Down-regulation of Mcl-1 by small interfering RNA sensitizes resistant melanoma cells to Fas-mediated apoptosis

Molecular Cancer Research

Volumn 6, Issue 1, 2008, Pages 42-52

  Chetoui, Nizar ^a   Sylla, Khaoussou ^b   Gagnon Houde, Jean Vincent ^a   Alcaide Loridan, Catherine ^c   Charron, Dominique ^b   Al Daccak, Reem ^b   Aoudjit, Fawzi ^a  

^a LAVAL UNIVERSITY   (Canada)

^b SAINT LOUIS HOSPITAL   (France)

^c INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 9; CYCLOHEXIMIDE; FAS ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MELANOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; UPREGULATION;

ANTIGENS, CD95; APOPTOSIS; BUTADIENES; CELL LINE, TUMOR; CYCLOHEXIMIDE; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE KINASE 1; MELANOMA; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM PROTEINS; NITRILES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, SMALL INTERFERING; THERMODYNAMICS; UP-REGULATION;

EID: 40749122965     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-07-0080     Document Type: Article

References (85)

1. Thompson JF, Scolyer RA, Kefford RF. Cutaneous melanoma. Lancet 2005;365:687-701.
2. Soengas MS, Lowe SW. Apoptosis and melanoma chemoresistance. Oncogene 2003;22:3138-51.
3. Chin L, Garraway LA, Fisher DE. Malignant melanoma: genetics and therapeutics in the genomic era. Genes Dev 2006;20:2149-82.
4. Ivanov VN, Bhoumik A, Ronai Z. Death receptors and melanoma resistance to apoptosis. Oncogene 2003;22:3152-61.
5. Hofbauer GF, Hatta N, Daigle I, et al. Fas ligand reduces viability in primary melanoma short-term cell cultures more than in metastatic melanoma short-term cell cultures. Dermatology 2005;211:318-24.
6. Hersey P. Apoptosis and melanoma: how new insights are effecting the development of new therapies for melanoma. Curr Opin Oncol 2006;18:189-96.
7. Brunner T, Wasem C, Torgler R, Cima I, Jakob S, Corazza N. Fas (CD95/Apo-1) ligand regulation in T cell homeostasis, cell-mediated cytotoxicity and immune pathology. Semin Immunol 2003;15:167-76.
8. Wajant H. CD95L/FasL and TRAIL in tumour surveillance and cancer therapy. Cancer Treat Res 2006;130:141-65.
9. Andersen MH, Schrama D, Thor Straten P, Becker JC. Cytotoxic T cells. J Invest Dermatol 2006;126:32-41.
10. Screpanti V, Wallin RP, Grandien A, Ljunggren HG. Impact of FASL-induced apoptosis in the elimination of tumor cells by NK cells. Mol Immunol 2005;42:495-9.
11. Scaffidi C, Fulda S, Srinivasan A, et al. Two CD95 (APO-1/Fas) signaling pathways. Embo J 1998;17:1675-87.
12. Barnhart BC, Alappat EC, Peter ME. The CD95 type I/type II model. Semin Immunol 2003;15:185-93.
13. Mouawad R, Khayat D, Soubrane C. Plasma Fas ligand, an inducer of apoptosis, and plasma soluble Fas, an inhibitor of apoptosis, in advanced melanoma. Melanoma Res 2000;10:461-7.
14. Rivoltini L, Carrabba M, Huber V, et al. Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol Rev 2002;188:97-113.
15. Frost PJ, Butterfield LH, Dissette VB, Economou JS, Bonavida B. Immunosensitization of melanoma tumor cells to non-MHC Fas-mediated killing by MART-1-specific CTL cultures. J Immunol 2001;166:3564-73.
16. Yang S, Haluska FG. Treatment of melanoma with 5-fluorouracil or dacarbazine in vitro sensitizes cells to antigen-specific CTL lysis through perforin/granzyme- and Fas-mediated pathways. J Immunol 2004;172:4599-608.
17. Wang Y, Li G. ING3 promotes UV-induced apoptosis via Fas/caspase-8 pathway in melanoma cells. J Biol Chem 2006;281:11887-93.
18. Mottolese M, Buglioni S, Bracalenti C, et al. Prognostic relevance of altered Fas (CD95)-system in human breast cancer. Int J Cancer 2000;89:127-32.
19. Gopalan B, Litvak A, Sharma S, Mhashilkar AM, Chada S, Ramesh R. Activation of the Fas-FasL signaling pathway by MDA-7/IL-24 kills human ovarian cancer cells. Cancer Res 2005;65:3017-24.
