pVHL Acts as an Adaptor to Promote the Inhibitory Phosphorylation of the NF-κB Agonist Card9 by CK2

Molecular Cell

Volumn 28, Issue 1, 2007, Pages 15-27

  Yang, Haifeng ^b   Minamishima, Yoji Andrew ^b   Yan, Qin ^a,b   Schlisio, Susanne ^a,b   Ebert, Benjamin L ^b,c   Zhang, Xiaoping ^d   Zhang, Liang ^d   Kim, William Y ^e   Olumi, Aria F ^d   Kaelin Jr , William G ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

CELLCYCLE; SIGNALING

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; CASEIN KINASE II; CASPASE RECRUITMENT DOMAIN 9; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CONTROLLED STUDY; DOWN REGULATION; FAST PROTEIN LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; KIDNEY CARCINOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; TUMOR GROWTH; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CARCINOMA, RENAL CELL; CARD SIGNALING ADAPTOR PROTEINS; CASEIN KINASE II; HELA CELLS; HUMANS; KIDNEY NEOPLASMS; LIVER; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; NEOPLASM TRANSPLANTATION; NF-KAPPA B; PC12 CELLS; PHOSPHORYLATION; RATS; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; TUMOR NECROSIS FACTOR-ALPHA; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 34948883495     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.09.010     Document Type: Article

References (48)

