TCTP increases stability of hypoxia-inducible factor 1α by interaction with and degradation of the tumour suppressor VHL

Biology of the Cell

Volumn 105, Issue 5, 2013, Pages 208-218

  Chen, Ke ^a   Chen, Shuliang ^a   Huang, Chunhua ^a   Cheng, Hanhua ^a   Zhou, Rongjia ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Oncogene; Protein stability; Transcriptional activity; Tumour suppressor

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; SEPHAROSE; TRANSLATIONALLY CONTROLLED TUMOR PROTEIN; TUMOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN;

ARTICLE; CARCINOGENESIS; CELL LYSATE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSCRIPTION INITIATION; UBIQUITINATION;

ANIMALS; BINDING, COMPETITIVE; CERCOPITHECUS AETHIOPS; COS CELLS; GENE EXPRESSION; HEK293 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN STABILITY; PROTEOLYSIS; TRANSCRIPTIONAL ACTIVATION; TUMOR MARKERS, BIOLOGICAL; UBIQUITINATION; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84877609869     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1111/boc.201200080     Document Type: Article

References (49)

1. Amson, R., Pece, S., Lespagnol, A., Vyas, R., Mazzarol, G., Tosoni, D., Colaluca, I., Viale, G., Rodrigues-Ferreira, S., Wynendaele, J., Chaloin, O., Hoebeke, J., Marine, J.C., Di Fiore, P.P. and Telerman, A. (2012) Reciprocal repression between P53 and TCTP. Nat. Med. 18, 91-99
2. Amzallag, N., Passer, B.J., Allanic, D., Segura, E., Thery, C., Goud, B., Amson, R. and Telerman, A. (2004) TSAP6 facilitates the secretion of translationally controlled tumor protein/histamine-releasing factor via a nonclassical pathway. J. Biol. Chem. 279, 46104-46112
3. Bazile, F., Pascal, A., Arnal, I., Le Clainche, C., Chesnel, F. and Kubiak, J.Z. (2009) Complex relationship between TCTP, microtubules and actin microfilaments regulates cell shape in normal and cancer cells. Carcinogenesis 30, 555-565
4. Bommer, U.A. and Thiele, B.J. (2004) The translationally controlled tumour protein (TCTP). Int. J. Biochem. Cell. Biol. 36, 379-385
5. Burgess, A., Labbe, J.C., Vigneron, S., Bonneaud, N., Strub, J.M., Van Dorsselaer, A., Lorca, T. and Castro, A. (2008) Chfr interacts and colocalizes with TCTP to the mitotic spindle. Oncogene 27, 5554-5566
6. Cai, Q. and Robertson, E.S. (2010) Ubiquitin/SUMO modification regulates VHL protein stability and nucleocytoplasmic localization. PloS ONE 5, e12636
7. Cai, Q.L., Knight, J.S., Verma, S.C., Zald, P. and Robertson, E.S. (2006) EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors. PLoS Path 2, e116
8. Cans, C., Passer, B.J., Shalak, V., Nancy-Portebois, V., Crible, V., Amzallag, N., Allanic, D., Tufino, R., Argentini, M., Moras, D., Fiucci, G., Goud, B., Mirande, M., Amson, R. and Telerman, A. (2003) Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc. Natl. Acad. Sci. U.S.A. 100, 13892-13897
9. Chan, T.H., Chen, L., Liu, M., Hu, L., Zheng, B.J., Poon, V.K., Huang, P., Yuan, Y.F., Huang, J.D., Yang, J., Tsao, G.S. and Guan, X.Y. (2012) Translationally controlled tumor protein induces mitotic defects and chromosome missegregation in hepatocellular carcinoma development. Hepatology 55, 491-505
10. Chen, S.H., Wu, P.S., Chou, C.H., Yan, Y.T., Liu, H., Weng, S.Y. and Yang-Yen, H.F. (2007) A knockout mouse approach reveals that TCTP functions as an essential factor for cell proliferation and survival in a tissue- or cell type-specific manner. Mol. Biol. Cell. 18, 2525-2532
11. de Bie, P. and Ciechanover, A. (2011) Ubiquitination of E3 ligases: self-regulation of the ubiquitin system via proteolytic and non-proteolytic mechanisms. Cell. Death Differ. 18, 1393-1402
12. Dong, X., Yang, B., Li, Y., Zhong, C. and Ding, J. (2009) Molecular basis of the acceleration of the GDP-GTP exchange of human ras homolog enriched in brain by human translationally controlled tumor protein. J. Biol. Chem. 284, 23754-23764
