The X-linked inhibitor of apoptosis protein (XIAP) is up-regulated in metastatic melanoma, and XIAP cleavage by Phenoxodiol is associated with Carboplatin sensitization

Journal of Translational Medicine

Volumn 5, Issue , 2007, Pages

  Kluger, Harriet M ^a   McCarthy, Mary M ^a   Alvero, Ayesha B ^a   Sznol, Mario ^a   Ariyan, Stephan ^a   Camp, Robert L ^a   Rimm, David L ^a   Mor, Gil ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; CARBOPLATIN; CYSTEINE; PHENOXODIOL; PROTEIN S 100; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; IDRONOXIL; ISOFLAVONE DERIVATIVE;

ADULT; AGED; APOPTOSIS; ARTICLE; AUTOMATION; CANCER CELL CULTURE; CANCER INHIBITION; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MELANOMA; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; TISSUE MICROARRAY; UPREGULATION; ADOLESCENT; CELL SURVIVAL; DRUG EFFECT; DRUG POTENTIATION; DRUG SCREENING; METABOLISM; METASTASIS; MIDDLE AGED; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; CARBOPLATIN; CELL LINE, TUMOR; CELL SURVIVAL; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; FEMALE; HUMANS; ISOFLAVONES; MALE; MELANOMA; MIDDLE AGED; NEOPLASM METASTASIS; PROGNOSIS; UP-REGULATION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 33846973344     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-5-6     Document Type: Article

References (64)

1. Rigel DS Malignant melanoma: Incidence issues and their effect on diagnosis and treatment in the 1990s Mayo Clin Proc 1997 72 4 367-371 9121186
2. Jemal A Siegel R Ward E Murray T Xu J Smigal C Thun MJ Cancer statistics, 2006 CA Cancer J Clin 2006 56 2 106-130 16514137
3. Chapman PB Einhorn LH Meyers ML Saxman S Destro AN Panageas KS Begg CB Agarwala SS Schuchter LM Ernstoff MS Houghton AN Kirkwood JM Phase III multicenter randomized trial of the Dartmouth regimen versus dacarbazine in patients with metastatic melanoma J Clin Oncol 1999 17 9 2745-2751 10561349
4. Falkson CI Ibrahim J Kirkwood JM Coates AS Atkins MB Blum RH Phase III trial of dacarbazine versus dacarbazine with interferon alpha-2b versus dacarbazine with tamoxifen versus dacarbazine with interferon alpha-2b and tamoxifen in patients with metastatic malignant melanoma: An Eastern Cooperative Oncology Group study J Clin Oncol 1998 16 5 1743-1751 9586887
5. Tsao H Atkins MB Sober AJ Management of cutaneous melanoma N Engl J Med 2004 351 10 998-1012 10.1056/NEJMra041245 15342808
6. Piro LD Apoptosis, Bcl-2 antisense, and cancer therapy Oncology (Williston Park) 2004 18 13 Suppl 10 5-10 15651171
7. Glover D Ibrahim J Kirkwood J Glick J Karp D Stewart J Ewell M Borden E Phase II randomized trial of cisplatin and WR-2721 versus cisplatin alone for metastatic melanoma: An Eastern Cooperative Oncology Group Study (E1686) Melanoma Res 2003 13 6 619-626 10.1097/ 00008390-200312000-00012 14646626
8. Gogas H Bafaloukos D Bedikian AY The role of taxanes in the treatment of metastatic melanoma Melanoma Res 2004 14 5 415-420 10.1097/ 00008390-200410000-00013 15457099
9. Schmitt CA Lowe SW Apoptosis is critical for drug response in vivo Drug Resist Updat 2001 4 2 132-134 10.1054/drup.2001.0188 11512522
10. Schmitt CA Lowe SW Apoptosis and chemoresistance in transgenic cancer models J Mol Med 2002 80 3 137-146 10.1007/s00109-001-0293-3 11894140
11. Hengartner MO The biochemistry of apoptosis Nature 2000 407 6805 770-776 10.1038/35037710 11048727
12. Ivanov VN Bhoumik A Ronai Z Death receptors and melanoma resistance to apoptosis Oncogene 2003 22 20 3152-3161 10.1038/sj.onc.1206456 12789291
13. Schimmer AD Welsh K Pinilla C Wang Z Krajewska M Bonneau MJ Pedersen IM Kitada S Scott FL Bailly-Maitre B Glinsky G Scudiero D Sausville E Salvesen G Nefzi A Ostresh JM Houghten RA Reed JC Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity Cancer Cell 2004 5 1 25-35 10.1016/S1535-6108(03)00332-5 14749124
