mda-7/IL-24, novel anticancer cytokine: Focus on bystander antitumor, radiosensitization and antiangiogenic properties and overview of the phase I clinical experience

International Journal of Oncology

Volumn 31, Issue 5, 2007, Pages 985-1007

  Lebedeva, Irina V ^a   Emdad, Luni ^a   Su, Zao Zhong ^a   Gupta, Pankaj ^a   Sauane, Moira ^a   Sarkar, Devanand ^a   Staudt, Michelle R ^a   Liu, Shi Jian ^a   Taher, Mohiuddin M ^a   Xiao, Ruoyu ^a   Barral, Paola ^a   Lee, Seok Geun ^a   Wang, Dongning ^a   Vozhilla, Nicollaq ^a   Park, Eun Sook ^a   Chatman, Lejuan ^a   Boukerche, Habib ^a,i   Ramesh, Rajagopal ^b   Inoue, Satoshi ^b   Chada, Sunil ^c   Li, Rong ^d   De Pass, Anthony L ^d   Mahasreshti, Parameshwar J ^e   Dmitriev, Igor P ^e   Curiel, David T ^e   Yacoub, Adly ^f   Grant, Steven ^g   Dent, Paul ^f   Senzer, Neil ^h   Nemunaitis, John J ^h   Fisher, Paul B ^a   more..

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

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c Introgen Therapeutics Inc   (United States)

^d LONG ISLAND UNIVERSITY   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

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

^h Mary Crowley Medical Research Center   (United States)

ⁱ INSERM   (France)

Author keywords

Antiangiogenesis; Apoptosis; Bystander effect; mda 7 IL 24; Phase I clinical trial; Radio sensitization

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; INTERLEUKIN 24; INTERLEUKIN DERIVATIVE; INTERLEUKIN-24; RADIOSENSITIZING AGENT; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER INVASION; CELL MOTION; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETICS; HUMAN; METABOLISM; PHASE 1 CLINICAL TRIAL; REVIEW; SIGNAL TRANSDUCTION; TRANSGENE;

ANGIOGENESIS INHIBITORS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL MOVEMENT; CLINICAL TRIALS, PHASE I AS TOPIC; ENDOPLASMIC RETICULUM; HUMANS; INTERLEUKINS; NEOPLASM INVASIVENESS; RADIATION-SENSITIZING AGENTS; SIGNAL TRANSDUCTION; TRANSGENES;

EID: 38449096542     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: None     Document Type: Review

References (124)

