Hypoxia Causes the Activation of Nuclear Factor kB through the Phosphorylation of IkBα on Tyrosine Residues1

Cancer Research

Volumn 54, Issue 6, 1994, Pages 1425-1430

  Koong, Albert C ^a   Chen, Eunice Y ^a   Giaccia, Amato J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ARTICLE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; ENZYME PHOSPHORYLATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INDUCTION; HUMAN; HUMAN CELL; HYPOXIA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOLID TUMOR; STRESS; TRANSCRIPTION REGULATION;

BASE SEQUENCE; CELL HYPOXIA; CELL NUCLEUS; CELLS, CULTURED; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMAN; KINETICS; MOLECULAR SEQUENCE DATA; NF-KAPPA B; ONCOGENE PROTEIN P65(GAG-JUN); PHOSPHORYLATION; PROTEIN-TYROSINE KINASE; SUPPORT, U.S. GOV'T, P.H.S.; T-LYMPHOCYTES; TETRADECANOYLPHORBOL ACETATE; TRANS-ACTIVATION (GENETICS); TRANSLOCATION (GENETICS); TUMOR NECROSIS FACTOR; TYROSINE;

EID: 0028268629     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. Moulder, J.E., and Rockwell, S. Tumor hypoxia: its impact on cancer therapy. Cancer Metastasis Rev., 5: 313-341, 1987.
2. Gatenby, R.A., Kessler, H.B., Rosenblum, J.S., Coia, L.R., Moldofsky, P.J., Hartz, W.H., and Broder, G.J. Oxygen distribution in squamous cell carcinoma metastases and its relationship to outcome of radiation therapy. Int. J. Radiat. Oncol. Biol. Phys., 14: 831-838, 1988.
3. Bush, R.S., Jenkin, R.D.T., Allt, W.E.C., Beale, F.A., Bean, H., Denbo, A.J., and Pringle, J.F. Definite evidence for hypoxic cells influencing cure in cancer therapy. Br. J. Cancer, 57(Suppl. 3): 302-306, 1978.
4. Heacock, C.S., and Sutherland, R.M. Enhanced synthesis of stress proteins caused by hypoxia and relation to altered cell growth and metabolism. Br. J. Cancer, 62: 217-225, 1990.
5. Koong, A.C., Auger, E.A., Chen, E.Y., and Giaccia, A.J. The regulation of GRP78 protein and messenger RNA levels by hypoxia is modulated by protein kinase C activators and inhibitors. Radiat. Res., in press, 1994.
6. Graeber, S.E., and Krantz, S.B. Erythropoietin: biology and clinical use. Hematol. Ocol. Clin. North Am., 3: 369, 1989.
7. Semenza, G.L., and Wang, G.L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol., 12: 5447-5454, 1992.
8. Giaccia, A.J., Auger, E.A., Koong, A., Terrace, D., Minchinton, A., Hahn, G.M., and Brown, J.M. Activation of the heat shock transcription factor by hypoxia in normal and tumor cell lines in vivo and in vitro. Int. J. Radiat. Oncol. Biol. Phys., 23: 891-897, 1992.
9. Molitor, J.A., Walker, W.H., Doerre, S., Ballard, D.W., and Greene, W.C. NF-kB; a family of inducible and differentially expressed enhancer-binding proteins in human T cells. Proc. Natl. Acad. Sci. USA, 87: 10028-10032, 1990.
10. Perkins, N.D., Schmid, R.M., Duckett, C.S., Leung, K., Rice, N.R., and Nabel, G.J. Distinct combinations of NF-kB subunits determine the specificity of transcriptional activation. Proc. Natl. Acad. Sci. USA, 89: 1529-1533, 1992.
11. Radler-Pohl, A., Pfeuffer, I., Karin, M., and Sterfling, E. A novel T-cell trans-activator that recognizes a phorbol ester-inducible element of the interleukin-2 promotor. New Biol., 2: 566-573, 1990.
12. Baeuerle, P.A., and Baltimore, D. The physiology of the NF-kB transcription factor. In: P. Cohen and J.G. Foulkes (eds.), Molecular Aspects of Cellular Regulation pp. 409-432. Amsterdam: Elseviier/North-Holland Biomedical Press, 1991.
13. Leonardo, M.J., and Baltimore, D. NF-kB: a pleiotrophic mediator of inducible and tissue specific gene control. Cell, 58: 227-229, 1989.
