Role of Apollon in human melanoma resistance to antitumor agents that activate the intrinsic or the extrinsic apoptosis pathways

Clinical Cancer Research

Volumn 18, Issue 12, 2012, Pages 3316-3327

  Tassi, Elena ^a   Zanon, Marina ^a,d   Vegetti, Claudia ^a   Molla, Alessandra ^a   Bersani, Ilaria ^a   Perotti, Valentina ^a   Pennati, Marzia ^a   Zaffaroni, Nadia ^a   Milella, Michele ^b   Ferrone, Soldano ^c   Carlo Stella, Carmelo ^a,e   Gianni, Alessandro M ^a   Mortarini, Roberta ^a   Anichini, Andrea ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^d Medical Clinic   (Italy)

^e HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; APOLLON; CAMPTOTHECIN; CASPASE 2; CASPASE 3; CASPASE 8; CASPASE 9; CELECOXIB; FOTEMUSTINE; INHIBITOR OF APOPTOSIS PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; KILLERTRAIL; LACTACYSTIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY H2 27.F5; MONOCLONAL ANTIBODY TP25.99; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; PROTEASOME; RAPAMYCIN; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; SMALL INTERFERING RNA; TEMOZOLOMIDE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BENIGN MELANOCYTIC LESION; CANCER RESISTANCE; CANCER TISSUE; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE SILENCING; GENETIC REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MELANOMA CELL; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL DEPOLARIZATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN DEFECT; TREATMENT RESPONSE; WESTERN BLOTTING;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 2; CASPASE 3; CASPASE 8; CASPASE 9; CELL LINE, TRANSFORMED; CELL POLARITY; DOWN-REGULATION; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION PROFILING; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MELANOMA; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS B-RAF; RNA INTERFERENCE; RNA, SMALL INTERFERING; TOR SERINE-THREONINE KINASES;

EID: 84862536510     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-2232     Document Type: Article

References (43)

