reactive oxygen species. J Virol 2010, 84:5909-5922.
17. Engelsma D, Valle N, Fish A, Salome N, Almendral JM, Fornerod M: A supraphysiological nuclear export signal is required for parvovirus nuclear export. Mol Biol Cell 2008, 19:2544-2552.
18. Zadori Z, Szelei J, Tijssen P: SAT: a late NS protein of porcine parvovirus. J Virol 2005, 79:13129-13138.
19. Vihinen-Ranta M, Wang D, Weichert WS, Parrish CR: The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J Virol 2002, 76:1884-1891.
20. Tullis GE, Burger LR, Pintel DJ: The trypsin-sensitive RVER domain in the capsid proteins of minute virus of mice is required for efficient cell binding and viral infection but not for proteolytic processing in vivo. Virology 1992, 191:846-857.
21. Canaan S, Zadori Z, Ghomashchi F, Bollinger J, Sadilek M, Moreau ME, Tijssen P, Gelb MH: Interfacial enzymology of parvovirus phospholipases A2. J Biol Chem 2004, 279:14502-14508.
22. Suikkanen S, Antila M, Jaatinen A, Vihinen-Ranta M, Vuento M: Release of canine parvovirus from endocytic vesicles. Virology 2003, 316:267-280.
23. Dorsch S, Liebisch G, Kaufmann B, Von Landenberg P, Hoffmann JH, Drobnik W, Modrow S: The VP1 unique region of parvovirus B19 and its constituent phospholipase A2-like activity. J Virol 2002, 76:2014-2018.
24. Zadori Z, Szelei J, Lacoste MC, Li Y, Gariepy S, Raymond P, Allaire M, Nabi IR, Tijssen P: A viral phospholipase A2 is required for parvovirus infectivity. Dev Cell 2001, 1:291-302.
25. Weichert WS, Parker JS, Wahid AT, Chang SF, Meier E, Parrish CR: Assaying for structural variation in the parvovirus capsid and its role in infection. Virology 1998, 250:106-117.
26. Parker JS, Murphy WJ, Wang D, O'Brien SJ, Parrish CR: Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J Virol 2001, 75:3896-3902.
27. Lopez-Bueno A, Rubio MP, Bryant N, McKenna R, Agbandje-McKenna M, Almendral JM: Host-selected amino acid changes at the sialic acid binding pocket of the parvovirus capsid modulate cell binding affinity and determine virulence. J Virol 2006, 80:1563-1573.
28. Allaume X, El-Andaloussi N, Leuchs B, Bonifati S, Kulkarni A, Marttila T, Kaufmann JK, Nettelbeck DM, Kleinschmidt J, Rommelaere J, Marchini A: Retargeting of rat parvovirus H-1PV to cancer cells through genetic engineering of the viral capsid. J Virol 2012, 86:3452-3465.
29. Halder S, Cotmore S, Heimburg-Molinaro J, Smith DF, Cummings RD, Chen X, Trollope AJ, North SJ, Haslam SM, Dell A, Tattersall P, McKenna R, Agbandje-McKenna M: Profiling of glycan receptors for minute virus of mice in permissive cell lines towards understanding the mechanism of cell recognition. PLoS One 2014, 9:e86909.
30. Vihinen-Ranta M, Suikkanen S, Parrish CR: Pathways of cell infection by parvoviruses and adeno-associated viruses. J Virol 2004, 78:6709-6714.
31. Suikkanen S, Saajarvi K, Hirsimaki J, Valilehto O, Reunanen H, Vihinen-Ranta M, Vuento M: Role of recycling endosomes and lysosomes in dyneindependent entry of canine parvovirus. J Virol 2002, 76:4401-4411.
32. Parker JS, Parrish CR: Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J Virol 2000, 74:1919-1930.
33. Nuesch JP, Lachmann S, Rommelaere J: Selective alterations of the host cell architecture upon infection with parvovirus minute virus of mice. Virology 2005, 331:159-174.
34. Porwal M, Cohen S, Snoussi K, Popa-Wagner R, Anderson F, Dugot-Senant N, Wodrich H, Dinsart C, Kleinschmidt JA, Pante N, Kann M: Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis. PLoS Pathog 2013, 9:e1003671.