1. Jiang H and Fisher PB: Use of a sensitive and efficient subtraction hybridization protocol for the identification of genes differentially regulated during the induction of differentiation in human melanoma cells. Mol Cell Differ 1: 285-299, 1993.
2. Jiang H, Lin JJ, Su ZZ, Goldstein NI and Fisher PB: Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 11: 2477-2486, 1995.
3. Pestka S, Krause CD, Sarkar D, Walter MR, Shi Y and Fisher PB: Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 22: 929-979, 2004.
4. Sauane M, Gopalkrishnan RV, Sarkar D, Su ZZ, Lebedeva IV, Dent P, Pestka S and Fisher PB: MDA-7/IL-24: novel cancer growth suppressing and apoptosis inducing cytokine. Cytokine Growth Factor Rev 14: 35-51, 2003.
5. 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 and Fisher PB: 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, 2001.
6. Fisher PB, Gopalkrishnan RV, Chada S, Ramesh R, Grimm EA, Rosenfeld MR, Curiel DT and Dent P: Mda-7/IL-24, a novel cancer selective apoptosis inducing cytokine gene: from the laboratory into the clinic. Cancer Biol Ther 2: S23-S37, 2003.
7. Caudell EG, Mumm JB, Poindexter N, Ekmekcioglu S, Mhashilkar AM, Yang XH, Retter MW, Hill P, Chada S and Grimm EA: 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, 2002. (Pubitemid 34620018)
8. Sarkar D, Su ZZ, Lebedeva IV, Sauane M, Gopalkrishnan RV, Dent P and Fisher PB: Mda-7 (IL-24): signaling and functional roles. Biotechniques (Suppl): 30-39, 2002.
9. Wolk K, Kunz S, Asadullah K and Sabat R: Cutting edge: immune cells as sources and targets of the IL-10 family members? J Immunol 168: 5397-5402, 2002.
10. Ellerhorst JA, Prieto VG, Ekmekcioglu S, Broemeling L, Yekell S, Chada S and Grimm EA: Loss of MDA-7 expression with progression of melanoma. J Clin Oncol 20: 1069-1074, 2002.
11. Ekmekcioglu S, Ellerhorst J, Mhashilkar AM, Sahin AA, Read CM, Prieto VG, Chada S and Grimm EA: Down-regulated melanoma differentiation associated gene (mda-7) expression in human melanomas. Int J Cancer 94: 54-59, 2001.
12. Lebedeva IV, Su ZZ, Chang Y, Kitada S, Reed JC and Fisher PB: The cancer growth suppressing gene mda-7 induces apoptosis selectively in human melanoma cells. Oncogene 21: 708-718, 2002. (Pubitemid 34146283)
13. Jiang H, Su ZZ, Lin JJ, Goldstein NI, Young CS and Fisher PB: The melanoma differentiation associated gene mda-7 suppresses cancer cell growth. Proc Natl Acad Sci USA 93: 9160-9165, 1996.
14. Fisher PB: Is mda-7/IL-24 a 'magic bullet' for cancer? Cancer Res 65: 10128-10138, 2005.
15. Gopalkrishnan RV, Sauane M and Fisher PB: Cytokine and tumor cell apoptosis inducing activity of mda-7/IL-24. Int Immunopharmacol 4: 635-647, 2004.
16. Chada S, Sutton RB, Ekmekcioglu S, Ellerhorst J, Mumm JB, Leitner WW, Yang HY, Sahin AA, Hunt KK, Fuson KL, Poindexter N, Roth JA, Ramesh R, Grimm EA and Mhashilkar AM: MDA-7/IL-24 is a unique cytokine-tumor suppressor in the IL-10 family. Int Immunopharmacol 4: 649-667, 2004.
17. Lebedeva IV, Sauane M, Gopalkrishnan RV, Sarkar D, Su ZZ, Gupta P, Nemunaitis J, Cunningham C, Yacoub A, Dent P and Fisher PB: Mda-7/IL-24: exploiting cancer's Achilles' heel. Mol Ther 11: 4-18, 2005.
18. Gupta P, Su ZZ, Lebedeva IV, Sarkar D, Sauane M, Emdad L, Bachelor MA, Grant S, Curiel DT, Dent P and Fisher PB: Mda-7/IL-24: multifunctional cancer-specific apoptosis-inducing cytokine. Pharmacol Ther 111: 596-628, 2006.
19. Sarkar D, Dent P and Fisher PB: 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 and anti-allergy agents in medicinal chemistry 5: 259-274, 2006.
20. Inoue S, Shanker M, Miyahara R, Gopalan B, Patel S, Oida Y, Branch CD, Munshi A, Meyn RE, Aandreeff M, Tanaka F, Mhashilkar AM, Chada S and Ramesh R: MDA-7/IL-24-based cancer gene therapy: translation from the laboratory to the clinic. Curr Gene Ther 6: 73-91, 2006.
