SCP phosphatases suppress renal cell carcinoma by stabilizing PML and inhibiting mTOR/HIF signaling

Cancer Research

Volumn 74, Issue 23, 2014, Pages 6935-6946

  Lin, Yu Ching ^a,b   Lu, Li Ting ^a,b   Chen, Hsin Yi ^a,c   Duan, Xueyan ^d   Lin, Xia ^d   Feng, Xin Hua ^d   Tang, Ming Jer ^e   Chen, Ruey Hwa ^a,b  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

JUGLONE; MAMMALIAN TARGET OF RAPAMYCIN; ONCOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN PROMYELOCYTIC LEUKEMIA; PROTEIN SCP1; PROTEIN SCP2; PROTEIN SCP3; TEMSIROLIMUS; UNCLASSIFIED DRUG; VASCULOTROPIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CARRIER PROTEIN; MTOR PROTEIN, HUMAN; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; NUCLEAR PROTEIN; PEPTIDYLPROLYL ISOMERASE; PHOSPHATASE; PML PROTEIN, HUMAN; STEROL CARRIER PROTEINS; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER GRADING; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG RESPONSE; FEMALE; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RENAL CELL CARCINOMA CELL LINE; TUMOR GROWTH; UBIQUITINATION; UPREGULATION; CELL LINE; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; KIDNEY TUMOR; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARCINOMA, RENAL CELL; CARRIER PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HELA CELLS; HUMANS; KIDNEY NEOPLASMS; NUCLEAR PROTEINS; PEPTIDYLPROLYL ISOMERASE; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84917708469     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1330     Document Type: Article

References (40)

