Targeting inhibition of K-ras enhances Ad.mda-7-induced growth suppression and apoptosis in mutant K-ras colorectal cancer cells

Oncogene

Volumn 26, Issue 5, 2007, Pages 733-744

  Lebedeva, I V ^a   Su, Z Z ^a   Emdad, L ^a   Kolomeyer, A ^a   Sarkar, D ^a   Kitada, S ^b   Waxman, S ^c   Reed, J C ^b   Fisher, P B ^a  

^a College of Physicians and Surgeons ^*  (United States)

^b BURNHAM INSTITUTE   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Bcl family of proteins; Bipartite adenovirus; Colorectal carcinoma; K ras AS; K ras single chain antibody; mda 7 IL 24

Indexed keywords

ADENOVIRUS VECTOR; INTERLEUKIN 24; P21 ACTIVATED KINASE; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY;

ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL KILLING; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; GENE MUTATION; GENE REPRESSION; GENE TARGETING; GENETIC ENGINEERING; HUMAN; HUMAN CELL; ONCOGENE K RAS; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS INHIBITION; VIRUS REPLICATION; WILD TYPE;

ADENOVIRIDAE; ADJUVANTS, IMMUNOLOGIC; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; COLORECTAL NEOPLASMS; GENE THERAPY; GENES, RAS; GENETIC VECTORS; HUMANS; INTERLEUKINS; MUTATION; NECROSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED;

ADENOVIRIDAE;

EID: 33846798357     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/sj.onc.1209813     Document Type: Article

References (60)

