Oncogenic B-RAF signaling in melanoma impairs the therapeutic advantage of autophagy inhibition

Clinical Cancer Research

Volumn 17, Issue 8, 2011, Pages 2216-2226

  Armstrong, Jane L ^a   Corazzari, Marco ^b   Martin, Shaun ^a   Pagliarini, Vittoria ^b   Falasca, Laura ^b   Hill, David S ^a   Ellis, Nicola ^a   Sabah, Salim Al ^a   Redfern, Christopher P F ^a   Fimia, Gian Maria ^b   Piacentini, Mauro ^b,c   Lovat, Penny E ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ACTIVATING TRANSCRIPTION FACTOR 4; AUTOPHAGY PROTEIN 7; BECLIN 1; BORTEZOMIB; FENRETINIDE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; RAPAMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; B RAF GENE; CELL VACUOLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMAN; HUMAN CELL; LYSOSOME; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; ONCOGENE; PHAGOSOME; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; AUTOPHAGY; BIPHENYL COMPOUNDS; BLOTTING, WESTERN; BORONIC ACIDS; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; FEMALE; FENRETINIDE; HUMANS; LUMINESCENT PROTEINS; MELANOMA; MICE; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; NITROPHENOLS; PIPERAZINES; PROTO-ONCOGENE PROTEINS B-RAF; PYRAZINES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SULFONAMIDES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79954609211     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-3003     Document Type: Article

References (46)