21. Lebedeva IV, Sarkar D, Su ZZ, Kitada S, Dent P, Stein CA, Reed JC and Fisher PB: 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, 2003.
22. Mhashilkar AM, Schrock RD, Hindi M, Liao J, Sieger K, Kourouma F, Zou-Yang XH, Onishi E, Takh O, Vedvick TS, Fanger G, Stewart L, Watson GJ, Snary D, Fisher PB, Saeki T, Roth JA, Ramesh R and Chada S: Melanoma differentiation associated gene-7 (mda-7): a novel anti-tumor gene for cancer gene therapy. Mol Med 7: 271-282, 2001.
23. Nishikawa T, Ramesh R, Munshi A, Chada S and Meyn RE: Adenovirus-mediated mda-7 (IL-24) gene therapy suppresses angiogenesis and sensitizes NSCLC xenograft tumors to radiation. Mol Ther 9: 818-828, 2004.
24. Saeki T, Mhashilkar A, Swanson X, Zou-Yang XH, Sieger K, Kawabe S, Branch CD, Zumstein L, Meyn RE, Roth JA, Chada S and Ramesh R: Inhibition of human lung cancer growth following adenovirus-mediated mda-7 gene expression in vivo. Oncogene 21: 4558-4566, 2002. (Pubitemid 34785732)
25. Su ZZ, Madireddi MT, Lin JJ, Young CS, Kitada S, Reed JC, Goldstein NI and Fisher PB: 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, 1998.
26. Yacoub A, Mitchell C, Lister A, Lebedeva IV, Sarkar D, Su ZZ, Sigmon C, McKinstry R, Ramakrishnan V, Qiao L, Broaddus WC, Gopalkrishnan RV, Grant S, Fisher PB and Dent P: 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, 2003.
27. 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 and Chada S: Intratumoral injection of INGN 241, a non-replicating adenovector expressing the melanoma-differentiation associated gene-7 (mda-7/IL24): biologic outcome in advanced cancer patients. Mol Ther 11: 160-172, 2005.
28. Cunningham CC, Chada S, Merritt JA, Tong A, Senzer N, Zhang Y, Mhashilkar A, Parker K, Vukelja S, Richards D, Hood J, Coffee K and Nemunaitis J: 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, 2005.
29. Fisher PB, Sarkar D, Lebedeva IV, Emdad L, Gupta P, Sauane M, Su Z-Z, Grant S, Dent P, Curiel DT, Senzer N and Nemunaitis J: Melanoma differentiation associated gene-7/interleukin-24 (mda-7/IL-24): novel gene therapeutic for metastatic melanoma. Toxicol Appl Pharmacol 2006, Nov 23 [epub ahead of print].
30. 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 and Chandrasekher YA: 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, 2002.
31. Sauane M, Gopalkrishnan RV, Lebedeva I, Mei MX, Sarkar D, Su ZZ, Kang DC, Dent P, Pestka S and Fisher PB: Mda-7/IL-24 induces apoptosis of diverse cancer cell lines through JAK/STAT-independent pathways. J Cell Physiol 196: 334-345, 2003.
32. Wang M, Tan Z, Zhang R, Kotenko SV and Liang P: Interleukin 24 (MDA-7/MOB-5) signals through two heterodimeric receptors, IL-22R1/IL-20R2 and IL-20R1/IL-20R2. J Biol Chem 277: 7341-7347, 2002.
33. Dumoutier L, Leemans C, Lejeune D, Kotenko SV and Renauld JC: Cutting edge: STAT activation by IL-19, IL-20 and mda-7 through IL-20 receptor complexes of two types. J Immunol 167: 3545-3549, 2001.
34. Chada S, Mhashilkar AM, Ramesh R, Mumm JB, Sutton RB, Bocangel D, Zheng M, Grimm EA and Ekmekcioglu S: 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, 2004.
35. Su Z, Emdad L, Sauane M, Lebedeva IV, Sarkar D, Gupta P, James CD, Randolph A, Valerie K, Walter MR, Dent P and Fisher PB: 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, 2005. (Pubitemid 41638030)
36. Madireddi MT, Su ZZ, Young CS, Goldstein NI and Fisher PB: Mda-7, a novel melanoma differentiation associated gene with promise for cancer gene therapy. Adv Exp Med Biol 465: 239-261, 2000.
37. Su ZZ, Lebedeva IV, Sarkar D, Gopalkrishnan RV, Sauane M, Sigmon C, Yacoub A, Valerie K, Dent P and Fisher PB: 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, 2003. (Pubitemid 36363380)
