Mixed-Lineage Kinase 3 Delivers CD3/CD28-Derived Signals into the IκB Kinase Complex

REFERENCES

• Baichwal, V. R., and Baeuerle, P. A.. 1997. Activate NF-κB or die? Curr. Biol. 7:R94–R96
   PubMed Web of Science ®Google Scholar
• Baldwin, A. S.Jr. 1996. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649–683
   PubMed Web of Science ®Google Scholar
• Bender, K., Göttlicher, M., Whiteside, S., Rahmsdorf, H. J., and Herrlich, P.. 1998. Sequential DNA damage-independent and -dependent activation of NF-κB by UV. EMBO J. 17:5170–5181
   PubMedGoogle Scholar
• Beraud, C., Henzel, W. J., and Baeuerle, P. A.. 1999. Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NF-κB activation. Proc. Natl. Acad. Sci. USA 96:429–434
   PubMed Web of Science ®Google Scholar
• Cantrell, D.. 1998. Lymphocyte signalling: a coordinating role for Vav? Curr. Biol. 8:R535–R538
   PubMedGoogle Scholar
• Chen, Z. J., Parent, L., and Maniatis, T.. 1996. Site-specific phosphorylation of IκBα by a novel ubiquitination-dependent protein kinase activity. Cell 84:853–862
   PubMed Web of Science ®Google Scholar
• Cohen, L., Henzel, W. J., and Baeuerle, P. A.. 1998. IKAP is a scaffold protein of the IκB kinase complex. Nature 395:292–296
   PubMedGoogle Scholar
• Coso, O. A., Chiariello, M., Yu, J. C., Teramoto, H., Crespo, P., Xu, N., Miki, T., and Gutkind, J. S.. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81:1137–1146
   PubMed Web of Science ®Google Scholar
• Costello, P. S., Walters, A. E., Mee, P. J., Turner, M., Reynolds, L. F., Prisco, A., Sarner, N., Zamoyska, R., and Tybulewicz, V. L. J.. 1999. The Rho family GTP exchange factor Vav is a critical transducer of T cell receptor signals to the calcium, ERK and NF-κB pathways. Proc. Natl. Acad. Sci. USA 96:3035–3040
   PubMed Web of Science ®Google Scholar
• Crespo, P., Schuebel, K. E., Ostrom, A. A., Gutkind, J. S., and Bustelo, X. R.. 1997. Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature 385:169–172
   PubMed Web of Science ®Google Scholar
• De Bosscher, K., Schmitz, M. L., Plaisance, S., Vanden Berghe, W., Fiers, W., and Haegeman, G.. 1997. Glucocorticoid-mediated repression of NF-κB dependent transcription involves direct interference with transactivation. Proc. Natl. Acad. Sci. USA 94:13504–13509
   PubMed Web of Science ®Google Scholar
• Delhase, M., Hayakawa, M., Chen, Y., and Karin, M.. 1999. Positive and negative regulation of IκB kinase activity through IKKβ subunit phosphorylation. Science 284:309–313
   PubMed Web of Science ®Google Scholar
• DiDonato, J. A., Hayakawa, M., Rothwarf, D. M., Zandi, E., and Karin, M.. 1997. A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388:548–554
   PubMed Web of Science ®Google Scholar
• Dorow, D. S., Devereux, L., Dietzsch, E., and DeKretser, T.. 1993. Identification of a new family of human epithelial protein kinases containing two leucine/isoleucine-zipper domains. Eur. J. Biochem. 213:701–710
   PubMedGoogle Scholar
• Dorow, D. S., Devereux, L., Tu, G. F., Price, G., Nicholl, J. K., Sutherland, G. R., and Simpson, R. J.. 1995. Complete nucleotide sequence, expression, and chromosomal localisation of human mixed-lineage kinase 2. Eur. J. Biochem. 234:492–500
   PubMedGoogle Scholar
• Ezoe, K., Lee, S. T., Strunk, K. M., and Spritz, R. A.. 1994. PTK1, a novel protein kinase required for proliferation of human melanocytes. Oncogene 9:935–938