14. Brach, M.A., Hass, R., Sherman, M.L., Gunji, H., Weichselbaum, R.R., and Kufe, D. Ionizing radiation induces expression and binding activity of the nuclear factor kB.J. Clin. Invest., 88: 691-695, 1991.
15. Ghosh, S., Gifford, A.M., Riviere, L.R., Tempst, P., Nolan, G.P., and Baltimore, D. Coning of the p. 0 DNA binding subunit of NF-kB: homology to rel and dorsal. Cell, 62: 1019-1029, 1990.
16. Neri, A., Chang, C.G., Lombardi, L., Salina, M., Corradini, P., Maiolo, A.T., Changanti, R.S.K., and Dalla-Favera, R. B cell lymphoma-associated chromosomal translocation involves candidate oncogene, lyt-10, homologous to NFkB p. 0. Cell, 67: 1075-1087, 1991.
17. Nolan, G.P., Ghosh, S., Liou, H.G., Tempst, P., and Baltimore, D. DNA binding and IkB inhibition of the cloned p. 5 subunit of NFkB, a rel-related polypeptide. Cell, 64: 961-969, 1991.
18. Ryseck, R.P., Bull, P., Takamiya, M., Bours, V., Siebenlist, U., Dobrzanski, P., and Bravo, R. RelB, a new Rel family transcription activator that can interact with p. 0-NFkB. Mol. Cell. Biol., 12: 674-684, 1992.
19. Stephens, R.M., Rice, N.R., Hiebsch, R.R., Bose, H.R., and Gilden, R.V. Nucleotide sequence of v-rel: the oncogene of reticuloendotheliosis virus. Proc. Natl. Acad. Sci. USA, 80: 6229-6233, 1983.
20. Steward, R. Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-onogene, c-rel. Science (Washington DC), 238: 692-694, 1987.
21. Ballard, D.W., Walker, W.H., Doerre, S., Sista, P., Molitor, J.A., Dixon, E.P., Peffer, N.J., Hannink, M., and Greene, W.C. The v-rel oncogene encodes a kB enhancer binding protein that inhibits NF-kB function. Cell, 63: 803-814, 1990.
22. Mercurio, F., Didonato, J.A., Rosette, C., and Karin, M. p. 05 and p. 8 precursor proteins play an active role in NF-kB mediated signal transduction. Genes & Dev., 7: 705-718, 1993.
23. Rice, N.R., MacKichan, M.L., and Israel, A. The precursor of NF-kB p. 0 has IkB like functions. Cell, 71: 243-253, 1992.
24. Davis, N.S., Ghosh, S., Simmons, D.L., Tempst, P., Liou, H.G., Baltimore, D., and Bose, H.R. Rel-associated pp. 40: an inhibitor of the Rel family of transcription factors. Science (Washington DC), 253: 1268-1271, 1991.
25. Franzoso, G., Bours, V., Park, S., Tomita-Yamaguchi, M., Kelly, K., and Siebenlist, U. The candidate oncoprotein Bcl-3 is an antagonist of p. 0/NF-kb mediated inhibition. Nature (Lond.), 359: 339-342, 1992.
26. Haskill, S., Beg, A.A., Thompkins, S.M., Morris, J.S., Yurochko, A.D., Sampson-Johannes, A., Mondai, K., Ralph, P., and Baldwin, A.S. Characterization of an immediate-early gene induced in aderent monocytes that encodes IkB-like activity. Cell, 65: 1281-1289, 1991.
27. Hatada, E.N., Nieters, A., Wulczyn, F.G., Naumann, M., Meyer, R., Nucifora, G., McKeithan, T.W., and Scheidereit, C. The ankyrin repeat domains of the NF-kB precursor p. 05 and the proto-oncogene bcl-3 act as specific inhibitors of NF-kB DNA binding. Proc. Natl. Acad. Sci. USA, 89: 2489-2493, 1992.
28. Inoue, J.I., Kerr, L.D., Kakizuka, A., and Verma, I.M. IkBg, a 70 kd protein identical to the C-terminal half of p. 10 NF-kB: a new member of the IkB family. Cell, 68: 1109-1120, 1992.
29. Ghosh, S., and Baltimore, D. Activation in vitro of NF-kB by phosphorylation of its inhibitor IkB. Nature (Lond.), 344: 678-682, 1990.
30. Shirakawa, F., and Mizel, S.B. In vitro activation and nuclear translocation of NF-kB catalyzed by the cyclic AMP-dependent protein kinase and protein kinase C. Mol. Cell. Biol., 9: 2424-2430, 1989.
31. Beg, A.A., Finco, T.S., Nantermet, P.V., and Baldwin, A.S. Tùmor necrosis factor and interleukin-1 lead to phophorylation and loss of IkBα: a mechanism for NF-kB activation. Mol. Cell. Biol., 13: 3301-3310, 1993.