38. Yacoub A, Mitchell C, Hong Y, Gopalkrishnan RV, Su ZZ, Gupta P, Sauane M, Lebedeva IV, Curiel DT, Mahasreshti PJ, Rosenfeld MR, Broaddus WC, James CD, Grant S, Fisher PB and Dent P: MDA-7 regulates cell growth and radiosensitivity in vitro of primary (non-established) human glioma cells. Cancer Biol Ther 3: 739-751, 2004.
39. Yacoub A, Mitchell C, Brannon J, Rosenberg E, Qiao L, McKinstry R, Linehan WM, Su ZS, Sarkar D, Lebedeva IV, Valerie K, Gopalkrishnan RV, Grant S, Fisher PB and Dent P: MDA-7 (interleukin-24) inhibits the proliferation of renal carcinoma cells and interacts with free radicals to promote cell death and loss of reproductive capacity. Mol Cancer Ther 2: 623-632, 2003.
40. Su ZZ, Lebedeva IV, Sarkar D, Emdad L, Gupta P, Kitada S, Dent P, Reed JC and Fisher PB: 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-xL or bcl-2. Oncogene 25: 2339-2348, 2006.
41. Saito Y, Miyahara R, Gopalan B, Litvak A, Inoue S, Shanker M, Branch CD, Mhashilkar AM, Roth JA, Chada S and Ramesh R: Selective induction of cell cycle arrest and apoptosis in human prostate cancer cells through adenoviral transfer of the melanoma differentiation-associated-7 (mda-7)/interleukin-24 (IL-24) gene. Cancer Gene Ther 12: 238-247, 2005. (Pubitemid 40315183)
42. Lebedeva IV, Su ZZ, Sarkar D, Gopalkrishnan RV, Waxman S, Yacoub A, Dent P and Fisher PB: 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, 2005.
43. Lebedeva IV, Su ZZ, Sarkar D, Kitada S, Dent P, Waxman S, Reed JC and Fisher PB: Melanoma differentiation associated gene-7, mda-7/interleukin-24, induces apoptosis in prostate cancer cells by promoting mitochondrial dysfunction and inducing reactive oxygen species. Cancer Res 63: 8138-8144, 2003.
44. Su Z, Lebedeva IV, Gopalkrishnan RV, Goldstein NI, Stein CA, Reed JC, Dent P and Fisher PB: A combinatorial approach for selectively inducing programmed cell death in human pancreatic cancer cells. Proc Natl Acad Sci USA 98: 10332-10337, 2001.
45. Sauane M, Lebedeva IV, Su ZZ, Choo HT, Randolph A, Valerie K, Dent P, Gopalkrishnan RV and Fisher PB: Melanoma differentiation associated gene-7/interleukin-24 promotes tumor cell-specific apoptosis through both secretory and nonsecretory pathways. Cancer Res 64: 2988-2993, 2004.
46. Gupta P, Walter MR, Su ZZ, Lebedeva IV, Emdad L, Randolph A, Valerie K, Sarkar D and Fisher PB: BiP/GRP78 is an intracellular target for MDA-7/IL-24 induction of cancer-specific apoptosis. Cancer Res 66: 8182-8191, 2006. (Pubitemid 44299186)
47. Sauane M, Gupta P, Lebedeva IV, Su Z-Z, Sarkar D, Randolph A, Valerie K, Gopalkrishnan R and Fisher PB: N-glycosylation of MDA-7/IL-24 is dispensable for tumor cell-specific apoptosis and bystander anti-tumor activity. Cancer Res 66: 11869-11877, 2006.
48. Berridge MJ: The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32: 235-249, 2002.
49. Berridge MJ, Lipp P and Bootman MD: The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11-21, 2000.
50. Sarkar D, Su ZZ, Lebedeva IV, Sauane M, Gopalkrishnan RV, Valerie K, Dent P and Fisher PB: Mda-7 (IL-24) mediates selective apoptosis in human melanoma cells by inducing the coordinated overexpression of the GADD family of genes by means of p38 MAPK. Proc Natl Acad Sci USA 99: 10054-10059, 2002.
51. Lingappa VR and Blobel G: Early events in the biosynthesis of secretory and membrane proteins: the signal hypothesis. Recent Prog Horm Res 36: 451-475, 1980.
52. Sieger KA, Mhashilkar AM, Stewart A, Sutton RB, Strube RW, Chen SY, Pataer A, Swisher SG, Grimm EA, Ramesh R and Chada S: The tumor suppressor activity of MDA-7/IL-24 is mediated by intracellular protein expression in NSCLC cells. Mol Ther 9: 355-367, 2004.
53. Sauane M, Gopalkrishnan RV, Choo HT, Gupta P, Lebedeva IV, Yacoub A, Dent P and Fisher PB: Mechanistic aspects of mda-7/IL-24 cancer cell selectivity analysed via a bacterial fusion protein. Oncogene 23: 7679-7690, 2004.