35. Bashir T, Horlein R, Rommelaere J, Willwand K: Cyclin A activates the DNA polymerase delta -dependent elongation machinery in vitro: a parvovirus DNA replication model. Proc Natl Acad Sci U S A 2000, 97:5522-5527.
36. Christensen J, Tattersall P: Parvovirus initiator protein NS1 and RPA coordinate replication fork progression in a reconstituted DNA replication system. J Virol 2002, 76:6518-6531.
37. Deleu L, Pujol A, Faisst S, Rommelaere J: Activation of promoter P4 of the autonomous parvovirus minute virus of mice at early S phase is required for productive infection. J Virol 1999, 73:3877-3885.
38. Op De Beeck A, Anouja F, Mousset S, Rommelaere J, Caillet-Fauquet P: The nonstructural proteins of the autonomous parvovirus minute virus of mice interfere with the cell cycle, inducing accumulation in G2. Cell Growth Differ 1995, 6:781-787.
39. Adeyemi RO, Fuller MS, Pintel DJ: Efficient parvovirus replication requires CRL4Cdt2-targeted depletion of p21 to prevent its inhibitory interaction with PCNA. PLoS Pathog 2014, 10:e1004055.
40. Bar S, Daeffler L, Rommelaere J, Nuesch JP: Vesicular egress of non-enveloped lytic parvoviruses depends on gelsolin functioning. PLoS Pathog 2008, 4:e1000126.
41. Bar S, Rommelaere J, Nuesch JP: Vesicular transport of progeny parvovirus particles through ER and Golgi regulates maturation and cytolysis. PLoS Pathog 2013, 9:e1003605.
42. Adeyemi RO, Pintel DJ: Replication of minute virus of mice in murine cells is facilitated by virally induced depletion of p21. J Virol 2012, 86:8328-8332.
43. Bashir T, Rommelaere J, Cziepluch C: In vivo accumulation of cyclin A and cellular replication factors in autonomous parvovirus minute virus of mice-associated replication bodies. J Virol 2001, 75:4394-4398.
44. Adeyemi RO, Landry S, Davis ME, Weitzman MD, Pintel DJ: Parvovirus minute virus of mice induces a DNA damage response that facilitates viral replication. PLoS Pathog 2010, 6:e1001141.
45. Ruiz Z, Mihaylov IS, Cotmore SF, Tattersall P: Recruitment of DNA replication and damage response proteins to viral replication centers during infection with NS2 mutants of Minute Virus of Mice (MVM). Virology 2011, 410:375-384.
46. Op De Beeck A, Caillet-Fauquet P: The NS1 protein of the autonomous parvovirus minute virus of mice blocks cellular DNA replication: a consequence of lesions to the chromatin? J Virol 1997, 71:5323-5329.
47. Adeyemi RO, Pintel DJ: Parvovirus-induced depletion of cyclin B1 prevents mitotic entry of infected cells. PLoS Pathog 2014, 10:e1003891.
48. Lacroix J, Leuchs B, Li J, Hristov G, Deubzer HE, Kulozik AE, Rommelaere J, Schlehofer JR, Witt O: Parvovirus H1 selectively induces cytotoxic effects on human neuroblastoma cells. Int J Cancer 2010, 127:1230-1239.
49. Sieben M, Herzer K, Zeidler M, Heinrichs V, Leuchs B, Schuler M, Cornelis JJ, Galle PR, Rommelaere J, Moehler M: Killing of p53-deficient hepatoma cells by parvovirus H-1 and chemotherapeutics requires promyelocytic leukemia protein. World J Gastroenterol 2008, 14:3819-3828.
50. Ohshima T, Iwama M, Ueno Y, Sugiyama F, Nakajima T, Fukamizu A, Yagami K: Induction of apoptosis in vitro and in vivo by H-1 parvovirus infection. J Gen Virol 1998, 79(Pt 12):3067-3071.
51. Rayet B, Lopez-Guerrero JA, Rommelaere J, Dinsart C: Induction of programmed cell death by parvovirus H-1 in U937 cells: connection with the tumor necrosis factor alpha signalling pathway. J Virol 1998, 72:8893-8903.
