The von Hippel-Lindau tumor suppressor complex and regulation of hypoxia-inducible transcription

Advances in Cancer Research

Volumn 85, Issue , 2002, Pages 1-12

  Conaway, Ronald C ^a,b   Conaway, Joan W ^a,b,c  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ELONGIN B; ELONGIN C; GENE PRODUCT; GLUCOSE TRANSPORTER 1; HELIX LOOP HELIX PROTEIN; LIGASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN CUL2; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; UBIQUITIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN;

AMINO ACID SEQUENCE; BRAIN HYPOXIA; CHROMOSOME 3P; COMPLEX FORMATION; DNA RESPONSIVE ELEMENT; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; VON HIPPEL LINDAU DISEASE;

EID: 0036383262     PISSN: 0065230X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-230X(02)85001-1     Document Type: Review

References (64)

1. Aravind, L., and Koonin, E. V. (2001). The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2.
2. Aso, T., Haque, D., Barstead, R. J., Conaway, R. C., and Conaway, J. W. (1996). The inducible elongin A elongation activation domain: Structure, function, and interaction with the elongin BC complex. EMBO J. 15, 5557.
3. Aso, T., Lane, W. S., Conaway, J. W., and Conaway, R. C. (1995). Elongin (SIII): A multisubunit regulator of elongation by RNA polymerase II. Science 269, 1439.
4. Bai, C., Sen, P., Hofmann, K., Ma, L., Goebl, M., Harper, J. W., and Elledge, S. J. (1996). SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86, 263.
5. Blondel, M., Galan, J. M., and Peter, M. (2000). Isolation and characterization of HRT1 using a genetic screen for mutants unable to degrade Gic2p in Saccaromyces cerevisiae. Genetics 155, 1033.
6. Bruick, R. K., and McKnight, S. L. (2001). A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337.
7. Burnatowska-Hledin, M., Spielman, W. S., Smith, W. L., Meyer, J. M., and Dewitt, D. L. (1995). Expression cloning of an AVP-activated, calcium-mobilizing receptor from rabbit kidney medulla. Am. J. Physiol. 268, F1198-F1210.
8. Burnatowska-Hledin, M., Zhao, P., Capps, B., Poel, A., Parmelee, K., Mungall, C., Sharangpani, A., and Listenberger, L. (2000). VACM-1, a cullin gene family member, regulates cellular signaling. Am. J. Physiol. 279, C266-C273.
9. Cockman, M. E., Masson, N., Mole, D. R., Jaakkola, P., Chang, G. W., Clifford, S. C., Maher, E. R., Pugh, C. W., Ratcliffe, P. J., and Maxwell, P. H. (2000). Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J. Biol. Chem. 275, 25,733.
10. Dealy, M. J., Nguyen, K. V., Lo, J., Gstaiger, M., Krek, W., Elson, D., Argeit, J., Kipreos, E. T., and Johnson, R. S. (1999). Loss of Cull results in early embryonic lethality and dysregulation of cyclin E. Nat. Genet. 23, 245.
11. -1- clear cell renal carcinoma cell proliferation: A possible mechanism coupling VHL tumor suppressor inactivation and tumorigenesis. Proc. Natl. Acad. Sci. USA 98, 1387.
12. Deshaies, R. J. (1999). SCF and Cullin/RING H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15, 435.
13. Duan, D. R., Pause, A., Burgess, W. H., Aso, T., Chen, D. Y. T., Garrett, K. P., Conaway, R. C., Conaway, J. W., Linehan, W. M., and Klausner. (1995). Inhibition of transcription elongation by the VHL tumor suppressor protein. Science 269, 1402.
14. 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., Tian, Y. M., Masson, Hamilton, D. L., Jaakkola, P., Barstead, R., Hodgkin, J., Maxwell, P. H., Pugh, C. W., Schofield, C. J., and Ratcliffe, P. (2001). C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate, HIF by prolyl hydroxylation. Cell 107, 43.
15. Feng, H., Zhong, W., Punkosdy, G., Gu, S., Zhou, L., Seabolt, E. K., and Kipreos, E. T. (1999). Nat. Cell Biol. 1, 486.
16. Gorospe, M., Egan, J. M., Zbar, B., Lerman, M., Geil, L., Kuzmin, I., and Holbrook, N. J. (1999). Protective function of the von Hippel-Lindau protein against impaired protein processing in renal carcinoma cells. Mol. Cell. Biol. 19, 1289.
17. Gnarra, J. R., Tory, K., Weng, Y., Schmidt, L., Wei, M. H., Li, H., Latif, F., Liu, S., Chen, F., Duh, F. M., Lubensky, I., Duan, D. R., Florence, C., Pozzatti, R., Walther, M. M., Bander, N. H., Gorssman, H. B., Brauch, H., Pomer, S., Brooks, J. D., Isaacs, W. B., Lerman, M. I., Zbar, B., and Linehan, W. M. (1994). Mutations of the VHL tumor suppressor gene in renal carcinoma. Nat. Genet. 7, 85.
