Oncolytic vesicular stomatitis virus in an immunocompetent model of MUC1-positive or MUC1-null pancreatic ductal adenocarcinoma

Journal of Virology

Volumn 87, Issue 18, 2013, Pages 10283-10294

  Hastie, Eric ^a   Besmer, Dahlia M ^a   Shah, Nirav R ^a   Murphy, Andrea M ^a   Moerdyk Schauwecker, Megan ^a   Molestina, Carlos ^a   Roy, Lopamudra Das ^a   Curry, Jennifer M ^a   Mukherjee, Pinku ^a   Grdzelishvili, Valery Z ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GEMCITABINE; INTERFERON; MUCIN 1; ONCOLYTIC VESICULAR STOMATITIS VIRUS; ONCOLYTIC VIRUS; STAT1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CELL VIABILITY; DRUG EFFICACY; DRUG RESPONSE; HUMORAL IMMUNITY; IMMUNE RESPONSE; MALE; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR VOLUME; VESICULAR STOMATITIS VIRUS; VIRUS REPLICATION;

ADENOCARCINOMA; ANIMALS; BIOLOGICAL THERAPY; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; HUMANS; MALE; MICE; MUCIN-1; ONCOLYTIC VIRUSES; TREATMENT OUTCOME; VESICULOVIRUS;

EID: 84883274264     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01412-13     Document Type: Article

References (89)

1. Tarver T. 2012. Cancer facts & figures 2012. American Cancer Society (ACS). J. Consum. Health Internet 16:366-367.
2. Stathis A, Moore MJ. 2010. Advanced pancreatic carcinoma: current treatment and future challenges. Nat. Rev. Clin. Oncol. 7:163-172.
3. Farrow B, Albo D, Berger DH. 2008. The role of the tumor microenvironment in the progression of pancreatic cancer. J. Surg. Res. 149:319-328.
4. Lindsay TH, Jonas BM, Sevcik MA, Kubota K, Halvorson KG, Ghilardi JR, Kuskowski MA, Stelow EB, Mukherjee P, Gendler SJ, Wong GY, Mantyh PW. 2005. Pancreatic cancer pain and its correlation with changes in tumor vasculature, macrophage infiltration, neuronal innervation, body weight and disease progression. Pain 119:233-246.
5. Jonckheere N, Skrypek S, Van Seuningen I. 2010. Mucins and pancreatic cancer. Cancers 2:1794-1812.
6. Reichert M, Rustgi AK. 2011. Pancreatic ductal cells in development, regeneration, and neoplasia. J. Clin. Invest. 121:4572-4578.
7. Besmer DM, Curry JM, Roy LD, Tinder TL, Sahraei M, Schettini JL, Hwang SI, Lee YY, Gendler SJ, Mukherjee P. 2011. Pancreatic ductal adenocarcinoma (PDA) mice lacking Mucin 1 have a profound defect in tumor growth and metastasis. Cancer Res. 71:4432-4442.
8. Horm TM, Schroeder JA. 2013. MUC1 and metastatic cancer: expression, function and therapeutic targeting. Cell Adh. Migr. 7:187-198.
9. Kalra AV, Campbell RB. 2007. Mucin impedes cytotoxic effect of 5-FU against growth of human pancreatic cancer cells: overcoming cellular barriers for therapeutic gain. Br. J. Cancer 97:910-918.
10. Kalra AV, Campbell RB. 2009. Mucin overexpression limits the effectiveness of 5-FU by reducing intracellular drug uptake and antineoplastic drug effects in pancreatic tumours. Eur. J. Cancer. 45:164-173.
11. Roy LD, Sahraei M, Subramani DB, Besmer D, Nath S, Tinder TL, Bajaj E, Shanmugam K, Lee YY, Hwang SI, Gendler SJ, Mukherjee P. 2011. MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 30:1449-1459.
12. Habte HH, Kotwal GJ, Lotz ZE, Tyler MG, Abrahams M, Rodriques J, Kahn D, Mall AS. 2007. Antiviral activity of purified human breast milk mucin. Neonatology 92:96-104.