   PubMedGoogle Scholar
• Gallo, K. A., Mark, M. R., Scadden, D. T., Wang, Z., Gu, Q., and Godowski, P. J.. 1994. Identification and characterization of SPRK, a novel src-homology 3 domain-containing proline-rich kinase with serine/threonine kinase activity. J. Biol. Chem. 269:15092–15100
   PubMedGoogle Scholar
• Guttridge, D. C., Albanese, C., Reuther, J. Y., Pestell, R. G., Baldwin, A. S.Jr.. 1999. NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell. Biol. 19:5785–5799
   PubMed Web of Science ®Google Scholar
• Han, J., Luby Phelps, K., Das, B., Shu, X., Xia, Y., Mosteller, R. D., Krishna, U. M., Falck, J. R., White, M. A., and Broek, D.. 1998. Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279:558–560
   PubMedGoogle Scholar
• Harhaj, E. W., and Sun, S. C.. 1998. IκB kinases serve as a target of CD28 signaling. J. Biol. Chem. 273:25185–25190
   PubMedGoogle Scholar
• Hehner, S. P., Heinrich, M., Bork, P. M., Vogt, M., Ratter, F., Lehmann, V., Schulze-Osthoff, K., Dröge, W., and Schmitz, M. L.. 1998. Sesquiterpene lactones specifically inhibit activation of NF-κB by preventing the degradation of IκB-α and IκB-β. J. Biol. Chem. 273:1288–1298
   PubMed Web of Science ®Google Scholar
• Hinz, M., Krappmann, D., Eichten, A., Heder, A., Scheidereit, C., and Strauss, M.. 1999. NF-κB function in growth control: regulation of cyclin D1 expression and G0/G1-to-S-phase transition. Mol. Cell. Biol. 19:2690–2698
   PubMed Web of Science ®Google Scholar
• Hu, Y., Baud, V., Delhase, M., Zhang, P., Deerinck, T., Ellisman, M., Johnson, R., and Karin, M.. 1999. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKα subunit of IκB kinase. Science 284:316–320
   PubMed Web of Science ®Google Scholar
• Huxford, T., Huang, D. B., Malek, S., and Ghosh, G.. 1998. The crystal structure of the IκBα/NF-κB complex reveals mechanisms of NF-κB inactivation. Cell 95:759–770
   PubMed Web of Science ®Google Scholar
• Ichijo, H., Nishida, E., Irie, K., Ten-Dijke, P., Saitoh, M., Moriguchi, T., Takagi, M., Matsumoto, K., Miyazono, K., and Gotoh, Y.. 1997. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90–94
   PubMed Web of Science ®Google Scholar
• Ing, Y. L., Leung, I. W., Heng, H. H., Tsui, L. C., and Lassam, N. J.. 1994. MLK-3: identification of a widely-expressed protein kinase bearing an SH3 domain and a leucine zipper-basic region domain. Oncogene 9:1745–1750
   PubMed Web of Science ®Google Scholar
• Jacinto, E., Werlen, G., and Karin, M.. 1998. Cooperation between Syk and Rac1 leads to synergistic JNK activation in T lymphocytes. Immunity 8:31–41
   PubMedGoogle Scholar
• Jain, J., Loh, C., and Rao, A.. 1995. Transcriptional regulation of the IL2 gene. Curr. Opin. Immunol. 7:333–342
   PubMed Web of Science ®Google Scholar
• Jung, S., Yaron, A., Alkalay, I., Hatzubai, A., Avraham, A., and Ben-Neriah, Y.. 1995. Costimulation requirement for AP-1 and NF-κB transcription factor activation in T cells. Ann. N. Y. Acad. Sci. 766:245–252
   PubMedGoogle Scholar
• Kaltschmidt, B., Kaltschmidt, C., Hehner, S. P., Dröge, W., and Schmitz, M. L.. 1999. Repression of NF-κB impairs HeLa cell proliferation by functional interference with cell cycle checkpoint regulators. Oncogene 18:3213–3225
   PubMed Web of Science ®Google Scholar