20. Eason DD, Blanck G. High level class II trans-activator induction does not occur with transient activation of the IFN-γ signaling pathway. J Immunol 2001;166:1041-8.
21. Ivanov VN, Hei TK. Dual treatment with COX-2 inhibitor and sodium arsenite leads to induction of surface Fas ligand expression and Fas-ligand-mediated apoptosis in human melanoma cells. Exp Cell Res 2006;312:1401-17.
22. Hussein MR, Haemel AK, Wood GS. Apoptosis and melanoma: molecular mechanisms. J Pathol 2003;199:275-88.
23. Raisova M, Bektas M, Wieder T, et al. Resistance to CD95/Fas-induced and ceramide-mediated apoptosis of human melanoma cells is caused by a defective mitochondrial cytochrome c release. FEBS Lett 2000;473:27-32.
24. Raisova M, Hossini AM, Eberle J, et al. The Bax/Bcl-2 ratio determines the susceptibility of human melanoma cells to CD95/Fas-mediated apoptosis. J Invest Dermatol 2001;117:333-40.
25. Ugurel S, Seiter S, Rappl G, Stark A, Tilgen W, Reinhold U. Heterogenous susceptibility to CD95-induced apoptosis in melanoma cells correlates with bcl-2 and bcl-x expression and is sensitive to modulation by interferon-γ. Int J Cancer 1999;82:727-36.
26. Fecker LF, Geilen CC, Tchernev G, et al. Loss of proapoptotic Bcl-2-related multidomain proteins in primary melanomas is associated with poor prognosis. J Invest Dermatol 2006;126:1366-71.
27. Thomas WD, Zhang XD, Franco AV, Nguyen T, Hersey P. TNF-related apoptosis-inducing ligand-induced apoptosis of melanoma is associated with changes in mitochondrial membrane potential and perinuclear clustering of mitochondria. J Immunol 2000;165:5612-20.
28. Sun XM, Bratton SB, Butterworth M, MacFarlane M, Cohen GM. Bcl-2 and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J Biol Chem 2002;277:11345-51.
29. Larribere L, Khaled M, Tartare-Deckert S, et al. PI3K mediates protection against TRAIL-induced apoptosis in primary human melanocytes. Cell Death Differ 2004;11:1084-91.
30. Stahl JM, Cheung M, Sharma A, Trivedi NR, Shanmugam S, Robertson GP. Loss of PTEN promotes tumor development in malignant melanoma. Cancer Res 2003;63:2881-90.
31. Zhang XD, Borrow JM, Zhang XY, Nguyen T, Hersey P. Activation of ERK1/2 protects melanoma cells from TRAIL-induced apoptosis by inhibiting Smac/DIABLO release from mitochondria. Oncogene 2003;22:2869-81.
32. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci U S A 1993;90:3516-20.
33. Derouet M, Thomas L, Cross A, Moots RJ, Edwards SW. Granulocyte macrophage colony-stimulating factor signaling and proteasome inhibition delay neutrophil apoptosis by increasing the stability of Mcl-1. J Biol Chem 2004;279:26915-21.
34. Nencioni A, Hua F, Dillon CP, et al. Evidence for a protective role of Mcl-1 in proteasome inhibitor-induced apoptosis. Blood 2005;105:3255-62.
35. Shin MS, Park WS, Kim SY, et al. Alterations of Fas (Apo-1/CD95) gene in cutaneous malignant melanoma. Am J Pathol 1999;154:1785-91.
36. Soubrane C, Mouawad R, Antoine EC, Verola O, Gil-Delgado M, Khayat D. A comparative study of Fas and Fas-ligand expression during melanoma progression. Br J Dermatol 2000;143:307-12.
37. Selzer E, Schlagbauer-Wadl H, Okamoto I, Pehamberger H, Potter R, Jansen B. Expression of Bcl-2 family members in human melanocytes, in melanoma metastases and in melanoma cell lines. Melanoma Res 1998;8:197-203.
38. Tang L, Tron VA, Reed JC, et al. Expression of apoptosis regulators in cutaneous malignant melanoma. Clin Cancer Res 1998;4:1865-71.
39. Jansen B, Wacheck V, Heere-Ress E, et al. Chemosensitisation of malignant melanoma by BCL2 antisense therapy. Lancet 2000;356:1728-33.
40. Jansen B, Schlagbauer-Wadl H, Brown BD, et al. bcl-2 antisense therapy chemosensitizes human melanoma in SCID mice. Nat Med 1998;4:232-4.
41. Heere-Ress E, Thallinger C, Lucas T, et al. Bcl-X(L) is a chemoresistance factor in human melanoma cells that can be inhibited by antisense therapy. Int J Cancer 2002;99:29-34.