13. Habte HH, de Beer C, Lotz ZE, Tyler MG, Kahn D, Mall AS. 2008. Inhibition of human immunodeficiency virus type 1 activity by purified human breast milk mucin (MUC1) in an inhibition assay. Neonatology 93:162-170.
14. Saeland E, de Jong MA, Nabatov AA, Kalay H, Geijtenbeek TB, van Kooyk Y. 2009. MUC1 in human milk blocks transmission of human immunodeficiency virus from dendritic cells to T cells. Mol. Immunol. 46:2309-2316.
15. Kvistgaard AS, Pallesen LT, Arias CF, Lopez S, Petersen TE, Heegaard CW, Rasmussen JT. 2004. Inhibitory effects of human and bovine milk constituents on rotavirus infections. J. Dairy Sci. 87:4088-4096.
16. Walters RW, Pilewski JM, Chiorini JA, Zabner J. 2002. Secreted and transmembrane mucins inhibit gene transfer with AAV4 more efficiently than AAV5. J. Biol. Chem. 277:23709-23713.
17. Hastie E, Grdzelishvili V. 2012. Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer. J. Gen. Virol. 93:2529-2545.
18. Wollmann G, Rogulin V, Simon I, Rose JK, van den Pol AN. 2010. Some attenuated variants of vesicular stomatitis virus show enhanced oncolytic activity against human glioblastoma cells relative to normal brain cells. J. Virol. 84:1563-1573.
19. Ahmed M, McKenzie MO, Puckett S, Hojnacki M, Poliquin L, Lyles DS. 2003. Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J. Virol. 77:4646-4657.
20. Kopecky SA, Willingham MC, Lyles DS. 2001. Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J. Virol. 75:12169-12181.
21. Stojdl DF, Lichty BD, ten Oever BR, Paterson JM, Power AT, Knowles S, Marius R, Reynard J, Poliquin L, Atkins H, Brown EG, Durbin RK, Durbin JE, Hiscott J, Bell JC. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
22. Obuchi M, Fernandez M, Barber GN. 2003. Development of recombinant vesicular stomatitis viruses that exploit defects in host defense to augment specific oncolytic activity. J. Virol. 77:8843-8856.
23. Moerdyk-Schauwecker M, Shah NR, Murphy AM, Hastie E, Mukherjee P, Grdzelishvili VZ. 2013. Resistance of pancreatic cancer cells to oncolytic vesicular stomatitis virus: role of type I interferon signaling. Virology 436:221-234.
24. Murphy AM, Besmer DM, Moerdyk-Schauwecker M, Moestl N, Ornelles DA, Mukherjee P, Grdzelishvili VZ. 2012. Vesicular stomatitis virus as an oncolytic agent against pancreatic ductal adenocarcinoma. J. Virol. 86:3073-3087.
25. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, Ross S, Conrads TP, Veenstra TD, Hitt BA, Kawaguchi Y, Johann D, Liotta LA, Crawford HC, Putt ME, Jacks T, Wright CV, Hruban RH, Lowy AM, Tuveson DA. 2003. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4:437-450.
26. Morikane K, Tempero RM, Sivinski CL, Nomoto M, Van Lith ML, Muto T, Hollingsworth MA. 1999. Organ-specific pancreatic tumor growth properties and tumor immunity. Cancer Immunol. Immunother. 47:287-296.
27. Schroeder JA, Thompson MC, Gardner MM, Gendler SJ. 2001. Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J. Biol. Chem. 276:13057-13064.
28. Taylor-Papadimitriou J, Peterson JA, Arklie J, Burchell J, Ceriani RL, Bodmer WF. 1981. Monoclonal antibodies to epithelium-specific components of the human milk fat globule membrane: production and reaction with cells in culture. Int. J. Cancer 28:17-21.
29. Croce MV, Isla-Larrain M, Remes-Lenicov F, Colussi AG, Lacunza E, Kim KC, Gendler SJ, Segal-Eiras A. 2006. MUC1 cytoplasmic tail detection using CT33 polyclonal and CT2 monoclonal antibodies in breast and colorectal tissue. Histol. Histopathol. 21:849-855.
