IL-24 gene transfer sensitizes melanoma cells to erlotinib through modulation of the Apaf-1 and Akt signaling pathways

Melanoma Research

Volumn 21, Issue 1, 2011, Pages 44-56

  Deng, Wu Guo ^a   Kwon, John ^a   Ekmekcioglu, Suhendan ^a   Poindexter, Nancy J ^a   Grimm, Elizabeth A ^a  

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

Author keywords

Akt; Apaf 1; Epidermal growth factor receptor; Erlotinib; Interleukin 24; Melanoma

Indexed keywords

ADENOVIRUS VECTOR; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 9; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; INTERLEUKIN 24; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; APAF1 PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE; INTERLEUKIN-24; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER GENE THERAPY; CANCER INHIBITION; CELL SURVIVAL; CELL VIABILITY; DRUG POTENCY; GENE TRANSFER; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MELANOMA CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MELANOMA; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TRANSFER TECHNIQUES; HUMANS; INTERLEUKINS; MELANOMA; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; QUINAZOLINES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 78649309946     PISSN: 09608931     EISSN: None     Source Type: Journal    
DOI: 10.1097/CMR.0b013e3283382155     Document Type: Article

References (58)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin 2007; 57:43-66.
2. Chada S, Sutton RB, Ekmekcioglu S, Ellerhorst J, Mumm JB, Leitner WW, et al. MDA-7/IL-24 is a unique cytokine-tumor suppressor in the IL-10 family. Int Immunopharmacol 2004; 4:649-667. (Pubitemid 38553886)
3. Sauane M, Gopalkrishnan RV, Sarkar D, Su ZZ, Lebedeva IV, Dent P, et al. MDA-7/IL-24: novel cancer growth suppressing and apoptosis inducing cytokine. Cytokine Growth Factor Rev 2003; 14:35-51. (Pubitemid 36098430)
4. Allen M, Pratscher B, Roka F, Krepler C, Wacheck V, Schofer C, et al. Loss of novel mda-7 splice variant (mda-7s) expression is associated with metastatic melanoma. J Invest Dermatol 2004; 123:583-588. (Pubitemid 39095631)
5. Ekmekcioglu S, Ellerhorst JA, Mumm JB, Zheng M, Broemeling L, Prieto VG, et al. 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 2003; 2:9-17.
6. Chada S, Mhashilkar AM, Ramesh R, Mumm JB, Sutton RB, Bocangel D, et al. Bystander activity of Ad-mda7: human MDA-7 protein kills melanoma cells via an IL-20 receptor-dependent but STAT3-independent mechanism. Mol Ther 2004; 10:1085-1095. (Pubitemid 39625252)
7. Lebedeva IV, Su ZZ, Sarkar D, Kitada S, Dent P, Waxman S, et al. 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 2003; 63:8138-8144. (Pubitemid 37549460)
8. Ekmekcioglu S, Mumm JB, Udtha M, Chada S, Grimm EA. Killing of human melanoma cells induced by activation of class I interferon-regulated signaling pathways via MDA-7/IL-24. Cytokine 2008; 43:34-44.
9. Gupta P, Emdad L, Lebedeva IV, Sarkar D, Dent P, Curiel DT, et al. Targeted combinatorial therapy of non-small cell lung carcinoma using a GST-fusion protein of full-length or truncated MDA-7/IL-24 with Tarceva. J Cell Physiol 2008; 215:827-836. (Pubitemid 351632704)
10. Gopalan B, Shanker M, Chada S, Ramesh R. MDA-7/IL-24 suppresses human ovarian carcinoma growth in vitro and in vivo. Mol Cancer 2007; 6:11.
