MEK Kinase 1, a Substrate for DEVD-Directed Caspases, Is Involved in Genotoxin-Induced Apoptosis

REFERENCES

• Alnemri, E. S., D. J. Livingston, D. W. Nicholson, G. S. Salvesen, N. A. Thornberry, W. W. Wong, and J. Yuan 1996. Human ICE/CED-3 protease nomenclature. Cell 87: 171.
   PubMed Web of Science ®Google Scholar
• An, B., and Q. P. Dou 1996. Cleavage of retinoblastoma protein during apoptosis: an interleukin 1β-converting enzyme-like protease as candidate. Cancer Res. 56: 438–442.
   PubMedGoogle Scholar
• Avdi, N. J., B. W. Winston, M. Russel, S. K. Young, G. L. Johnson, and G. S. Worthen 1996. Activation of MEKK by formyl-methionyl-leucyl-phenylalanine in human neutrophils. Mapping pathways for mitogen-activated protein kinase activation. J. Biol. Chem. 271: 33598–33606.
   PubMed Web of Science ®Google Scholar
• Baeuerle, P. A., and D. Baltimore 1996. NF-(kappa)B: ten years after. Cell 87: 13–20.
   PubMed Web of Science ®Google Scholar
• Beidler, D. R., M. Tewari, P. D. Friesen, G. Poirier, and V. M. Dixit 1996. The baculovirus p35 protein inhibits Fas- and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 270: 16526–16528.
   Google Scholar
• Blank, J. L., P. Gerwins, E. M. Elliott, S. Sather, and G. L. Johnson 1996. Molecular cloning of mitogen-activated protein/ERK kinase kinases (MEKK) 2 and 3. Regulation of sequential phosphorylation pathways involving mitogen-activated protein kinase and c-Jun kinase. J. Biol. Chem. 271: 5361–5368.
   PubMed Web of Science ®Google Scholar
• Cardone, M., G. S. Salvesen, C. Widmann, G. L. Johnson, and S. M. Frisch 1997. The regulation of anoikis: MEKK-1 activation requires cleavage by caspases. Cell 90: 315–323.
   PubMed Web of Science ®Google Scholar
• Cartier, J. L., P. A. Hershberger, and P. D. Friesen 1994. Suppression of apoptosis in insect cells stably transfected with baculovirus p35: dominant interference by N-terminal sequences p351–76. J. Virol. 68: 7728–7737.
   PubMedGoogle Scholar
• Casciola-Rosen, L. A., G. J. Anhalt, and A. Rosen 1995. DNA-dependent protein kinase is one of a subset of antoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182: 1625–1634.
   PubMedGoogle Scholar
• Casciola-Rosen, L. A., D. K. Miller, G. J. Anhalt, and A. Rosen 1994. Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol. Chem. 269: 30757–30760.
   PubMed Web of Science ®Google Scholar
• Chen, Y.-R., X. Wang, D. Templeton, R. J. Davis, and T.-H. Tan 1996. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma irradiation. Duration of JNK activation may determine cell death and proliferation. J. Biol. Chem. 271: 31929–31936.
   PubMed Web of Science ®Google Scholar
• Clem, R. J., J. M. Hardwick, and L. K. Miller 1996. Anti-apoptotic genes of baculoviruses. Death Differ. 3: 9–16.
   PubMedGoogle Scholar
• Cryns, V. L., L. Bergeron, H. Zhu, H. Li, and J. Yuan 1996. Specific cleavage of α-fodrin during Fas- and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1β-converting enzyme/Ced-3 protease distinct from the poly(ADP-ribose) polymerase protease. J. Biol. Chem. 271: 31277–31282.
   PubMedGoogle Scholar
• Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. E. Greenberg 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231–241.
   PubMed Web of Science ®Google Scholar
• Deak, J. C., and D. J. Templeton 1997. Regulation of the activity of MEK kinase 1 (MEKK1) by autophosphorylation within the kinase activation domain. Biochem. J. 322: 185–192.
   PubMedGoogle Scholar
• del Peso, L., M. Gonzalez-Garcia, C. Page, R. Herrera, and G. Nunez 1997. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278: 687–689.
   PubMed Web of Science ®Google Scholar
• Dive, C., and J. A. Hickman 1991. Drug-target interactions: only the first step in the commitment to a programmed cell death? Br. J. Cancer 64: 192–196.
   PubMed Web of Science ®Google Scholar
• Emoto, Y., Y. Manome, G. Meinhardt, H. Kisaki, S. Kharbanda, M. Robertson, T. Ghayur, W. W. Wong, R. Kamen, R. Weichselbaum, and D. Kufe 1995. Proteolytic activation of protein kinase C δ by an ICE-like protease in apoptotic cells. EMBO J. 14: 6148–6156.