30. Moyer SA, Baker SC, Lessard JL. 1986. Tubulin: a factor necessary for the synthesis of both Sendai virus and vesicular stomatitis virus RNAs. Proc. Natl. Acad. Sci. U. S. A. 83:5405-5409.
31. Lawson ND, Stillman EA, Whitt MA, Rose JK. 1995. Recombinant vesicular stomatitis viruses from DNA. Proc. Natl. Acad. Sci. U. S. A. 92:4477-4481.
32. Das SC, Nayak D, Zhou Y, Pattnaik AK. 2006. Visualization of intracellular transport of vesicular stomatitis virus nucleocapsids in living cells. J. Virol. 80:6368-6377.
33. Kalvodova L, Sampaio JL, Cordo S, Ejsing CS, Shevchenko A, Simons K. 2009. The lipidomes of vesicular stomatitis virus, Semliki Forest virus, and the host plasma membrane analyzed by quantitative shotgun mass spectrometry. J. Virol. 83:7996-8003.
34. Rowse GJ, Tempero RM, VanLith ML, Hollingsworth MA, Gendler SJ. 1998. Tolerance and immunity to MUC1 in a human MUC1 transgenic murine model. Cancer Res. 58:315-321.
35. Tinder TL, Subramani DB, Basu GD, Bradley JM, Schettini J, Million A, Skaar T, Mukherjee P. 2008. MUC1 enhances tumor progression and contributes toward immunosuppression in a mouse model of spontaneous pancreatic adenocarcinoma. J. Immunol. 181:3116-3125.
36. Spicer AP, Rowse GJ, Lidner TK, Gendler SJ. 1995. Delayed mammary tumor progression in Muc-1 null mice. J. Biol. Chem. 270:30093-30101.
37. Corbett TH, Roberts BJ, Leopold WR, Peckham JC, Wilkoff LJ, Griswold DP, Jr, Schabel FM, Jr. 1984. Induction and chemotherapeutic response of two transplantable ductal adenocarcinomas of the pancreas in C57BL/6 mice. Cancer Res. 44:717-726.
38. Ahmed M, Marino TR, Puckett S, Kock ND, Lyles DS. 2008. Immune response in the absence of neurovirulence in mice infected withMprotein mutant vesicular stomatitis virus. J. Virol. 82:9273-9277.
39. Johnson JE, Nasar F, Coleman JW, Price RE, Javadian A, Draper K, Lee M, Reilly PA, Clarke DK, Hendry RM, Udem SA. 2007. Neurovirulence properties of recombinant vesicular stomatitis virus vectors in nonhuman primates. Virology 360:36-49.
40. Dalton KP, Rose JK. 2001. Vesicular stomatitis virus glycoprotein containing the entire green fluorescent protein on its cytoplasmic domain is incorporated efficiently into virus particles. Virology 279:414-421.
41. Fernandez M, Porosnicu M, Markovic D, Barber GN. 2002. Genetically engineered vesicular stomatitis virus in gene therapy: application for treatment of malignant disease. J. Virol. 76:895-904.
42. Wu L, Huang TG, Meseck M, Altomonte J, Ebert O, Shinozaki K, García-Sastre A, Fallon J, Mandeli J, Woo SL. 2008. rVSV(M Delta 51)-M3 is an effective and safe oncolytic virus for cancer therapy. Hum. Gene Ther. 19:635-647.
43. Bi Z, Barna M, Komatsu T, Reiss CS. 1995. Vesicular stomatitis virus infection of the central nervous system activates both innate and acquired immunity. J. Virol. 69:6466-6472.
44. Reiss CS, Plakhov IV, Komatsu T. 1998. Viral replication in olfactory receptor neurons and entry into the olfactory bulb and brain. Ann. N. Y. Acad. Sci. 855:751-761.
45. van den Pol A, Dalton K, Rose J. 2002. Relative neurotropism of a recombinant rhabdovirus expressing a green fluorescent envelope glycoprotein. J. Virol. 76:1309-1327.
46. Ansari D, Tingstedt B, Andersson R. 2013. Pancreatic cancer-cost for overtreatment with gemcitabine. Acta Oncol. 52:1146-1151.