1. de The H, Chomienne C, Lanotte M, Degos L, Dejean A. The t(15;17) translocation of acute promyelocytic leukaemia fuses the retinoic acid receptor alpha gene to a novel transcribed locus. Nature 1990;347: 558-61.
2. de The H, Lavau C, Marchio A, Chomienne C, Degos L, Dejean A. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 1991;66:675-84.
3. Bernardi R, Guernah I, Jin D, Grisendi S, Alimonti A, Teruya-Feldstein J, et al. PML inhibits HIF-1alpha translation and neoangiogenesis through repression of mTOR. Nature 2006;442:779-85.
4. Bernardi R, Pandolfi PP. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 2007;8: 1006-16.
5. Reineke EL, Liu Y, Kao HY. Promyelocytic leukemia protein controls cell migration in response to hydrogen peroxide and insulin-like growth factor-1. J Biol Chem 2010;285:9485-92.
6. Salomoni P, Ferguson BJ, Wyllie AH, Rich T. New insights into the role of PML in tumour suppression. Cell Res 2008;18:622-40.
7. Bernardi R, Pandol fi PP. Role of PML and the PML-nuclear body in the control of programmed cell death. Oncogene 2003;22:9048-57.
8. Takahashi Y, Lallemand-Breitenbach V, Zhu J, de The H. PML nuclear bodies and apoptosis. Oncogene 2004;23:2819-24.
9. Giorgi C, Ito K, Lin HK, Santangelo C, Wieckowski MR, Lebiedzinska M, et al. PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 2010;330:1247-51.
10. Song MS, Salmena L, Carracedo A, Egia A, Lo-Coco F, Teruya- Feldstein J, et al. The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 2008;455:813-7.
11. Bernardi R, Papa A, Egia A, Coltella N, Teruya-Feldstein J, Signoretti S, et al. Pml represses tumour progression through inhibition of mTOR. EMBO Mol Med 2011;3:249-57.
12. Scaglioni PP, Yung TM, Cai LF, Erdjument-Bromage H, Kaufman AJ, Singh B, et al. A CK2-dependent mechanism for degradation of the PML tumor suppressor. Cell 2006;126:269-83.
13. Trotman LC, Alimonti A, Scaglioni PP, Koutcher JA, Cordon-Cardo C, Pandolfi PP. Identification of a tumour suppressor network opposing nuclear Akt function. Nature 2006;441:523-7.
14. Wang ZG, Delva L, Gaboli M, Rivi R, Giorgio M, Cordon-Cardo C, et al. Role of PML in cell growth and the retinoic acid pathway. Science 1998;279:1547-51.
15. Gurrieri C, Capodieci P, Bernardi R, Scaglioni PP, Nafa K, Rush LJ, et al. Loss of the tumor suppressor PML in human cancers of multiple histologic origins. J Natl Cancer Inst 2004;96:269-79.
16. Chen RH, Lee YR, Yuan WC. The role of PML ubiquitination in human malignancies. J Biomed Sci 2012;19:81.
17. Rabellino A, Carter B, Konstantinidou G, Wu SY, Rimessi A, Byers LA, et al. The SUMOE3-ligase PIAS1 regulates the tumor suppressor PML and its oncogenic counterpart PML-RARA. Cancer Res 2012;72: 2275-84.
18. Wolyniec K, Shortt J, de Stanchina E, Levav-Cohen Y, Alsheich-Bartok O, Louria-Hayon I, et al. E6AP ubiquitin ligase regulates PML-induced senescence in Myc-driven lymphomagenesis. Blood 2012;120: 822-32.
19. Yuan WC, Lee YR, Huang SF, Lin YM, Chen TY, Chung HC, et al. A Cullin3-KLHL20 Ubiquitin ligase-dependent pathway targets PML to potentiate HIF-1 signaling and prostate cancer progression. Cancer Cell 2011;20:214-28.
20. Chambers RS, Dahmus ME. Purification and characterization of a phosphatase from HeLa cells which dephosphorylates the C-terminal domain of RNA polymerase II. J Biol Chem 1994;269:26243-8.
21. Kamenski T, Heilmeier S, Meinhart A, Cramer P. Structure and mechanism of RNA polymerase II CTD phosphatases. Mol Cell 2004;15: 399-407.
22. Meinhart A, Kamenski T, Hoeppner S, Baumli S, Cramer P. A structural perspective of CTD function. Genes Dev 2005;19:1401-15.
23. Yeo M, Lin PS, Dahmus ME, Gill GN. A novel RNA polymerase II C-terminal domain phosphatase that preferentially dephosphorylates serine 5. J Biol Chem 2003;278:26078-85.
24. Yeo M, Lee SK, Lee B, Ruiz EC, Pfaff SL, Gill GN. Small CTD phosphatases function in silencing neuronal gene expression. Science 2005;307:596-600.
25. Thompson J, Lepikhova T, Teixido-Travesa N, Whitehead MA, Palvimo JJ, Janne OA. Small carboxyl-terminal domain phosphatase 2 attenuates androgen-dependent transcription. EMBO J 2006;25:2757-67.
26. Knockaert M, Sapkota G, Alarcon C, Massague J, Brivanlou AH. Unique players in the BMP pathway: small C-terminal domain phosphatases dephosphorylate Smad1 to attenuate BMP signaling. Proc Natl Acad Sci U S A 2006;103:11940-5.
27. Sapkota G, Knockaert M, Alarcon C, Montalvo E, Brivanlou AH, Massague J. Dephosphorylation of the linker regions of Smad1 and Smad2/3 by small C-terminal domain phosphatases has distinct outcomes for bone morphogenetic protein and transforming growth factor-beta pathways. J Biol Chem 2006;281:40412-9.
28. Wrighton KH, Willis D, Long J, Liu F, Lin X, Feng XH. Small C-terminal domain phosphatases dephosphorylate the regulatory linker regions of Smad2 and Smad3 to enhance transforming growth factor-beta signaling. J Biol Chem 2006;281:38365-75.
29. Kashuba VI, Li J, Wang F, Senchenko VN, Protopopov A, Malyukova A, et al. RBSP3 (HYA22) is a tumor suppressor gene implicated in major epithelial malignancies. Proc Natl Acad Sci U S A 2004;101: 4906-11.
30. Cohen HT, McGovern FJ. Renal-cell carcinoma. N Engl J Med 2005;353:2477-90.
31. Rini BI, Campbell SC, Escudier B. Renal cell carcinoma. Lancet 2009;373:1119-32.
32. Gossage L, Eisen T. Alterations in VHL as potential biomarkers in renalcell carcinoma. Nat Rev Clin Oncol 2010;7:277-88.
33. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008;30:393-402.
34. Heng DY, Bukowski RM. Anti-angiogenic targets in the treatment of advanced renal cell carcinoma. Curr Cancer Drug Targets 2008;8: 676-82.
35. Lee YR, Yuan WC, Ho HC, Chen CH, Shih HM, Chen RH. The Cullin 3 substrate adaptor KLHL20 mediates DAPK ubiquitination to control interferon responses. EMBO J 2010;29:1748-61.
36. Wang WJ, Kuo JC, Ku W, Lee YR, Lin FC, Chang YL, et al. The tumor suppressor DAPK is reciprocally regulated by tyrosine kinase Src and phosphatase LAR. Mol Cell 2007;27:701-16.
37. Reineke EL, Lam M, Liu Q, Liu Y, Stanya KJ, Chang KS, et al. Degradation of the tumor suppressor PML by Pin1 contributes to the cancer phenotype of breast cancer MDA-MB-231 cells. Mol Cell Biol 2008;28:997-1006.
38. Carracedo A, Weiss D, Leliaert AK, Bhasin M, de Boer VC, Laurent G, et al. Ametabolic prosurvival role forPMLin breast cancer. J Clin Invest 2012;122:3088-100.
39. Wu Y, Evers BM, Zhou BP. Small C-terminal domain phosphatase enhances snail activity through dephosphorylation. J Biol Chem 2009;284:640-8.
40. Shaw PE. Peptidyl-prolyl cis/trans isomerases and transcription: is there a twist in the tail/EMBO Rep 2007;8:40-5.