54. Zhan Q, Lord KA, Alamo I Jr, Hollander MC, Carrier F, Ron D, Kohn KW, Hoffman B, Liebermann DA and Fornace AJ Jr: The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol Cell Biol 14: 2361-2371, 1994.
55. Sainz-Perez A, Gary-Gouy H, Portier A, Davi F, Merle-Beral H, Galanaud P and Dalloul A: High Mda-7 expression promotes malignant cell survival and p38 MAP kinase activation in chronic lymphocytic leukemia. Leukemia 20: 498-504, 2006.
56. Pataer A, Vorburger SA, Barber GN, Chada S, Mhashilkar AM, Zou-Yang H, Stewart AL, Balachandran S, Roth JA, Hunt KK and Swisher SG: Adenoviral transfer of the melanoma differentiation-associated gene 7 (mda7) induces apoptosis of lung cancer cells via up-regulation of the double-stranded RNA-dependent protein kinase (PKR). Cancer Res 62: 2239-2243, 2002.
57. Emdad L, Lebedeva IV, Su Z-Z, Gupta P, Sarkar D, Settleman J and Fisher PB: Combinatorial treatment of non-small-cell lung cancers with gefitinib and Ad.mda-7 enhances apoptosis-induction and reverses resistance to a single therapy. J Cell Physiol 210: 549-559, 2006.
58. Chada S, Mhashilkar AM, Liu Y, Nishikawa T, Bocangel D, Zheng M, Vorburger SA, Pataer A, Swisher SG, Ramesh R, Kawase K, Meyn RE and Hunt KK: 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, 2006.
59. Pataer A, Vorburger SA, Chada S, Balachandran S, Barber GN, Roth JA, Hunt KK and Swisher SG: Melanoma differentiation-associated gene-7 protein physically associates with the double-stranded RNA-activated protein kinase PKR. Mol Ther 11: 717-723, 2005.
60. Fawcett TW, Martindale JL, Guyton KZ, Hai T and Holbrook NJ: Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem J 339: 135-141, 1999.
61. Yacoub A, Mitchell C, Lebedeva IV, Sarkar D, Su ZZ, McKinstry R, Gopalkrishnan RV, Grant S, Fisher PB and Dent P: Mda-7 (IL-24) inhibits growth and enhances radiosensitivity of glioma cells in vitro via JNK signaling. Cancer Biol Ther 2: 347-353, 2003.
62. Kawabe S, Nishikawa T, Munshi A, Roth JA, Chada S and Meyn RE: Adenovirus-mediated mda-7 gene expression radiosensitizes non-small cell lung cancer cells via TP53-independent mechanisms. Mol Ther 6: 637-644, 2002.
63. Mhashilkar AM, Stewart AL, Sieger K, Yang HY, Khimani AH, Ito I, Saito Y, Hunt KK, Grimm EA, Roth JA, Meyn RE, Ramesh R and Chada S: MDA-7 negatively regulates the beta-catenin and PI3K signaling pathways in breast and lung tumor cells. Mol Ther 8: 207-219, 2003.
64. Gopalan B, Litvak A, Sharma S, Mhashilkar AM, Chada S and Ramesh R: Activation of the Fas-FasL signaling pathway by MDA-7/IL-24 kills human ovarian cancer cells. Cancer Res 65: 3017-3024, 2005.
65. Emdad L, Sarkar D, Lebedeva IV, Su ZZ, Gupta P, Mahasreshti PJ, Dent P, Curiel DT and Fisher PB: Ionizing radiation enhances adenoviral vector expressing mda-7/IL-24-mediated apoptosis in human ovarian cancer. J Cell Physiol 208: 298-306, 2006.
66. Leach JK, van Tuyle G, Lin PS, Schmidt-Ullrich R and Mikkelsen RB: Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res 61: 3894-3901, 2001.
67. Leach JK, Black SM, Schmidt-Ullrich RK and Mikkelsen RB: Activation of constitutive nitric-oxide synthase activity is an early signaling event induced by ionizing radiation. J Biol Chem 277: 15400-15406, 2002.
68. Nishikawa T, Munshi A, Story MD, Ismail S, Stevens C, Chada S and Meyn RE: Adenoviral-mediated mda-7 expression suppresses DNA repair capacity and radiosensitizes non-small-cell lung cancer cells. Oncogene 23: 7125-7131, 2004.
69. Su Z, Shi Y and Fisher PB: Cooperation between AP1 and PEA3 sites within the progression elevated gene-3 (PEG-3) promoter regulate basal and differential expression of PEG-3 during progression of the oncogenic phenotype in transformed rat embryo cells. Oncogene 19: 3411-3421, 2000.