1. Garbe C, Eigentler TK, Keilholz U, Hauschild A, Kirkwood JM. Systematic review of medical treatment in melanoma: current status and future prospects. Oncologist 2011;16:5-24.
2. Hocker TL, Singh MK, Tsao H. Melanoma genetics and therapeutic approaches in the 21st century: moving from the benchside to the bedside. J Invest Dermatol 2008;128:2575-95.
3. Smalley KS. Understanding melanoma signaling networks as the basis for molecular targeted therapy. J Invest Dermatol 2010;130:28-37.
4. Hersey P, Zhang XD. Treatment combinations targeting apoptosis to improve immunotherapy of melanoma. Cancer Immunol Immunother 2009;58:1749-59.
5. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H, et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 2010;467:596-9.
6. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved Survival with vemurafenib in melanoma with BRAF V600E Mutation. N Engl J Med 2011;364:2507-16.
7. Tsai J, Lee JT, Wang W, Zhang J, Cho H, Mamo S, et al. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci U S A 2008;105:3041-6. (Pubitemid 351723664)
8. Jiang CC, Lai F, Tay KH, Croft A, Rizos H, Becker TM, et al. Apoptosis of human melanoma cells induced by inhibition of B-RAFV600E involves preferential splicing of bimS. Cell Death Dis 2010;1:e69.
9. Shao Y, Aplin AE. Akt3-mediated resistance to apoptosis in B-RAF-targeted melanoma cells. Cancer Res 2010;70:6670-81.
10. Xing F, Persaud Y, Pratilas CA, Taylor BS, Janakiraman M, She QB, et al. Concurrent loss of the PTEN and RB1 tumor suppressors attenuates RAF dependence in melanomas harboring (V600E) BRAF. Oncogene 2012 31:446-57.
11. Poulikakos PI, Rosen N. Mutant BRAF melanomas-dependence and resistance. Cancer Cell 2011;19:11-5.
12. Ribas A, Flaherty KT. BRAF targeted therapy changes the treatment paradigm in melanoma. Nat Rev Clin Oncol 2011;8:426-33.
13. LaCasse EC, Mahoney DJ, Cheung HH, Plenchette S, Baird S, Korneluk RG. IAP-targeted therapies for cancer. Oncogene 2008; 27:6252-75.
14. Hao Y, Sekine K, Kawabata A, Nakamura H, Ishioka T, Ohata H, et al. Apollon ubiquitinates SMAC and caspase-9, and has an essential cytoprotection function. Nat Cell Biol 2004;6:849-60. (Pubitemid 39207250)
15. Qiu XB, Goldberg AL. The membrane-associated inhibitor of apoptosis protein, BRUCE/Apollon, antagonizes both the precursor and mature forms of Smac and caspase-9. J Biol Chem 2005;280:174-82. (Pubitemid 40164978)
16. Ren J, Shi M, Liu R, Yang QH, Johnson T, Skarnes WC, et al. The Birc6 (Bruce) gene regulates p53 and the mitochondrial pathway of apoptosis and is essential for mouse embryonic development. Proc Natl Acad Sci U S A 2005;102:565-70. (Pubitemid 40282705)
17. Lopergolo A, Pennati M, Gandellini P, Orlotti NI, Poma P, Daidone MG, et al. Apollon gene silencing induces apoptosis in breast cancer cells through p53 stabilisation and caspase-3 activation. Br J Cancer 2009;100:739-46.
18. Grossman D, McNiff JM, Li F, Altieri DC. Expression and targeting of the apoptosis inhibitor, survivin, in human melanoma. J Invest Dermatol 1999;113:1076-81. (Pubitemid 30013356)
19. 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. (Pubitemid 39139750)
20. Yan H, Brouha B, Liu T, Raj D, Biddle D, Lee R, et al. Proteolytic cleavage of Livin (ML-IAP) in apoptotic melanoma cells potentially mediated by a non-canonical caspase. J Dermatol Sci 2006;43:189-200. (Pubitemid 44189199)
21. Anichini A, Mortarini R, Nonaka D, Molla A, Vegetti C, Montaldi E, et al. Association of antigen-processing machinery and HLA antigen phenotype of melanoma cells with survival in American Joint Committee on Cancer stage III and IV melanoma patients. Cancer Res 2006;66:6405-11.
22. Zanon M, Piris A, Bersani I, Vegetti C, Molla A, Scarito A, et al. Apoptosis protease activator protein-1 expression is dispensable for response of human melanoma cells to distinct proapoptotic agents. Cancer Res 2004;64:7386-94. (Pubitemid 39372078)
23. Daniotti M, Oggionni M, Ranzani T, Vallacchi V, Campi V, Di Stasi D, et al. BRAF alterations are associated with complex mutational profiles in malignant melanoma. Oncogene 2004;23:5968-77. (Pubitemid 39093541)
24. Sensi M, Nicolini G, Petti C, Bersani I, Lozupone F, Molla A, et al. Mutually exclusive NRASQ61R and BRAFV600E mutations at the single cell level in the same human melanoma. Oncogene 2006;25: 3357-64. (Pubitemid 43877040)
