Concomitant inhibition of AKT and autophagy is required for efficient cisplatin-induced apoptosis of metastatic skin carcinoma

International Journal of Cancer

Volumn 127, Issue 12, 2010, Pages 2790-2803

  Claerhout, Sofie ^a,d   Verschooten, Lien ^a   Van Kelst, Sofie ^a   De Vos, Rita ^a   Proby, Charlotte ^b   Agostinis, Patrizia ^c   Garmyn, Marjan ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

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

Author keywords

AKT; Autophagy; Cisplatin; SCC

Indexed keywords

3 METHYLADENINE; ACTIN; BIOLOGICAL MARKER; CASPASE 3; CASPASE 9; CISPLATIN; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; GREEN FLUORESCENT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; PROTEIN LC3 II; UNCLASSIFIED DRUG;

ADVANCED CANCER; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CANCER RESISTANCE; CANCER STAGING; CAUCASIAN; CONTROLLED STUDY; DRUG CYTOTOXICITY; EARLY CANCER; ELECTRON MICROSCOPY; ENZYME INHIBITION; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; KERATINOCYTE; LYMPH NODE METASTASIS; MALIGNANT TRANSFORMATION; METASTASIS; PHAGOSOME; PRIORITY JOURNAL; PROGNOSIS; SKIN CARCINOMA; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH;

ADENINE; ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELLS, CULTURED; CISPLATIN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; KERATINOCYTES; LYMPHATIC METASTASIS; MEMBRANE POTENTIAL, MITOCHONDRIAL; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS C-AKT; SKIN NEOPLASMS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 77955714496     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25300     Document Type: Article

References (53)