70. Su Z, Shi Y, Friedman R, Qiao L, McKinstry R, Hinman D, Dent P and Fisher PB: PEA3 sites within the progression elevated gene-3 (PEG-3) promoter and mitogen-activated protein kinase contribute to differential PEG-3 expression in Ha-ras and v-raf oncogene transformed rat embryo cells. Nucleic Acids Res 29: 1661-1671, 2001.
71. Su ZZ, Goldstein NI, Jiang H, Wang MN, Duigou GJ, Young CS and Fisher PB: PEG-3, a nontransforming cancer progression gene, is a positive regulator of cancer aggressiveness and angiogenesis. Proc Natl Acad Sci USA 96: 15115-15120, 1999.
72. Emdad L, Sarkar D, Su ZZ, Boukerche H, Bar-Eli M and Fisher PB: Progression elevated gene-3 (PEG-3) induces pleiotropic effects on tumor progression: modulation of genomic stability and invasion. J Cell Physiol 202: 135-146, 2005.
73. Sarkar D, Su ZZ, Vozhilla N, Park ES, Gupta P and Fisher PB: Dual cancer-specific targeting strategy cures primary and distant breast carcinomas in nude mice. Proc Natl Acad Sci USA 102: 14034-14039, 2005.
74. Sarkar D, Su ZZ, Vozhilla N, Park ES, Randolph A, Valerie K and Fisher PB: Targeted virus replication plus immunotherapy eradicates primary and distant pancreatic tumors in nude mice. Cancer Res 65: 9056-9063, 2005.
75. Chen J, Chada S, Mhashilkar A and Miano JM: Tumor suppressor MDA-7/IL-24 selectively inhibits vascular smooth muscle cell growth and migration. Mol Ther 8: 220-229, 2003. (Pubitemid 37062832)
76. Ramesh R, Ito I, Saito Y, Wu Z, Mhashikar AM, Wilson DR, Branch CD, Roth JA and Chada S: Local and systemic inhibition of lung tumor growth after nanoparticle-mediated mda-7/IL-24 gene delivery. DNA Cell Biol 23: 850-857, 2004.
77. Welch DR, Bisi JE, Miller BE, Conaway D, Seftor EA, Yohem KH, Gilmore LB, Seftor RE, Nakajima M and Hendrix MJ: Characterization of a highly invasive and spontaneously metastatic human malignant melanoma cell line. Int J Cancer 47: 227-237, 1991.
78. Folkman J: The role of angiogenesis in tumor growth. Semin Cancer Biol 3: 65-71, 1992.
79. Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27-31, 1995.
80. Fidler IJ and Ellis LM: The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell 79: 185-188, 1994.
81. Cristofanilli M, Charnsangavej C and Hortobagyi GN: Angiogenesis modulation in cancer research: novel clinical approaches. Nat Rev Drug Discov 1: 415-426, 2002.
82. Kerr DJ: Targeting angiogenesis in cancer: clinical development of bevacizumab. Nat Clin Pract Oncol 1: 39-43, 2004. (Pubitemid 40812647)
83. O'Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH and Folkman J: Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79: 315-328, 1994.
84. O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR and Folkman J: Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88: 277-285, 1997.
85. Shaheen RM, Davis DW, Liu W, Zebrowski BK, Wilson MR, Bucana CD, McConkey DJ, McMahon G and Ellis LM: Antiangiogenic therapy targeting the tyrosine kinase receptor for vascular endothelial growth factor receptor inhibits the growth of colon cancer liver metastasis and induces tumor and endothelial cell apoptosis. Cancer Res 59: 5412-5416, 1999.
86. Moses MA, Sudhalter J and Langer R: Identification of an inhibitor of neovascularization from cartilage. Science 248: 1408-1410, 1990.
87. Laird AD, Vajkoczy P, Shawver LK, Thurnher A, Liang C, Mohammadi M, Schlessinger J, Ullrich A, Hubbard SR, Blake RA, Fong TA, Strawn LM, Sun L, Tang C, Hawtin R, Tang F, Shenoy N, Hirth KP, McMahon G and Cherrington S: U6668 is a potent antiangiogenic and antitumor agent that induces regression of established tumors. Cancer Res 60: 4152-4160, 2000.
88. Kumar CC, Malkowski M, Yin Z, Tanghetti E, Yaremko B, Nechuta T, Varner J, Liu M, Smith EM, Neustadt B, Presta M and Armstrong L: Inhibition of angiogenesis and tumor growth by SCH221153, a dual alpha(v)beta3 and alpha(v)beta5 integrin receptor antagonist. Cancer Res 61: 2232-2238, 2001.