13. Ewing, R.M., Chu, P., Elisma, F., Li, H., Taylor, P., Climie, S., McBroom-Cerajewski, L., Robinson, M.D., O'Connor, L., Li, M., Taylor, R., Dharsee, M., Ho, Y., Heilbut, A., Moore, L., Zhang, S., Ornatsky, O., Bukhman, Y.V., Ethier, M., Sheng, Y., Vasilescu, J., Abu-Farha, M., Lambert, J.P., Duewel, H.S., Stewart, II, Kuehl, B., Hogue, K., Colwill, K., Gladwish, K., Muskat, B., Kinach, R., Adams, S.L., Moran, M.F., Morin, G.B., Topaloglou, T. and Figeys, D. (2007) Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol. Systems Biol. 3, 89
14. Franovic, A., Gunaratnam, L., Smith, K., Robert, I., Patten, D. and Lee, S. (2007) Translational up-regulation of the EGFR by tumor hypoxia provides a nonmutational explanation for its overexpression in human cancer. Proc. Natl. Acad. Sci. U.S.A. 104, 13092-13097
15. Funston, G., Goh, W., Wei, S.J., Tng, Q.S., Brown, C., Jiah Tong, L., Verma, C., Lane, D. and Ghadessy, F. (2012) Binding of translationally controlled tumour protein to the N-terminal domain of HDM2 is inhibited by nutlin-3. PLoS One 7, e42642
16. Gachet, Y., Tournier, S., Lee, M., Lazaris-Karatzas, A., Poulton, T. and Bommer, U.A. (1999) The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J. Cell. Sci. 112 (Pt 8), 1257-1271
17. Gamper, A.M., Qiao, X., Kim, J., Zhang, L., DeSimone, M.C., Rathmell, W.K. and Wan, Y. (2012) Regulation of KLF4 turnover reveals an unexpected tissue-specific role of pVHL in tumorigenesis. Mol. Cell. 45, 233-243
18. Hinojosa-Moya, J., Xoconostle-Cazares, B., Piedra-Ibarra, E., Mendez-Tenorio, A., Lucas, W.J. and Ruiz-Medrano, R. (2008) Phylogenetic and structural analysis of translationally controlled tumor proteins. J. Mol. Evol. 66, 472-483
19. Hsu, Y.C., Chern, J.J., Cai, Y., Liu, M. and Choi, K.W. (2007) Drosophila TCTP is essential for growth and proliferation through regulation of dRheb GTPase. Nature 445, 785-788
20. Kaelin, W.G., Jr. (2008) The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat. Rev. Cancer 8, 865-873
21. Kim, J.W., Tchernyshyov, I., Semenza, G.L. and Dang, C.V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell. Metab. 3, 177-185
22. Koziol, M.J., Garrett, N. and Gurdon, J.B. (2007) Tpt1 activates transcription of oct4 and nanog in transplanted somatic nuclei. Curr. Biol. 17, 801-807
23. Kuznetsova, A.V., Meller, J., Schnell, P.O., Nash, J.A., Ignacak, M.L., Sanchez, Y., Conaway, J.W., Conaway, R.C. and Czyzyk-Krzeska, M.F. (2003) von Hippel-Lindau protein binds hyperphosphorylated large subunit of RNA polymerase II through a proline hydroxylation motif and targets it for ubiquitination. Proc. Natl. Acad. Sci. U.S.A. 100, 2706-2711
24. Lee, J.H., Rho, S.B., Park, S.Y. and Chun, T. (2008) Interaction between fortilin and transforming growth factor-beta stimulated clone-22 (TSC-22) prevents apoptosis via the destabilization of TSC-22. FEBS Lett. 582, 1210-1218
25. Li, Z., Na, X., Wang, D., Schoen, S.R., Messing, E.M. and Wu, G. (2002a) Ubiquitination of a novel deubiquitinating enzyme requires direct binding to von Hippel-Lindau tumor suppressor protein. J. Biol. Chem. 277, 4656-4662
26. Li, Z., Wang, D., Na, X., Schoen, S.R., Messing, E.M. and Wu, G. (2002b) Identification of a deubiquitinating enzyme subfamily as substrates of the von Hippel-Lindau tumor suppressor. Biochem. Biophys. Res. Commun. 294, 700-709
27. Liu, H., Peng, H.W., Cheng, Y.S., Yuan, H.S. and Yang-Yen, H.F. (2005) Stabilization and enhancement of the antiapoptotic activity of mcl-1 by TCTP. Mol. Cell. Biol. 25, 3117-3126
28. MacDonald, S.M., Rafnar, T., Langdon, J. and Lichtenstein, L.M. (1995) Molecular identification of an IgE-dependent histamine-releasing factor. Science 269, 688-690
29. Maxwell, P.H., Wiesener, M.S., Chang, G.W., Clifford, S.C., Vaux, E.C., Cockman, M.E., Wykoff, C.C., Pugh, C.W., Maher, E.R. and Ratcliffe, P.J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275