11. Fisher PB, Sarkar D, Lebedeva IV, Emdad L, Gupta P, Sauane M, et al. Melanoma differentiation associated gene-7/interleukin-24 (mda-7/IL-24): novel gene therapeutic for metastatic melanoma. Toxicol Appl Pharmacol 2007; 224:300-307. (Pubitemid 47575670)
12. Bocangel D, Zheng M, Mhashilkar A, Liu Y, Ramesh R, Hunt KK, et al. Combinatorial synergy induced by adenoviral-mediated mda-7 and Herceptin in Her-2+ breast cancer cells. Cancer Gene Ther 2006; 13:958-968. (Pubitemid 44373796)
13. McKenzie T, Liu Y, Fanale M, Swisher SG, Chada S, Hunt KK. Combination therapy of Ad-mda7 and trastuzumab increases cell death in Her-2/ neuoverexpressing breast cancer cells. Surgery 2004; 136:437-442. (Pubitemid 39037685)
14. Emdad L, Lebedeva IV, Su ZZ, Gupta P, Sarkar D, Settleman J, et al. 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 2007; 210:549-559. (Pubitemid 44956899)
15. Pataer A, Vorburger SA, Chada S, Balachandran S, Barber GN, Roth JA, et al. Melanoma differentiation-associated gene-7 protein physically associates with the double-stranded RNA-activated protein kinase PKR. Mol Ther 2005; 11:717-723. (Pubitemid 40567976)
16. Mhashilkar AM, Stewart AL, Sieger K, Yang HY, Khimani AH, Ito I, et al. MDA-7 negatively regulates the beta-catenin and PI3K signaling pathways in breast and lung tumor cells. Mol Ther 2003; 8:207-219. (Pubitemid 37062831)
17. Pataer A, Vorburger SA, Barber GN, Chada S, Mhashilkar AM, Zou-Yang H, et al. 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 2002; 62:2239-2243.
18. Akslen LA, Puntervoll H, Bachmann IM, Straume O, Vuhahula E, Kumar R, et al. Mutation analysis of the EGFR-NRAS-BRAF pathway in melanomas from black Africans and other subgroups of cutaneous melanoma. Melanoma Res 2008; 18:29-35. (Pubitemid 351628053)
19. Qiu L, Wang Q, Di W, Jiang Q, Schefeller E, Derby S, et al. Transient activation of EGFR/AKT cell survival pathway and expression of survivin contribute to reduced sensitivity of human melanoma cells to betulinic acid. Int J Oncol 2005; 27:823-830.
20. Andl CD, Mizushima T, Oyama K, Bowser M, Nakagawa H, Rustgi AK. EGFR-induced cell migration is mediated predominantly by the JAK-STAT pathway in primary esophageal keratinocytes. Am J Physiol Gastrointest Liver Physiol 2004; 287:G1227-G1237. (Pubitemid 39551854)
21. Woodburn JR. The epidermal growth factor receptor and its inhibition in cancer therapy. Pharmacol Ther 1999; 82:241-250. (Pubitemid 29255919)
22. Qiu X, Montgomery E. Expression of EGFR in gastric stromal tumors: a clinicopathologic study. Appl Immunohistochem Mol Morphol 2008; 16:310-315.
23. Magkou C, Nakopoulou L, Zoubouli C, Karali K, Theohari I, Bakarakos P, et al. Expression of the epidermal growth factor receptor (EGFR) and the phosphorylated EGFR in invasive breast carcinomas. Breast Cancer Res 2008; 10:R49.
24. Pryczynicz A, Guzinska-Ustymowicz K, Kemona A, Czyzewska J. Expression of EGF and EGFR strongly correlates with metastasis of pancreatic ductal carcinoma. Anticancer Res 2008; 28:1399-1404. (Pubitemid 351578886)
25. Marks RA, Zhang S, Montironi R, McCarthy RP, MacLennan GT, Lopez-Beltran A, et al. Epidermal growth factor receptor (EGFR) expression in prostatic adenocarcinoma after hormonal therapy: a fluorescence in situ hybridization and immunohistochemical analysis. Prostate 2008; 68:919-923. (Pubitemid 351794156)
26. Berghmans T, Mascaux C, Haller A, Meert AP, Van HP, Sculier JP. EGFR, TTF-1 and Mdm2 expression in stage III non-small cell lung cancer: a positive association. Lung Cancer 2008; 62:35-44.