89. Lingen MW, Polverini PJ and Bouck NP: Inhibition of squamous cell carcinoma angiogenesis by direct interaction of retinoic acid with endothelial cells. Lab Invest 74: 476-483, 1996. (Pubitemid 26072088)
90. Voest EE, Kenyon BM, O'Reilly MS, Truitt G, D'Amato RJ and Folkman J: Inhibition of angiogenesis in vivo by interleukin 12. J Natl Cancer Inst 87: 581-586, 1995.
91. Singh RK, Gutman M, Bucana CD, Sanchez R, Llansa N and Fidler IJ: Interferons alpha and beta down-regulate the expression of basic fibroblast growth factor in human carcinomas. Proc Natl Acad Sci USA 92: 4562-4566, 1995.
92. 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 and Boquio A: 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, 2003.
93. Yu H and Jove R: The STATs of cancer - new molecular targets come of age. Nat Rev Cancer 4: 97-105, 2004.
94. Ramesh R, Ito I, Gopalan B, Saito Y, Mhashilkar AM and Chada S: Ectopic production of MDA-7/IL-24 inhibits invasion and migration of human lung cancer cells. Mol Ther 9: 510-518, 2004.
95. Tedjarati S, Baker CH, Apte S, Huang S, Wolf JK, Killion JJ and Fidler IJ: Synergistic therapy of human ovarian carcinoma implanted orthotopically in nude mice by optimal biological dose of pegylated interferon alpha combined with paclitaxel. Clin Cancer Res 8: 2413-2422, 2002. (Pubitemid 34753617)
96. Inoue K, Chikazawa M, Fukata S, Yoshikawa C and Shuin T: Frequent administration of angiogenesis inhibitor TNP-470 (AGM-1470) at an optimal biological dose inhibits tumor growth and metastasis of metastatic human transitional cell carcinoma in the urinary bladder. Clin Cancer Res 8: 2389-2398, 2002.
97. Hirata A, Ogawa S, Kometani T, Kuwano T, Naito S, Kuwano M and Ono M: ZD1839 (Iressa) induces antiangiogenic effects through inhibition of epidermal growth factor receptor tyrosine kinase. Cancer Res 62: 2554-2560, 2002.
98. Inoue S, Branch CD, Gallick GE, Chada S and Ramesh R: Inhibition of Src kinase activity by Ad-mda7 suppresses vascular endothelial growth factor expression in prostate carcinoma cells. Mol Ther 12: 707-715, 2005.
99. Lebedeva IV, Sarkar D, Su ZZ, Gopalkrishnan RV, Athar M, Randolph A, Valerie K, Dent P and Fisher PB: Molecular target-based therapy of pancreatic cancer. Cancer Res 66: 2403-2413, 2006.
100. Madireddi MT, Dent P and Fisher PB: Regulation of mda-7 gene expression during human melanoma differentiation. Oncogene 19: 1362-1368, 2000.
101. Madireddi MT, Dent P and Fisher PB: AP-1 and C/EBP transcription factors contribute to mda-7 gene promoter activity during human melanoma differentiation. J Cell Physiol 185: 36-46, 2000.
102. Ekmekcioglu S, Ellerhorst JA, Mumm JB, Zheng M, Broemeling L, Prieto VG, Stewart AL, Mhashilkar AM, Chada S and Grimm EA: Negative association of melanoma differentiation-associated gene (mda-7) and inducible nitric oxide synthase (iNOS) in human melanoma: MDA-7 regulates iNOS expression in melanoma cells. Mol Cancer Ther 2: 9-17, 2003.
103. Schaefer G, Venkataraman C and Schindler U: Cutting edge: FISP (IL-4-induced secreted protein), a novel cytokine-like molecule secreted by Th2 cells. J Immunol 166: 5859-5863, 2001.
104. Ekmekcioglu S, Okcu MF, Colome-Grimmer MI, Owen-Schaub L, Buzaid AC and Grimm EA: Differential increase of Fas ligand expression on metastatic and thin or thick primary melanoma cells compared with interleukin-10. Melanoma Res 9: 261-272, 1999. (Pubitemid 29461144)
105. Garn H, Schmidt A, Grau V, Stumpf S, Kaufmann A, Becker M, Gemsa D and Siese A: IL-24 is expressed by rat and human macrophages. Immunobiology 205: 321-334, 2002. (Pubitemid 34846740)
106. Poindexter NJ, Walch ET, Chada S and Grimm EA: Cytokine induction of interleukin-24 in human peripheral blood mononuclear cells. J Leukoc Biol 78: 745-752, 2005.