18. Gnarra, J. R., Zhou, S., Merrill, M. J., Wagner, J. R., Krumm, A., Papavassiliou, E., Oldfield, E. H., Klausner, R. D., and Linehan, W. M. (1996). Post-transcriptional regulation of vascular endothelial growth factor mRNA by the product of the VHL tumor suppressor gene. Proc. Natl. Acad. Sci. USA 93, 10,589.
19. Huang, L. E., Arany, Z., Livingston, D. M., and Bunn, H. F. (1996). Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J. Biol. Chem. 271, 32,253.
20. Huang, L. E., Gu, J., Schau, M., and Bunn, H. F. (1998). Regulation of hypoxia-inducible factor 1 alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 95, 7987.
21. Iliopoulos, O., Levy, A. P., Jiang, C., Kaelin, W. G., and Goldberg, M. A. (1996). Negative regulation of hypoxia-inducible genes by the von Hippel-Lindau protein. Proc. Natl. Acad. Sci. USA 93, 10,595.
22. 19 is a biologically active product of the von Hippel-Lindau gene arising from internal translation initiation. Proc. Natl. Acad. Sci. USA 95, 11,661.
23. 2 sensing. Science 292, 464.
24. Iwai, K., Yamanaka, K., Kamura, T., Minato, N., Conaway, R. C., Conaway, J. W., Klausner, R. D., and Pause, A. (1999). Identification of the von Hippel-Lindau tumor suppressor protein as the substrate recognition subunit of an E3 ubiquitin ligase complex. Proc. Natl. Acad. Sci. USA 96, 12,436.
25. 2-regulated prolyl hydroxylation. Science 292, 468.
26. Kamura, T., Koepp, D. M., Conrad, M. N., Skowyra, D., Moreland, R. J., Iliopoulos, O., Lane, W. S., Kaelin, W. G., Elledge, S. J., Conaway, R. C., Harper, J. W., and Conaway, J. W. (1999). Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 284, 657.
27. Kamura, T., Sato, S., Iwai, K., Czyzyk-Krezeska, M. F., Conaway, R. C., and Conaway, J. W. (2000). Activation of HIF1α ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc. Natl. Acad. Sci. USA 97, 10,430.
28. Kanno, H., Kondo, K., Ito, S., Yamamoto, I., Fujii, S., Torigoe, S., Sakai, N., Hosaka, M., Shuin, T., and Yao, M. (1994). Somatic mutations of the von Hippel-Lindau tumor suppressor gene in sporadic central nervous system hemangioblastomas. Cancer Res. 54, 4845.
29. Kibel, A., Iliopoulos, O., DeCaprio, J. A., and Kaelin, W. G. (1995). Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C. Science 269, 1444.
30. Kipreos, E. T., Lander, L. E., Wing, J. P., He, W. H., and Hedgecock, E. M. (1996). cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829.
31. Kishida, T., Stackhouse, T. M., Chen, F., Lerman, M. I., and Zbar, B. (1995). Cellular proteins that bind the von Hippel-Lindau disease gene product: Mapping of binding domains and the effect of missense mutations. Cancer Res. 20, 4544.
32. Knebelmann, B., Ananth, S., Cohen, H. T., and Sukhatme, V. P. (1998). Transforming growth factor alpha is a target for the von Hippel-Lindau tumor suppressor. Cancer Res. 58, 226.
33. Fbw7 ubiquitin ligase. Science 294, 173.
34. Latif, F., Tory, K., Gnarra, J., Yao, M., Duh, E M., Orcutt, M. L., Stackhouse, T., Kuzmin, I., Modi, W., Geil, L., Schmidt, L., Zhou, F., Li, H., Wei, M. H., Chen, F., Glenn, G., Choyke, P., Walther, M. M., Weng, Y., Duan, D. R., Dean, M., Glavac, K., Richards, F. M., Crossey, P. A., Ferguson-Smith, M. A., Le Paslier, D., Chumakov, I., Cohen, D., Chinault, A. C., Maher, E. R., Linehan, W. M., Zbar, B., and Lerman, M. I. (1993). Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 260, 1317.
35. Li, H., Ko, H. P., and Whitlock, J. P. (1996). Induction of phosphoglycerate kinase 1 gene expression by hypoxia. J. Biol. Chem. 271, 21,262.
36. Lisztwan, J., Imbert, G., Gstaiger, M., and Krek, W. (1999). The von Hippel-Lindau tumor suppressor protein is a component of an E3 ubiquitin-protein ligase activity. Genes Dev. 13, 1822.
37. Lonergan, K. M., Iliopoulos, O., Ohh, M., Kamura, T., Conaway, R. C., Conaway, J. W., and Kaelin, W. G. (1998). Regulation of hypoxia-inducible mRNAs by the von Hippel-Lindau tumor suppressor protein requires binding to complexes containing Elongins B/C and Cul2. Mol. Cell. Biol. 18, 732.
38. Masson, N., William, C., Maxwell, P. H., Pugh, C. W., and Ratcliffe, P. J. (2001). Independent function of two destruction domains in hypoxia-inducible factor-α chains activated by prolyl hydroxylation. EMBO J. 20, 5197.
39. Maxwell, P. H., Wiggener, 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 tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271.