52. Di Piazza M, Mader C, Geletneky K, Herrero YCM, Weber E, Schlehofer J, Deleu L, Rommelaere J: Cytosolic activation of cathepsins mediates parvovirus H-1-induced killing of cisplatin and TRAIL-resistant glioma cells. J Virol 2007, 81:4186-4198.
53. Chen AY, Qiu J: Parvovirus infection-induced cell death and cell cycle arrest. Future Virol 2010, 5:731-743.
54. Ran Z, Rayet B, Rommelaere J, Faisst S: Parvovirus H-1-induced cell death: influence of intracellular NAD consumption on the regulation of necrosis and apoptosis. Virus Res 1999, 65:161-174.
55. Nuesch JP, Rommelaere J: A viral adaptor protein modulating casein kinase II activity induces cytopathic effects in permissive cells. Proc Natl Acad Sci U S A 2007, 104:12482-12487.
56. Lachmann S, Bar S, Rommelaere J, Nuesch JP: Parvovirus interference with intracellular signalling: mechanism of PKCeta activation in MVM-infected A9 fibroblasts. Cell Microbiol 2008, 10:755-769.
57. Mousset S, Ouadrhiri Y, Caillet-Fauquet P, Rommelaere J: The cytotoxicity of the autonomous parvovirus minute virus of mice nonstructural proteins in FR3T3 rat cells depends on oncogene expression. J Virol 1994, 68:6446-6453.
58. Chen YQ, De Foresta F, Hertoghs J, Avalosse BL, Cornelis JJ, Rommelaere J: Selective killing of simian virus 40-transformed human fibroblasts by parvovirus H-1. Cancer Res 1986, 46:3574-3579.
59. Rommelaere J, Geletneky K, Angelova AL, Daeffler L, Dinsart C, Kiprianova I, Schlehofer JR, Raykov Z: Oncolytic parvoviruses as cancer therapeutics. Cytokine Growth Factor Rev 2010, 21:185-195.
60. Grekova S, Zawatzky R, Horlein R, Cziepluch C, Mincberg M, Davis C, Rommelaere J, Daeffler L: Activation of an antiviral response in normal but not transformed mouse cells: a new determinant of minute virus of mice oncotropism. J Virol 2010, 84:516-531.
61. Paglino JC, Andres W, Van Den Pol AN: Autonomous parvoviruses neither stimulate nor are inhibited by the type I interferon response in human normal or cancer cells. J Virol 2014, 88:4932-4942.
62. Nuesch JP, Rommelaere J: Tumor suppressing properties of rodent parvovirus NS1 proteins and their derivatives. Adv Exp Med Biol 2014, 818:99-124.
63. Grekova SP, Raykov Z, Zawatzky R, Rommelaere J, Koch U: Activation of a glioma-specific immune response by oncolytic parvovirus minute virus of mice infection. Cancer Gene Ther 2012, 19:468-475.
64. Moehler MH, Zeidler M, Wilsberg V, Cornelis JJ, Woelfel T, Rommelaere J, Galle PR, Heike M: 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 2005, 16:996-1005.
65. Angelova AL, Grekova SP, Heller A, Kuhlmann O, Soyka E, Giese T, Aprahamian M, Bour G, Ruffer S, Cziepluch C, Daeffler L, Rommelaere J, Werner J, Raykov Z, Giese NA: Complementary induction of immunogenic cell death by oncolytic parvovirus H-1PV and gemcitabine in pancreatic cancer. J Virol 2014, 88:5263-5276.
66. Bhat R, Rommelaere J: 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 2013, 13:367.
67. Raykov Z, Grekova S, Galabov AS, Balboni G, Koch U, Aprahamian M, Rommelaere J: Combined oncolytic and vaccination activities of parvovirus H-1 in a metastatic tumor model. Oncol Rep 2007, 17:1493-1499.
68. Grekova SP, Aprahamian M, Giese NA, Bour G, Giese T, Grewenig A, Leuchs B, Hörlein R, Heller A, Angelova AL, Rommelaere J, Raykov Z: Genomic CpG enrichment of oncolytic parvoviruses as a potent anticancer vaccination strategy for the treatment of pancreatic adenocarcinoma. J Vaccines Vaccin 2014, 5:2.
