Activation of the human immune system by chemotherapeutic or targeted agents combined with the oncolytic parvovirus H-1

BMC Cancer

Volumn 11, Issue , 2011, Pages

  Moehler, Markus ^a   Sieben, Maike ^a   Roth, Susanne ^a   Springsguth, Franziska ^a   Leuchs, Barbara ^b   Zeidler, Maja ^a   Dinsart, Christiane ^b   Rommelaere, Jean ^b   Galle, Peter R ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; HLA A2 ANTIGEN; INTERLEUKIN 6; NONSTRUCTURAL PROTEIN 1; ONCOLYTIC PARVOVIRUS; ONCOLYTIC PARVOVIRUS H 1; SUNITINIB; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VINCRISTINE; ANTINEOPLASTIC AGENT; CYTOKINE; ONCOLYTIC VIRUS; VIRUS PROTEIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL LYSATE; CELL MATURATION; CELL VIABILITY; COCULTURE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG POTENTIATION; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INFLAMMATION; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MELANOMA CELL; MONOTHERAPY; ONCOLYTIC VIROTHERAPY; PHAGOCYTOSIS; PROTEIN EXPRESSION; TUMOR CELL DESTRUCTION; BIOLOGICAL MODEL; CELL SURVIVAL; H-1 PARVOVIRUS; MELANOMA; METABOLISM; METHODOLOGY; MULTIMODALITY CANCER THERAPY; PARVOVIRUS INFECTION; PHYSIOLOGY; SKIN TUMOR; TUMOR CELL CULTURE; VIROLOGY;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL SURVIVAL; COMBINED MODALITY THERAPY; CYTOKINES; H-1 PARVOVIRUS; HUMANS; MELANOMA; MODELS, BIOLOGICAL; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PARVOVIRIDAE INFECTIONS; SKIN NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR CELLS, CULTURED; VIRAL PROTEINS;

EID: 82955239884     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-11-464     Document Type: Article

References (62)

1. Chan CW, Housseau F. The 'kiss of death' by dendritic cells to cancer cells. Cell Death Differ 2008, 15:58-69. 10.1038/sj.cdd.4402235, 17948029.
2. van Mierlo GJ, Boonman ZF, Dumortier HM, den Boer AT, Fransen MF, Nouta J, van der Voort EI, Offringa R, Toes RE, Melief CJ. Activation of dendritic cells that cross-present tumor-derived antigen licenses CD8+ CTL to cause tumor eradication. J Immunol 2004, 173:6753-6759.
3. Janeway CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002, 20:197-216. 10.1146/annurev.immunol.20.083001.084359, 11861602.
4. Chalikonda S, Kivlen MH, O'Malley ME, Eric Dong XD, McCart JA, Gorry MC, Yin XY, Brown CK, Zeh HJ, Guo ZS, Bartlett DL. Oncolytic virotherapy for ovarian carcinomatosis using a replication-selective vaccinia virus armed with a yeast cytosine deaminase gene. Cancer Gene Ther 2008, 15:115-125. 10.1038/sj.cgt.7701110, 2975702, 18084242.
5. Mace AT, Harrow SJ, Ganly I, Brown SM. Cytotoxic effects of the oncolytic herpes simplex virus HSV1716 alone and in combination with cisplatin in head and neck squamous cell carcinoma. Acta Otolaryngol 2007, 127:880-887. 10.1080/00016480601075381, 17763002.
6. 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. 10.1089/hum.2005.16.996, 16076257.
7. Kay MA, Glorioso JC, Naldini L. Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat Med 2001, 7:33-40. 10.1038/83324, 11135613.
8. 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. 10.1038/sj.cgt.7700288, 11332986.
9. Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 2003, 4:346-358. 10.1038/nrg1066, 12728277.
10. Moehler M, Zeidler M, Schede J, Rommelaere J, Galle PR, Cornelis JJ, Heike M. 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 2003, 10:477-480. 10.1038/sj.cgt.7700591, 12768193.
11. 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. 10.3748/wjg.14.3819, 2721438, 18609705.
12. 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. 10.1016/j.cytogfr.2010.02.011, 20211577.
13. Bhat R, Dempe S, Dinsart C, Rommelaere J. Enhancement of NK cell antitumor responses using an oncolytic parvovirus. Int J Cancer 128:908-919.
14. Angelova AL, Aprahamian M, Balboni G, Delecluse HJ, Feederle R, Kiprianova I, Grekova SP, Galabov AS, Witzens-Harig M, Ho AD, et al. 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. 10.1038/mt.2009.78, 2835199, 19367260.
15. 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 10:1280-1289.
