Candidate tumor suppressor and pVHL partner Jade-1 binds and inhibits AKT in renal cell carcinoma

Cancer Research

Volumn 73, Issue 17, 2013, Pages 5371-5380

  Zeng, Liling ^a   Bai, Ming ^b   Mittal, Amit K ^a   El Jouni, Wassim ^b   Zhou, Jing ^b   Cohen, David M ^c   Zhou, Mina I ^a   Cohen, Herbert T ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; JADE 1 PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN AKT1; PROTEIN KINASE B; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ADULT; AKT1 GENE; AMINO TERMINAL SEQUENCE; ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER STEM CELL; CARBOXY TERMINAL SEQUENCE; CARCINOMA CELL; CATALYSIS; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; FEMALE; GENE; GENE ACTIVATION; GENE TARGETING; HUMAN; HUMAN CELL; JADE 1 GENE; KIDNEY CARCINOMA; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TARGETING;

APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, RENAL CELL; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION PROFILING; HOMEODOMAIN PROTEINS; HUMANS; KIDNEY NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN ARRAY ANALYSIS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RNA, SMALL INTERFERING; TOR SERINE-THREONINE KINASES; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84883479915     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4707     Document Type: Article

References (50)

1. Cohen HT, McGovern FJ. Renal-cell carcinoma. N Engl J Med 2005;353:2477-90. (Pubitemid 41770167)
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
3. Li L, Kaelin WG Jr. New insights into the biology of renal cell carcinoma. Hematol Oncol Clin North Am 2011;25:667-86.
4. Latif F, Tory K, Gnarra J, Yao M, Duh FM, Orcutt ML, et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993;260:1317-20. (Pubitemid 23231974)
5. Gnarra JR, Tory K, Weng Y, Schmidt L, Wei MH, Li H, et al. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat Genet 1994;7:85-90. (Pubitemid 24232386)
6. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell 2007;129:1261-74. (Pubitemid 46962095)
7. Frew IJ, Thoma CR, Georgiev S, Minola A, Hitz M, Montani M, et al. pVHL and PTEN tumour suppressor proteins cooperatively suppress kidney cyst formation. EMBO J 2008;27:1747-57.
8. Hager M, Haufe H, Kemmerling R, Hitzl W, Mikuz G, Moser PL, et al. Increased activated Akt expression in renal cell carcinomas and prognosis. J Cell Mol Med 2009;13:2181-8.
9. Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH, et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet 1997;15:356-62. (Pubitemid 27147102)
10. Ikediobi ON, Davies H, Bignell G, Edkins S, Stevens C, O'Meara S, et al. Mutation analysis of 24 known cancer genes in the NCI-60 cell line set. Mol Cancer Ther 2006;5:2606-12. (Pubitemid 44848987)
11. Velickovic M, Delahunt B, McIver B, Grebe SK. Intragenic PTEN/MMAC1 loss of heterozygosity in conventional (clear-cell) renal cell carcinoma is associated with poor patient prognosis. Mod Pathol 2002;15:479-85. (Pubitemid 34521396)
12. Shin Lee J, Seok Kim H, Bok Kim Y, Cheol Lee M, Soo Park C. Expression of PTEN in renal cell carcinoma and its relation to tumor behavior and growth. J Surg Oncol 2003;84:166-72.
13. Cho D, Signoretti S, Dabora S, Regan M, Seeley A, Mariotti M, et al. Potential histologic and molecular predictors of response to temsirolimus in patients with advanced renal cell carcinoma. Clin Genitourin Cancer 2007;5:379-85. (Pubitemid 47584475)