   PubMed Web of Science ®Google Scholar
• Erhardt, P., K. J. Tomaselli, and G. M. Cooper 1997. Identification of the MDM2 oncoprotein as a substrate for CPP32-like apoptotic proteases. J. Biol. Chem. 272: 15049–15052.
   PubMedGoogle Scholar
• Fanger, G. R., C. Widmann, A. C. Porter, S. Sather, G. L. Johnson, and R. R. Vaillancourt 1998. 14-3-3 proteins interact with specific MEK kinases. J. Biol. Chem. 273: 3476–3483.
   PubMedGoogle Scholar
• Fisher, D. E. 1994. Apoptosis in cancer therapy: crossing the threshold. Cell 78: 539–542.
   PubMed Web of Science ®Google Scholar
• Fraser, A., and G. Evan 1996. A license to kill. Cell 85: 781–784.
   PubMedGoogle Scholar
• Gardner, A. M., and G. L. Johnson 1996. Fibroblast growth factor-2 suppression of tumor necrosis factor α-mediated apoptosis requires Ras and the activation of mitogen-activated protein kinase. J. Biol. Chem. 271: 14560–14566.
   PubMed Web of Science ®Google Scholar
• Gerwins, P., J. L. Blank, and G. L. Johnson 1997. Cloning of a novel mitogen-activated protein kinase kinase kinase, MEKK4, that selectively regulates the c-Jun amino terminal kinase pathway. J. Biol. Chem. 272: 8288–8295.
   PubMedGoogle Scholar
• Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7: 2135–2148.
   PubMed Web of Science ®Google Scholar
• Hickman, J. A., C. S. Potten, A. J. Merritt, and T. C. Fisher 1994. Apoptosis and cancer chemotherapy. Philos. Trans. R. Soc. London Ser. B 345: 319–325.
   PubMed Web of Science ®Google Scholar
• Hirano, M., S.-I. Osada, T. Aoki, S.-I. Hirai, M. Hosaka, J.-I. Inoue, and S. Ohno 1996. MEK kinase is involved in tumor necrosis factor α-induced NF-kB activation and degradation of IkB-α. J. Biol. Chem. 271: 13234–13238.
   PubMedGoogle Scholar
• Howard, A. D., M. J. Kostura, N. Thornberry, G. J.-F. Ding, G. Limjuco, J. Weidner, J. P. Salley, K. A. Hogquist, D. D. Chaplin, R. A. Mumford, J. A. Schmidt, and M. J. Tocci 1991. IL-1-converting enzyme requires aspartic acid residues for processing of the IL-1β precursor at two distinct sites and does not cleave 31-kDa IL-1α. J. Immunol. 147: 2964–2969.
   PubMed Web of Science ®Google Scholar
• Jarpe, M. Unpublished observations.
   Google Scholar
• Juo, P., C. J. Kuo, S. E. Reynolds, R. F. Konz, J. Raingeaud, R. J. Davis, H.-P. Biemann, and J. Blenis 1997. Fas activation of the p38 mitogen-activated protein kinase signalling pathway requires ICE/CED-3 family proteases. Mol. Cell. Biol. 17: 24–35.
   PubMed Web of Science ®Google Scholar
• Khwaja, A., and J. Downward 1997. Lack of correlation between activation of Jun-NH2-terminal kinase and induction of apoptosis after detachment of epithelial cells. J. Cell Biol. 139: 1017–1023.
   PubMed Web of Science ®Google Scholar
• Kim, T.-W., W. H. Pettingell, Y.-K. Jung, D. M. Kovacs, and R. E. Tanzi 1997. Alternative cleavage of Alzheimer-associated presenilins during apoptosis by a caspase-3 family protease. Science 277: 373–376.
   PubMed Web of Science ®Google Scholar
• Lange-Carter, C. A., and G. L. Johnson 1994. Ras-dependent growth factor regulation of MEK kinase in PC12 cells. Science 265: 1458–1461.
   PubMed Web of Science ®Google Scholar
• Lange-Carter, C. A., C. M. Pleiman, A. M. Gardner, K. J. Blumer, and G. L. Johnson 1993. A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf. Science 260: 315–319.
   PubMed Web of Science ®Google Scholar
• Lassignal Johnson, N., A. M. Gardner, K. M. Diener, C. A. Lange-Carter, J. Gleavy, M. B. Jarpe, A. Minden, M. Karin, L. I. Zon, and G. L. Johnson 1996. Signal transduction pathways regulated by mitogen-activated/extracellular response kinase kinase kinase induce cell death. J. Biol. Chem. 271: 3229–3237.