16. Cornelis JJ, Lang SI, Stroh-Dege AY, Balboni G, Dinsart C, Rommelaere J. Cancer gene therapy through autonomous parvovirus--mediated gene transfer. Curr Gene Ther 2004, 4:249-261.
17. Malerba M, Daeffler L, Rommelaere J, Iggo RD. Replicating parvoviruses that target colon cancer cells. J Virol 2003, 77:6683-6691. 10.1128/JVI.77.12.6683-6691.2003, 156172, 12767988.
18. Wetzel K, Menten P, Opdenakker G, Van Damme J, Grone HJ, Giese N, Vecchi A, Sozzani S, Cornelis JJ, Rommelaere J, Dinsart C. Transduction of human MCP-3 by a parvoviral vector induces leukocyte infiltration and reduces growth of human cervical carcinoma cell xenografts. J Gene Med 2001, 3:326-337.
19. Olijslagers S, Dege AY, Dinsart C, Voorhoeve M, Rommelaere J, Noteborn MH, Cornelis JJ. Potentiation of a recombinant oncolytic parvovirus by expression of Apoptin. Cancer Gene Ther 2001, 8:958-965. 10.1038/sj.cgt.7700392, 11781658.
20. Christensen JG. A preclinical review of sunitinib, a multitargeted receptor tyrosine kinase inhibitor with anti-angiogenic and antitumour activities. Ann Oncol 2007, 18(Suppl 10):x3-10.
21. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008, 359:378-390. 10.1056/NEJMoa0708857, 18650514.
22. Lennerz V, Fatho M, Gentilini C, Frye RA, Lifke A, Ferel D, Wolfel C, Huber C, Wolfel T. The response of autologous T cells to a human melanoma is dominated by mutated neoantigens. Proc Natl Acad Sci USA 2005, 102:16013-16018. 10.1073/pnas.0500090102, 1266037, 16247014.
23. Wang Z, Seliger B, Mike N, Momburg F, Knuth A, Ferrone S. Molecular analysis of the HLA-A2 antigen loss by melanoma cells SK-MEL-29.1.22 and SK-MEL-29.1.29. Cancer Res 1998, 58:2149-2157.
24. Wolfel T, Van Pel A, Brichard V, Schneider J, Seliger B, Meyer zum Buschenfelde KH, Boon T. Two tyrosinase nonapeptides recognized on HLA-A2 melanomas by autologous cytolytic T lymphocytes. Eur J Immunol 1994, 24:759-764. 10.1002/eji.1830240340, 8125142.
25. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 2000, 192:1213-1222. 10.1084/jem.192.9.1213, 2193357, 11067871.
26. Wrzesinski C, Tesfay L, Salome N, Jauniaux JC, Rommelaere J, Cornelis J, Dinsart C. Chimeric and pseudotyped parvoviruses minimize the contamination of recombinant stocks with replication-competent viruses and identify a DNA sequence that restricts parvovirus H-1 in mouse cells. J Virol 2003, 77:3851-3858. 10.1128/JVI.77.6.3851-3858.2003, 149498, 12610161.
27. Faisst S, Faisst SR, Dupressoir T, Plaza S, Pujol A, Jauniaux JC, Rhode SL, Rommelaere J. Isolation of a fully infectious variant of parvovirus H-1 supplanting the standard strain in human cells. J Virol 1995, 69:4538-4543. 189201, 7769719.
28. Jonuleit H, Giesecke A, Kandemir A, Paragnik L, Knop J, Enk AH. Induction of tumor peptide-specific cytotoxic T cells under serum-free conditions by mature human dendritic cells. Arch Dermatol Res 2000, 292:325-332. 10.1007/s004030000144, 10966056.
29. 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 84:5909-5922.
30. Rommelaere J, Cornelis JJ. Autonomous Parvoviruses. Monographs in Virology 2001, 22:100-129.
31. Algarra I, Cabrera T, Garrido F. The HLA crossroad in tumor immunology. Hum Immunol 2000, 61:65-73. 10.1016/S0198-8859(99)00156-1, 10658979.
32. Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 2001, 19:47-64. 10.1146/annurev.immunol.19.1.47, 11244030.
33. Duverger V, Sartorius U, Klein-Bauernschmitt P, Krammer PH, Schlehofer JR. Enhancement of cisplatin-induced apoptosis by infection with adeno-associated virus type 2. Int J Cancer 2002, 97:706-712. 10.1002/ijc.10077, 11807802.
34. Cinatl J, Cinatl J, Michaelis M, Kabickova H, Kotchetkov R, Vogel JU, Doerr HW, Klingebiel T, Driever PH. Potent oncolytic activity of multimutated herpes simplex virus G207 in combination with vincristine against human rhabdomyosarcoma. Cancer Res 2003, 63:1508-1514.
