The von Hippel-Lindau tumor suppressor regulates programmed cell death 5-mediated degradation of Mdm2

Oncogene

Volumn 34, Issue 6, 2015, Pages 771-779

  Essers, P B ^a   Klasson, T D ^a   Pereboom, T C ^a   Mans, D A ^b,c   Nicastro, M ^a   Boldt, K ^d   Giles, R H ^a   Macinnes, A W ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

programmed cell death 5; renal cell carcinoma; von Hippel Lindau tumor suppressor

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; MDM2 PROTEIN, HUMAN; PDCD5 PROTEIN, HUMAN; PROTEIN MDM2; PROTEIN P53; SURVIVIN 1 PROTEIN, ZEBRAFISH; TP53 PROTEIN, HUMAN; TUMOR PROTEIN; UBIQUITIN PROTEIN LIGASE; VHL PROTEIN, HUMAN; VON HIPPEL LINDAU PROTEIN; ZEBRAFISH PROTEIN;

ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL NUCLEUS; DNA DAMAGE; GENETICS; HUMAN; KIDNEY CARCINOMA; METABOLISM; PATHOLOGY; PROTEIN DEGRADATION; ZEBRA FISH;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CARCINOMA, RENAL CELL; CELL NUCLEUS; DNA DAMAGE; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; NEOPLASM PROTEINS; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84927170688     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.598     Document Type: Article

References (59)

1. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012; 366: 883-892.
2. Sato Y, Yoshizato T, Shiraishi Y, Maekawa S, Okuno Y, Kamura T et al. Integrated molecular analysis of clear-cell renal cell carcinoma. Nat Genet 2013; 45: 860-867.
3. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 2013; 499: 43-49.
4. Cohen HT, McGovern FJ. Renal-cell carcinoma. N Engl J Med 2005; 353: 2477-2490.
5. Motzer RJ, Bander NH, Nanus DM. Renal-cell carcinoma. N Engl J Med 1996; 335: 865-875.
6. Hsu T. Complex cellular functions of the von Hippel-Lindau tumor suppressor gene: insights from model organisms. Oncogene 2012; 31: 2247-2257.
7. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003; 3: 721-732.
8. Kondo K, Klco J, Nakamura E, Lechpammer M, Kaelin Jr WG. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 2002; 1: 237-246.
9. Mack FA, Rathmell WK, Arsham AM, Gnarra J, Keith B, Simon MC. Loss of pVHL is sufficient to cause HIF dysregulation in primary cells but does not promote tumor growth. Cancer Cell 2003; 3: 75-88.
10. Maranchie JK, Vasselli JR, Riss J, Bonifacino JS, Linehan WM, Klausner RD. The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 2002; 1: 247-255.
11. Horn HF, Vousden KH. Coping with stress: multiple ways to activate p53. Oncogene 2007; 26: 1306-1316.
12. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997; 387: 299-303.
13. Graeber TG, Peterson JF, Tsai M, Monica K, Fornace Jr AJ, Giaccia AJ. Hypoxia induces accumulation of p53 protein, but activation of a G1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol Cell Biol 1994; 14: 6264-6277.
14. Alarcon R, Koumenis C, Geyer RK, Maki CG, Giaccia AJ. Hypoxia induces p53 accumulation through MDM2 down-regulation and inhibition of E6-mediated degradation. Cancer Res 1999; 59: 6046-6051.
15. Sermeus A, Michiels C. Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis 2011; 2: e164.
16. Chen LN, Wang Y, Ma DL, Chen YY. Short interfering RNA against the PDCD5 attenuates cell apoptosis and caspase-3 activity induced by Bax overexpression. Apoptosis 2006; 11: 101-111.
17. Xu L, Chen Y, Song Q, Xu D, Wang Y, Ma D. PDCD5 interacts with Tip60 and functions as a cooperator in acetyltransferase activity and DNA damage-induced apoptosis. Neoplasia 2009; 11: 345-354.
18. Xu L, Hu J, Zhao Y, Hu J, Xiao J, Wang Y et al. PDCD5 interacts with p53 and functions as a positive regulator in the p53 pathway. Apoptosis 2012; 17: 1235-1245.
19. Chen Y, Sun R, Han W, Zhang Y, Song Q, Di C et al. Nuclear translocation of PDCD5 (TFAR19): an early signal for apoptosis?. FEBS Lett 2001; 509: 191-196.
20. Zucchi I, Mento E, Kuznetsov VA, Scotti M, Valsecchi V, Simionati B et al. Gene expression profiles of epithelial cells microscopically isolated from a breastinvasive ductal carcinoma and a nodal metastasis. Proc Natl Acad Sci USA 2004; 101: 18147-18152.
21. Yang YH, Zhao M, Li WM, Lu YY, Chen YY, Kang B et al. Expression of programmed cell death 5 gene involves in regulation of apoptosis in gastric tumor cells. Apoptosis 2006; 11: 993-1001.
22. Spinola M, Meyer P, Kammerer S, Falvella FS, Boettger MB, Hoyal CR et al. Association of the PDCD5 locus with lung cancer risk and prognosis in smokers. J Clin Oncol 2006; 24: 1672-1678.
23. Xiong L, Tan WL, Yu ZC, Wu YD, Huang H, Zhao GZ et al. [Expression of TFAR19(PDCD5) in normal human kidney, renal clear cell carcinoma, normal human bladder and bladder carcinoma]. Nan Fang Yi Ke Da Xue Xue Bao 2006; 26: 805-809.
24. Tan WL, Xiong L, Zheng SB, Yu ZC, Qi H, Du YJ et al. [Relationship between programmed cell death 5 protein expression and prognosis of renal clear cell carcinoma]. Nan Fang Yi Ke Da Xue Xue Bao 2006; 26: 1316-1318.
25. Szymanska K, Moore LE, Rothman N, Chow WH, Waldman F, Jaeger E et al. TP53, EGFR, and KRAS mutations in relation to VHL inactivation and lifestyle risk factors in renal-cell carcinoma from central and eastern Europe. Cancer Lett 2010; 293: 92-98.
26. Albers J, Rajski M, Schonenberger D, Harlander S, Schraml P, von Teichman A et al. Combined mutation of Vhl and Trp53 causes renal cysts and tumours in mice. EMBO Mol Med 2013; 5: 949-964.
27. Roe JS, Kim H, Lee SM, Kim ST, Cho EJ, Youn HD. p53 stabilization and transactivation by a von Hippel-Lindau protein. Mol Cell 2006; 22: 395-405.
28. Lane DP. Exploiting the p53 pathway for the diagnosis and therapy of human cancer. Cold Spring Harb Symp Quant Biol 2005; 70: 489-497.
29. Dong Z, Nishiyama J, Yi X, Venkatachalam MA, Denton M, Gu S et al. Gene promoter of apoptosis inhibitory protein IAP2: identification of enhancer elements and activation by severe hypoxia. Biochem J 2002; 364: 413-421.
30. Dong Z, Wang JZ, Yu F, Venkatachalam MA. Apoptosis-resistance of hypoxic cells: multiple factors involved and a role for IAP-2. Am J Pathol 2003; 163: 663-671.
31. Qi H, Ohh M. The von Hippel-Lindau tumor suppressor protein sensitizes renal cell carcinoma cells to tumor necrosis factor-induced cytotoxicity by suppressing the nuclear factor-kappaB-dependent antiapoptotic pathway. Cancer Res 2003; 63: 7076-7080.