1. Lefranc F, Facchini V, Kiss R. Proautophagic drugs: a novel means to combat apoptosis-resistant cancers, with a special emphasis on glioblastomas. Oncologist 2007;12:1395-403.
2. Yang Z, Klionsky DJ. An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 2009;335:1-32.
3. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for selfeating. Cell Death Differ 2005;12:1542-52.
4. White E, Karp C, Strohecker AM, Guo Y, Mathew R. Role of autophagy in suppression of inflammation and cancer. Curr Opin Cell Biol 2010;22:212-7.
5. Maiuri M, Tasdemir E, Criollo A, Morselli E, Vicencio JM, Carnuccio R, et al. Control of autophagy by oncogenes and tumor suppressor genes. Cell Death Differ 2009;16:87-93.
6. Scarlatti F, Granata R, Meijer AJ, Codogno P. Does autophagy have a license to kill mammalian cells? Cell Death Differ 2009;16:12-20.
7. Eisenberg-Lerner A, Bialik S, Simon H-U, Kimchi A. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 2009;16:966-75.
8. Qin L, Wang Z, Tao L, Wang Y. ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 2010;6:239-47.
9. Salazar M, Carracedo A, Salanueva IJ, Hernández-Tiedra S, Lorente M, Egia A, et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest 2009;119:1359-72.
10. Park MA, Yacoub A, Sarkar D, Emdad L, Rahmani M, Spiegel S, et al. PERK-dependent regulation of MDA-7/IL-24-induced autophagy in primary human glioma cells. Autophagy 2008;4:513-5. (Pubitemid 351705149)
11. Hill D, Martin S, Armstrong JL, Flockhart R, Tonison JJ, Simpson DG, et al. Combining the ER stress-inducing agents bortezomib and fenretinide as a novel therapeutic strategy for metastatic melanoma. Clin Cancer Res 2009;15:1192-8.
12. Lovat PE, Corazzari M, Armstrong JL, Martin S, Pagliarini V, Hill D, et al. Increasing melanoma cell death using inhibitors of protein disulfide isomerases to abrogate survival responses to endoplasmic reticulum stress. Cancer Res 2008;68:5363-9.
13. Corazzari M, Lovat PE, Armstrong JL, Fimia GM, Hill DS, Birch-Machin M, et al. Targeting homeostatic mechanisms of endoplasmic reticulum stress to increase susceptibility of cancer cells to fenretinide induced apoptosis: the role of stress proteins ERdj5 and ERp57. Br J Cancer 2007;96:1062-71. (Pubitemid 46608316)
14. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007;171:512-24.
15. Tiwari M, Bajpai VK, Sahasrabuddhe AA, Kumar A, Sinha RA, Behari S, et al. Inhibition of N-(4-hydroxyphenyl) retinamide-induced autophagy at a lower dose enhances cell death in malignant glioma cells. Carcinogenesis 2008;29:600-9. (Pubitemid 351404878)
16. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-54. (Pubitemid 34716871)
17. Dong J, Phelps RG, Qiao R, Yao S, Benard O, Ronai Z, et al. BRAF oncogenic mutations correlate with progression rather than initiation of human melanoma. Cancer Res 2003;63:3883-5. (Pubitemid 36917898)
18. Dhomen N, Marais R. BRAF signaling and targeted therapies in melanoma. Hematol Oncol Clin North Am 2009;23:529-45.
19. Corcelle E, Nebout M, Bekri S, Gauthier N, Hofman P, Poujeol P, et al. Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res 2006;66:6861-70. (Pubitemid 44085647)
20. Cagnol S, Chambard JC. ERK and cell death: mechanisms of ERKinduced cell death - apoptosis, autophagy and senescence. FEBS J 2010;277:2-21.
21. Maddodi N, Huang W, Havighurst T, Kim K, Longley BJ, Setaluri V. Induction of autophagy and inhibition of melanoma growth in vitro and in vivo by hyperactivation of oncogenic BRAF. J Invest Dermatol 2010;130:1657-67.
22. Armstrong JL, Veal GJ, Redfern CP, Lovat PE. Role of Noxa in p53-independent fenretinide-induced apoptosis of neuroectodermal tumours. Apoptosis 2007;12:613-22.
23. Flockhart R, Armstrong JL, Reynolds NJ, Lovat PE. NFAT signalling is a novel target of oncogenic BRAF in metastatic melanoma. Br J Cancer 2009;101:1448-55.
24. Armstrong JL, Flockhart R, Veal GJ, Lovat PE, Redfern C P F. Regulation of ER stress-induced cell death by ATF4 in neuroectodermal tumour cells. J Biol Chem 2010;285:6091-100.
25. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, et al. Ambra1 regulates autophagy and development of the nervous system. Nature 2007;447:1121-5. (Pubitemid 47014434)
26. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescenttagged LC3. Autophagy 2007;3:452-60. (Pubitemid 47293726)
27. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000;19:5720-8.
28. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008;4:151-75. (Pubitemid 351231180)
29. Formelli F, Cavadini E, Luksch R, Garaventa A, Villani MG, Appierto V, et al. Pharmacokinetics of oral fenretinide in neuroblastoma patients: indications for optimal dose and dosing schedule also with respect to the active metabolite 4-oxo-fenretinide. Cancer Chemother Pharmacol 2008;62:655-65.
30. Moreau P, Coiteux V, Hulin C, Leleu X, van de Velde H, Acharya M, et al. Prospective comparison of subcutaneous versus intravenous administration of bortezomib in patients with multiple myeloma. Haematologica 2008;93:1908-11.
31. Dhomen N, Reis-Filho JS, Da Rocha Dias S, Hayward R, Savage K, Delmas V, et al. Oncogenic Braf induces melanocyte senescence and melanoma in mice. Cancer Cell 2009;15:294-303.
32. Buytaert E, Callewaert G, Hendrickx N, Scorrano L, Hartmann D, Missiaen L, et al. Role of endoplasmic reticulum depletion and multidomain proapoptotic BAX and BAK proteins in shaping cell death after hypericin-mediated photodynamic therapy. FASEB J 2006;20:756-8. (Pubitemid 46671205)
33. Fazi B, Bursch W, Fimia GM, Nardacci R, Piacentini M, Di Sano F, et al. Fenretinide induces autophagic cell death in caspase-defective breast cancer cells. Autophagy 2008;4:435-41. (Pubitemid 351705140)
34. Balmanno K, Cook SJ. Tumour cell survival signalling by the ERK1/2 pathway. Cell Death Differ 2009;16:368-77.
35. Levine B, Sinha S, Kroemer G. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 2008;4:600-6.
36. Maiuri MC, Criollo A, Tasdemir E, Vicencio JM, Tajeddine N, Hickman JA, et al. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X (L). Autophagy 2007;3:374-6. (Pubitemid 46986348)
37. Belloni D, Veschini L, Foglieni C, Dell'Antonio G, Caligaris-Cappio F, Ferrarini M, et al. Bortezomib induces autophagic death in proliferating human endothelial cells. Exp Cell Res 2010;316:1010-8.
38. Seibenhener LM, Babu JR, Geetha T, Wong HC, Krishna NR, Wooten MW. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol Cell Biol 2004;24:8055-68. (Pubitemid 39167456)
39. Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell 2009;34:259-69.
40. Verfaillie T, Salazar M, Velasco G, Agostinis P. Linking ER stress to autophagy: potential implications for cancer therapy. Int J Cell Biol 2010; doi:2010:ID 930509.
41. Salazar M, Carracedo A, Salanueva IJ, Hernández-Tiedra S, Egia A, Lorente M, et al. TRB3 links ER stress to autophagy in cannabinoid anti-tumoral action. Autophagy 2009;5:1048-9.
42. Jin HO, Seo SK, Woo SH, Kim ES, Lee HC, Yoo DH, et al. Activating transcription factor 4 and CCAAT/enhancer-binding protein-beta negatively regulate the mammalian target of rapamycin via Redd1 expression in response to oxidative and endoplasmic reticulum stress. Free Radic Biol Med 2009;46:1158-67.
43. Rzymski T, Milani M, Pike L, Buffa F, Mellor HR, Winchester L, et al. Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene 2010;29:4424-35.
44. Gao Z, Gammoh N, Wong PM, Erdjument-Bromage H, Tempst P, Jiang X. Processing of autophagic protein LC3 by the 20S proteasome. Autophagy 2010;6:126-37.
45. Karbowniczek M, Spittle CS, Morrison T, Wu H, Henske EP. mTOR is activated in the majority of malignant melanomas. J Invest Dermatol 2008;128:980-7. (Pubitemid 351374287)
46. Zhuang L, Lee CS, Scolyer RA, McCarthy SW, Zhang XD, Thompson JF, 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. (Pubitemid 46482365)