Enhanced delivery of mda-7/IL-24 using a serotype chimeric adenovirus (Ad.5/3) in combination with the apogossypol derivative BI-97C1 (Sabutoclax) improves therapeutic efficacy in low CAR colorectal cancer cells

Journal of Cellular Physiology

Volumn 227, Issue 5, 2012, Pages 2145-2153

  Azab, Belal ^a   Dash, Rupesh ^a   Das, Swadesh K ^a   Bhutia, Sujit K ^a,f   Shen, Xue Ning ^a   Quinn, Bridget A ^a   Sarkar, Siddik ^a   Wang, Xiang Yang ^a,b   Hedvat, Michael ^a,c   Dmitriev, Igor P ^d   Curiel, David T ^d   Grant, Steven ^a,b,e   Dent, Paul ^a,b   Reed, John C ^c   Pellecchia, Maurizio ^c   Sarkar, Devanand ^a,b   Fisher, Paul B ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c BURNHAM INSTITUTE   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL INSTITUTE OF TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; INTERLEUKIN 24; PROTEIN BCL 2; RECOMBINANT CYTOKINE; SABUTOCLAX; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADENOVIRUS 5; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; COLORECTAL CANCER; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; GENE DELIVERY SYSTEM; GENE THERAPY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; SEROTYPE;

ADENOVIRIDAE; ANIMALS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DRUG SYNERGISM; GENE TRANSFER TECHNIQUES; GOSSYPOL; HUMANS; INTERLEUKINS; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; RECEPTORS, VIRUS; TRANSGENES; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

ADENOVIRIDAE; MUS MUSCULUS;

EID: 84862908037     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22947     Document Type: Article

References (44)