• Karin, M., Liu, Z., and Zandi, E.. 1997. AP-1 function and regulation. Curr. Opin. Cell Biol. 9:240–246
   PubMed Web of Science ®Google Scholar
• Karin, M., and Delhase, M.. 1998. JNK or IKK, AP-1 or NF-κB, which are the targets for MEK kinase 1 action? Proc. Natl. Acad. Sci. USA 95:9067–9069
   PubMed Web of Science ®Google Scholar
• Katoh, M., Hirai, M., Sugimura, T., and Terada, M.. 1995. Cloning and characterization of MST, a novel (putative) serine/threonine kinase with SH3 domain. Oncogene 10:1447–1451
   PubMedGoogle Scholar
• Kempiak, S. J., Hiura, T. S., and Nel, A. E.. 1999. The Jun kinase cascade is responsible for activating the CD28 response element of the IL-2 promoter: proof of cross-talk with the IκB kinase cascade. J. Immunol. 162:3176–3187
   PubMedGoogle Scholar
• Köntgen, F., Grumont, R. J., Strasser, A., Metcalf, D., Li, R., Tarlinton, D., and Gerondakis, S.. 1995. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9:1965–1977
   PubMed Web of Science ®Google Scholar
• Leung, I. W., and Lassam, N.. 1998. Dimerization via tandem leucine zippers is essential for the activation of the mitogen-activated protein kinase kinase kinase, MLK-3. J. Biol. Chem. 273:32408–32415
   PubMedGoogle Scholar
• Lee, F. S., Hagler, J., Chen, Z. J., and Maniatis, T.. 1997. Activation of the IκBα kinase complex by MEKK1, a kinase of the JNK pathway. Cell 88:213–222
   PubMed Web of Science ®Google Scholar
• Lee, F. S., Peters, R. T., Dang, L. C., and Maniatis, T.. 1998. MEKK1 activates both IκB kinase α and IκB kinase β. Proc. Natl. Acad. Sci. USA 95:9319–9324
   PubMed Web of Science ®Google Scholar
• Li, N., and Karin, M.. 1998. Ionizing radiation and short wavelength UV activate NF-κB through two distinct mechanisms. Proc. Natl. Acad. Sci. USA 95:13012–13017
   PubMed Web of Science ®Google Scholar
• Li, Q., Van Antwerp, D., Mercurio, F., Lee, K. F., and Verma, I. M.. 1999a. Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science 284:321–325
   PubMed Web of Science ®Google Scholar
• Li, Q., Lu, Q., Hwang, J. Y., Buscher, D., Lee, K. F., Izpisua-Belmonte, J. C., and Verma, I. M.. 1999b. IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev. 13:1322–1328
   PubMed Web of Science ®Google Scholar
• Lin, A., Minden, A., Martinetto, H., Claret, F. X., Lange-Carter, C., Mercurio, F., Johnson, G. L., and Karin, M.. 1995. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268:286–290
   PubMed Web of Science ®Google Scholar
• Lin, X., Cunningham, E. T.Jr, Mu, Y., Geleziunas, R., and Greene, W. C.. 1999. The proto-oncogene Cot kinase participates in CD3/CD28 induction of NF-κB acting through the NF-κB-inducing kinase and IκB kinases. Immunity 10:271–280
   PubMed Web of Science ®Google Scholar
• Ling, L., Cao, Z., and Goeddel, D. V.. 1998. NF-κB-inducing kinase activates IKK-α by phosphorylation of Ser-176. Proc. Natl. Acad. Sci. USA 95:3792–3797
   PubMed Web of Science ®Google Scholar
• Malinin, N. L., Boldin, M. P., Kovalenko, A. V., and Wallach, D.. 1997. MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature 385:540–544
   PubMed Web of Science ®Google Scholar
• Maniatis, T.. 1997. Catalysis by a multiprotein IκB kinase complex. Science 278:818–819
   PubMed Web of Science ®Google Scholar
• Maniatis, T.. 1999. A ubiquitin ligase complex essential for the NF-κB, Wnt/Wingless and Hedgehog signaling pathways. Genes Dev. 13:505–510