27. Leibl S, Zigeuner R, Hutterer G, Chromecki T, Rehak P, Langner C. EGFR expression in urothelial carcinoma of the upper urinary tract is associated with disease progression and metaplastic morphology. APMIS 2008; 116:27-32. (Pubitemid 351191103)
28. Vasile E, Tibaldi C, Chella A, Falcone A. Erlotinib after failure of gefitinib in patients with advanced non-small cell lung cancer previously responding to gefitinib. J Thorac Oncol 2008; 3:912-914.
29. Bozec A, Sudaka A, Fischel JL, Brunstein MC, Etienne-Grimaldi MC, Milano G. Combined effects of bevacizumab with erlotinib and irradiation: a preclinical study on a head and neck cancer orthotopic model. Br J Cancer 2008; 99:93-99. (Pubitemid 351920227)
30. Altavilla G, Arrigo C, Santarpia MC, Galletti G, Picone G, Marabello G, et al. Erlotinib therapy in a patient with non-small-cell lung cancer and brain metastases. J Neurooncol 2008; 90:31-33.
31. Twelves C, Trigo JM, Jones R, De RF, Rakhit A, Fettner S, et al. Erlotinib in combination with capecitabine and docetaxel in patients with metastatic breast cancer: a dose-escalation study. Eur J Cancer 2008; 44:419-426.
32. Welch SA, Moore MJ. Erlotinib: success of a molecularly targeted agent for the treatment of advanced pancreatic cancer. Future Oncol 2007; 3:247-254. (Pubitemid 47018635)
33. Dragovich T, Huberman M, Von Hoff DD, Rowinsky EK, Nadler P, Wood D, et al. Erlotinib plus gemcitabine in patients with unresectable pancreatic cancer and other solid tumors: phase IB trial. Cancer Chemother Pharmacol 2007; 60:295-303. (Pubitemid 46742546)
34. Catania C, De Pas TM, Pelosi G, Manzotti M, Adamoli L, Nole F, et al. Erlotinib-induced breast cancer regression. Ann Pharmacother 2006; 40:2043-2047. (Pubitemid 44747477)
35. Hightower M. Erlotinib (OSI-774, Tarceva), a selective epidermal growth factor receptor tyrosine kinase inhibitor, in combination with chemotherapy for advanced non-small-cell lung cancer. Clin Lung Cancer 2003; 4:336-338. (Pubitemid 36798555)
36. Jackman DM, Yeap BY, Lindeman NI, Fidias P, Rabin MS, Temel J, et al. Phase II clinical trial of chemotherapy-naive patients ≥70 years of age treated with erlotinib for advanced non-small-cell lung cancer. J Clin Oncol 2007; 25:760-766. (Pubitemid 350002874)
37. Yamasaki F, Johansen MJ, Zhang D, Krishnamurthy S, Felix E, Bartholomeusz C, et al. Acquired resistance to erlotinib in A-431 epidermoid cancer cells requires down-regulation of MMAC1/PTEN and up-regulation of phosphorylated Akt. Cancer Res 2007; 67:5779-5788. (Pubitemid 46985011)
38. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005; 2:e73.
39. Pao W, Wang TY, Riely GJ, Miller VA, Pan Q, Ladanyi M, et al. KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2005; 2:e17.
40. Lasithiotakis KG, Sinnberg TW, Schittek B, Flaherty KT, Kulms D, Maczey E, et al. Combined inhibition of MAPK and mTOR signaling inhibits growth, induces cell death, and abrogates invasive growth of melanoma cells. J Invest Dermatol 2008; 128:2013-2023. (Pubitemid 352001225)
41. Meier F, Busch S, Lasithiotakis K, Kulms D, Garbe C, Maczey E, et al. Combined targeting of MAPK and AKT signalling pathways is a promising strategy for melanoma treatment. Br J Dermatol 2007; 156:1204-1213. (Pubitemid 47029801)
42. Collisson EA, De A, Suzuki H, Gambhir SS, Kolodney MS. Treatment of metastatic melanoma with an orally available inhibitor of the Ras-Raf-MAPK cascade. Cancer Res 2003; 63:5669-5673. (Pubitemid 37187459)