32. Polonis, V.R., Anderson, G.R., Vahey, M.T., Morrow, P.J., Stoler, D., and Redfield, R.R. Anoxia induces human immunodeficiency virus in infected T cell lines. J. Biol. Chem., 266: 11421-11424, 1991.
33. Fordis, C.M., and Howard, B.H. Use of CAT reporter gene for optimization of gene transfer into eukaryotic cells. Methods Enzymol., 151: 382-397, 1987.
34. Sun, S.C., Ganchi, P.A., Ballard, D.W., and Greene, W.C. NF-kB controls expression of inhibitor I IkBα: evidence for an inducible autoregulatory pathway. Science (Washington DC), 259: 1912-1915, 1993.
35. Nabel, G., and Baltimore, D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature (Lond.), 326: 711-713, 1987.
36. Schreck, R., Reiber, P., and Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kB transcription factor and HIV-1. EMBO, 10: 2247-2258, 1991.
37. Uckum, F.M., Schieven, G.L., Tuel-Ahlgren, L.M., Dibirdik, I., Myers, D.E., Ledbetter, J.A., and Song, C.W. Tyrosine phosphorylation is a mandatory proximal step in radiation-induced activation of the protein kinase C signaling pathway in human B-lymphocyte precursors. Proc. Natl. Acad. Sci. USA, 90: 252-256, 1993.
38. Devary, Y., Rosette, C., DiDonato, J.A., and Karin, M. NF-kB activation by ultraviolet light not dependent on a nuclear signal. Science (Washington DC), 261: 1442-1445, 1993.
39. Casnellie, J.E. Protein kinase inhibitors: probes for the functions of protein phosphorylation. Adv. Pharmacol., 22: 157-205, 1991.
40. Cohen, B., Yoakim, M., Piwnica-Worms, H., Roberts, T.M., and Schaffhausen, B.S. Tyrosine phosphorylation is a signal for the trafficking of pp. 85, an 85-kDa phosphorylated polypeptide associated with phosphatidylinositol kinase activity. Proc. Natl. Acad. Sci. USA, 87: 4458-4462, 1990.
41. Kanakura, Y., Druker, B., DiCarlo, J., Cannistra, S.A., and Griffin, J.D. Phorbol 12-myristate 13-acetate inhibits granulocyte-macrophage colony stimulating factor-induced protein tyrosine phosphorylation in a human factor-dependent hematopoietic cell line. J. Biol. Chem., 266: 490-495, 1991.
42. Bruder, J.T., Heidecker, G., and Rapp, U.R. Serum-, TPA-, and Ras-induced expression from Ap. 1/Ets-driven promoters. Genes & Dev., 6: 545-556, 1992.
43. Finco, T.S., and Baldwin, A.S. kB site-dependent induction of gene expression by diverse inducers of kB requires Raf-1. J. Biol. Chem., 268: 17676-17679, 1993.
44. Folkman, J. Tumor angiogenesis. In: E.F.J. Holland, R. Bast, D. Kufe, R.L. Morton, and R.R. Weichselbaum (eds.), Cancer Medicine, Ed. 3, pp. 153-170. Philadelphia: Lea & Febiger, 1993.
45. Hansen, S., Nerlov, C., Zabel, U., Verde, P., Johnsen, M., Baeuerle, P.A., and Blasi, F. A novel complex between the p. 5 subunit of NF-kB and c-Rel binds to a DNA element involved in the phorbol ester induction of the human urokinase gene. EMBO, 11: 205-213, 1992.
46. Schutze, S., Machleidt, T., and Kronke, M. Mechanisms of tumor necrosis factor action. Semin. Oncol., 19: 16-14, 1992.
47. Takao, S., and Jacob, C. Mouse tumor necrosis factor receptor type I: genomic structure, polymorphism, and identification of regulatory regions. Int. Immunol., 5: 775-782, 1993.
48. Higgins, K.A., Perez, J.R., Coleman, T.A., Dorshkind, K., McComas, W.A., Sariento, U.M., Rosen, C.A., and Narayanan, R. Antisense inhibition of the p. 5 subunit of NF-kB blocks tumorigenicity and causes tumor regression. Proc. Natl. Acad. Sci. USA, 90: 9901-9905, 1993.
49. Brown, J.M., and Giaccia, A.J. Tumor hypoxia: the picture has changed in the 1990′s. Int. J. Radiat. Oncol. Biol. Phys., in press, 1994.