47. Kovarik A, Peat N, Wilson D, Gendler SJ, Taylor-Papadimitriou J. 1993. Analysis of the tissue-specific promoter of the MUC1 gene. J. Biol. Chem. 268:9917-9926.
48. Mukherjee P, Basu GD, Tinder TL, Subramani DB, Bradley JM, Arefayene M, Skaar T, De Petris G. 2009. Progression of pancreatic adenocarcinoma is significantly impeded with a combination of vaccine and COX-2 inhibition. J. Immunol. 182:216-224.
49. Jonckheere N, Van Seuningen I. 2010. The membrane-bound mucins: from cell signalling to transcriptional regulation and expression in epithelial cancers. Biochimie 92:1-11.
50. Kim GE, Bae HI, Park HU, Kuan SF, Crawley SC, Ho JJ, Kim YS. 2002. Aberrant expression of MUC5AC and MUC6 gastric mucins and sialyl Tn antigen in intraepithelial neoplasms of the pancreas. Gastroenterology 123:1052-1060.
51. Muik A, Dold C, Geiβ Y, Volk A, Werbizki M, Dietrich U, von Laer D. 2012. Semireplication-competent vesicular stomatitis virus as a novel platform for oncolytic virotherapy. J. Mol. Med. (Berl.) 90:959-970.
52. Wu Y, Lun X, Zhou H, Wang L, Sun B, Bell JC, Barrett JW, McFadden G, Biegel JA, Senger DL, Forsyth PA. 2008. Oncolytic efficacy of recombinant vesicular stomatitis virus and myxoma virus in experimental models of rhabdoid tumors. Clin. Cancer Res. 14:1218-1227.
53. Hadaschik BA, Zhang K, So AI, Fazli L, Jia W, Bell JC, Gleave ME, Rennie PS. 2008. Oncolytic vesicular stomatitis viruses are potent agents for intravesical treatment of high-risk bladder cancer. Cancer Res. 68: 4506-4510.
54. Naik S, Nace R, Barber GN, Russell SJ. 2012. Potent systemic therapy of multiple myeloma utilizing oncolytic vesicular stomatitis virus coding for interferon-beta. Cancer Gene Ther. 19:443-450.
55. Galivo F, Diaz RM, Wongthida P, Thompson J, Kottke T, Barber G, Melcher A, Vile R. 2010. Single-cycle viral gene expression, rather than progressive replication and oncolysis, is required for VSV therapy of B16 melanoma. Gene Ther. 17:158-170.
56. Chen N, Restivo A, Reiss CS. 2001. Leukotrienes play protective roles early during experimental VSV encephalitis. J. Neuroimmunol. 120:94-102.
57. Altomonte J, Wu L, Chen L, Meseck M, Ebert O, García-Sastre A, Fallon J, Woo SL. 2008. Exponential enhancement of oncolytic vesicular stomatitis virus potency by vector-mediated suppression of inflammatory responses in vivo. Mol. Ther. 16:146-153.
58. Altomonte J, Wu L, Meseck M, Chen L, Ebert O, Garcia-Sastre A, Fallon J, Mandeli J, Woo SL. 2009. Enhanced oncolytic potency of vesicular stomatitis virus through vector-mediated inhibition of NK and NKT cells. Cancer Gene Ther. 16:266-278.
59. Kottke T, Diaz RM, Kaluza K, Pulido J, Galivo F, Wongthida P, Thompson J, Willmon C, Barber GN, Chester J, Selby P, Strome S, Harrington K, Melcher A, Vile RG. 2008. Use of biological therapy to enhance both virotherapy and adoptive T-cell therapy for cancer. Mol. Ther. 16:1910-1918.
60. Qiao J, Wang H, Kottke T, Diaz RM, Willmon C, Hudacek A, Thompson J, Parato K, Bell J, Naik J, Chester J, Selby P, Harrington K, Melcher A, Vile RG. 2008. Loading of oncolytic vesicular stomatitis virus onto antigen-specific T cells enhances the efficacy of adoptive T-cell therapy of tumors. Gene Ther. 15:604-616.