1. de Vries E, Steliarova-Foucher E, Spatz A, Ardanaz E, Eggermont AM, Coebergh JW,. Skin cancer incidence and survival in European children and adolescents (1978-1997). Report from the Automated Childhood Cancer Information System project. Eur J Cancer 2006; 42: 2170 -82.
2. Staples MP, Elwood M, Burton RC, Williams JL, Marks R, Giles GG,. Non-melanoma skin cancer in Australia: the 2002 national survey and trends since 1985. Med J 2006; 184: 6 -10.
3. de Vries E, van de Poll-Franse LV, Louwman WJ, de Gruijl FR, Coebergh JW,. Predictions of skin cancer incidence in the Netherlands up to 2015. Br J Dermatol 2005; 152: 481 -8.
4. Martinez JC, Otley CC, Okuno SH, Foote RL, Kasperbauer JL,. Chemotherapy in the management of advanced cutaneous squamous cell carcinoma in organ transplant recipients: theoretical and practical considerations. Dermatol Surg 2004; 30: 679 -86.
5. Moloney FJ, Comber H, O'Lorcain P, O'Kelly P, Conlon PJ, Murphy GM,. A population-based study of skin cancer incidence and prevalence in renal transplant recipients. Br J Dermatol 2006; 154: 498 -504.
6. Shin DM, Glisson BS, Khuri FR, Clifford JL, Clayman G, Benner SE, Forastiere AA, Ginsberg L, Liu D, Lee JJ, Myers J, Goepfert H, et al. Phase II and biologic study of interferon alfa, retinoic acid, and cisplatin in advanced squamous skin cancer. J Clin Oncol 2002; 20: 364 -70.
7. Neville JA, Welch E, Leffell DJ,. Management of nonmelanoma skin cancer in 2007. Nat Clin Pract Oncol 2007; 4: 462 -9.
8. Kelland L,. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 2007; 7: 573 -84.
9. Siddik ZH,. Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 2003; 22: 7265 -79.
10. Manning BD, Cantley LC,. AKT/PKB signaling: navigating downstream. Cell 2007; 129: 1261 -74.
11. Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB,. Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat Rev Drug Discov 2005; 4: 988 -1004.
12. Carpten JD, Faber AL, Horn C, Donoho GP, Briggs SL, Robbins CM, Hostetter G, Boguslawski S, Moses TY, Savage S, Uhlik M, Lin A, et al. A transforming mutation in the pleckstrin homology domain of AKT1 in cancer. Nature 2007; 448: 439 -44.
13. Vivanco I, Sawyers CL,. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002; 2: 489 -501.
14. Lin N, Moroi Y, Uchi H, Fukiwake N, Dainichi T, Takeuchi S, Takahara M, Tu Y, Furue M, Urabe K,. Significance of the expression of phosphorylated-STAT3, -Akt, and -ERK1/2 in several tumors of the epidermis. J Dermatol Sci 2007; 48: 71 -3.
15. DiGiovanni J, Bol DK, Wilker E, Beltran L, Carbajal S, Moats S, Ramirez A, Jorcano J, Kiguchi K,. Constitutive expression of insulin-like growth factor-1 in epidermal basal cells of transgenic mice leads to spontaneous tumor promotion. Cancer Res 2000; 60: 1561 -70.
16. Segrelles C, Lu J, Hammann B, Santos M, Moral M, Cascallana JL, Lara MF, Rho O, Carbajal S, Traag J, Beltran L, Martanez-Cruz AB, et al. Deregulated activity of Akt in epithelial basal cells induces spontaneous tumors and heightened sensitivity to skin carcinogenesis. Cancer Res 2007; 67: 10879 -88.
17. Guertin DA, Sabatini DM,. An expanding role for mTOR in cancer. Trends Mol Med 2005; 11: 353 -61.
18. Debnath J, Baehrecke EH, Kroemer G,. Does autophagy contribute to cell death? Autophagy 2005; 1: 66 -74.
19. Hait WN, Jin S, Yang JM,. A matter of life or death (or both): understanding autophagy in cancer. Clin Cancer Res 2006; 12: 1961 -5.
20. Ferraro E, Cecconi F,. Autophagic and apoptotic response to stress signals in mammalian cells. Arch Biochem Biophys 2007; 462: 210 -19.
21. Levine B,. Cell biology: autophagy and cancer. Nature 2007; 446: 745 -7.
22. Mizushima N, Levine B, Cuervo AM, Klionsky DJ,. Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069 -75.
23. Claerhout S, Decraene D, Van Laethem A, Van Kelst S, Agostinis P, Garmyn M,. AKT delays the early-activated apoptotic pathway in UVB-irradiated keratinocytes via BAD translocation. J Invest Dermatol 2007; 127: 429 -38.
24. Proby CM, Purdie KJ, Sexton CJ, Purkis P, Navsaria HA, Stables JN, Leigh IM,. Spontaneous keratinocyte cell lines representing early and advanced stages of malignant transformation of the epidermis. Exp Dermatol 2000; 9: 104 -17.
25. Popp S, Waltering S, Holtgreve-Grez H, Jauch A, Proby C, Leigh IM, Boukamp P,. Genetic characterization of a human skin carcinoma progression model: from primary tumor to metastasis. J Invest Dermatol 2000; 115: 1095 -103.
26. Gilchrest BA,. In vitro assessment of keratinocyte aging. J Invest Dermatol 1983; 81: 184s -189s.
27. Altomare DA, Testa JR,. Perturbations of the AKT signaling pathway in human cancer. Oncogene 2005; 24: 7455 -64.