40. 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., 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.
41. Ohh, M., Park, C. W., Ivan, M., Hoffman, M. A., Kin, 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.
42. Ohh, M., Takagi, Y., Aso, T., Stebbins, C. E., Pavletich, N. P., Zbar, B., Conaway, R. C., Conaway, J. W., and Kaelin, W. G. (1999). Synthetic peptides define critical contacts between elongin C, elongin B, and the von Hippel-Lindau tumor suppressor protein. J. Clin. Invest. 104, 1583.
43. Ohta, T., Michel, J. J., Schottelius, A. J., and Xiong, Y. (1999). ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol. Cell 3, 535.
44. Patton, E. E., Willems, A. R., and Tyers, M. (1998). Combinatorial control in ubiquitin-dependent proteolysis: Don't Skp the F-box hypothesis. Trends Genet. 14, 236.
45. Pause, A., Lee, S., Lonergan, K. M., and Klausner, R. D. (1998). The von Hippel-Lindau tumor suppressor gene is required for cell cycle exit upon serum withdrawal. Proc. Natl. Acad. Sci. USA 95, 993.
46. Pause, A., Lee, S., Worrell, R. A., Chen, D. Y. T., Burgess, W. H., Linehan, W. M., and Klausner, R. D. (1997). 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 94, 2156.
47. Pause, A., Peterson, B., Schaffar, G., Stearman, R., and Klausner, R. D. (1999). Studying interactions of four proteins in the yeast two-hybrid system: Structural resemblance of the pVHL/elongin BC/hCul-2 complex with the ubiquitin ligase complex SKP1/cullin/F-box protein. Proc. Natl. Acad. Sci. USA 96, 9533.
48. Salceda, S., and Caro, J. (1997). Hypoxia-inducible factor 1 alpha (HIF-1 alpha) protein in rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. J. Biol. Chem. 272, 22,642.
49. Schoenfeld, A., Davidowitz, E. J., and Burk, R. D. (1998). A second major native von Hippel-Lindau gene product, initiated from an internal translation start site, functions as a tumor suppressor. Proc. Natl. Acad. Sci. USA 95, 8817.
50. Schoenfeld, A. R., Parris, T., Eisenberger, A., Davidowitz, E. J., DeLeon, M., Talasazan, F., Devarajan, P., and Burk, R. D. (2000). The von Hippel-Lindau tumor suppressor gene protects cells from UV-mediated apoptosis. Oncogene 19, 5851.
51. Semenza, G. L. (1999). Perspectives on oxygen sensing. Cell 98, 281.
52. Semanza, G. L. (2000a). Regulation of mammalian O2 homeostasis by hypoxia-inducible factor. Annu. Rev. Cell Dev. Biol. 15, 551.
53. Semenza, G. L. (2000b). HIF-1 and human disease: One highly involved factor. Genes Dev. 14, 1983.
54. Seol, J. H., Feldman, R. M., Zachariae, W., Shevchenko, A., Correll, C. C., Lyapina, S. A., Chi, Y., Galova, M., Claypool, J., Sandmeyer, S., Nasmyth, K., and Deshaies, R. J. (1999). Cdc53/cullin and the essential hrtl RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme cdc34. Genes Dev. 13, 1614.
55. Siemeister, G., Weindel, K., Mohrs, K., Barleon, B., Martiny-Baron, G., and Marme, D. (1996). Reversion of deregulated expression of vascular endothelial growth factor in human renal carcinoma cells by von Hippel-Lindau tumor suppressor protein. Cancer Res. 56, 2299.
56. Singer, J. D., Gurian-West, M., Clurman, B., and Roberts, J. M. (1999). Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev. 13, 2375.
57. Grr1 and Rbx1. Science 284, 662.
58. Stebbins, C. E., Kaelin, W. G., and Pavletich, N. P. (1999). Structure of the VHL-ElonginC-ElonginB complex: Implications for VHL tumor suppressor function. Science 284, 455.
59. Tan, P., Fuchs, S. Y., Chen, A., Wu, K., Gomez, C., Ronai, Z., and Pan, Z. Q. (1999). Recruitment of a ROC1-CUL1 ubiquitin ligase by Skp1 and HOS to catalyze the ubiquitination of Iκ Bα. Mol. Cell 3, 527.
60. Tanimoto, K., Makino, Y., Pereira, T., and Poellinger, L. (2000). Mechanism of regulation of the hypoxia-inducible factor 1-alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J. 19, 4298.
61. Wang, G. L., Jiang, B. H., Rue, E. A., and Semenza, G. L. (1995). Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular oxygen tension. Proc. Natl. Acad. Sci. USA 92, 5510.
62. Yu, H., Peters, J. M., King, R. W., Page, A. M., Hieter, P., and Kirschner, M. (1998). Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science 279, 1219.
63. Yu, F., White, S. B., Zhao, Q., and Lee, F. S. (2001). HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. USA 98, 9630.
64. Zhu, H., and Bunn, H. F. (2001). How do cells sense oxygen? Science 292, 449.