35. Lyros O, Mueller A, Heidel F, Schimanski CC, Gockel I, Galle PR, Lang H, Moehler M. Analysis of anti-proliferative and chemosensitizing effects of sunitinib on human esophagogastric cancer cells: Synergistic interaction with vandetanib via inhibition of multi-receptor tyrosine kinase pathways. Int J Cancer 2009,
36. Wagner AD, Moehler M. Development of targeted therapies in advanced gastric cancer: promising exploratory steps in a new era. Curr Opin Oncol 2009, 21:381-385. 10.1097/CCO.0b013e32832c42e0, 19412098.
37. Enderlin M, Kleinmann EV, Struyf S, Buracchi C, Vecchi A, Kinscherf R, Kiessling F, Paschek S, Sozzani S, Rommelaere J, et al. TNF-alpha and the IFN-gamma-inducible protein 10 (IP-10/CXCL-10) delivered by parvoviral vectors act in synergy to induce antitumor effects in mouse glioblastoma. Cancer Gene Ther 2009, 16:149-160. 10.1038/cgt.2008.62, 18670452.
38. 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. 10.1158/1078-0432.CCR-08-1088, 19147756.
39. Cepeda V, Fuertes MA, Castilla J, Alonso C, Quevedo C, Perez JM. Biochemical mechanisms of cisplatin cytotoxicity. Anticancer Agents Med Chem 2007, 7:3-18. 10.2174/187152007779314044, 17266502.
40. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat Rev Cancer 2004, 4:253-265. 10.1038/nrc1317, 15057285.
41. Tuve S, Racek T, Niemetz A, Schultz J, Soengas MS, Putzer BM. Adenovirus-mediated TA-p73beta gene transfer increases chemosensitivity of human malignant melanomas. Apoptosis 2006, 11:235-243. 10.1007/s10495-006-3407-0, 16502261.
42. Lee JH, Roh MS, Lee YK, Kim MK, Han JY, Park BH, Trown P, Kirn DH, Hwang TH. Oncolytic and immunostimulatory efficacy of a targeted oncolytic poxvirus expressing human GM-CSF following intravenous administration in a rabbit tumor model. Cancer Gene Ther 2010, 17:73-79. 10.1038/cgt.2009.50, 2834359, 19629143.
43. McCart JA, Puhlmann M, Lee J, Hu Y, Libutti SK, Alexander HR, Bartlett DL. Complex interactions between the replicating oncolytic effect and the enzyme/prodrug effect of vaccinia-mediated tumor regression. Gene Ther 2000, 7:1217-1223. 10.1038/sj.gt.3301237, 10918490.
44. Freytag SO, Stricker H, Pegg J, Paielli D, Pradhan DG, Peabody J, DePeralta-Venturina M, Xia X, Brown S, Lu M, Kim JH. Phase I study of replication-competent adenovirus-mediated double-suicide gene therapy in combination with conventional-dose three-dimensional conformal radiation therapy for the treatment of newly diagnosed, intermediate-to high-risk prostate cancer. Cancer Res 2003, 63:7497-7506.
45. Khuri FR, Nemunaitis J, Ganly I, Arseneau J, Tannock IF, Romel L, Gore M, Ironside J, MacDougall RH, Heise C, et al. a controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat Med 2000, 6:879-885. 10.1038/78638, 10932224.
46. Lamfers ML, Fulci G, Gianni D, Tang Y, Kurozumi K, Kaur B, Moeniralm S, Saeki Y, Carette JE, Weissleder R, et al. Cyclophosphamide increases transgene expression mediated by an oncolytic adenovirus in glioma-bearing mice monitored by bioluminescence imaging. Mol Ther 2006, 14:779-788. 10.1016/j.ymthe.2006.08.008, 2819149, 16996314.
47. Wakimoto H, Fulci G, Tyminski E, Chiocca EA. Altered expression of antiviral cytokine mRNAs associated with cyclophosphamide's enhancement of viral oncolysis. Gene Ther 2004, 11:214-223. 10.1038/sj.gt.3302143, 2825886, 14712306.
48. Lun XQ, Jang JH, Tang N, Deng H, Head R, Bell JC, Stojdl DF, Nutt CL, Senger DL, Forsyth PA, McCart JA. Efficacy of systemically administered oncolytic vaccinia virotherapy for malignant gliomas is enhanced by combination therapy with rapamycin or cyclophosphamide. Clin Cancer Res 2009, 15:2777-2788. 10.1158/1078-0432.CCR-08-2342, 19351762.