30. Mukhopadhyay, D., Knebelmann, B., Cohen, H.T., Ananth, S. and Sukhatme, V.P. (1997) The von Hippel-Lindau tumor suppressor gene product interacts with Sp1 to repress vascular endothelial growth factor promoter activity. Mol. Cell. Biol. 17, 5629-5639
31. Na, X., Duan, H.O., Messing, E.M., Schoen, S.R., Ryan, C.K., di Sant'Agnese, P.A., Golemis, E.A. and Wu, G. (2003) Identification of the RNA polymerase II subunit hsRPB7 as a novel target of the von Hippel-Lindau protein. EMBO J. 22, 4249-4259
32. Ohh, M., Park, C.W., Ivan, M., Hoffman, M.A., Kim, T.Y., Huang, L.E., Pavletich, N., Chau, V. and Kaelin, W.G. (2000) Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat. Cell. Biol. 2, 423-427
33. Ohh, M., Yauch, R.L., Lonergan, K.M., Whaley, J.M., Stemmer-Rachamimov, A.O., Louis, D.N., Gavin, B.J., Kley, N., Kaelin, W.G., Jr. and Iliopoulos, O. (1998) The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol. Cell. 1, 959-968
34. Rho, S.B., Lee, J.H., Park, M.S., Byun, H.J., Kang, S., Seo, S.S., Kim, J.Y. and Park, S.Y. (2011) Anti-apoptotic protein TCTP controls the stability of the tumor suppressor p53. FEBS Lett. 585, 29-35
35. Roe, J.S., Kim, H., Lee, S.M., Kim, S.T., Cho, E.J. and Youn, H.D. (2006) p53 stabilization and transactivation by a von Hippel-Lindau protein. Mol. Cell. 22, 395-405
36. Semenza, G.L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
37. Semenza, G.L. (2012) Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharm. Sci. 33, 207-214
38. Sendoel, A., Kohler, I., Fellmann, C., Lowe, S.W. and Hengartner, M.O. (2010) HIF-1 antagonizes p53-mediated apoptosis through a secreted neuronal tyrosinase. Nature 465, 577-583
39. Susini, L., Besse, S., Duflaut, D., Lespagnol, A., Beekman, C., Fiucci, G., Atkinson, A.R., Busso, D., Poussin, P., Marine, J.C., Martinou, J.C., Cavarelli, J., Moras, D., Amson, R. and Telerman, A. (2008) TCTP protects from apoptotic cell death by antagonizing bax function. Cell. Death Differ. 15, 1211-1220
40. Tang, N., Mack, F., Haase, V.H., Simon, M.C. and Johnson, R.S. (2006) pVHL function is essential for endothelial extracellular matrix deposition. Mol. Cell. Biol. 26, 2519-2530
41. Tang, N., Wang, L., Esko, J., Giordano, F.J., Huang, Y., Gerber, H.P., Ferrara, N. and Johnson, R.S. (2004) Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell. 6, 485-495
42. Telerman, A. and Amson, R. (2009) The molecular programme of tumour reversion: the steps beyond malignant transformation. Nat. Rev. Cancer 9, 206-216
43. Thoma, C.R., Frew, I.J., Hoerner, C.R., Montani, M., Moch, H. and Krek, W. (2007) pVHL and GSK3beta are components of a primary cilium-maintenance signalling network. Nat. Cell. Biol. 9, 588-595
44. Tsarova, K., Yarmola, E.G. and Bubb, M.R. (2010) Identification of a cofilin-like actin-binding site on translationally controlled tumor protein (TCTP). FEBS Lett. 584, 4756-4760
45. Tuynder, M., Fiucci, G., Prieur, S., Lespagnol, A., Geant, A., Beaucourt, S., Duflaut, D., Besse, S., Susini, L., Cavarelli, J., Moras, D., Amson, R. and Telerman, A. (2004) Translationally controlled tumor protein is a target of tumor reversion. Proc. Natl. Acad. Sci. U.S.A. 101, 15364-15369
46. Tuynder, M., Susini, L., Prieur, S., Besse, S., Fiucci, G., Amson, R. and Telerman, A. (2002) Biological models and genes of tumor reversion: cellular reprogramming through tpt1/TCTP and SIAH-1. Proc. Natl. Acad. Sci. U.S.A. 99, 14976-14981
47. Xiong, H., Wang, D., Chen, L., Choo, Y.S., Ma, H., Tang, C., Xia, K., Jiang, W., Ronai, Z., Zhuang, X. and Zhang, Z. (2009) Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation. J. Clin. Invest. 119, 650-660
48. Yang, Y., Yang, F., Xiong, Z., Yan, Y., Wang, X., Nishino, M., Mirkovic, D., Nguyen, J., Wang, H. and Yang, X.F. (2005) An N-terminal region of translationally controlled tumor protein is required for its antiapoptotic activity. Oncogene 24, 4778-4788
49. Yoon, T., Kim, M. and Lee, K. (2006) Inhibition of Na, K-ATPase-suppressive activity of translationally controlled tumor protein by sorting nexin 6. FEBS Lett. 580, 3558-3564