   PubMedGoogle Scholar
• May, M. J., and Ghosh, S.. 1999. IκB kinases: kinsmen with different crafts. Science 284:271–273
   PubMed Web of Science ®Google Scholar
• McGuire, K. L., and Iacobelli, M.. 1997. Involvement of Rel, Fos and Jun proteins in binding activity to the IL2 promoter CD28 response element/AP-1 sequence in human T cells. J. Immunol. 159:1319–1327
   PubMedGoogle Scholar
• Mercurio, F., Zhu, H., Murray, B. W., Shevchenko, A., Bennett, B. L., Li, J., Young, D. B., Barbosa, M., Mann, M., Manning, A., and Rao, A.. 1997. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation. Science 278:860–866
   PubMed Web of Science ®Google Scholar
• Mercurio, F., Murray, B. W., Shevchenko, A., Bennett, B. L., Young, D. B., Li, J. W., Pascual, G., Motiwala, A., Zhu, H., Mann, M., and Manning, A. M.. 1999. IκB kinase (IKK)-associated protein 1, a common component of the heterogeneous IKK complex. Mol. Cell. Biol. 19:1526–1538
   PubMedGoogle Scholar
• Miyazaki, T., Liu, Z. J., Kawahara, A., Minami, Y., Yamada, K., Tsujimoto, Y., Barsoumian, E. L., Permutter, R. M., and Taniguchi, T.. 1995. Three distinct IL-2 signaling pathways mediated by bcl-2, c-myc and lck cooperate in hematopoietic cell proliferation. Cell 81:223–231
   PubMed Web of Science ®Google Scholar
• Montaner, S., Perona, R., Saniger, L., and Lacal, J. C.. 1999. Activation of serum response factor by RhoA is mediated by the nuclear factor-κB and C/EBP transcription factors. J. Biol. Chem. 274:8506–8515
   PubMedGoogle Scholar
• Nakano, H., Shindo, M., Sakon, S., Nishinaka, S., Mihara, M., Yagita, H., and Okumura, K.. 1998. Differential regulation of IκB kinase α and β by two upstream kinases, NF-κB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1. Proc. Natl. Acad. Sci. USA 95:3537–3542
   PubMed Web of Science ®Google Scholar
• Nemoto, S., DiDonato, J. A., and Lin, A.. 1998. Coordinate regulation of IκB kinases by mitogen-activated protein kinase kinase kinase 1 and NF-κB-inducing kinase. Mol. Cell. Biol. 18:7336–7343
   PubMedGoogle Scholar
• Ninomiya-Tsuji, J., Kishimoto, K., Hiyama, A., Inoue, J., Cao, Z., and Matsumoto, K.. 1999. The kinase TAK1 can activate the NIK-IκB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398:252–256
   PubMed Web of Science ®Google Scholar
• Penninger, J. M., Fischer, K. D., Sasaki, T., Kozieradzki, I., Le, J., Tedford, K., Bachmaier, K., Ohashi, P. S., and Bachmann, M. F.. 1999. The oncogene product Vav is a crucial regulator of primary cytotoxic T cell responses but has no apparent role in CD28-mediated co-stimulation. Eur. J. Immunol. 29:1709–1718
   PubMedGoogle Scholar
• Perona, R., Montaner, S., Saniger, L., Sanchez-Perez, I., Bravo, R., and Lacal, J. C.. 1997. Activation of the nuclear factor-κB by Rho, CDC42, and Rac-1 proteins. Genes Dev. 11:463–475
   PubMed Web of Science ®Google Scholar
• Rana, A., Gallo, K., Godowski, P., Hirai, S., Ohno, S., Zon, L., Kyriakis, J. M., and Avruch, J.. 1996. The mixed lineage kinase SPRK phosphorylates and activates the stress-activated protein kinase activator, SEK-1. J. Biol. Chem. 271:19025–19028
   PubMed Web of Science ®Google Scholar
• Regnier, C. H., Song, H. Y., Gao, X., Goeddel, D. V., Cao, Z., and Rothe, M.. 1997. Identification and characterization of an IκB kinase. Cell 90:373–383