1. An J., and Rettig M.B. Mechanism of von Hippel-Lindau protein-mediated suppression of nuclear factor kappa B activity. Mol. Cell. Biol. 25 (2005) 7546-7556
2. An J., Fisher M., and Rettig M.B. VHL expression in renal cell carcinoma sensitizes to bortezomib (PS-341) through an NF-kappaB-dependent mechanism. Oncogene 24 (2005) 1563-1570
3. Beg A.A., and Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274 (1996) 782-784
4. Bertin J., Guo Y., Wang L., Srinivasula S.M., Jacobson M.D., Poyet J.L., Merriam S., Du M.Q., Dyer M.J., Robison K.E., et al. CARD9 is a novel caspase recruitment domain-containing protein that interacts with BCL10/CLAP and activates NF-kappa B. J. Biol. Chem. 275 (2000) 41082-41086
5. Bishop T., Lau K.W., Epstein A.C., Kim S.K., Jiang M., O'Rourke D., Pugh C.W., Gleadle J.M., Taylor M.S., Hodgkin J., et al. Genetic analysis of pathways regulated by the von hippel-lindau tumor suppressor in Caenorhabditis elegans. PLoS Biol. 2 (2004) e289 10.1371/journal.pbio.0020289
6. Brummelkamp T.R., Nijman S.M., Dirac A.M., and Bernards R. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424 (2003) 797-801
7. Bukowski R.M. Cytokine combinations: therapeutic use in patients with advanced renal cell carcinoma. Semin. Oncol. 27 (2000) 204-212
8. Caldwell M.C., Hough C., Furer S., Linehan W.M., Morin P.J., and Gorospe M. Serial analysis of gene expression in renal carcinoma cells reveals VHL-dependent sensitivity to TNFalpha cytotoxicity. Oncogene 21 (2002) 929-936
9. Calzada M.J., Esteban M.A., Feijoo-Cuaresma M., Castellanos M.C., Naranjo-Suarez S., Temes E., Mendez F., Yanez-Mo M., Ohh M., and Landazuri M.O. von Hippel-Lindau tumor suppressor protein regulates the assembly of intercellular junctions in renal cancer cells through hypoxia-inducible factor-independent mechanisms. Cancer Res. 66 (2006) 1553-1560
10. Clifford S., Cockman M., Smallwood A., Mole D., Woodward E., Maxwell P., Ratcliffe P., and Maher E. Contrasting effects on HIF-1alpha regulation by disease-causing pVHL mutations correlate with patterns of tumourigenesis in von Hippel-Lindau disease. Hum. Mol. Genet. 10 (2001) 1029-1038
11. Colonna M. All roads lead to Card9. Nat. Immunol. 8 (2007) 554-555
12. Czyzyk-Krzeska M.F., and Meller J. von Hippel-Lindau tumor suppressor: not only HIF's executioner. Trends Mol. Med. 10 (2004) 146-149
13. Gnarra J.R., Duan D.R., Weng Y., Humphrey J.S., Chen D.Y.T., Lee S., Pause A., Dudley C.F., Latif F., Kuzmin I., et al. Molecular cloning of the von Hippel-Lindau tumor suppressor gene and its role in renal cell carcinoma. Biochim. Biophys. Acta 1242 (1996) 201-210
14. Golde D.W., and Hocking W.G. Polycythemia: mechanisms and management. Ann. Intern. Med. 95 (1981) 71-87
15. Gordeuk V.R., Sergueeva A.I., Miasnikova G.Y., Okhotin D., Voloshin Y., Choyke P.L., Butman J.A., Jedlickova K., Prchal J.T., and Polyakova L.A. Congenital disorder of oxygen sensing: association of the homozygous Chuvash polycythemia VHL mutation with thrombosis and vascular abnormalities but not tumors. Blood 103 (2004) 3924-3932
16. Gross O., Gewies A., Finger K., Schafer M., Sparwasser T., Peschel C., Forster I., and Ruland J. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 442 (2006) 651-656
17. Haase V., Glickman J., Socolovsky M., and Jaenisch R. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc. Natl. Acad. Sci. USA 98 (2001) 1583-1588
18. Hoffman E.C., Reyes H., Chu F.F., Sander F., Conley L.H., Brooks B.A., and Hankinson O. Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 252 (1991) 954-958
19. Hoffman M., Ohh M., Yang H., Klco J., Ivan M., and Kaelin W.J. von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF. Hum. Mol. Genet. 10 (2001) 1019-1027
20. Hon W.C., Wilson M.I., Harlos K., Claridge T.D., Schofield C.J., Pugh C.W., Maxwell P.H., Ratcliffe P.J., Stuart D.I., and Jones E.Y. Structural basis for the recognition of hydroxyproline in HIF-1alpha by pVHL. Nature 417 (2002) 975-978
21. Iliopoulos O., Kibel A., Gray S., and Kaelin W.G. Tumor suppression by the Human von Hippel-Lindau gene product. Nat. Med. 1 (1995) 822-826
22. Kaelin W.G. Molecular basis of the VHL hereditary cancer syndrome. Nat. Rev. Cancer 2 (2002) 673-682
23. Kaelin Jr. W.G. von Hippel-Lindau disease. Annual Review of Pathology: Mechanisms of Disease 2 (2007) 145-173
24. Karin M., Cao Y., Greten F.R., and Li Z.W. NF-kappaB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer 2 (2002) 301-310