61. Labib M, Zamay AS, Muharemagic D, Chechik A, Bell JC, Berezovski MV. 2012. Electrochemical sensing of aptamer-facilitated virus immunoshielding. Anal. Chem. 84:1677-1686.
62. Tesfay MZ, Kirk AC, Hadac EM, Griesmann GE, Federspiel MJ, Barber GN, Henry SM, Peng KW, Russell SJ. 2013. PEGylation of vesicular stomatitis virus extends virus persistence in blood circulation of passively immunized mice. J. Virol. 87:3752-3759.
63. Peng KW, Myers R, Greenslade A, Mader E, Greiner S, Federspiel MJ, Dispenzieri A, Russell SJ. 2013. Using clinically approved cyclophosphamide regimens to control the humoral immune response to oncolytic viruses. Gene Ther. 20:255-261.
64. Willmon C, Diaz RM, Wongthida P, Galivo F, Kottke T, Thompson J, Albelda S, Harrington K, Melcher A, Vile R. 2011. Vesicular stomatitis virus-induced immune suppressor cells generate antagonism between intratumoral oncolytic virus and cyclophosphamide. Mol. Ther. 19:140-149.
65. Leveille S, Samuel S, Goulet ML, Hiscott J. 2011. Enhancing VSV oncolytic activity with an improved cytosine deaminase suicide gene strategy. Cancer Gene Ther. 18:435-443.
66. Porosnicu M, Mian A, Barber GN. 2003. The oncolytic effect of recombinant vesicular stomatitis virus is enhanced by expression of the fusion cytosine deaminase/uracil phosphoribosyltransferase suicide gene. Cancer Res. 63:8366-8376.
67. Ebert O, Shinozaki K, Kournioti C, Park MS, Garcia-Sastre A, Woo SL. 2004. Syncytia induction enhances the oncolytic potential of vesicular stomatitis virus in virotherapy for cancer. Cancer Res. 64:3265-3270.
68. Shin EJ, Chang JI, Choi B, Wanna G, Ebert O, Genden EM, Woo SL. 2007. Fusogenic vesicular stomatitis virus for the treatment of head and neck squamous carcinomas. Otolaryngol. Head Neck Surg. 136:811-817.
69. Chang G, Xu S, Watanabe M, Jayakar HR, Whitt MA, Gingrich JR. 2010. Enhanced oncolytic activity of vesicular stomatitis virus encoding SV5-F protein against prostate cancer. J. Urol. 183:1611-1618.
70. Altomonte J, Braren R, Schulz S, Marozin S, Rummeny EJ, Schmid RM, Ebert O. 2008. Synergistic antitumor effects of transarterial viroembolization for multifocal hepatocellular carcinoma in rats. Hepatology 48: 1864-1873.
71. Breitbach CJ, De Silva NS, Falls TJ, Aladl U, Evgin L, Paterson J, Sun YY, Roy DG, Rintoul JL, Daneshmand M, Parato K, Stanford MM, Lichty BD, Fenster A, Kirn D, Atkins H, Bell JC. 2011. Targeting tumor vasculature with an oncolytic virus. Mol. Ther. 19:886-894.
72. Melcher A, Parato K, Rooney CM, Bell JC. 2011. Thunder and lightning: immunotherapy and oncolytic viruses collide. Mol. Ther. 19:1008-1016.
73. Boudreau JE, Bridle BW, Stephenson KB, Jenkins KM, Brunelliere J, Bramson JL, Lichty BD, Wan Y. 2009. Recombinant vesicular stomatitis virus transduction of dendritic cells enhances their ability to prime innate and adaptive antitumor immunity. Mol. Ther. 17:1465-1472.
74. Bridle BW, Hanson S, Lichty BD. 2010. Combining oncolytic virotherapy and tumour vaccination. Cytokine Growth Factor Rev. 21:143-148.
75. Diaz RM, Galivo F, Kottke T, Wongthida P, Qiao J, Thompson J, Valdes M, Barber G, Vile RG. 2007. Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res. 67:2840-2848.
76. Galivo F, Diaz RM, Thanarajasingam U, Jevremovic D, Wongthida P, Thompson J, Kottke T, Barber GN, Melcher A, Vile RG. 2010. Interference of CD40L-mediated tumor immunotherapy by oncolytic VSV. Hum. Gene Ther. 21:439-450.