107. Aggarwal S, Takada Y, Mhashilkar AM, Sieger K, Chada S and Aggarwal BB: Melanoma differentiation-associated gene-7/IL-24 gene enhances NF-kappa B activation and suppresses apoptosis induced by TNF. J Immunol 173: 4368-4376, 2004.
108. Kumar A, Haque J, Lacoste J, Hiscott J and Williams BR: Double-stranded RNA-dependent protein kinase activates transcription factor NF-kappa B by phosphorylating I kappa B. Proc Natl Acad Sci USA 91: 6288-6292, 1994.
109. Bonnet MC, Weil R, Dam E, Hovanessian AG and Meurs EF: PKR stimulates NF-kappaB irrespective of its kinase function by interacting with the IkappaB kinase complex. Mol Cell Biol 20: 4532-4542, 2000. (Pubitemid 30396101)
110. Ishii T, Kwon H, Hiscott J, Mosialos G and Koromilas AE: Activation of the I kappa B alpha kinase (IKK) complex by double-stranded RNA-binding defective and catalytic inactive mutants of the interferon-inducible protein kinase PKR. Oncogene 20: 1900-1912, 2001.
111. Miyahara R, Banerjee S, Kawano K, Efferson C, Tsuda N, Miyahara Y, Ioannides CG, Chada S and Ramesh R: Melanoma differentiation-associated gene-7 (mda-7)/interleukin (IL)-24 induces anticancer immunity in a syngeneic murine model. Cancer Gene Ther 13: 753-761, 2006. (Pubitemid 44100488)
112. Bardeesy N and De Pinho RA: Pancreatic cancer biology and genetics. Nat Rev Cancer 2: 897-909, 2002.
113. Su ZZ, Shi Y and Fisher PB: 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, 1997.
114. Smyth MJ, Hayakawa Y, Takeda K and Yagita H: New aspects of natural-killer-cell surveillance and therapy of cancer. Nat Rev Cancer 2: 850-861, 2002.
115. Zheng M, Bocangel D, Doneske B, Mhashilkar A, Ramesh R, Hunt KK, Ekmekcioglu S, Sutton RB, Poindexter N, Grimm EA and Chada S: Human interleukin 24 (MDA-7/IL-24) protein kills breast cancer cells via the IL-20 receptor and is antagonized by IL-10. Cancer Immunol Immunother 56: 205-215, 2007. (Pubitemid 44833094)
116. Saeki T, Mhashilkar A, Chada S, Branch C, Roth JA and Ramesh R: Tumor-suppressive effects by adenovirus-mediated mda-7 gene transfer in non-small cell lung cancer cell in vitro. Gene Ther 7: 2051-2057, 2000.
117. McKenzie T, Liu Y, Fanale M, Swisher SG, Chada S and Hunt KK: Combination therapy of Ad-mda7 and trastuzumab increases cell death in Her-2/neu- overexpressing breast cancer cells. Surgery 136: 437-442, 2004.
118. Oida Y, Gopalan B, Miyahara R, Inoue S, Branch CD, Mhashilkar AM, Lin E, Bekele BN, Roth JA, Chada S and Ramesh R: Sulindac enhances adenoviral vector expressing mda-7/IL-24-mediated apoptosis in human lung cancer. Mol Cancer Ther 4: 291-304, 2005.
119. Swisher SG, Roth JA, Nemunaitis J, et al: Adenovirus-mediated p53 gene transfer in advanced non-small-cell lung cancer. J Natl Cancer Inst 91: 763-771, 1999.
120. Lang FF, Bruner JM, Fuller GN, Aldape K, Prados MD, Chang S, Berger MS, McDermott MW, Kunwar SM, Junck LR, Chandler W, Zwiebel JA, Kaplan RS and Yung WK: Phase I trial of adenovirus-mediated p53 gene therapy for recurrent glioma: biological and clinical results. J Clin Oncol 21: 2508-2518, 2003.
121. Bocangel D, Zheng M, Mhashilkar A, Liu Y, Ramesh R, Hunt KK and Chada S: Combinatorial synergy induced by adenoviral-mediated mda-7 and Herceptin in Her-2+ breast cancer cells. Cancer Gene Ther 13: 958-968, 2006.
122. Zhao L, Gu J, Dong A, Zhang Y, Zhong L, He L, Wang Y, Zhang J, Zhang Z, Huiwang J, Qian Q, Qian C and Liu X: Potent antitumor activity of oncolytic adenovirus expressing mda-7/IL-24 for colorectal cancer. Hum Gene Ther 16: 845-858, 2005.
123. Sarkar D, Lebedeva IV, Su ZZ, Park ES, Chatman L, Vozhilla N, Dent P, Curiel DT and Fisher PB: Eradication of therapy resistant human prostate tumors using a cancer terminator virus. Cancer Res (In press).
124. Zerbini LF, Czibere A, Wang Y, et al: A novel pathway involving mda-7/IL-24 mediates NSAID induced apoptosis and growth arrest of cancer cells. Cancer Res 66: 11922-11931, 2006.