Oncogenic suppression of PHLPP1 in human melanoma

Oncogene

Volumn 33, Issue 39, 2014, Pages 4756-4766

  Dong, L ^a   Jin, L ^a   Tseng, H Y ^a   Wang, C Y ^b   Wilmott, J S ^c,d   Yosufi, B ^c   Yan, X G ^a   Jiang, C C ^a   Scolyer, R A ^c,d,e   Zhang, X D ^a   Guo, S T ^b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b SHANXI MEDICAL UNIVERSITY   (China)

^c MELANOMA INSTITUTE AUSTRALIA   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e ROYAL PRINCE ALFRED HOSPITAL   (Australia)

Author keywords

Akt; DNA methylation; Melanoma; PHLPP1

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 1; PLECKSTRIN; PROTEIN KINASE B; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SP1; NUCLEAR PROTEIN; PHLPP1 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN PHOSPHATASE;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; GENE INTERACTION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MELANOCYTE; MELANOMA; MELANOMA CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SKIN CARCINOGENESIS; TUMOR XENOGRAFT; ANIMAL; CELL SURVIVAL; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DNA METHYLATION; DOWN-REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; MALE; MELANOMA; MICE; MICE, NUDE; NUCLEAR PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEIN PHOSPHATASES; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; SP1 TRANSCRIPTION FACTOR; TUMOR BURDEN;

EID: 84921774323     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.420     Document Type: Article

References (60)