43. Ivanov VN, Hei TK. Combined treatment with EGFR inhibitors and arsenite upregulated apoptosis in human EGFR-positive melanomas: a role of suppression of the PI3K-AKT pathway. Oncogene 2005; 24:616-626. (Pubitemid 40188566)
44. Ye M, Hu D, Tu L, Zhou X, Lu F, Wen B, et al. Involvement of PI3K/Akt signaling pathway in hepatocyte growth factor-induced migration of uveal melanoma cells. Invest Ophthalmol Vis Sci 2008; 49:497-504.
45. Meier F, Schittek B, Busch S, Garbe C, Smalley K, Satyamoorthy K, et al. The RAS/RAF/MEK/ERK and PI3K/AKT signaling pathways present molecular targets for the effective treatment of advanced melanoma. Front Biosci 2005; 10:2986-3001. (Pubitemid 40910537)
46. Ueno Y, Sakurai H, Tsunoda S, Choo MK, Matsuo M, Koizumi K, et al. Heregulin-induced activation of ErbB3 by EGFR tyrosine kinase activity promotes tumor growth and metastasis in melanoma cells. Int J Cancer 2008; 123:340-347. (Pubitemid 351842018)
47. Deng WG, Wu G, Ueda K, Xu K, Roth JA, Ji L. Enhancement of antitumor activity of cisplatin in human lung cancer cells by tumor suppressor FUS1. Cancer Gene Ther 2008; 15:29-39. (Pubitemid 350261296)
48. Deng WG, Kawashima H, Wu G, Jayachandran G, Xu K, Minna JD, et al. Synergistic tumor suppression by coexpression of FUS1 and p53 is associated with down-regulation of murine double min-2 and activation of the apoptotic protease-activating factor 1-dependent apoptotic pathway in human non-small cell lung cancer cells. Cancer Res 2007; 67:709-717. (Pubitemid 46192211)
49. Mustika R, Budiyanto A, Nishigori C, Ichihashi M, Ueda M. Decreased expression of Apaf-1 with progression of melanoma. Pigment Cell Res 2005; 18:59-62. (Pubitemid 40170607)
50. Sarkar D, Su ZZ, Lebedeva IV, Sauane M, Gopalkrishnan RV, Valerie K, et al. 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 p38MAPK. Proc Natl Acad Sci U S A 2002; 99:10054-10059. (Pubitemid 34831171)
51. Bratton SB, Walker G, Srinivasula SM, Sun XM, Butterworth M, Alnemri ES, et al. Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J 2001; 20:998-1009. (Pubitemid 32186791)
52. Soengas MS, Alarcon RM, Yoshida H, Giaccia AJ, Hakem R, Mak TW, et al. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science 1999; 284:156-159. (Pubitemid 29282071)
53. Rudin CM, Liu W, Desai A, Karrison T, Jiang X, Janisch L, et al. Pharmacogenomic and pharmacokinetic determinants of erlotinib toxicity. J Clin Oncol 2008; 26:1119-1127.
54. Perez-Soler R, Saltz L. Cutaneous adverse effects with HER1/EGFR-targeted agents: is there a silver lining? J Clin Oncol 2005; 23:5235-5246. (Pubitemid 46224035)
55. Tsao MS, Sakurada A, Cutz JC, Zhu CQ, Kamel-Reid S, Squire J, et al. Erlotinib in lung cancer-molecular and clinical predictors of outcome. N Engl J Med 2005; 353:133-144. (Pubitemid 41058345)
56. Lebedeva IV, Sauane M, Gopalkrishnan RV, Sarkar D, Su ZZ, Gupta P, et al. mda-7/IL-24: exploiting cancer's Achilles' heel. Mol Ther 2005; 11:4-18. (Pubitemid 40011994)
57. Fisher PB, Gopalkrishnan RV, Chada S, Ramesh R, Grimm EA, Rosenfeld MR, et al. mda-7/IL-24, a novel cancer selective apoptosis inducing cytokine gene: from the laboratory into the clinic. Cancer Biol Ther 2003; 2 (4 Suppl 1):S23-S37.
58. Cunningham CC, Chada S, Merritt JA, Tong A, Senzer N, Zhang Y, et al. 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 2005; 11:149-159. (Pubitemid 40012009)