1. Anders M, Hansen R, Ding RX, Rauen KA, Bissell MJ, Korn WM. 2003. Disruption of 3D tissue integrity facilitates adenovirus infection by deregulating the coxsackievirus and adenovirus receptor. Proc Natl Acad Sci USA 100: 1943-1948.
2. Caudell EG, Mumm JB, Poindexter N, Ekmekcioglu S, Mhashilkar AM, Yang XH, Retter MW, Hill P, Chada S, Grimm EA. 2002. The protein product of the tumor suppressor gene, melanoma differentiation-associated gene 7, exhibits immunostimulatory activity and is designated IL-24. J Immunol 168: 6041-6046.
3. Chu RL, Post DE, Khuri FR, Van Meir EG. 2004. Use of replicating oncolytic adenoviruses in combination therapy for cancer. Clin Cancer Res 10: 5299-5312.
4. Cunningham CC, Chada S, Merritt JA, Tong A, Senzer N, Zhang Y, Mhashilkar A, Parker K, Vukelja S, Richards D, Hood J, Coffee K, Nemunaitis J. 2005. Clinical and local biological effects of an intratumoral injection of mda-7 (IL24; INGN 241) in patients with advanced carcinoma: A phase I study. Mol Ther 11: 149-159.
5. Dash R, Richards JE, Su ZZ, Bhutia SK, Azab B, Rahmani M, Dasmahapatra G, Yacoub A, Dent P, Dmitriev IP, Curiel DT, Grant S, Pellecchia M, Reed JC, Sarkar D, Fisher PB. 2010a. Mechanism by which Mcl-1 regulates cancer-specific apoptosis triggered by mda-7/IL-24, an IL-10-related cytokine. Cancer Res 70: 5034-5045.
6. Dash R, Dmitriev I, Su ZZ, Bhutia SK, Azab B, Vozhilla N, Yacoub A, Dent P, Curiel DT, Sarkar D, Fisher PB. 2010b. Enhanced delivery of mda-7/IL-24 using a serotype chimeric adenovirus (Ad.5/3) improves therapeutic efficacy in low CAR prostate cancer cells. Cancer Gene Ther 17: 447-456.
7. Dash R, Azab B, Quinn BA, Shen X, Wang XY, Das SK, Rahmani M, Wei J, Hedvat M, Dent P, Dmitriev IP, Curiel DT, Grant S, Wu B, Stebbins JL, Pellecchia M, Reed JC, Sarkar D, Fisher PB. 2011. Apogossypol derivative BI-97C1 (Sabutoclax) targeting Mcl-1 sensitizes prostate cancer cells to mda-7/IL-24-mediated toxicity. Proc Natl Acad Sci USA 108: 8785-8790.
8. Emdad L, Lebedeva IV, Su ZZ, Gupta P, Sauane M, Dash R, Grant S, Dent P, Curiel DT, Sarkar D, Fisher PB. 2009. Historical perspective and recent insights into our understanding of the molecular and biochemical basis of the antitumor properties of mda-7/IL-24. Cancer Biol Ther 8: 391-400.
9. Eulitt PJ, Park MA, Hossein H, Cruikshanks N, Yang C, Dmitriev IP, Yacoub A, Curiel DT, Fisher PB, Dent P. 2011. Enhancing mda-7/IL-24 therapy in renal carcinoma cells by inhibiting multiple protective signaling pathways using sorafenib and by Ad.5/3 gene delivery. Cancer Biol Ther 10: 1290-1305.
10. Fickenscher H, Hör S, Küpers H, Knappe A, Wittmann S, Sticht H. 2002. The interleukin-10 family of cytokines. Trends Immunol 23: 89-96.
11. Fisher PB. 2005. Is mda-7/IL-24 a "magic bullet" for cancer? Cancer Res 65: 10128-10138.
12. Fong Y, Kemeny N, Paty P, Blumgart LH, Cohen AM. 1996. Treatment of colorectal cancer: Hepatic metastasis. Semin Surg Oncol 12: 219-252.
13. Glasgow JN, Bauerschmitz GJ, Curiel DT, Hemminki A. 2004. Transductional and transcriptional targeting of adenovirus for clinical applications. Curr Gene Ther 4: 1-14.
14. Gupta P, Su ZZ, Lebedeva IV, Sarkar D, Sauane M, Emdad L, Bachelor MA, Grant S, Curiel DT, Dent P, Fisher PB. 2006. mda-7/IL-24: Multifunctional cancer-specific apoptosis-inducing cytokine. Pharmacol Ther 111: 596-628.
15. Hamed HA, Yacoub A, Park MA, Eulitt PJ, Dash R, Sarkar D, Dmitriev IP, Lesniak MS, Shah K, Grant S, Curiel DT, Fisher PB, Dent P. 2010. Inhibition of multiple protective signaling pathways and Ad.5/3 delivery enhances mda-7/IL-24 therapy of malignant glioma. Mol Ther 18: 1130-1142.