1. Courtney KD, Corcoran RB, Engelman JA. The PI3K pathway as drug target in human cancer. J Clin Oncol 2010;28:1075-1083.
2. Ferte C, Andre F, Soria JC. Molecular circuits of solid tumors: prognostic and predictive tools for bedside use. Nat Rev Clin Oncol 2010;7:367-380.
3. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-954.
4. Smalley KS. Understanding melanoma signaling networks as the basis for molecular targeted therapy. J Invest Dermatol 2010;130:28-37.
5. 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;364:2507-2516.
6. Houslay MD. Hard times for oncogenic BRAF-expressing melanoma cells. Cancer Cell 2011;19:3-4.
7. Ribas A, Flaherty KT. BRAF targeted therapy changes the treatment paradigm in melanoma. Nat Rev Clin Oncol 2011;8:426-433.
8. Jiang CC, Lai F, Thorne RF, Yang F, Liu H, Hersey P et al. MEK-independent survival of B-RAFV600E melanoma cells selected for resistance to apoptosis induced by the RAF inhibitor PLX4720. Clin Cancer Res 2011;17:721-730.
9. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG et al. In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 2011;147:382-395.
10. Paraiso KH, Xiang Y, Rebecca VW, Abel EV, Chen YA, Munko AC et al. PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res 2011;71:2750-2760.
11. Poulikakos PI, Rosen N. Mutant BRAF melanomas-dependence and resistance. Cancer Cell 2011;19:11-15.
12. Cheung M, Sharma A, Madhunapantula SV, Robertson GP. Akt3 and mutant V600E B-Raf cooperate to promote early melanoma development. Cancer Res 2008;68:3429-3439.
13. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky Jr. WE et al. Braf (V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009;41:544-552.
14. Franke TF, Kaplan DR, Cantley LC. PI3K: downstream AKTion blocks apoptosis. Cell 1997;88:435-437.
15. Majerus PW, Kisseleva MV, Norris FA. The role of phosphatases in inositol signaling reactions. J Biol Chem 1999;274:10669-10672.
16. Park SJ, Itoh T, Takenawa T. Phosphatidylinositol 4-phosphate 5-kinase type I is regulated through phosphorylation response by extracellular stimuli. J Biol Chem 2001;276:4781-4787.
17. Bozulic L, Hemmings BA. PIKKing on PKB: regulation of PKB activity by phosphorylation. Curr Opin Cell Biol 2009;21:256-261.
18. Franke TF. PI3K/Akt: getting it right matters. Oncogene 2008;27:6473-6488.
19. Fayard E, Tintignac LA, Baudry A, Hemmings BA. Protein kinase B/Akt at a glance. J Cell Sci 2005;118:5675-5678.
20. O'Neill AK, Niederst MJ, Newton AC. Suppression of survival signalling pathways by the phosphatase PHLPP. FEBS J 2013;280:572-583.
21. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY et al. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 2006;127:125-137.
22. Gao T, Furnari F, Newton AC. PHLPP: a phosphatase that directly dephosphorylates Akt, promotes apoptosis, and suppresses tumor growth. Mol Cell 2005;18:13-24.
23. Chen M, Pratt CP, Zeeman ME, Schultz N, Taylor BS, O'Neill A et al. Identification of PHLPP1 as a tumor suppressor reveals the role of feedback activation in PTEN-mutant prostate cancer progression. Cancer Cell 2011;20:173-186.
24. Warfel NA, Newton AC. Pleckstrin homology domain leucine-rich repeat protein phosphatase (PHLPP): a new player in cell signaling. J Biol Chem 2012;287:3610-3616.
25. Nitsche C, Edderkaoui M, Moore RM, Eibl G, Kasahara N, Treger J et al. The phosphatase PHLPP1 regulates Akt2, promotes pancreatic cancer cell death, and inhibits tumor formation. Gastroenterology 2012;142:e371-e375.
26. Liu J, Weiss HL, Rychahou P, Jackson LN, Evers BM, Gao T. Loss of PHLPP expression in colon cancer: role in proliferation and tumorigenesis. Oncogene 2009;28:994-1004.
27. O'Hayre M, Niederst M, Fecteau JF, Nguyen VM, Kipps TJ, Messmer D et al. Mechanisms and consequences of the loss of PHLPP1 phosphatase in chronic lymphocytic leukemia (CLL). Leukemia 2012;26:1689-1692.
28. Molina JR, Agarwal NK, Morales FC, Hayashi Y, Aldape KD, Cote G et al. PTEN, NHERF1 and PHLPP form a tumor suppressor network that is disabled in glioblastoma. Oncogene 2012;31:1264-1274.
29. Gao T, Brognard J, Newton AC. The phosphatase PHLPP controls the cellular levels of protein kinase C. J Biol Chem 2008;283:6300-6311.
30. Liu J, Stevens PD, Li X, Schmidt MD, Gao T. PHLPP-mediated dephosphorylation of S6K1 inhibits protein translation and cell growth. Mol Cell Biol 2011;31:4917-4927.
31. Qiao M, Wang Y, Xu X, Lu J, Dong Y, Tao W et al. Mst1 is an interacting protein that mediates PHLPPs' induced apoptosis. Mol Cell 2010;38:512-523.
32. Brognard J, Sierecki E, Gao T, Newton AC. PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol Cell 2007;25:917-931.
33. Shimizu K, Okada M, Nagai K, Fukada Y. Suprachiasmatic nucleus circadian oscillatory protein, a novel binding partner of K-Ras in the membrane rafts, negatively regulates MAPK pathway. J Biol Chem 2003;278:14920-14925.