14. Schimmer AD Dalili S Targeting the IAP Family of Caspase Inhibitors as an Emerging Therapeutic Strategy Hematology (Am Soc Hematol Educ Program) 2005 215-219 16304383
15. Schimmer AD Dalili S Batey RA Riedl SJ Targeting XIAP for the treatment of malignancy Cell Death Differ 2006 13 2 179-188 10.1038/sj.cdd.4401826 16322751
16. Yang Y Fang S Jensen JP Weissman AM Ashwell JD Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli Science 2000 288 5467 874-877 10.1126/ science.288.5467.874 10797013
17. Sapi E Alvero AB Chen W O'Malley D Hao XY Dwipoyono B Garg M Kamsteeg M Rutherford T Mor G Resistance of ovarian carcinoma cells to docetaxel is XIAP dependent and reversible by phenoxodiol Oncol Res 2004 14 11-12 567-578 15666998
18. Muris JJ Cillessen SA Vos W van Houdt IS Kummer JA van Krieken JH Jiwa NM Jansen PM Kluin-Nelemans HC Ossenkoppele GJ Gundy C Meijer CJ Oudejans JJ Immunohistochemical profiling of caspase signaling pathways predicts clinical response to chemotherapy in primary nodal diffuse large B-cell lymphomas Blood 2005 105 7 2916-2923 10.1182/ blood-2004-07-2716 15576477
19. Alvero AB O'Malley, D., Brown, D., Kelly, G., Garg, M., Chen, W., Rutherford, T., Mor, G. Molecular mechanism of phenoxodiol-induced apoptosis in ovarian cancer cells Cancer 2006 in press
20. Cao C Mu Y Hallahan DE Lu B XIAP and survivin as therapeutic targets for radiation sensitization in preclinical models of lung cancer Oncogene 2004 23 42 7047-7052 10.1038/sj.onc.1207929 15258565
21. Holcik M Yeh C Korneluk RG Chow T Translational upregulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death Oncogene 2000 19 36 4174-4177 10.1038/sj.onc.1203765 10962579
22. Carter BZ Gronda M Wang Z Welsh K Pinilla C Andreeff M Schober WD Nefzi A Pond GR Mawji IA Houghten RA Ostresh J Brandwein J Minden MD Schuh AC Wells RA Messner H Chun K Reed JC Schimmer AD Small-molecule XIAP inhibitors derepress downstream effector caspases and induce apoptosis of acute myeloid leukemia cells Blood 2005 105 10 4043-4050 10.1182/ blood-2004-08-3168 15687241
23. Cummings J Ward TH LaCasse E Lefebvre C St-Jean M Durkin J Ranson M Dive C Validation of pharmacodynamic assays to evaluate the clinical efficacy of an antisense compound (AEG 35156) targeted to the X-linked inhibitor of apoptosis protein XIAP Br J Cancer 2005 92 3 532-538 15685240
24. 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 8 915-923 10.1038/sj.cdd.4401416 15118763
25. Ramp U Krieg T Caliskan E Mahotka C Ebert T Willers R Gabbert HE Gerharz CD XIAP expression is an independent prognostic marker in clear-cell renal carcinomas Hum Pathol 2004 35 8 1022-1028 10.1016/ j.humpath.2004.03.011 15297970
26. Hofmann HS Simm A Hammer A Silber RE Bartling B Expression of inhibitors of apoptosis (IAP) proteins in non-small cell human lung cancer J Cancer Res Clin Oncol 2002 128 10 554-560 10.1007/s00432-002-0364-z 12384799
27. Parton M Krajewski S Smith I Krajewska M Archer C Naito M Ahern R Reed J Dowsett M Coordinate expression of apoptosis-associated proteins in human breast cancer before and during chemotherapy Clin Cancer Res 2002 8 7 2100-2108 12114409
28. Zhang XD Zhang XY Gray CP Nguyen T Hersey P Tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis of human melanoma is regulated by smac/DIABLO release from mitochondria Cancer Res 2001 61 19 7339-7348 11585775
29. Bowen AR Hanks AN Allen SM Alexander A Diedrich MJ Grossman D Apoptosis regulators and responses in human melanocytic and keratinocytic cells J Invest Dermatol 2003 120 1 48-55 10.1046/j.1523-1747.2003.12010.x 12535197
30. Kamsteeg M Rutherford T Sapi E Hanczaruk B Shahabi S Flick M Brown D Mor G Phenoxodiol - an isoflavone analog - induces apoptosis in chemoresistant ovarian cancer cells Oncogene 2003 22 17 2611-2620 10.1038/sj.onc.1206422 12730675