1. Adjei AA. (2001). Blocking oncogenic Ras signaling for cancer therapy. J Natl Cancer Inst 93: 1062-1074.
2. Andreyev HJ, Norman AR, Cunningham D, Oates J, Dix BR, Iacopetta BJ et al. (2001). Kirsten ras mutations in patients with colorectal cancer: the 'RASCAL II' study. Br J Cancer 85: 692-696.
3. Aoki K, Yoshida T, Matsumoto N, Ide H, Sugimura T, Terada M. (1997). Suppression of Ki-ras p21 levels leading to growth inhibition of pancreatic cancer cell lines with Ki-ras mutation but not those without Ki-ras mutation. Mol Carcinogen 20: 251-258.
4. Barbacid M. (1987). ras genes. Annu Rev Biochem 56: 779-827.
5. Bos JL. (1989). ras oncogenes in human cancer: a review. Cancer Res 49: 4682-4689.
6. Bos JL, Fearon ER, Hamilton SR, Verlaan-de Vries M, van Boom JH, van der Eb AJ et al. (1987). Prevalence of ras gene mutations in human colorectal cancers. Nature 327: 293-297.
7. Brand K, Klocke R, Possling A, Paul D, Strauss M. (1999). Induction of apoptosis and G2/M arrest by infection with replication-deficient adenovirus at high multiplicity of infection. Gene Therapy 6: 1054-1063.
8. Canevari S, Biocca S, Figini M. (2002). Re: Blocking oncogenic Ras signaling for cancer therapy. J Natl Cancer Inst 94: 1031-1032 (author reply 1032).
9. Cardinale A, Lener M, Messina S, Cattaneo A, Biocca S. (1998). The mode of action of Y13-259 scFv fragment intracellularly expressed in mammalian cells. FEBS Lett 439: 197-202.
10. Chada S, Mhashilkar AM, Liu Y, Nishikawa T, Bocangel D, Zheng M et al. (2005b). Mda-7 gene transfer sensitizes breast carcinoma cells to chemotherapy, biologic therapies and radiotherapy: correlation with expression of bcl-2 family members. Cancer Gene Ther 13: 490-502.
11. Chada S, Mhashilkar AM, Ramesh R, Mumm JB, Sutton RB, Bocangel D et al. (2004a). Bystander activity of Ad-mda7: human MDA-7 protein kills melanoma cells via an IL-20 receptor-dependent but STAT3-independent mechanism. Mol Ther 10: 1085-1095.
12. Chada S, Sutton RB, Ekmekcioglu S, Ellerhorst J, Mumm JB, Leitner WW et al. (2004b). MDA-7/IL-24 is a unique cytokine-tumor suppressor in the IL-10 family. Int Immunopharmacol 4: 649-667.
13. Cochet O, Kenigsberg M, Delumeau I, Virone-Oddos A, Multon MC, Fridman WH et al. (1998). Intracellular expression of an antibody fragment-neutralizing p21 ras promotes tumor regression. Cancer Res 58: 1170-1176.
14. Cunningham CC, Chada S, Merritt JA, Tong A, Senzer N, Zhang Y et al. (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.
15. Fearon ER, Vogelstein B. (1990). A genetic model for colorectal tumorigenesis. Cell 61: 759-767.
16. Fernandez-Sarabia MJ, Bischoff JR. (1993). Bcl-2 associates with the ras-related protein R-ras p23. Nature 366: 274-275.
17. Fisher PB. (2005). Is mda-7/IL-24a 'magic bullet' for cancer? Cancer Res 65: 10128-10138.
18. Fisher PB, Gopalkrishnan RV, Chada S, Ramesh R, Grimm EA, Rosenfeld MR et al. (2003). Mda-7/IL-24, a novel cancer selective apoptosis inducing cytokine gene: from the laboratory into the clinic. Cancer Biol Ther 2: S23-S37.
19. Gupta P, Su ZZ, Lebedeva IV, Sarkar D, Sauane M, Emdad L et al. (2006). Mda-7/IL-24: multifunctional cancer-specific apoptosis-inducing cytokine. Pharmacol Ther (in press).
20. Hague A, Moorghen M, Hicks D, Chapman M, Paraskeva C. (1994). BCL-2 expression in human colorectal adenomas and carcinomas. Oncogene 9: 3367-3370.
21. Holmes M, Rosenberg E, Valerie K. (2003). Adenovirus expressing p53. Methods Mol Biol 234: 1-16.
22. Hoshino R, Chatani Y, Yamori T, Tsuruo T, Oka H, Yoshida O et al. (1999). Constitutive activation of the 41-/43-kDa mitogen-activated protein kinase signaling pathway in human tumors. Oncogene 18: 813-822.
23. 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.
24. Kinoshita T, Yokota T, Arai K, Miyajima A. (1995). Regulation of Bcl-2 expression by oncogenic Ras protein in hematopoietic cells. Oncogene 10: 2207-2212.
25. Kita K, Saito S, Morioka CY, Watanabe A. (1999). Growth inhibition of human pancreatic cancer cell lines by anti-sense oligonucleotides specific to mutated K-ras genes. Int J Cancer 80: 553-558.
26. Krajewska M, Krajewski S, Epstein JI, Shabaik A, Sauvageot J, Song K et al. (1996a). Immunohistochemical analysis of bcl-2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol 148: 1567-1576.
27. Krajewska M, Moss SF, Krajewski S, Song K, Holt PR, Reed JC. (1996b). Elevated expression of Bcl-X and reduced Bak in primary colorectal adenocarcinomas. Cancer Res 56: 2422-2427.
28. Krajewski S, Thor AD, Edgerton SM, Moore II DH, Krajewska M, Reed JC. (1997). Analysis of Bax and Bcl-2 expression in p53-immunopositive breast cancers. Clin Cancer Res 3: 199-208.
29. Lebedeva IV, Sarkar D, Su ZZ, Gopalkrishnan RV, Athar M, Randolph A et al. (2006). Molecular target-based therapy of pancreatic cancer. Cancer Res 66: 2403-2413.
30. Lebedeva IV, Sarkar D, Su ZZ, Kitada S, Dent P, Stein CA et al. (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.
31. Lebedeva IV, Sauane M, Gopalkrishnan RV, Sarkar D, Su ZZ, Gupta P et al. (2005a). Mda-7/IL-24: exploiting cancer's Achilles' heel. Mol Ther 11: 4-18.
32. 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.
33. Lebedeva IV, Su ZZ, Sarkar D, Gopalkrishnan RV, Waxman S, Yacoub A et al. (2005b). Induction of reactive oxygen species renders mutant and wild-type K-ras pancreatic carcinoma cells susceptible to Ad.mda-7-induced apoptosis. Oncogene 24: 585-596.