34. Davies MA, Stemke-Hale K, Lin E, Tellez C, Deng W, Gopal YN et al. Integrated molecular and clinical analysis of AKT activation in metastatic melanoma. Clin Cancer Res 2009;15:7538-7546.
35. Curtin JA, Stark MS, Pinkel D, Hayward NK, Bastian BC. PI3-kinase subunits are infrequent somatic targets in melanoma. J Invest Dermatol 2006;126:1660-1663.
36. Curtin JA, Busam K, Pinkel D, Bastian BC. Somatic activation of KIT in distinct subtypes of melanoma. J Clin Oncol 2006;24:4340-4346.
37. Ye Y, Jin L, Wilmott JS, Hu WL, Yosufi B, Thorne RF et al. PI (4, 5) P2 5-phosphatase A regulates PI3K/Akt signalling and has a tumour suppressive role in human melanoma. Nat Commun 2013;4:1508.
38. Liang J, Slingerland JM. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003;2:339-345.
39. Govindarajan B, Sligh JE, Vincent BJ, Li M, Canter JA, Nickoloff BJ et al. Overexpression of Akt converts radial growth melanoma to vertical growth melanoma. J Clin Invest 2007;117:719-729.
40. Stark M, Hayward N. Genome-wide loss of heterozygosity and copy number analysis in melanoma using high-density single-nucleotide polymorphism arrays. Cancer Res 2007;67:2632-2642.
41. Bradley EW, Carpio LR, Westendorf JJ. Histone deacetylase 3 suppression increases PH domain and leucine-rich repeat phosphatase (Phlpp) 1 expression in chondrocytes to suppress Akt signaling and matrix secretion. J Biol Chem 2013;288:9572-9582.
42. Klug M, Rehli M. Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 2006;1:127-130.
43. Rishi V, Bhattacharya P, Chatterjee R, Rozenberg J, Zhao J, Glass K et al. CpG methylation of half-CRE sequences creates C/EBPalpha binding sites that activate some tissue-specific genes. Proc Natl Acad Sci USA 2010;107:20311-20316.
44. Carver BS, Chapinski C, Wongvipat J, Hieronymus H, Chen Y, Chandarlapaty S et al. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 2011;19:575-586.
45. Gewinner C, Wang ZC, Richardson A, Teruya-Feldstein J, Etemadmoghadam D, Bowtell D et al. Evidence that inositol polyphosphate 4-phosphatase type II is a tumor suppressor that inhibits PI3K signaling. Cancer Cell 2009;16:115-125.
46. Fedele CG, Ooms LM, Ho M, Vieusseux J, O'Toole SA, Millar EK et al. Inositol polyphosphate 4-phosphatase II regulates PI3K/Akt signaling and is lost in human basal-like breast cancers. Proc Natl Acad Sci USA 2010;107:22231-22236.
47. Stahl JM, Sharma A, Cheung M, Zimmerman M, Cheng JQ, Bosenberg MW et al. Deregulated Akt3 activity promotes development of malignant melanoma. Cancer Res 2004;64:7002-7010.
48. Warfel NA, Niederst M, Stevens MW, Brennan PM, Frame MC, Newton AC. Mislocalization of the E3 ligase, beta-transducin repeat-containing protein 1 (beta-TrCP1), in glioblastoma uncouples negative feedback between the pleckstrin homology domain leucine-rich repeat protein phosphatase 1 (PHLPP1) and Akt. J Biol Chem 2011;286:19777-19788.
49. Mirmohammadsadegh A, Marini A, Nambiar S, Hassan M, Tannapfel A, Ruzicka T et al. Epigenetic silencing of the PTEN gene in melanoma. Cancer Res 2006;66:6546-6552.
50. Beezhold K, Liu J, Kan H, Meighan T, Castranova V, Shi X et al. miR-190-mediated downregulation of PHLPP contributes to arsenic-induced Akt activation and carcinogenesis. Toxicol Sci 2011;123:411-420.
51. Li L, Davie JR. The role of Sp1 and Sp3 in normal and cancer cell biology. Ann Anat 2010;192:275-283.
52. Saavedra A, Garcia-Martinez JM, Xifro X, Giralt A, Torres-Peraza JF, Canals JM et al. PH domain leucine-rich repeat protein phosphatase 1 contributes to maintain the activation of the PI3K/Akt pro-survival pathway in Huntington's disease striatum. Cell Death Differ 2010;17:324-335.
53. Patterson SJ, Han JM, Garcia R, Assi K, Gao T, O'Neill A et al. Cutting edge: PHLPP regulates the development, function, and molecular signaling pathways of regulatory T cells. J Immunol 2011;186:5533-5537.
54. Madhunapantula SV, Robertson GP. The PTEN-AKT3 signaling cascade as a therapeutic target in melanoma. Pigment Cell Melanoma Res 2009;22:400-419.
55. Gillespie S, Zhang XD, Hersey P. Variable expression of protein kinase C epsilon in human melanoma cells regulates sensitivity to TRAIL-induced apoptosis. Mol Cancer Ther 2005;4:668-676.
56. ∗, a p53-responsive microRNA, functions as an oncogenic regulator in human melanoma. Proc Natl Acad Sci USA 2011;108:15840-15845.
57. Tay KH, Jin L, Tseng HY, Jiang CC, Ye Y, Thorne RF et al. Suppression of PP2A is critical for protection of melanoma cells upon endoplasmic reticulum stress. Cell death & disease 2012;3:e337.
58. Zhuang L, Scolyer RA, Lee CS, McCarthy SW, Cooper WA, Zhang XD et al. Expression of glucose-regulated stress protein GRP78 is related to progression of melanoma. Histopathology 2009;54:462-470.
59. Guo ST, Jiang CC, Wang GP, Li YP, Wang CY, Guo XY et al. MicroRNA-497 targets insulin-like growth factor 1 receptor and has a tumour suppressive role in human colorectal cancer. Oncogene 2013;32:1910-1920.
60. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996;93:9821-9826.