16. Haviv YS, Blackwell JL, Kanerva A, Nagi P, Krasnykh V, Dmitriev I, Wang M, Naito S, Lei X, Hemminki A, Carey D, Curiel DT. 2002. Adenoviral gene therapy for renal cancer requires retargeting to alternative cellular receptors. Cancer Res 62: 4273-4281.
17. Huang EY, Madireddi MT, Gopalkrishnan RV, Leszczyniecka M, Su Z, Lebedeva IV, Kang D, Jiang H, Lin JJ, Alexandre D, Chen Y, Vozhilla N, Mei MX, Christiansen KA, Sivo F, Goldstein NI, Mhashilkar AB, Chada S, Huberman E, Pestka S, Fisher PB. 2001. Genomic structure, chromosomal localization and expression profile of a novel melanoma differentiation associated (mda-7) gene with cancer specific growth suppressing and apoptosis inducing properties. Oncogene 20: 7051-7063.
18. Jiang H, Su ZZ, Lin JJ, Goldstein NI, Young CS, Fisher PB. 1996. The melanoma differentiation associated gene mda-7 suppresses cancer cell growth. Proc Natl Acad Sci USA 93: 9160-9165.
19. Jiang H, Lin JJ, Su ZZ, Goldstein NI, Fisher PB. 1995. Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 11: 2477-2486.
20. Kanerva A, Mikheeva GV, Krasnykh V, Coolidge CJ, Lam JT, Mahasreshti PJ, Barker SD, Straughn M, Barnes MN, Alvarez RD, Hemminki A, Curiel DT. 2002. Targeting adenovirus to the serotype 3 receptor increases gene transfer efficiency to ovarian cancer cells. Clin Cancer Res 8: 275-280.
21. Korn WM, Macal M, Christian C, Lacher MD, McMillan A, Rauen KA, Warren RS, Ferrell L. 2006. Expression of the coxsackievirus- and adenovirus receptor in gastrointestinal cancer correlates with tumor differentiation. Cancer Gene Ther 13: 792-797.
22. Lebedeva IV, Su ZZ, Chang Y, Kitada S, Reed JC, Fisher PB. 2002. The cancer growth suppressing gene mda-7 induces apoptosis selectively in human melanoma cells. Oncogene 21: 708-718.
23. Lebedeva IV, Sarkar D, Su ZZ, Kitada S, Dent P, Stein CA, Reed JC, Fisher PB. 2003. Bcl-2 and Bcl-x(L) differentially protect human prostate cancer cells from induction of apoptosis by melanoma differentiation associated gene-7, mda-7/IL-24. Oncogene 22: 8758-8773.
24. Lynch HT, de la Chapelle A. 2003. Hereditary colorectal cancer. N Engl J Med 348: 919-932 (in Eng).
25. Mathis JM, Stewart PL, Zhu ZB, Curiel DT. 2006. Advanced generation adenoviral virotherapy agents embody enhanced potency upon CAR-independent tropism. (Translated from eng) Clin Cancer Res 12: 2651-2656.
26. Pandha HS, Stockwin LH, Eaton J, Clarke IA, Dalgleish AG, Todryk SM, Blair GE. 2003. Coxsackie B and adenovirus receptor, integrin and major histocompatibility complex class I expression in human prostate cancer cell lines: Implications for gene therapy strategies. Prostate Cancer Prostatic Dis 6: 6-11.
27. Parrish-Novak J, Xu W, Brender T, Yao L, Jones C, West J, Brandt C, Jelinek L, Madden K, McKernan PA, Foster DC, Jaspers S, Chandrasekher YA. 2002. Interleukins 19, 20 and 24 signal through two distinct receptor complexes. Differences in receptor-ligand interactions mediate unique biological functions. J Biol Chem 277: 47517-47523.
28. Paul CP, Everts M, Glasgow JN, Dent P, Fisher PB, Ulasov IV, Lesniak MS, Stoff-Khalili MA, Roth JC, Preuss MA, Dirven CM, Lamfers ML, Siegal GP, Zhu ZB, Curiel DT. 2008. Characterization of infectivity of knob-modified adenoviral vectors in glioma. Cancer Biol Ther 7: 786-793.
29. Ramesh R, Mhashilkar AM, Tanaka F, Saito Y, Branch CD, Sieger K, Mumm JB, Stewart AL, Boquoi A, Dumoutier L, Grimm EA, Renauld JC, Kotenko S, Chada S. 2003. Melanoma differentiation-associated gene 7/interleukin (IL)-24 is a novel ligand that regulates angiogenesis via the IL-22 receptor. Cancer Res 63: 5105-5113.
30. Rauen KA, Sudilovsky D, Le JL, Chew KL, Hann B, Weinberg V, Schmitt LD, McCormick F. 2002. Expression of the coxsackie adenovirus receptor in normal prostate and in primary and metastatic prostate carcinoma: Potential relevance to gene therapy. Cancer Res 62: 3812-3818.