31. Choueiri TK Mekhail T Hutson TE Ganapathi R Kelly GE Bukowski RM Phase I trial of phenoxodiol delivered by continuous intravenous infusion in patients with solid cancer Ann Oncol 2006 17 5 860-865 10.1093/annonc/ mdl010 16524966
32. Rutherford T O'Malley, D., Makkenchery A., Baker, L., Azodi, M., Schwartz, P., Mor, G. Phenoxodiol Phase Ib/II Study in Patients with Recurrent Ovarian Cancer that are Resistant to = Second Line Chemotherapy Journal for the Society of Gynecologic Investigation 2004 11
33. Camp RL Chung GG Rimm DL Automated subcellular localization and quantification of protein expression in tissue microarrays Nat Med 2002 8 11 1323-1327 10.1038/nm791 12389040
34. Rubin MA Zerkowski MP Camp RL Kuefer R Hofer MD Chinnaiyan AM Rimm DL Quantitative determination of expression of the prostate cancer protein alpha-methylacyl-CoA racemase using automated quantitative analysis (AQUA): A novel paradigm for automated and continuous biomarker measurements Am J Pathol 2004 164 3 831-840 14982837
35. Berger AJ Camp RL Divito KA Kluger HM Halaban R Rimm DL Automated quantitative analysis of HDM2 expression in malignant melanoma shows association with early-stage disease and improved outcome Cancer Res 2004 64 23 8767-8772 10.1158/0008-5472.CAN-04-1384 15574789
36. Berger AJ Davis DW Tellez C Prieto VG Gershenwald JE Johnson MM Rimm DL Bar-Eli M Automated quantitative analysis of activator protein-2alpha subcellular expression in melanoma tissue microarrays correlates with survival prediction Cancer Res 2005 65 23 11185-11192 10.1158/ 0008-5472.CAN-05-2300 16322269
37. Divito KA Berger AJ Camp RL Dolled-Filhart M Rimm DL Kluger HM Automated quantitative analysis of tissue microarrays reveals an association between high Bcl-2 expression and improved outcome in melanoma Cancer Res 2004 64 23 8773-8777 10.1158/0008-5472.CAN-04-1387 15574790
38. Garraway LA Widlund HR Rubin MA Getz G Berger AJ Ramaswamy S Beroukhim R Milner DA Granter SR Du J Lee C Wagner SN Li C Golub TR Rimm DL Meyerson ML Fisher DE Sellers WR Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma Nature 2005 436 7047 117-122 10.1038/nature03664 16001072
39. Kluger HM DiVito K Berger AJ Halaban R Ariyan S Camp RL Rimm DL Her2/neu is not a commonly expressed therapeutic target in melanoma - a large cohort tissue microarray study Melanoma Res 2004 14 3 207-210 10.1097/ 01.cmr.0000130874.33504.2f 15179190
40. McCarthy M.M. DVKA Sznol M., Kovacs D., Halaban R., Berger A.J., Flaherty K.T., Camp R.L., Lazova R., Rimm D.L., and Kluger H.M. Expression of TRAIL Receptors 1 and 2 in Melanoma Clinical Cancer Research 2006 in press
41. McCarthy MM DiVito KA Sznol M Kovacs D Halaban R Berger AJ Flaherty KT Camp RL Lazova R Rimm DL Kluger HM Expression of tumor necrosis factor - related apoptosis-inducing ligand receptors 1 and 2 in melanoma Clin Cancer Res 2006 12 12 3856-3863 10.1158/1078-0432.CCR-06-0190 16778114
42. Kluger HM Kluger Y Gilmore-Hebert M DiVito K Chang JT Rodov S Mironenko O Kacinski BM Perkins AS Sapi E cDNA microarray analysis of invasive and tumorigenic phenotypes in a breast cancer model Lab Invest 2004 84 3 320-331 10.1038/labinvest.3700044 14767486
43. von Willebrand M Zacksenhaus E Cheng E Glazer P Halaban R The tyrphostin AG1024 accelerates the degradation of phosphorylated forms of retinoblastoma protein (pRb) and restores pRb tumor suppressive function in melanoma cells Cancer Res 2003 63 6 1420-1429 12649208
44. Neale D Demasio K Illuzi J Chaiworapongsa T Romero R Mor G Maternal serum of women with pre-eclampsia reduces trophoblast cell viability: evidence for an increased sensitivity to Fas-mediated apoptosis J Matern Fetal Neonatal Med 2003 13 1 39-44 12710855
45. Lev DC Onn A Melinkova VO Miller C Stone V Ruiz M McGary EC Ananthaswamy HN Price JE Bar-Eli M Exposure of melanoma cells to dacarbazine results in enhanced tumor growth and metastasis in vivo J Clin Oncol 2004 22 11 2092-2100 10.1200/JCO.2004.11.070 15123733