69. Grekova SP, Aprahamian M, Daeffler L, Leuchs B, Angelova A, Giese T, Galabov A, Heller A, Giese NA, Rommelaere J, Raykov Z: Interferon gamma improves the vaccination potential of oncolytic parvovirus H-1PV for the treatment of peritoneal carcinomatosis in pancreatic cancer. Cancer Biol Ther 2011, 12:888-895.
70. Grekova S, Aprahamian M, Giese N, Schmitt S, Giese T, Falk CS, Daeffler L, Cziepluch C, Rommelaere J, Raykov Z: 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 2010, 10:1280-1289.
71. Lang SI, Giese NA, Rommelaere J, Dinsart C, Cornelis JJ: Humoral immune responses against minute virus of mice vectors. J Gene Med 2006, 8:1141-1150.
72. McKisic MD, Macy JD Jr, Delano ML, Jacoby RO, Paturzo FX, Smith AL: Mouse parvovirus infection potentiates allogeneic skin graft rejection and induces syngeneic graft rejection. Transplantation 1998, 65:1436-1446.
73. Guglielmino S, Tempera G, Pappalardo G, Castro A: H-1 and X14 parvovirus antibodies in women with abortions or still-births. Acta Virol 1978, 22:426-428.
74. Miller CG, Fraser NW: Requirement of an integrated immune response for successful neuroattenuated HSV-1 therapy in an intracranial metastatic melanoma model. Mol Ther 2003, 7:741-747.
75. Diaz RM, Galivo F, Kottke T, Wongthida P, Qiao J, Thompson J, Valdes M, Barber G, Vile RG: Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res 2007, 67:2840-2848.
76. Geletneky K, Huesing J, Rommelaere J, Schlehofer JR, Leuchs B, Dahm M, Krebs O, Von Knebel DM, Huber B, Hajda J: 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 2012, 12:99.
77. Herrero YCM, Cornelis JJ, Herold-Mende C, Rommelaere J, Schlehofer JR, Geletneky K: Parvovirus H-1 infection of human glioma cells leads to complete viral replication and efficient cell killing. Int J Cancer 2004, 109:76-84.
78. Geletneky K, Hartkopf AD, Krempien R, Rommelaere J, Schlehofer JR: Improved killing of human high-grade glioma cells by combining ionizing radiation with oncolytic parvovirus H-1 infection. J Biomed Biotechnol 2010, 2010:350748.
79. Geletneky K, Herrero YCM, Rommelaere J, Schlehofer JR: Oncolytic potential of rodent parvoviruses for cancer therapy in humans: a brief review. J Vet Med B Infect Dis Vet Public Health 2005, 52:327-330.
80. Kiprianova I, Thomas N, Ayache A, Fischer M, Leuchs B, Klein M, Rommelaere J, Schlehofer JR: Regression of glioma in rat models by intranasal application of parvovirus h-1. Clin Cancer Res 2011, 17:5333-5342.
81. Paglino JC, Ozduman K, Van Den Pol AN: LuIII parvovirus selectively and efficiently targets, replicates in, and kills human glioma cells. J Virol 2012, 86:7280-7291.
82. Yu L, Baxter PA, Zhao X, Liu Z, Wadhwa L, Zhang Y, Su JM, Tan X, Yang J, Adesina A, Perlaky L, Hurwitz M, Idamakanti N, Police SR, Hallenbeck PL, Blaney SM, Chintagumpala M, Hurwitz RL, Li XN: A single intravenous injection of oncolytic picornavirus SVV-001 eliminates medulloblastomas in primary tumor-based orthotopic xenograft mouse models. Neuro Oncol 2011, 13:14-27.
83. Studebaker AW, Hutzen B, Pierson CR, Russell SJ, Galanis E, Raffel C: Oncolytic measles virus prolongs survival in a murine model of cerebral spinal fluid-disseminated medulloblastoma. Neuro Oncol 2012, 14:459-470.