25. Lavazza C, Carlo-Stella C, Di Nicola M, Longoni P, Milanesi M, Magni M, et al. Highly efficient gene transfer into mobilized CD34+ hematopoietic cells using serotype-5 adenoviral vectors and BoosterExpress Reagent. Exp Hematol 2007;35:888-97. (Pubitemid 46802980)
26. Temponi M, Kekish U, Hamby CV, Nielsen H, Marboe CC, Ferrone S. Characterization of anti-HLA class II monoclonal antibody LGII-612.14 reacting with formalin fixed tissues. J Immunol Methods 1993;161:239-56.
27. Desai SA, Wang X, Noronha EJ, Zhou Q, Rebmann V, Grosse-Wilde H, et al. Structural relatedness of distinct determinants recognized by monoclonal antibody TP25.99 on beta 2-microglobulin-associated and beta 2-microglobulin-free HLA class I heavy chains. J Immunol 2000;165:3275-83.
28. Temponi M, Kageshita T, Perosa F, Ono R, Okada H, Ferrone S. Purification of murine IgG monoclonal antibodies by precipitation with caprylic acid: comparison with other methods of purification. Hybridoma 1989;8:85-95. (Pubitemid 19082761)
29. Mortarini R, Vegetti C, Molla A, Arienti F, Ravagnani F, Maurichi A, et al. Impaired STAT phosphorylation in T cells from melanoma patients in response to IL-2: association with clinical stage. Clin Cancer Res 2009;15:4085-94.
30. Nagy ZA, Hubner B, Lohning C, Rauchenberger R, Reiffert S, Thomassen- Wolf E, et al. Fully human, HLA-DR-specific monoclonal antibodies efficiently induce programmed death of malignant lymphoid cells. Nat Med 2002;8:801-7.
31. Carlo-Stella C, Di Nicola M, Turco MC, Cleris L, Lavazza C, Longoni P, et al. The anti-human leukocyte antigen-DR monoclonal antibody 1D09C3 activates the mitochondrial cell death pathway and exerts a potent antitumor activity in lymphoma-bearing nonobese diabetic/severe combined immunodeficient mice. Cancer Res 2006;66:1799-808. (Pubitemid 43259966)
32. Qiu X, Markant SL, Yuan J, Goldberg AL. Nrdp1-mediated degradation of the gigantic IAP BRUCE, is a novel pathway for triggering apoptosis. EMBO J 2004;23:800-10. (Pubitemid 38418747)
33. Seeger JM, Schmidt P, Brinkmann K, Hombach AA, Coutelle O, Zigrino P, et al. The proteasome inhibitor bortezomib sensitizes melanoma cells toward adoptive CTL attack. Cancer Res 2010;70:1825-34.
34. Jaks V, Joers A, Kristjuhan A, Maimets T. p53 protein accumulation in addition to the transactivation activity is required for p53-dependent cell cycle arrest after treatment of cells with camptothecin. Oncogene 2001;20:1212-9. (Pubitemid 32226247)
35. Liu HF, Hsiao PW, Chao JI. Celecoxib induces p53-PUMA pathway for apoptosis in human colorectal cancer cells. Chem Biol Interact 2008;176:48-57.
36. Avery-Kiejda KA, Zhang XD, Adams LJ, Scott RJ, Vojtesek B, Lane DP, et al. Small molecular weight variants of p53 are expressed in human melanoma cells and are induced by the DNA-damaging agent cisplatin. Clin Cancer Res 2008;14:1659-68. (Pubitemid 351469449)
37. Fu K, Ren H, Wang Y, Fei E, Wang H, Wang G. DJ-1 inhibits TRAIL-induced apoptosis by blocking pro-caspase-8 recruitment to FADD. Oncogene 2012;31:1311-22.
38. Mannhold R, Fulda S, Carosati E. IAP antagonists: promising candidates for cancer therapy. Drug Discov Today 2010;15:210-219.
39. Lecis D, Drago C, Manzoni L, Seneci P, Scolastico C, Mastrangelo E, et al. Novel SMAC-mimetics synergistically stimulate melanoma cell death in combination with TRAIL and bortezomib. Br J Cancer 2010;102:1707-16.
40. Lu J, McEachern D, Sun H, Bai L, Peng Y, Qiu S, et al. Therapeutic potential and molecular mechanism of a novel, potent, nonpeptide, Smac mimetic SM-164 in combination with TRAIL for cancer treatment. Mol Cancer Ther 2011;10:902-14.
41. Eckelman BP, Draf M, Snipas SJ, Salvesen GS. The mechanism of peptide-binding specificity of IAP BIR domains. Cell Death Differ 2008;15:920-928. (Pubitemid 351524433)
42. Miura K, Karasawa H, Sasaki I. cIAP2 as a therapeutic target in colorectal cancer and other malignancies. Expert Opin Ther Targets 2009;13:1333-45.
43. Chu L, Gu J, Sun L, Qian Q, Qian C, Liu X. Oncolytic adenovirus-mediated shRNA against Apollon inhibits tumor cell growth and enhances antitumor effects of 5-fluorouracil. Gene Ther 2008;15:484-94. (Pubitemid 351405088)