77. Kottke T, Galivo F, Wongthida P, Diaz RM, Thompson J, Jevremovic D, Barber GN, Hall G, Chester J, Selby P, Harrington K, Melcher A, Vile RG. 2008. Treg depletion-enhanced IL-2 treatment facilitates therapy of established tumors using systemically delivered oncolytic virus. Mol. Ther. 16:1217-1226.
78. Qiao J, Kottke T, Willmon C, Galivo F, Wongthida P, Diaz RM, Thompson J, Ryno P, Barber GN, Chester J, Selby P, Harrington K, Melcher A, Vile RG. 2008. Purging metastases in lymphoid organs using a combination of antigen-nonspecific adoptive T cell therapy, oncolytic virotherapy and immunotherapy. Nat. Med. 14:37-44.
79. Willmon CL, Saloura V, Fridlender ZG, Wongthida P, Diaz RM, Thompson J, Kottke T, Federspiel M, Barber G, Albelda SM, Vile RG. 2009. Expression of IFN-beta enhances both efficacy and safety of oncolytic vesicular stomatitis virus for therapy of mesothelioma. Cancer Res. 69:7713-7720.
80. Wongthida P, Diaz RM, Galivo F, Kottke T, Thompson J, Pulido J, Pavelko K, Pease L, Melcher A, Vile R. 2010. Type III IFN interleukin-28 mediates the antitumor efficacy of oncolytic virus VSV in immunecompetent mouse models of cancer. Cancer Res. 70:4539-4549.
81. Wongthida P, Diaz RM, Galivo F, Kottke T, Thompson J, Melcher A, Vile R. 2011. VSV oncolytic virotherapy in the B16 model depends upon intact MyD88 signaling. Mol. Ther. 19:150-158.
82. Wongthida P, Diaz RM, Pulido C, Rommelfanger D, Galivo F, Kaluza K, Kottke T, Thompson J, Melcher A, Vile R. 2011. Activating systemic T-cell immunity against self tumor antigens to support oncolytic virotherapy with vesicular stomatitis virus. Hum. Gene Ther. 22:1343-1353.
83. Heiber JF, Barber GN. 2011. Vesicular stomatitis virus expressing tumor suppressor p53 is a highly attenuated, potent oncolytic agent. J. Virol. 85:10440-10450.
84. Cobleigh MA, Bradfield C, Liu Y, Mehta A, Robek MD. 2012. The immune response to a vesicular stomatitis virus vaccine vector is independent of particulate antigen secretion and protein turnover rate. J. Virol. 86:4253-4261.
85. Goel A, Carlson SK, Classic KL, Greiner S, Naik S, Power AT, Bell JC, Russell SJ. 2007. Radioiodide imaging and radiovirotherapy of multiple myeloma using VSV(Delta51)-NIS, an attenuated vesicular stomatitis virus encoding the sodium iodide symporter gene. Blood 110:2342-2350.
86. Tumilasci VF, Oliere S, Nguyen TL, Shamy A, Bell J, Hiscott J. 2008. Targeting the apoptotic pathway with BCL-2 inhibitors sensitizes primary chronic lymphocytic leukemia cells to vesicular stomatitis virus-induced oncolysis. J. Virol. 82:8487-8499.
87. Samuel S, Tumilasci VF, Oliere S, Nguyen TL, Shamy A, Bell J, Hiscott J. 2010. VSV oncolysis in combination with the BCL-2 inhibitor obatoclax overcomes apoptosis resistance in chronic lymphocytic leukemia. Mol. Ther. 18:2094-2103.
88. Schache P, Gurlevik E, Struver N, Woller N, Malek N, Zender L, Manns M, Wirth T, Kuhnel F, Kubicka S. 2009. VSV virotherapy improves chemotherapy by triggering apoptosis due to proteasomal degradation of Mcl-1. Gene Ther. 16:849-861.
89. Nowak AK, Robinson BW, Lake RA. 2002. Gemcitabine exerts a selective effect on the humoral immune response: implications for combination chemo-immunotherapy. Cancer Res. 62:2353-2358.