32. MacInnes AW, Amsterdam A, Whittaker CA, Hopkins N, Lees JA. Loss of p53 synthesis in zebrafish tumors with ribosomal protein gene mutations. Proc Natl Acad Sci USA 2008; 105: 10408-10413.
33. Esteban MA, Tran MG, Harten SK, Hill P, Castellanos MC, Chandra A et al. Regulation of E-cadherin expression by VHL and hypoxia-inducible factor. Cancer Res 2006; 66: 3567-3575.
34. Kibel A, Iliopoulos O, DeCaprio JA, Kaelin Jr WG. Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C. Science 1995; 269: 1444-1446.
35. Pause A, Lee S, Worrell RA, Chen DY, Burgess WH, Linehan WM et al. The von Hippel-Lindau tumor-suppressor gene product forms a stable complex with human CUL-2, a member of the Cdc53 family of proteins. Proc Natl Acad Sci USA 1997; 94: 2156-2161.
36. Kamura T, Koepp DM, Conrad MN, Skowyra D, Moreland RJ, Iliopoulos O et al. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 1999; 284: 657-661.
37. Tsuchiya H, Iseda T, Hino O. Identification of a novel protein (VBP-1) binding to the von Hippel-Lindau (VHL) tumor suppressor gene product. Cancer Res 1996; 56: 2881-2885.
38. Lai Y, Song M, Hakala K, Weintraub ST, Shiio Y. Proteomic dissection of the von Hippel-Lindau (VHL) interactome. J Proteome Res 2011; 10: 5175-5182.
39. Xu L, Hu J, Zhao Y, Xiao J, Wang Y, Ma D et al. PDCD5 interacts with p53 and functions as a positive regulator in the p53 pathway. Apoptosis 2012; 17: 1235-1245.
40. Sansam CL, Cruz NM, Danielian PS, Amsterdam A, Lau ML, Hopkins N et al. A vertebrate gene, ticrr, is an essential checkpoint and replication regulator. Genes Dev 2010; 24: 183-194.
41. Cui D, Li L, Lou H, Sun H, Ngai S-M, Shao G et al. The ribosomal protein S26 regulates p53 activity in response to DNA damage. Oncogene 2014; 33: 2225-2235.
42. Haase VH, Glickman JN, Socolovsky M, Jaenisch R. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci USA 2001; 98: 1583-1588.
43. Kleymenova E, Everitt JI, Pluta L, Portis M, Gnarra JR, Walker CL. Susceptibility to vascular neoplasms but no increased susceptibility to renal carcinogenesis in Vhl knockout mice. Carcinogenesis 2004; 25: 309-315.
44. Rankin EB, Tomaszewski JE, Haase VH. Renal cyst development in mice with conditional inactivation of the von Hippel-Lindau tumor suppressor. Cancer Res 2006; 66: 2576-2583.
45. Fu L, Wang G, Shevchuk MM, Nanus DM, Gudas LJ. Generation of a mouse model of Von Hippel-Lindau kidney disease leading to renal cancers by expression of a constitutively active mutant of HIF1alpha. Cancer Res 2011; 71: 6848-6856.
46. Albers J, Rajski M, Schonenberger D, Harlander S, Schraml P, von Teichman A et al. Combined mutation of Vhl and Trp53 causes renal cysts and tumours in mice. EMBO Mol Med 2013; 5: 949-964.
47. Roe JS, Kim H, Lee SM, Kim ST, Cho EJ, Youn HD. p53 stabilization and transactivation by a von Hippel-Lindau protein. Mol Cell 2006; 22: 395-405.
48. Mans DA, Vermaat JS, Weijts BG, van Rooijen E, van Reeuwijk J, Boldt K et al. Regulation of E2F1 by the von Hippel-Lindau tumour suppressor protein predicts survival in renal cell cancer patients. J Pathol 2013; 231: 117-129.
49. Roe JS, Kim HR, Hwang IY, Ha NC, Kim ST, Cho EJ et al. Phosphorylation of von Hippel-Lindau protein by checkpoint kinase 2 regulates p53 transactivation. Cell Cycle 2011; 10: 3920-3928.
50. Frew IJ, Krek W. pVHL: a multipurpose adaptor protein. Sci Signal 2008; 1: pe30.
51. Yuen JS, Sim MY, Siml HG, Chong TW, Lau WK, Cheng CW et al. Inhibition of angiogenic and non-angiogenic targets by sorafenib in renal cell carcinoma (RCC) in a RCC xenograft model. Br J Cancer 2011; 104: 941-947.
52. Westerfield M. The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). 4th edn (Univ. of Oregon Press: Eugene, OR, USA, 2000).
53. van Rooijen E, Santhakumar K, Logister I, Voest E, Schulte-Merker S, Giles R et al. A zebrafish model for VHL and hypoxia signaling. Methods Cell Biol 2011; 105: 163-190.
54. Pereboom TC, van Weele LJ, Bondt A, MacInnes AW. A zebrafish model of dyskeratosis congenita reveals hematopoietic stem cell formation failure resulting from ribosomal protein-mediated p53 stabilization. Blood 2011; 118: 5458-5465.
55. Kim EL, Wustenberg R, Rubsam A, Schmitz-Salue C, Warnecke G, Bucker EM et al. Chloroquine activates the p53 pathway and induces apoptosis in human glioma cells. Neuro Oncol 2010; 12: 389-400.
56. Coene KL, Mans DA, Boldt K, Gloeckner CJ, van Reeuwijk J, Bolat E et al. The ciliopathy-associated protein homologs RPGRIP1 and RPGRIP1L are linked to cilium integrity through interaction with Nek4 serine/threonine kinase. Hum Mol Genet 2011; 20: 3592-3605.
57. Boldt K, Mans DA, Won J, van Reeuwijk J, Vogt A, Kinkl N et al. Disruption of intraflagellar protein transport in photoreceptor cilia causes Leber congenital amaurosis in humans and mice. J Clin Invest 2011; 121: 2169-2180.
58. Shepard JL, Stern HM, Pfaff KL, Amatruda JF. Analysis of the cell cycle in zebrafish embryos. Methods Cell Biol 2004; 76: 109-125.
59. van Rooijen E, Voest EE, Logister I, Korving J, Schwerte T, Schulte-Merker S et al. Zebrafish mutants in the von Hippel-Lindau tumor suppressor display a hypoxic response and recapitulate key aspects of Chuvash polycythemia. Blood 2009; 113: 6449-6460.