46. Mandara M Nortilli R Sava T Cetto GL Chemotherapy for metastatic melanoma Expert Rev Anticancer Ther 2006 6 1 121-130 10.1586/ 14737140.6.1.121 16375649
47. Depeille P Cuq P Passagne I Evrard A Vian L Combined effects of GSTP1 and MRP1 in melanoma drug resistance Br J Cancer 2005 93 2 216-223 10.1038/sj.bjc.6602681 15999103
48. Frank NY Margaryan A Huang Y Schatton T Waaga-Gasser AM Gasser M Sayegh MH Sadee W Frank MH ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma Cancer Res 2005 65 10 4320-4333 10.1158/0008-5472.CAN-04-3327 15899824
49. Tang CH Grimm EA Depletion of endogenous nitric oxide enhances cisplatin-induced apoptosis in a p53-dependent manner in melanoma cell lines J Biol Chem 2004 279 1 288-298 10.1074/jbc.M310821200 14576150
50. Bradbury PA Middleton MR DNA repair pathways in drug resistance in melanoma Anticancer Drugs 2004 15 5 421-426 10.1097/ 01.cad.0000127665.74096.93 15166615
51. Soengas MS Lowe SW Apoptosis and melanoma chemoresistance Oncogene 2003 22 20 3138-3151 10.1038/sj.onc.1206454 12789290
52. Kumar R Angelini S Snellman E Hemminki K BRAF mutations are common somatic events in melanocytic nevi J Invest Dermatol 2004 122 2 342-348 10.1046/j.0022-202X.2004.22225.x 15009715
53. Wellbrock C Ogilvie L Hedley D Karasarides M Martin J Niculescu-Duvaz D Springer CJ Marais R V599EB-RAF is an oncogene in melanocytes Cancer Res 2004 64 7 2338-2342 10.1158/0008-5472.CAN-03-3433 15059882
54. Sanna MG da Silva Correia J Ducrey O Lee J Nomoto K Schrantz N Deveraux QL Ulevitch RJ IAP suppression of apoptosis involves distinct mechanisms: The TAK1/JNK1 signaling cascade and caspase inhibition Mol Cell Biol 2002 22 6 1754-1766 135597 11865055 10.1128/ MCB.22.6.1754-1766.2002
55. Hofer-Warbinek R Schmid JA Stehlik C Binder BR Lipp J de Martin R Activation of NF-kappa B by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1 J Biol Chem 2000 275 29 22064-22068 10.1074/jbc.M910346199 10807933
56. Levkau B Garton KJ Ferri N Kloke K Nofer JR Baba HA Raines EW Breithardt G xIAP induces cell-cycle arrest and activates nuclear factor-kappaB: new survival pathways disabled by caspase-mediated cleavage during apoptosis of human endothelial cells Circ Res 2001 88 3 282-290 11179195
57. Berezovskaya O Schimmer AD Glinskii AB Pinilla C Hoffman RM Reed JC Glinsky GV Increased expression of apoptosis inhibitor protein XIAP contributes to anoikis resistance of circulating human prostate cancer metastasis precursor cells Cancer Res 2005 65 6 2378-2386 10.1158/ 0008-5472.CAN-04-2649 15781653
58. Sasaki H Sheng Y Kotsuji F Tsang BK Down-regulation of X-linked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells Cancer Res 2000 60 20 5659-5666 11059757
59. Tong QS Zheng LD Wang L Zeng FQ Chen FM Dong JH Lu GC Downregulation of XIAP expression induces apoptosis and enhances chemotherapeutic sensitivity in human gastric cancer cells Cancer Gene Ther 2005 12 5 509-514 15706355
60. Harlin H Reffey SB Duckett CS Lindsten T Thompson CB Characterization of XIAP-deficient mice Mol Cell Biol 2001 21 10 3604-3608 100282 11313486 10.1128/MCB.21.10.3604-3608.2001
61. Casper ES Bajorin D Phase II trial of carboplatin in patients with advanced melanoma Invest New Drugs 1990 8 2 187-190 10.1007/BF00177256 1696568
62. Chang A Hunt M Parkinson DR Hochster H Smith TJ Phase II trial of carboplatin in patients with metastatic malignant melanoma. A report from the Eastern Cooperative Oncology Group Am J Clin Oncol 1993 16 2 152-155 10.1097/00000421-199304000-00015 8452109
63. Al-Sarraf M Fletcher W Oishi N Pugh R Hewlett JS Balducci L McCracken J Padilla F Cisplatin hydration with and without mannitol diuresis in refractory disseminated malignant melanoma: A southwest oncology group study Cancer Treat Rep 1982 66 1 31-35 6796269
64. Mor G Fu HH Alvero AB Phenoxodiol, a novel approach for the treatment of ovarian cancer Curr Opin Investig Drugs 2006 7 6 542-548 16784025