84. Lacroix J, Schlund F, Leuchs B, Adolph K, Sturm D, Bender S, Hielscher T, Pfister SM, Witt O, Rommelaere J, Schlehofer JR, Witt H: Oncolytic effects of parvovirus H-1 in medulloblastoma are associated with repression of master regulators of early neurogenesis. Int J Cancer 2014, 134:703-716.
85. Angelova AL, Aprahamian M, Balboni G, Delecluse HJ, Feederle R, Kiprianova I, Grekova SP, Galabov AS, Witzens-Harig M, Ho AD, Rommelaere J, Raykov Z: Oncolytic rat parvovirus H-1PV, a candidate for the treatment of human lymphoma: In vitro and in vivo studies. Mol Ther 2009, 17:1164-1172.
86. Dupressoir T, Vanacker JM, Cornelis JJ, Duponchel N, Rommelaere J: 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 1989, 49:3203-3208.
87. Muharram G, Le Rhun E, Loison I, Wizla P, Richard A, Martin N, Roussel A, Begue A, Devos P, Baranzelli MC, Bonneterre J, Caillet-Fauquet P, Stehelin D: Parvovirus H-1 induces cytopathic effects in breast carcinoma-derived cultures. Breast Cancer Res Treat 2010, 121:23-33.
88. Van Pachterbeke C, Tuynder M, Cosyn JP, Lespagnard L, Larsimont D, Rommelaere J: Parvovirus H-1 inhibits growth of short-term tumorderived but not normal mammary tissue cultures. Int J Cancer 1993, 55:672-677.
89. Van Pachterbeke C, Tuynder M, Brandenburger A, Leclercq G, Borras M, Rommelaere J: Varying sensitivity of human mammary carcinoma cells to the toxic effect of parvovirus H-1. Eur J Cancer 1997, 33:1648-1653.
90. Shi X, Liu S, Kleeff J, Friess H, Buchler MW: Acquired resistance of pancreatic cancer cells towards 5-Fluorouracil and gemcitabine is associated with altered expression of apoptosis-regulating genes. Oncology 2002, 62:354-362.
91. Angelova AL, Aprahamian M, Grekova SP, Hajri A, Leuchs B, Giese NA, Dinsart C, Herrmann A, Balboni G, Rommelaere J, Raykov Z: Improvement of gemcitabine-based therapy of pancreatic carcinoma by means of oncolytic parvovirus H-1PV. Clin Cancer Res 2009, 15:511-519.
92. Massague J, Gomis RR: The logic of TGFbeta signaling. FEBS Lett 2006, 580:2811-2820.
93. Dempe S, Stroh-Dege AY, Schwarz E, Rommelaere J, Dinsart C: SMAD4: a predictive marker of PDAC cell permissiveness for oncolytic infection with parvovirus H-1PV. Int J Cancer 2010, 126:2914-2927.
94. Bhat R, Dempe S, Dinsart C, Rommelaere J: Enhancement of NK cell antitumor responses using an oncolytic parvovirus. Int J Cancer 2011, 128:908-919.
95. Lorusso D, Petrelli F, Coinu A, Raspagliesi F, Barni S: A systematic review comparing cisplatin and carboplatin plus paclitaxel-based chemotherapy for recurrent or metastatic cervical cancer. Gynecol Oncol 2014, 117:123.
96. Faisst S, Guittard D, Benner A, Cesbron JY, Schlehofer JR, Rommelaere J, Dupressoir T: Dose-dependent regression of HeLa cell-derived tumours in SCID mice after parvovirus H-1 infection. Int J Cancer 1998, 75:584-589.
97. Liu J, Ran ZH, Xiao SD, Rommelaere J: Changes in gene expression profiles induced by parvovirus H-1 in human gastric cancer cells. Chin J Dig Dis 2005, 6:72-81.
98. Wang YY, Liu J, Zheng Q, Ran ZH, Salome N, Vogel M, Rommelaere J, Xiao SD, Wang Z: Effect of the parvovirus H-1 non-structural protein NS1 on the tumorigenicity of human gastric cancer cells. J Dig Dis 2012, 13:366-373.
99. Moehler M, Blechacz B, Weiskopf N, Zeidler M, Stremmel W, Rommelaere J, Galle PR, Cornelis JJ: 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 2001, 8:158-167.