28. Samuels Y, Velculescu VE,. Oncogenic mutations of PIK3CA in human cancers. Cell Cycle 2004; 3: 1221 -4.
29. Thomas RK, Baker AC, Debiasi RM, Winckler W, Laframboise T, Lin WM, Wang M, Feng W, Zander T, MacConaill L, Lee JC, Nicoletti R, et al. High-throughput oncogene mutation profiling in human cancer. Nat Genet 2007; 39: 347 -51.
30. Jurinke C, van den Boom D, Cantor CR, Köster H,. The use of MassARRAY technology for high throughput genotyping. Adv Biochem Eng Biotechnol 2002; 77: 57 -74.
31. Barnett SF, Defeo-Jones D, Fu S, Hancock PJ, Haskell KM, Jones RE, Kahana JA, Kral AM, Leander K, Lee LL, Malinowski J, McAvoy EM, et al. Identification and characterization of pleckstrin-homology-domain-dependent and isoenzyme-specific Akt inhibitors. Biochem J 2005; 385: 399 -408.
32. Degtyarev M, De Mazïre A, Orr C, Lin J, Lee BB, Tien JY, Prior WW, van Dijk S, Wu H, Gray DC, Davis DP, Stern HM, et al. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 2008; 183: 101 -16.
33. Mizushima N, Yoshimori T,. How to interpret LC3 immunoblotting. Autophagy 2007; 3: 542 -5.
34. Kimura S, Noda T, Yoshimori T,. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3: 452 -60.
35. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T,. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720 -8.
36. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4: 151 -75.
37. Bellacosa A, Kumar CC, Di Cristofano A, Testa JR,. Activation of AKT kinases in cancer: implications for therapeutic targeting. Adv Cancer Res 2005; 94: 29 -86.
38. Lee MW, Kim DS, Min NY, Kim HT,. Akt1 inhibition by RNA interference sensitizes human non-small cell lung cancer cells to cisplatin. Int J Cancer 2008; 122: 2380 -4.
39. Kim HJ, Oh JE, Kim SW, Chun YJ, Kim MY,. Ceramide induces p38 MAPK-dependent apoptosis and Bax translocation via inhibition of Akt in HL-60 cells. Cancer Lett 2008; 260: 88 -95.
40. Tanaka Y, Gavrielides MV, Mitsuuchi Y, Fujii T, Kazanietz MG,. Protein kinase C promotes apoptosis in LNCaP prostate cancer cells through activation of p38 MAPK and inhibition of the Akt survival pathway. J Biol Chem 2003; 278: 33753 -62.
41. Okamura A, Iwata N, Tamekane A, Yakushijin K, Nishikawa S, Hamaguchi M, Fukui C, Yamamoto K, Matsui T,. Casein kinase Iepsilon down-regulates phospho-Akt via PTEN, following genotoxic stress-induced apoptosis in hematopoietic cells. Life Sci 2006; 78: 1624 -9.
42. Cinar B, Fang PK, Lutchman M, Di Vizio D, Adam RM, Pavlova N, Rubin MA, Yelick PC, Freeman MR,. The pro-apoptotic kinase Mst1 and its caspase cleavage products are direct inhibitors of Akt1. EMBO J 2007; 26: 4523 -34.
43. Jahani-Asl A, Basak A, Tsang BK,. Caspase-3-mediated cleavage of Akt: involvement of non-consensus sites and influence of phosphorylation. FEBS Lett 2007; 581: 2883 -8.
44. Luo J, Manning BD, Cantley LC,. Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 2003; 4: 257 -62.
45. DeFeo-Jones D, Barnett SF, Fu S, Hancock PJ, Haskell KM, Leander KR, McAvoy E, Robinson RG, Duggan ME, Lindsley CW, Zhao Z, Huber HE, et al. Tumor cell sensitization to apoptotic stimuli by selective inhibition of specific Akt/PKB family members. Mol Cancer Ther 2005; 4: 271 -9.
46. Liu LZ, Zhou XD, Qian G, Shi X, Fang J, Jiang BH,. AKT1 amplification regulates cisplatin resistance in human lung cancer cells through the mammalian target of rapamycin/p70S6K1 pathway. Cancer Res 2007; 67: 6325 -32.
47. Gagnon V, Mathieu I, Sexton E, Leblanc K, Asselin E,. AKT involvement in cisplatin chemoresistance of human uterine cancer cells. Gynecol Oncol 2004; 94: 785 -95.
48. Mathew R, Karantza-Wadsworth V, White E,. Role of autophagy in cancer. Nat Rev Cancer 2007; 7: 961 -7.
49. Amaravadi RK, Thompson CB,. The roles of therapy-induced autophagy and necrosis in cancer treatment. Clin Cancer Res 2007; 13: 7271 -9.
50. Kondo Y, Kanzawa T, Sawaya R, Kondo S,. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5: 726 -34.
51. Ma WW, Adjei AA,. Novel agents on the horizon for cancer therapy. CA Cancer J Clin 2009; 59: 111 -37.
52. Sinnberg T, Lasithiotakis K, Niessner H, Schittek B, Flaherty KT, Kulms D, Maczey E, Campos M, Gogel J, Garbe C, Meier F,. Inhibition of PI3K-AKT-mTOR signaling sensitizes melanoma cells to cisplatin and temozolomide. J Invest Dermatol 2009; 129: 1500 -15.
53. Iwase M, Yoshiba S, Uchid M, Takaoka S, Kurihara Y, Ito D, Hatori M, Shintani S,. Enhanced susceptibility to apoptosis of oral squamous cell carcinoma cells subjected to combined treatment with anticancer drugs and phosphatidylinositol 3-kinase inhibitors. Int J Oncol 2007; 31: 1141 -7.