42. Adams KW, Cooper GM. Rapid turnover of mcl-1 couples translation to cell survival and apoptosis. J Biol Chem 2007;282:6192-200.
43. Nijhawan D, Fang M, Traer E, et al. Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev 2003;17:1475-86.
44. Rahmani M, Davis EM, Bauer C, Dent P, Grant S. Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J Biol Chem 2005;280:35217-27.
45. Ramsay JA, From L, Kahn HJ. bcl-2 protein expression in melanocytic neoplasms of the skin. Mod Pathol 1995;8:150-4.
46. Cerroni L, Soyer HP, Kerl H. bcl-2 protein expression in cutaneous malignant melanoma and benign melanocytic nevi. Am J Dermatopathol 1995;17:7-11.
47. Zhuang L, Lee CS, Scolyer RA, et al. Mcl-1, Bcl-XL and Stat3 expression are associated with progression of melanoma whereas Bcl-2, AP-2 and MITF levels decrease during progression of melanoma. Mod Pathol 2007;20:416-26.
48. Wolter KG, Verhaegen M, Fernandez Y, et al. Therapeutic window for melanoma treatment provided by selective effects of the proteasome on Bcl-2 proteins. Cell Death Differ 2007;14:1605-16.
49. Chawla-Sarkar M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, Borden EC. Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 2004;11:915-23.
50. Walczak H, Bouchon A, Stahl H, Krammer PH. Tumor necrosis factor-related apoptosis-inducing ligand retains its apoptosis-inducing capacity on Bcl-2-or Bcl-xL-overexpressing chemotherapy-resistant tumor cells. Cancer Res 2000;60:3051-7.
51. Fas SC, Baumann S, Krueger A, et al. In vitro generated human memory-like T cells are CD95 type II cells and resistant towards CD95-mediated apoptosis. Eur J Immunol 2006;36:2894-903.
52. Epling-Burnette PK, Liu JH, Catlett-Falcone R, et al. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J Clin Invest 2001;107:351-62.
53. Herrant M, Luciano F, Loubat A, Auberger P. The protective effect of phorbol esters on Fas-mediated apoptosis in T cells. Transcriptional and postranscriptional regulation. Oncogene 2002;21:4957-68.
54. Schulze-Bergkamen H, Brenner D, Krueger A, et al. Hepatocyte growth factor induces Mcl-1 in primary human hepatocytes and inhibits CD95-mediated apoptosis via Akt. Hepatology 2004;39:645-54.
55. Zhuang J, Brady HJ. Emerging role of Mcl-1 in actively counteracting BH3-only proteins in apoptosis. Cell Death Differ 2006;13:1263-7.
56. Clohessy JG, Zhuang J, de Boer J, Gil-Gomez G, Brady HJ. Mcl-1 interacts with truncated Bid and inhibits its induction of cytochrome c release and its role in receptor-mediated apoptosis. J Biol Chem 2006;281:5750-9.
57. Han J, Goldstein LA, Gastman BR, Rabinowich H. Interrelated roles for Mcl-1 and BIM in regulation of TRAIL-mediated mitochondrial apoptosis. J Biol Chem 2006;281:10153-63.
58. Cuconati A, Mukherjee C, Perez D, White E. DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells. Genes Dev 2003;17:2922-32.
59. Meng XW, Lee SH, Dai H, et al. Mcl-1 as a buffer for proapoptotic Bcl-2 family members during trail-induced apoptosis: a mechanistic basis for sorafenib (BAY 43-9006)-induced trail sensitization. J Biol Chem 2007;283:29831-46.
60. Sitailo LA, Tibudan SS, Denning MF. The protein kinase Cδ catalytic fragment targets Mcl-1 for degradation to trigger apoptosis. J Biol Chem 2006;281:29703-10.
61. Hahne M, Rimoldi D, Schroter M, et al. Melanoma cell expression of Fas(Apo-1/CD95) ligand: implications for tumor immune escape. Science 1996;274:1363-6.
62. Hallermalm K, De Geer A, Kiessling R, Levitsky V, Levitskaya J. Autocrine secretion of Fas ligand shields tumor cells from Fas-mediated killing by cytotoxic lymphocytes. Cancer Res 2004;64:6775-82.
63. Lin MT, Lee RC, Yang PC, Ho FM, Kuo ML. Cyclooxygenase-2 inducing Mcl-1-dependent survival mechanism in human lung adenocarcinoma CL1.0 cells. Involvement of phosphatidylinositol 3-kinase/Akt pathway. J Biol Chem 2001;276:48997-9002.