14. Morris ZS, McClatchey AI. Aberrant epithelial morphology and persistent epidermal growth factor receptor signaling in a mouse model of renal carcinoma. Proc Natl Acad Sci U S A 2009;106:9767-72.
15. Sourbier C, Lindner V, Lang H, Agouni A, Schordan E, Danilin S, et al. The phosphoinositide 3-kinase/Akt pathway: a new target in human renal cell carcinoma therapy. Cancer Res 2006;66:5130-42. (Pubitemid 43844935)
16. Zhou MI, Wang H, Ross JJ, Kuzmin I, Xu C, Cohen HT. The von Hippel-Lindau tumor suppressor stabilizes novel plant homeodomain protein Jade-1. J Biol Chem 2002;277:39887-98. (Pubitemid 35190975)
17. Zhou MI, Wang H, Foy RL, Ross JJ, Cohen HT. Tumor suppressor von Hippel-Lindau (VHL) stabilization of Jade-1 protein occurs through plant homeodomains and is VHL mutation dependent. Cancer Res 2004;64:1278-86. (Pubitemid 38235594)
18. Zhou MI, Foy RL, Chitalia VC, Zhao J, Panchenko MV, Wang H, et al. Jade-1, a candidate renal tumor suppressor that promotes apoptosis. Proc Natl Acad Sci U S A 2005;102:11035-40. (Pubitemid 41105988)
19. Chitalia VC, Foy RL, Bachschmid MM, Zeng L, Panchenko MV, Zhou MI, et al. Jade-1 inhibits Wnt signalling by ubiquitylating beta-catenin and mediates Wnt pathway inhibition by pVHL. Nat Cell Biol 2008;10:1208-16.
20. Panchenko MV, Zhou MI, Cohen HT. von Hippel-Lindau partner Jade-1 is a transcriptional co-activator associated with histone acetyltransferase activity. J Biol Chem 2004;279:56032-41. (Pubitemid 40066611)
21. Foy RL, Chitalia VC, Panchenko MV, Zeng L, Lopez D, Lee JW, et al. Polycystin-1 regulates the stability and ubiquitination of transcription factor Jade-1. Hum Mol Genet 2012;21:5456-71.
22. Lian X, Duan X, Wu X, Li C, Chen S, Wang S, et al. Expression and clinical significance of von Hippel-Lindau downstream genes: Jade-1 and beta-catenin related to renal cell carcinoma. Urology 2012;80:485.e7-13.
23. Tzouanacou E, Tweedie S, Wilson V. Identification of Jade-1, a gene encoding a PHD zinc finger protein, in a gene trap mutagenesis screen for genes involved in anteroposterior axis development. Mol Cell Biol 2003;23:8553-2.
24. Voas MG, Rebay I. The novel plant homeodomain protein rhinoceros antagonizes Ras signaling in the Drosophila eye. Genetics 2003;165:1993-2006. (Pubitemid 38040285)
25. Cui M, Chen J, Myers TR, Hwang BJ, Sternberg PW, Greenwald I, et al. SynMuv genes redundantly inhibit lin-3/EGF expression to prevent inappropriate vulval induction in C. elegans. Dev Cell 2006;10:667-72.
26. Fujio Y, Guo K, Mano T, Mitsuuchi Y, Testa JR, Walsh K. Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol Cell Biol 1999;19:5073-82. (Pubitemid 29289545)
27. Zhou GL, Tucker DF, Bae SS, Bhatheja K, Birnbaum MJ, Field J. Opposing roles for Akt1 and Akt2 in Rac/Pak signaling and cell migration. J Biol Chem 2006;281:36443-53. (Pubitemid 46041378)
28. Ryan MJ, Johnson G, Kirk J, Fuerstenberg SM, Zager RA, Torok-Storb B. HK-2: an immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int 1994;45:48-57. (Pubitemid 24045991)
29. Shiojima I, Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev 2006;20:3347-65. (Pubitemid 44969154)
30. Mayo LD, Donner DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci U S A 2001;98:11598-603. (Pubitemid 32928774)
31. Zhou BP, Liao Y, Xia W, Zou Y, Spohn B, Hung MC. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat Cell Biol 2001;3:973-82. (Pubitemid 34428742)