100. Li J, Werner E, Hergenhahn M, Poirey R, Luo Z, Rommelaere J, Jauniaux JC: Expression profiling of human hepatoma cells reveals global repression of genes involved in cell proliferation, growth, and apoptosis upon infection with parvovirus H-1. J Virol 2005, 79:2274-2286.
101. Shi ZY, Ma CW, Huang J, Lin WM, Dong RC, Luo ZY: Inhibition of parvovirus H-1 on transplantable human hepatoma and its histological and histobiochemical studies. Shi Yan Sheng Wu Xue Bao 1997, 30:247-259.
102. Malerba M, Daeffler L, Rommelaere J, Iggo RD: Replicating parvoviruses that target colon cancer cells. J Virol 2003, 77:6683-6691.
103. Geletneky K, Kiprianova I, Ayache A, Koch R, Herrero YCM, Deleu L, Sommer C, Thomas N, Rommelaere J, Schlehofer JR: Regression of advanced rat and human gliomas by local or systemic treatment with oncolytic parvovirus H-1 in rat models. Neuro Oncol 2010, 12:804-814.
104. Piao Y, Jiang H, Alemany R, Krasnykh V, Marini FC, Xu J, Alonso MM, Conrad CA, Aldape KD, Gomez-Manzano C, Fueyo J: Oncolytic adenovirus retargeted to Delta-EGFR induces selective antiglioma activity. Cancer Gene Ther 2009, 16:256-265.
105. El-Andaloussi N, Bonifati S, Kaufmann JK, Mailly L, Daeffler L, Deryckere F, Nettelbeck DM, Rommelaere J, Marchini A: Generation of an adenovirusparvovirus chimera with enhanced oncolytic potential. J Virol 2012, 86:10418-10431.
106. Raykov Z, Grekova S, Leuchs B, Aprahamian M, Rommelaere J: Arming parvoviruses with CpG motifs to improve their oncosuppressive capacity. Int J Cancer 2008, 122:2880-2884.
107. Friedel CC, Haas J: Virus-host interactomes and global models of virus-infected cells. Trends Microbiol 2011, 19:501-508.
108. Mahoney DJ, Lefebvre C, Allan K, Brun J, Sanaei CA, Baird S, Pearce N, Gronberg S, Wilson B, Prakesh M, Aman A, Isaac M, Mamai A, Uehling D, Al-Awar R, Falls T, Alain T, Stojdl DF: Virus-tumor interactome screen reveals ER stress response can reprogram resistant cancers for oncolytic virus-triggered caspase-2 cell death. Cancer Cell 2011, 20:443-456.
109. Passer BJ, Cheema T, Zhou B, Wakimoto H, Zaupa C, Razmjoo M, Sarte J, Wu S, Wu CL, Noah JW, Li Q, Buolamwini JK, Yen Y, Rabkin SD, Martuza RL: Identification of the ENT1 antagonists dipyridamole and dilazep as amplifiers of oncolytic herpes simplex virus-1 replication. Cancer Res 2010, 70:3890-3895.
110. Diallo JS, Le Boeuf F, Lai F, Cox J, Vaha-Koskela M, Abdelbary H, MacTavish H, Waite K, Falls T, Wang J, Brown R, Blanchard JE, Brown ED, Kirn DH, Hiscott J, Atkins H, Lichty BD, Bell JC: A high-throughput pharmacoviral approach identifies novel oncolytic virus sensitizers. Mol Ther 2010, 18:1123-1129.
111. Siolas D, Hannon GJ: Patient-derived tumor xenografts: transforming clinical samples into mouse models. Cancer Res 2013, 73:5315-5319.
112. Ito R, Takahashi T, Katano I, Ito M: Current advances in humanized mouse models. Cell Mol Immunol 2012, 9:208-214.
113. Wege AK, Ernst W, Eckl J, Frankenberger B, Vollmann-Zwerenz A, Mannel DN, Ortmann O, Kroemer A, Brockhoff G: Humanized tumor mice-a new model to study and manipulate the immune response in advanced cancer therapy. Int J Cancer J Int Du Cancer 2011, 129:2194-2206.