64. Fleischer B, Schulze-Bergkamen H, Schuchmann M, et al. Mcl-1 is an antiapoptotic factor for human hepatocellular carcinoma. Int J Oncol 2006;28:25-32.
65. Schubert KM, Duronio V. Distinct roles for extracellular-signal-regulated protein kinase (ERK) mitogen-activated protein kinases and phosphatidylinositol 3-kinase in the regulation of Mcl-1 synthesis. Biochem J 2001;356:473-80.
66. Niu G, Bowman T, Huang M, et al. Roles of activated Src and Stat3 signaling in melanoma tumor cell growth. Oncogene 2002;21:7001-10.
67. Cavarretta IT, Neuwirt H, Untergasser G, et al. The antiapoptotic effect of IL-6 autocrine loop in a cellular model of advanced prostate cancer is mediated by Mcl-1. Oncogene 2007;26:2822-32.
68. Domina AM, Vrana JA, Gregory MA, Hann SR, Craig RW. MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or Taxol. Oncogene 2004;23:5301-15.
69. Aoudjit F, Guo W, Gagnon-Houde JV, et al. HLA-DR signaling inhibits Fas-mediated apoptosis in A375 melanoma cells. Exp Cell Res 2004;299:79-90.
70. Opferman JT, Iwasaki H, Ong CC, et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 2005;307:1101-4.
71. Petlickovski A, Laurenti L, Li X, et al. Sustained signaling through the B-cell receptor induces Mcl-1 and promotes survival of chronic lymphocytic leukemia B cells. Blood 2005;105:4820-7.
72. Sorensen RB, Nielsen OJ, Thor Straten P, Andersen MH. Functional capacity of Mcl-1-specific cytotoxic T-cells. Leukemia 2006;20:1457-8.
73. Andersen MH, Becker JC, Thor Straten P. The antiapoptotic member of the Bcl-2 family Mcl-1 is a CTL target in cancer patients. Leukemia 2005;19:484-5.
74. Thallinger C, Wolschek MF, Wacheck V, et al. Mcl-1 antisense therapy chemosensitizes human melanoma in a SCID mouse xenotransplantation model. J Invest Dermatol 2003;120:1081-6.
75. Qin JZ, Xin H, Sitailo LA, Denning MF, Nickoloff BJ. Enhanced killing of melanoma cells by simultaneously targeting Mcl-1 and NOXA. Cancer Res 2006;66:9636-45.
76. Skvara H, Thallinger C, Wacheck V, et al. Mcl-1 blocks radiation-induced apoptosis and inhibits clonogenic cell death. Anticancer Res 2005;25:2697-703.
77. Taniai M, Grambihler A, Higuchi H, et al. Mcl-1 mediates tumor necrosis factor-related apoptosis-inducing ligand resistance in human cholangiocarcinoma cells. Cancer Res 2004;64:3517-24.
78. Hamai A, Richon C, Meslin F, et al. Imatinib enhances human melanoma cell susceptibility to TRAIL-induced cell death: relationship to Bcl-2 family and caspase activation. Oncogene 2006;25:7618-34.
79. Gillespie S, Borrow J, Zhang XD, Hersey P. Bim plays a crucial role in synergistic induction of apoptosis by the histone deacetylase inhibitor SBHA and TRAIL in melanoma cells. Apoptosis 2006;11:2251-65.
80. Bush JA, Li G. The role of Bcl-2 family members in the progression of cutaneous melanoma. Clin Exp Metastasis 2003;20:531-9.
81. Bullani RR, Wehrli P, Viard-Leveugle I, et al. Frequent down-regulation of Fas (CD95) expression and function in melanoma. Melanoma Res 2002;12:263-70.
82. Owen-Schaub LB, van Golen KL, Hill LL, Price JE. Fas and Fas ligand interactions suppress melanoma lung metastasis. J Exp Med 1998;188:1717-23.
83. Chetoui N, Gendron S, Chamoux E, Aoudjit F. Collagen type I-mediated activation of ERK/MAP Kinase is dependent on Ras, Raf-1 and protein phosphatase 2A in Jurkat T cells. Mol Immunol 2006;43:1687-93.
84. Gendron S, Couture J, Aoudjit F. Collagen type I signaling reduces the expression and the function of human receptor activator of nuclear factor-κB ligand (RANKL) in T lymphocytes. Eur J Immunol 2005;35:3673-82.
85. Ellerhorst JA, Ekmekcioglu S, Johnson MK, Cooke CP, Johnson MM, Grimm EA. Regulation of iNOS by the p44/42 mitogen-activated protein kinase pathway in human melanoma. Oncogene 2006;25:3956-62.