32. Kuhn I, Bartholdi MF, Salamon H, Feldman RI, Roth RA, Johnson PH. Identification of AKT-regulated genes in inducible MERAkt cells. Physiol Genomics 2001;7:105-14.
33. Tiwari G, Sakaue H, Pollack JR, Roth RA. Gene expression profiling in prostate cancer cells with Akt activation reveals Fra-1 as an Akt-inducible gene. Mol Cancer Res 2003;1:475-84. (Pubitemid 36459258)
34. Cohen P, Frame S. The renaissance of GSK3. Nat Rev Mol Cell Biol 2001;2:769-76. (Pubitemid 33679839)
35. Pekarsky Y, Koval A, Hallas C, Bichi R, Tresini M, Malstrom S, et al. Tcl1 enhances Akt kinase activity and mediates its nuclear translocation. Proc Natl Acad Sci U S A 2000;97:3028-33. (Pubitemid 30183249)
36. Du K, Herzig S, Kulkarni RN, Montminy M. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 2003;300:1574-7. (Pubitemid 36682889)
37. Maira SM, Galetic I, Brazil DP, Kaech S, Ingley E, Thelen M, et al. Carboxyl-terminal modulator protein (CTMP), a negative regulator of PKB/Akt and v-Akt at the plasma membrane. Science 2001;294:374-80. (Pubitemid 32963405)
38. Kumar CC, Madison V. AKT crystal structure and AKT-specific inhibitors. Oncogene 2005;24:7493-501. (Pubitemid 41637989)
39. Chan TO, Zhang J, Rodeck U, Pascal JM, Armen RS, Spring M, et al. Resistance of Akt kinases to dephosphorylation through ATP-dependent conformational plasticity. Proc Natl Acad Sci U S A 2011;108:E1120-7.
40. Lin K, Lin J, Wu WI, Ballard J, Lee BB, Gloor SL, et al. An ATP-site on-off switch that restricts phosphatase accessibility of Akt. Sci Signal 2012;5:ra37.
41. George S, Rochford JJ, Wolfrum C, Gray SL, Schinner S, Wilson JC, et al. A family with severe insulin resistance and diabetes due to a mutation in AKT2. Science 2004;304:1325-8. (Pubitemid 38697429)
42. Tan MH, Mester JL, Ngeow J, Rybicki LA, Orloff MS, Eng C. Lifetime cancer risks in individuals with germline PTEN mutations. Clin Cancer Res 2012;18:400-7.
43. Figlin RA, de Souza P, McDermott D, Dutcher JP, Berkenblit A, Thiele A, et al. Analysis of PTEN and HIF-1alpha and correlation with efficacy in patients with advanced renal cell carcinoma treated with temsirolimus versus interferon-alpha. Cancer 2009;115:3651-60.
44. Hara S, Oya M, Mizuno R, Horiguchi A, Marumo K, Murai M. Akt activation in renal cell carcinoma: contribution of a decreased PTEN expression and the induction of apoptosis by an Akt inhibitor. Ann Oncol 2005;16:928-33. (Pubitemid 40903919)
45. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-5. (Pubitemid 29246458)
46. Yang H, Minamishima YA, Yan Q, Schlisio S, Ebert BL, Zhang X, et al. pVHL acts as an adaptor to promote the inhibitory phosphorylation of the NF-kappaB agonist Card9 by CK2. Mol Cell 2007;28:15-27. (Pubitemid 47531976)
47. Hergovich A, Lisztwan J, Barry R, Ballschmieter P, Krek W. Regulation of microtubule stability by the von Hippel-Lindau tumour suppressor protein pVHL. Nat Cell Biol 2003;5:64-70. (Pubitemid 36054331)
48. Hsu T, Adereth Y, Kose N, Dammai V. Endocytic function of von Hippel-Lindau tumor suppressor protein regulates surface localization of fibroblast growth factor receptor 1 and cell motility. J Biol Chem 2006;281:12069-80. (Pubitemid 43855471)
49. Ohh M, Yauch RL, Lonergan KM, Whaley JM, Stemmer-Rachamimov AO, Louis DN, et al. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol Cell 1998;1:959-68. (Pubitemid 128379257)
50. Kirber MT, Chen K, Keaney JF Jr. YFP photoconversion revisited: confirmation of the CFP-like species. Nat Methods 2007;4:767-8. (Pubitemid 350055566)