49. Thomas MA, Spencer JF, Toth K, Sagartz JE, Phillips NJ, Wold WS. Immunosuppression enhances oncolytic adenovirus replication and antitumor efficacy in the Syrian hamster model. Mol Ther 2008, 16:1665-1673. 10.1038/mt.2008.162, 18665155.
50. Kottke T, Thompson J, Diaz RM, Pulido J, Willmon C, Coffey M, Selby P, Melcher A, Harrington K, Vile RG. Improved systemic delivery of oncolytic reovirus to established tumors using preconditioning with cyclophosphamide-mediated Treg modulation and interleukin-2. Clin Cancer Res 2009, 15:561-569. 10.1158/1078-0432.CCR-08-1688, 3046733, 19147761.
51. Chen G, Zhou J, Gao Q, Huang X, Li K, Zhuang L, Huang M, Xu G, Wang S, Lu Y, Ma D. Oncolytic adenovirus-mediated transfer of the antisense chk2 selectively inhibits tumor growth in vitro and in vivo. Cancer Gene Ther 2006, 13:930-939. 10.1038/sj.cgt.7700967, 16741520.
52. Zhou J, Gao Q, Chen G, Huang X, Lu Y, Li K, Xie D, Zhuang L, Deng J, Ma D. Novel oncolytic adenovirus selectively targets tumor-associated polo-like kinase 1 and tumor cell viability. Clin Cancer Res 2005, 11:8431-8440. 10.1158/1078-0432.CCR-05-1085, 16322306.
53. Motta I, Andre F, Lim A, Tartaglia J, Cox WI, Zitvogel L, Angevin E, Kourilsky P. Cross-presentation by dendritic cells of tumor antigen expressed in apoptotic recombinant canarypox virus-infected dendritic cells. J Immunol 2001, 167:1795-1802.
54. Prestwich RJ, Errington F, Steele LP, Ilett EJ, Morgan RS, Harrington KJ, Pandha HS, Selby PJ, Vile RG, Melcher AA. Reciprocal human dendritic cell-natural killer cell interactions induce antitumor activity following tumor cell infection by oncolytic reovirus. J Immunol 2009, 183:4312-4321. 10.4049/jimmunol.0901074, 19734207.
55. Rolle A, Olweus J. Dendritic cells in cytomegalovirus infection: viral evasion and host countermeasures. Apmis 2009, 117:413-426. 10.1111/j.1600-0463.2009.02449.x, 19400865.
56. Ramakrishna E, Woller N, Mundt B, Knocke S, Gurlevik E, Saborowski M, Malek N, Manns MP, Wirth T, Kuhnel F, Kubicka S. Antitumoral immune response by recruitment and expansion of dendritic cells in tumors infected with telomerase-dependent oncolytic viruses. Cancer Res 2009, 69:1448-1458. 10.1158/0008-5472.CAN-08-1160, 19190348.
57. Berwin B, Reed RC, Nicchitta CV. Virally induced lytic cell death elicits the release of immunogenic GRP94/gp96. J Biol Chem 2001, 276:21083-21088. 10.1074/jbc.M101836200, 11279246.
58. Kaneno R, Shurin GV, Tourkova IL, Shurin MR. Chemomodulation of human dendritic cell function by antineoplastic agents in low noncytotoxic concentrations. J Transl Med 2009, 7:58. 10.1186/1479-5876-7-58, 2716306, 19591684.
59. Pandha HS, Heinemann L, Simpson GR, Melcher A, Prestwich R, Errington F, Coffey M, Harrington KJ, Morgan R. Synergistic effects of oncolytic reovirus and cisplatin chemotherapy in murine malignant melanoma. Clin Cancer Res 2009, 15:6158-6166. 10.1158/1078-0432.CCR-09-0796, 19773377.
60. Hipp MM, Hilf N, Walter S, Werth D, Brauer KM, Radsak MP, Weinschenk T, Singh-Jasuja H, Brossart P. Sorafenib, but not sunitinib, affects function of dendritic cells and induction of primary immune responses. Blood 2008, 111:5610-5620. 10.1182/blood-2007-02-075945, 18310500.
61. Finke JH, Rini B, Ireland J, Rayman P, Richmond A, Golshayan A, Wood L, Elson P, Garcia J, Dreicer R, Bukowski R. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin Cancer Res 2008, 14:6674-6682. 10.1158/1078-0432.CCR-07-5212, 18927310.
62. Blattman JN, Greenberg PD. Cancer immunotherapy: a treatment for the masses. Science 2004, 305:200-205. 10.1126/science.1100369, 15247469.