   PubMed Web of Science ®Google Scholar
• Rothwarf, D. M., Zandi, E., Natoli, G., and Karin, M.. 1998. IKK-γ is an essential regulatory subunit of the IκB kinase complex. Nature 395:297–300
   PubMed Web of Science ®Google Scholar
• Shapiro, V. S., Truitt, K. E., Imboden, J. B., and Weiss, A.. 1997. CD28 mediates transcriptional upregulation of the interleukin-2 (IL2) promoter through a composite element containing the CD28RE and NF-IL2B AP-1 sites. Mol. Cell. Biol. 17:4051–4058
   PubMed Web of Science ®Google Scholar
• Su, B., Jacinto, E., Hibi, M., Kallunki, T., Karin, M., and Ben-Neriah, Y.. 1994. JNK is involved in signal integration during costimulation of T lymphocytes. Cell 77:727–736
   PubMed Web of Science ®Google Scholar
• Tanaka, M., Fuentes, M. E., Yamaguchi, K., Durnin, M. H., Dalrymple, S. A., Hardy, K. L., and Goeddel, D. V.. 1999. Embryonic lethality, liver degeneration and impaired NF-κB activation in IKK-β-deficient mice. Immunity 10:421–429
   PubMed Web of Science ®Google Scholar
• Teramoto, H., Coso, O. A., Miyata, H., Igishi, T., Miki, T., and Gutkind, J. S.. 1996. Signaling from the small GTP-binding proteins Rac and Cdc42 to the c-Jun N-terminal kinase/stress-activated protein kinase pathway. A role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family. J. Biol. Chem. 271:27225–27228
   PubMed Web of Science ®Google Scholar
• Tibbles, L. A., Ing, Y. L., Kiefer, F., Chan, J., Iscove, N., Woodgett, J. R., and Lassam, N. J.. 1996. MLK-3 activates the SAPK/JNK and p38/RK pathways via SEK1 and MKK3/6. EMBO J. 15:7026–7035
   PubMed Web of Science ®Google Scholar
• Verma, I. M., and Stevenson, J.. 1997. IκB kinase: beginning, not the end. Proc. Natl. Acad. Sci. USA 94:11758–11760
   PubMedGoogle Scholar
• Whitmarsh, A. J., Cavanagh, J., Tournier, C., Yasuda, J., and Davis, R. J.. 1998. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281:1671–1674
   PubMed Web of Science ®Google Scholar
• Woronicz, J. D., Gao, X., Cao, Z., Rothe, M., and Goeddel, D. V.. 1997. IκB kinase-β: NF-κB activation and complex formation with IκB kinase-α and NIK. Science 278:866–869
   PubMed Web of Science ®Google Scholar
• Yamaoka, S., Courtois, G., Bessia, C., Whiteside, S. T., Weil, R., Agou, F., Kirk, H. E., Kay, R. J., and Israel, A.. 1998. Complementation cloning of NEMO, a component of the IκB kinase complex essential for NF-κB activation. Cell 93:1231–1240
   PubMed Web of Science ®Google Scholar
• Yaron, A., Hatzubai, A., Davis, M., Lavon, I., Amit, S., Manning, A. M., Andersen, J. S., Mann, M., Mercurio, F., and Ben-Neriah, Y.. 1998. Identification of the receptor component of the IκBα-ubiquitin ligase. Nature 396:590–594
   PubMedGoogle Scholar
• Yujiri, T., Sather, S., Fanger, G. R., and Johnson, G. L.. 1998. Role of MEKK1 in cell survival and activation of JNK and ERK pathways defined by targeted gene disruption. Science 282:1911–1914
   PubMed Web of Science ®Google Scholar
• Zandi, E., Rothwarf, D. M., Delhase, M., Hayakawa, M., and Karin, M.. 1997. The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell 91:243–252
   PubMed Web of Science ®Google Scholar
• Zhao, Q., and Lee, F. S.. 1999. Mitogen-activated protein kinase/ERK kinase kinases 2 and 3 activate nuclear factor-κB through IκB kinase-α and IκB kinase-β. J. Biol. Chem. 274:8355–8358
   PubMed Web of Science ®Google Scholar