RACK1 Competes with HSP90 for Binding to HIF-1α and Is Required for O2-Independent and HSP90 Inhibitor-Induced Degradation of HIF-1α

Molecular Cell

Volumn 25, Issue 2, 2007, Pages 207-217

  Liu, Ye V ^a   Baek, Jin H ^a   Zhang, Huafeng ^a   Diez, Roberto ^a   Cole, Robert N ^a   Semenza, Gregg L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

PROTEINS

Indexed keywords

17 ALLYLAMINOGELDANAMYCIN; ELONGIN C; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; RECEPTOR; RECEPTOR OF ACTIVATED PROTEIN KINASE C; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; UBIQUITINATION;

AMINO ACID SEQUENCE; BENZOQUINONES; BINDING, COMPETITIVE; CELL LINE; GTP-BINDING PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LACTAMS, MACROCYCLIC; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; OXYGEN; PROTEIN BINDING; PROTEOMICS; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 33846254999     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.01.001     Document Type: Article

References (49)

1. Baek J.H., Mahon P.C., Oh J., Kelly B., Krishnamachary B., Pearson M., Chan D.A., Giaccia A.J., and Semenza G.L. OS-9 interacts with hypoxia-inducible factor 1α and prolyl hydroxylases to promote oxygen-dependent degradation of HIF-1α. Mol. Cell 17 (2005) 503-512
2. Berra E., Benizri E., Ginouves A., Volmat V., Roux D., and Pouyssegur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1α in normoxia. EMBO J. 22 (2003) 4082-4090
3. Bruick R.K., and McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294 (2001) 1337-1340
4. Ceci M., Gaviraghi C., Gorrini C., Sala L.A., Offenhauser N., Marchisio P.C., and Biffo S. Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426 (2003) 579-584
5. Elvidge G.P., Glenny L., Appelhoff R.J., Ratcliffe P.J., Ragoussis J., and Gleadle J.M. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1α, HIF-2α, and other pathways. J. Biol. Chem. 281 (2006) 15215-15226
6. Epstein A.C., Gleadle J.M., McNeill L.A., Hewitson K.S., O'Rourke J., Mole D.R., Mukherji M., Metzen E., Wilson M.I., Dhanda A., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107 (2001) 43-54
7. Fomenkov A., Zangen R., Huang Y.P., Osada M., Guo Z., Fomenkov T., Trink B., Sidransky D., and Ratovitski E.A. RACK1 and stratifin target ΔNp63α for proteasome degradation in head and neck squamous cell carcinoma cells upon DNA damage. Cell Cycle 3 (2004) 1285-1295
8. Gharahdaghi F., Weinberg C.R., Meagher D.A., Imai B.S., and Mische S.M. Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20 (1999) 601-605
9. Gradin K., McGuire J., Wenger R.H., Kvietkova I., Whitelaw M.L., Toftgard R., Tora L., Gassmann M., and Poellinger L. Functional interference between hypoxia and dioxin signal transduction pathways: competition for recruitment of the Arnt transcription factor. Mol. Cell. Biol. 16 (1996) 5221-5231
10. Hu C.J., Wang L.Y., Chodosh L.A., Keith B., and Simon M.C. Differential roles of hypoxia-inducible factor 1α (HIF-1α) and HIF-2α in hypoxic gene regulation. Mol. Cell. Biol. 23 (2003) 9361-9374
11. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 95 (1998) 7987-7992
12. Isaacs J.S., Jung Y.J., Mimnaugh E.G., Martinez A., Cuttitta F., and Neckers L.M. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J. Biol. Chem. 277 (2002) 29936-29944
13. Isaacs J.S., Jung Y.J., and Neckers L. Aryl hydrocarbon nuclear translocator (ARNT) promotes oxygen-independent stabilization of hypoxia-inducible factor-1α by modulating an Hsp90-dependent regulatory pathway. J. Biol. Chem. 279 (2004) 16128-16135
14. 2 sensing. Science 292 (2001) 464-468
15. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12 (1998) 149-162
16. 2-regulated prolyl hydroxylation. Science 292 (2001) 468-472
17. Jiang B.H., Rue E., Wang G.L., Roe R., and Semenza G.L. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem. 271 (1996) 17771-17778
18. 2 tension. Am. J. Physiol. 271 (1996) C1172-C1180
19. Kamal A., Thao L., Sensintaffar J., Zhang L., Boehm M.F., Fritz L.C., and Burrows F.J. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425 (2003) 407-410
20. Kamura T., Sato S., Iwai K., Czyzyk-Krzeska M., Conaway R.C., and Conaway J.W. Activation of HIF-1α ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc. Natl. Acad. Sci. USA 97 (2000) 10430-10435