31. Reid T, Galanis E, Abbruzzese J, Sze D, Wein LM, Andrews J, Randlev B, Heise C, Uprichard M, Hatfield M, Rome L, Rubin J, Kirn D. 2002. Hepatic arterial infusion of a replication-selective oncolytic adenovirus (dl1520): Phase II viral, immunologic, and clinical endpoints. Cancer Res 62: 6070-6079.
32. Sachs MD, Rauen KA, Ramamurthy M, Dodson JL, De Marzo AM, Putzi MJ, Schoenberg MP, Rodriguez R. 2002. Integrin alpha(v) and coxsackie adenovirus receptor expression in clinical bladder cancer. Urology 60: 531-536.
33. Sarkar D, Su ZZ, Vozhilla N, Park ES, Gupta P, Fisher PB. 2005a. Dual cancer-specific targeting strategy cures primary and distant breast carcinomas in nude mice. Proc Natl Acad Sci USA 102: 14034-14039.
34. Sarkar D, Su ZZ, Vozhilla N, Park ES, Randolph A, Valerie K, Fisher PB. 2005b. Targeted virus replication plus immunotherapy eradicates primary and distant pancreatic tumors in nude mice. Cancer Res 65: 9056-9063.
35. Su ZZ, Madireddi MT, Lin JJ, Young CS, Kitada S, Reed JC, Goldstein NI, Fisher PB. 1998. The cancer growth suppressor gene mda-7 selectively induces apoptosis in human breast cancer cells and inhibits tumor growth in nude mice. Proc Natl Acad Sci USA 95: 14400-14405.
36. Su Z, Lebedeva IV, Gopalkrishnan RV, Goldstein NI, Stein CA, Reed JC, Dent P, Fisher PB. 2001. A combinatorial approach for selectively inducing programmed cell death in human pancreatic cancer cells. Proc Natl Acad Sci USA 98: 10332-10337.
37. Su Z, Emdad L, Sauane M, Lebedeva IV, Sarkar D, Gupta P, James CD, Randolph A, Valerie K, Walter MR, Dent P, Fisher PB. 2005. Unique aspects of mda-7/IL-24 antitumor bystander activity: Establishing a role for secretion of MDA-7/IL-24 protein by normal cells. Oncogene 24: 7552-7566.
38. Tong AW, Nemunaitis J, Su D, Zhang Y, Cunningham C, Senzer N, Netto G, Rich D, Mhashilkar A, Parker K, Coffee K, Ramesh R, Ekmekcioglu S, Grimm EA, van Wart Hood J, Merritt J, Chada S. 2005. Intratumoral injection of INGN241, a nonreplicating adenovector expressing the melanoma-differentiation associated gene-7 (mda-7/IL24): Biologic outcome in advanced cancer patients. Mol Ther 11: 160-172.
39. Tsuruta Y, Pereboeva L, Glasgow JN, Rein DT, Kawakami Y, Alvarez RD, Rocconi RP, Siegal GP, Dent P, Fisher PB, Curiel DT. 2007. A mosaic fiber adenovirus serotype 5 vector containing reovirus sigma 1 and adenovirus serotype 3 knob fibers increases transduction in an ovarian cancer ex vivo system via a coxsackie and adenovirus receptor-independent pathway. Clin Cancer Res 13: 2777-2783.
40. Ulasov IV, Tyler MA, Zheng S, Han Y, Lesniak MS. 2006. CD46 represents a target for adenoviral gene therapy of malignant glioma. Human Gene Ther 17: 556-564.
41. Volk AL, Rivera AA, Kanerva A, Bauerschmitz G, Dmitriev I, Nettelbeck DM, Curiel DT. 2003. Enhanced adenovirus infection of melanoma cells by fiber-modification: Incorporation of RGD peptide or Ad5/3 chimerism. Cancer Biol Ther 2: 511-515.
42. Waehler R, Russell SJ, Curiel DT. 2007. Engineering targeted viral vectors for gene therapy. Nat Rev Genet 8: 573-587.
43. Wei J, Stebbins JL, Kitada S, Dash R, Placzek W, Rega MF, Wu B, Cellitti J, Zhai D, Yang L, Dahl R, Fisher PB, Reed JC, Pellecchia M. 2010. BI-97C1, an optically pure Apogossypol derivative as pan-active inhibitor of antiapoptotic B-cell lymphoma/leukemia-2 (Bcl-2) family proteins. J Med Chem 53: 4166-4176.
44. Yacoub A, Liu R, Park MA, Hamed HA, Dash R, Schramm DN, Sarkar D, Dimitriev IP, Bell JK, Grant S, Farrell NP, Curiel DT, Fisher PB, Dent P. 2010. Cisplatin enhances protein kinase R-like endoplasmic reticulum kinase- and CD95-dependent melanoma differentiation-associated gene-7/interleukin-24-induced killing in ovarian carcinoma cells. Mol Pharmacol 77: 298-310.