25. Kibel A., Iliopoulos O., DeCaprio J.D., and Kaelin W.G. Binding of the von Hippel-Lindau tumor suppressor protein to elongin B and C. Science 269 (1995) 1444-1446
26. Kim W.Y., and Kaelin W.G. Role of VHL gene mutation in human cancer. J. Clin. Oncol. 22 (2004) 4991-5004
27. Kim W.Y., Safran M., Buckley M.R., Ebert B.L., Glickman J., Bosenberg M., Regan M., and Kaelin Jr. W.G. Failure to prolyl hydroxylate hypoxia-inducible factor alpha phenocopies VHL inactivation in vivo. EMBO J. 25 (2006) 4650-4662
28. Kondo K., Klco J., Nakamura E., Lechpammer M., and Kaelin W.G. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 1 (2002) 237-246
29. Kondo K., Kim W.Y., Lechpammer M., and Kaelin Jr. W.G. Inhibition of HIF2alpha is sufficient to suppress pVHL-defective tumor growth. PLoS Biol. 1 (2003) E83 10.1371/journal.pbio.0000083
30. Lee S., Nakamura E., Yang H., Wei W., Linggi M.S., Sajan M.P., Farese R.V., Freeman R.S., Carter B.D., Kaelin Jr. W.G., et al. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 8 (2005) 155-167
31. Lolkema M.P., Gervais M.L., Snijckers C.M., Hill R.P., Giles R.H., Voest E.E., and Ohh M. Tumor suppression by the von Hippel-Lindau protein requires phosphorylation of the acidic domain. J. Biol. Chem. 280 (2005) 22205-22211
32. Maranchie J.K., Vasselli J.R., Riss J., Bonifacino J.S., Linehan W.M., and Klausner R.D. The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1 (2002) 247-255
33. Maxwell P., Weisner M., Chang G.-W., Clifford S., Vaux E., Pugh C., Maher E., and Ratcliffe P. The von Hippel-Lindau gene product is necessary for oxgyen-dependent proteolysis of hypoxia-inducible factor α subunits. Nature 399 (1999) 271-275
34. Min J.H., Yang H., Ivan M., Gertler F., Kaelin Jr. W.G., and Pavletich N.P. Structure of an HIF-1alpha -pVHL complex: hydroxyproline recognition in signaling. Science 296 (2002) 1886-1889
35. Nakanishi C., and Toi M. Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat. Rev. Cancer 5 (2005) 297-309
36. Oya M., Ohtsubo M., Takayanagi A., Tachibana M., Shimizu N., and Murai M. Constitutive activation of nuclear factor-kappaB prevents TRAIL-induced apoptosis in renal cancer cells. Oncogene 20 (2001) 3888-3896
37. Oya M., Takayanagi A., Horiguchi A., Mizuno R., Ohtsubo M., Marumo K., Shimizu N., and Murai M. Increased nuclear factor-kappa B activation is related to the tumor development of renal cell carcinoma. Carcinogenesis 24 (2003) 377-384
38. Percy M.J., Zhao Q., Flores A., Harrison C., Lappin T.R., Maxwell P.H., McMullin M.F., and Lee F.S. A family with erythrocytosis establishes a role for prolyl hydroxylase domain protein 2 in oxygen homeostasis. Proc. Natl. Acad. Sci. USA 103 (2006) 654-659
39. Plaisance S., Vanden Berghe W., Boone E., Fiers W., and Haegeman G. Recombination signal sequence binding protein Jkappa is constitutively bound to the NF-kappaB site of the interleukin-6 promoter and acts as a negative regulatory factor. Mol. Cell. Biol. 17 (1997) 3733-3743
40. Qi H., and 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. 63 (2003) 7076-7080
41. Raval R.R., Lau K.W., Tran M.G., Sowter H.M., Mandriota S.J., Li J.L., Pugh C.W., Maxwell P.H., Harris A.L., and Ratcliffe P.J. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol. Cell. Biol. 25 (2005) 5675-5686
42. Schofield C.J., and Ratcliffe P.J. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5 (2004) 343-354
43. Steiner T., Junker U., Henzgen B., Nuske K., Durum S.K., and Schubert J. Interferon-alpha suppresses the antiapoptotic effect of NF-kB and sensitizes renal cell carcinoma cells in vitro to chemotherapeutic drugs. Eur. Urol. 39 (2001) 478-483
44. Van Antwerp D.J., Martin S.J., Kafri T., Green D.R., and Verma I.M. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274 (1996) 787-789
45. Vooijs M., Jonkers J., and Berns A. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2 (2001) 292-297
46. Wang C.Y., Mayo M.W., and Baldwin Jr. A.S. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274 (1996) 784-787
47. Yang H., Ivan M., Min J., Kim W., and Kaelin W. Analysis of von Hippel-Lindau hereditary cancer syndrome: implications of oxygen sensing. Methods Enzymol. 381 (2004) 320-335
48. Zimmer M., Doucette D., Siddiqui N., and Iliopoulos O. Inhibition of hypoxia-inducible factor is sufficient for growth suppression of VHL-/- tumors. Mol. Cancer Res. 2 (2004) 89-95