21. Lando D., Peet D.J., Gorman J.J., Whelan D.A., Whitelaw M.L., and Bruick R.K. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16 (2002) 1466-1471
22. Lopez-Bergami P., Habelhah H., Bhoumik A., Zhang W., Wang L.H., and Ronai Z. RACK1 mediates activation of JNK by protein kinase C. Mol. Cell 19 (2005) 309-320
23. Mabjeesh N.J., Post D.E., Willard M.T., Kaur B., Van Meir E.G., Simons J.W., and Zhong H. Geldanamycin induces degradation of hypoxia-inducible factor 1α protein via the proteosome pathway in prostate cancer cells. Cancer Res. 62 (2002) 2478-2482
24. Mahon P.C., Hirota K., and Semenza G.L. FIH-1: a novel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15 (2001) 2675-2686
25. Manalo D.J., Rowan A., Lavoie T., Natarajan L., Kelly B.D., Ye S.Q., Garcia J.G., and Semenza G.L. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105 (2005) 659-669
26. 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. The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399 (1999) 271-275
27. McCahill A., Warwicker J., Bolger G.B., Houslay M.D., and Yarwood S.J. The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol. Pharmacol. 62 (2002) 1261-1273
28. Melillo G. HIF-1: a target for cancer, ischemia and inflammation-too good to be true?. Cell Cycle 3 (2004) 154-155
29. Min J.H., Yang H., Ivan M., Gertler F., Kaelin Jr. W.G., and Pavletich N.P. Structure of a HIF-1α-pVHL complex: hydroxyproline recognition in signaling. Science 296 (2002) 1886-1889
30. Moeller B.J., and Dewhirst M.W. HIF-1 and tumor radiosensitivity. Br. J. Cancer 95 (2006) 1-5
31. Neckers L., and Ivy S.P. Heat shock protein 90. Curr. Opin. Oncol. 15 (2003) 419-424
32. Ping P., Zhang J., Pierce Jr. W.M., and Bolli R. Functional proteomic analysis of protein kinase C ε signaling complexes in the normal heart and during cardioprotection. Circ. Res. 88 (2001) 59-62
33. Ran R., Xu H., Lu A., Bernaudin M., and Sharp F.R. Hypoxia preconditioning in the brain. Dev. Neurosci. 27 (2005) 87-92
34. Ron D., Chen C.H., Caldwell J., Jamieson L., Orr E., and Mochly-Rosen D. Cloning of an intracellular receptor for protein kinase C: a homolog of the β subunit of G proteins. Proc. Natl. Acad. Sci. USA 91 (1994) 839-843
35. Ryan H.E., Lo J., and Johnson R.S. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J. 17 (1998) 3005-3015
36. Salceda S., and Caro J. Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272 (1997) 22642-22647
37. Semenza G.L., Jiang B.H., Leung S.W., Passantino R., Concordet J.-P., Maire P., and Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J. Biol. Chem. 271 (1996) 32529-32537
38. Sharp S., and Workman P. Inhibitors of the HSP90 molecular chaperone: current status. Adv. Cancer Res. 95 (2006) 323-348
39. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858
40. Solit D.B., and Rosen N. Hsp90: a novel target for cancer therapy. Curr. Top. Med. Chem. 6 (2006) 1205-1214
41. Stebbins C.E., Kaelin Jr. W.G., and Pavletich N.P. Structure of the VHL-ElonginC-ElonginB complex: implications for VHL tumor suppressor function. Science 284 (1999) 455-461
42. Steele M.R., McCahill A., Thompson D.S., MacKenzie C., Isaacs N.W., Houslay M.D., and Bolger G.B. Identification of a surface on the β-propeller protein RACK1 that interacts with the cAMP-specific phosphodiesterase PDE4D5. Cell. Signal. 13 (2001) 507-513
43. Stroka D.M., Burkhardt T., Desbaillets I., Wenger R.H., Neil D.A., Bauer C., Gassmann M., and Candinas D. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J. 15 (2001) 2445-2453
44. Tanimoto K., Makino Y., Pereira T., and Poellinger L. Mechanism of regulation of the hypoxia-inducible factor-1α by the von Hippel-Lindau tumor suppressor protein. EMBO J. 19 (2000) 4298-4309
45. Thornton C., Tang K.C., Phamluong K., Luong K., Vagts A., Nikanjam D., Yaka R., and Ron D. Spatial and temporal regulation of RACK1 function and N-methyl-D-aspartate receptor activity through WD40 motif-mediated dimerization. J. Biol. Chem. 279 (2004) 31357-31364
46. 2 tension. Proc. Natl. Acad. Sci. USA 92 (1995) 5510-5514
47. Whitesell L., and Lindquist S.L. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5 (2005) 761-772
48. Wilkinson S.E., Parker P.J., and Nixon J.S. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem. J. 294 (1993) 335-337
49. Yu F., White S.B., Zhao Q., and Lee F.S. HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. USA 98 (2001) 9630-9635