34. Mukhopadhyay T, Tainsky M, Cavender AC, Roth JA. (1991). Specific inhibition of K-ras expression and tumorigenicity of lung cancer cells by antisense RNA. Cancer Res 51: 1744-1748.
35. Oida Y, Gopalan B, Miyahara R, Inoue S, Branch CD, Mhashilkar AM et al. (2005). Sulindac enhances adenoviral vector expressing mda-7/IL-24-mediated apoptosis in human lung cancer. Mol Cancer Ther 4: 291-304.
36. Ramesh R, Mhashilkar AM, Tanaka F, Saito Y, Branch CD, Sieger K et al. (2003). Melanoma differentiation-associated gene 7/interleukin (IL)-24is a novel ligand that regulates angiogenesis via the IL-22 receptor. Cancer Res 63: 5105-5113.
37. Russell JS, Lang FF, Huet T, Janicot M, Chada S, Wilson DR et al. (1999). Radiosensitization of human tumor cell lines induced by the adenovirus-mediated expression of an anti-Ras single-chain antibody fragment. Cancer Res 59: 5239-5244.
38. Russo P, Malacarne D, Falugi C, Trombino S, O'Connor PM. (2002). RPR-115135, a farnesyltransferase inhibitor, increases 5-FU-cytotoxicity in ten human colon cancer cell lines: role of p53. Int J Cancer 100: 266-275.
39. Sarkar D, Dent P, Fisher PB. (2006). Melanoma differentiation associated gene-7 (mda-7)/interleukin-24(IL-24 ), mda-7/IL-24: current perspectives on a unique member of the IL-10 family of cytokines. Anti-inflammatory Anti-allergy Agents Med Chem (in press).
40. 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.
41. Sarkar D, Su ZZ, Vozhilla N, Park ES, Randolph A, Valerie K et al. (2005b). Targeted virus replication plus immunotherapy eradicates primary and distant pancreatic tumors in nude mice. Cancer Res 65: 9056-9063.
42. Shirasawa S, Furuse M, Yokoyama N, Sasazuki T. (1993). Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 260: 85-88.
43. Sklar MD. (1988a). The ras oncogenes increase the intrinsic resistance of NIH 3T3 cells to ionizing radiation. Science 239: 645-647.
44. Sklar MD. (1988b). Increased resistance to cis-diamminedi- chloroplatinum(II) in NIH 3T3 cells transformed by ras oncogenes. Cancer Res 48: 793-797.
45. Su Z, Emdad L, Sauane M, Lebedeva IV, Sarkar D, Gupta P et al. (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.
46. Su Z, Lebedeva IV, Gopalkrishnan RV, Goldstein NI, Stein CA, Reed JC et al. (2001). A combinatorial approach for selectively inducing programmed cell death in human pancreatic cancer cells. Proc Natl Acad Sci USA 98: 10332-10337.
47. Su ZZ, Lebedeva IV, Sarkar D, Emdad L, Gupta P, Kitada S et al. (2006). Ionizing radiation enhances therapeutic activity of mda-7/IL-24: overcoming radiation- and mda-7/IL-24-resistance in prostate cancer cells overexpressing the antiapoptotic proteins bcl-x(L) or bcl-2. Oncogene 25: 2339-2348.
48. Su ZZ, Lebedeva IV, Sarkar D, Gopalkrishnan RV, Sauane M, Sigmon C et al. (2003). Melanoma differentiation associated gene-7, mda-7/IL-24, selectively induces growth suppression, apoptosis and radiosensitization in malignant gliomas in a p53-independent manner. Oncogene 22: 1164-1180.
49. Su ZZ, Madireddi MT, Lin JJ, Young CS, Kitada S, Reed JC et al. (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.
50. Su ZZ, Shi Y, Fisher PB. (1997). Subtraction hybridization identifies a transformation progression-associated gene PEG-3 with sequence homology to a growth arrest and DNA damage-inducible gene. Proc Natl Acad Sci USA 94: 9125-9130.
51. Tong AW, Nemunaitis J, Su D, Zhang Y, Cunningham C, Senzer N et al. (2005). Intratumoral injection of INGN 241, a nonreplicating adenovector expressing the melanoma-differentiation associated gene-7 (mda-7/IL24): biologic outcome in advanced cancer patients. Mol Ther 11: 160-172.
52. Viale PH, Fung A, Zitella L. (2005). Advanced colorectal cancer: current treatment and nursing management with economic considerations. Clin J Oncol Nurs 9: 541-552.
53. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M et al. (1988). Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525-532.
54. Ward RL, Todd AV, Santiago F, O'Connor T, Hawkins NJ. (1997). Activation of the K-ras oncogene in colorectal neoplasms is associated with decreased apoptosis. Cancer 79: 1106-1113.
55. Weinstein IB. (2002). Cancer. Addiction to oncogenes - the Achilles heal of cancer. Science 297: 63-64.
56. Yacoub A, Mitchell C, Hong Y, Schroeder M, Gopalkrishnan RV, Su Z-Z et al. (2004). MDA-7 regulates cell growth and radiosensitivity in vitro of primary (non-established) human glioma cells. Cancer Biol Ther 3: 739-751.
57. Yacoub A, Mitchell C, Lebedeva IV, Sarkar D, Su ZZ, McKinstry R et al. (2003a). mda-7 (IL-24) inhibits growth and enhances radiosensitivity of glioma cells in vitro via JNK signaling. Cancer Biol Ther 2: 347-353.
58. Yacoub A, Mitchell C, Lister A, Lebedeva IV, Sarkar D, Su ZZ et al. (2003b). Melanoma differentiation-associated 7 (interleukin 24) inhibits growth and enhances radiosensitivity of glioma cells in vitro and in vivo. Clin Cancer Res 9: 3272-3281.
59. Young IT. (1977). Proof without prejudice: use of the Kolmogorov-Smirnov test for the analysis of histograms from flow systems and other sources. J Histochem Cytochem 25: 935-941.
60. Zhao L, Gu J, Dong A, Zhang Y, Zhong L, He L et al. (2005). Potent antitumor activity of oncolytic adenovirus expressing mda-7/IL-24 for colorectal cancer. Hum Gene Ther 16: 845-858.