   PubMedGoogle Scholar
• Lazebnik, Y. A., S. H. Kaufmann, S. Desnoyers, G. G. Poirier, and W. C. Earnshaw 1994. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371: 346–347.
   PubMed Web of Science ®Google Scholar
• Lazebnik, Y. A., A. Takahashi, R. D. Moir, R. D. Goldman, G. G. Poirier, S. H. Kaufmann, and W. C. Earnshaw 1995. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92: 9042–9046.
   PubMed Web of Science ®Google Scholar
• Lee, F. S., J. Hagler, Z. J. Chen, and T. Maniatis 1997. Activation of the I-kappa-Bα kinase complex by MEKK1, a kinase of the JNK pathway. Cell 88: 213–222.
   PubMed Web of Science ®Google Scholar
• Liu, Z.-G., R. Baskaran, E. T. Lea-Chou, L. D. Wood, Y. Chen, M. Karin, and J. Y. J. Wang 1996. Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 384: 273–276.
   PubMed Web of Science ®Google Scholar
• Liu, Z.-G., H. Hsu, D. V. Goeddel, and M. Karin 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kB activation prevents cell death. Cell 87: 565–576.
   PubMed Web of Science ®Google Scholar
• Los, M., M. Van de Craen, L. C. Penning, H. Schenk, M. Westendorp, P. A. Baeuerle, W. Dröge, P. H. Krammer, W. Fiers, and K. Schulze-Osthoff 1995. Requirement of an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 375: 81–83.
   PubMed Web of Science ®Google Scholar
• Mercille, S., and B. Massie 1994. Induction of apoptosis in nutrient-deprived cultures of hybridoma and myeloma cells. Biotechnol. Bioeng. 44: 1140–1154.
   PubMed Web of Science ®Google Scholar
• Meyn, R. E., L. C. Stephens, N. R. Hunter, and L. Milas 1995. Apoptosis in murine tumors treated with chemotherapy agents. Anticancer Drugs 6: 443–450.
   PubMed Web of Science ®Google Scholar
• Moreira, L. F., Y. Naomoto, M. Hamada, Y. Kamikawa, and K. Orita 1995. Assessment of apoptosis in oesophageal carcinoma preoperatively treated by chemotherapy and radiotherapy. Anticancer Res. 15: 639–644.
   PubMed Web of Science ®Google Scholar
• Na, S., T.-H. Chuang, A. Cunningham, T. G. Turi, J. H. Hanke, G. M. Bokoch, and D. E. Danley 1996. D4-GDI, a substrate of CPP32, is proteolyzed during Fas-induced apoptosis. J. Biol. Chem. 271: 11209–11213.
   PubMedGoogle Scholar
• Nicholson, D. W., A. Ali, N. A. Thornberry, J. P. Vaillancourt, C. K. Ding, M. Gallan, Y. Gareau, P. R. Griffin, M. Labelle, Y. A. Lazebnik, N. A. Munday, S. M. Raju, M. E. Smulson, T.-T. Yamin, V. L. Yu, and D. K. Miller 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37–43.
   PubMed Web of Science ®Google Scholar
• Nicoletti, I., G. Miglioratti, M. C. Pagliacci, F. Grignani, and C. Riccardi 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139: 271–279.
   PubMed Web of Science ®Google Scholar
• Nishina, H., K. D. Fischer, L. Radvanyi, A. Shahinian, R. Hakem, E. A. Rubie, A. Bernstein, T. W. Mak, J. R. Woodgett, and J. M. Penninger 1997. Stress-signalling kinase Sek1 protects thymocytes from apoptosis mediated by CD95 and CD3. Nature 385: 350–353.
   PubMedGoogle Scholar
• Orth, K., K. O’Rourke, G. S. Salvesen, and V. M. Dixit 1996. Molecular ordering of apoptotic mammalian CED-3/ICE-like proteases. J. Biol. Chem. 271: 20977–20980.
   PubMedGoogle Scholar
• Park, D. S., L. Stefanis, C. Y. I. Yan, S. E. Farinelli, and L. A. Greene 1996. Ordering the cell death pathway. Differential effects of Bcl2, an interleukin-1β-converting enzyme family protease inhibitor, and other survival agents of JNK activation in serum/nerve growth factor-deprived PC12 cells. J. Biol. Chem. 271: 21898–21905.
   PubMed Web of Science ®Google Scholar
• Pickup, D. J., B. S. Ink, W. Hu, C. A. Ray, and W. K. Joklik 1986. Hemorrhage in lesions caused by cowpox virus is induced by a viral protein that is related to plasma protein inhibitors of serine proteases. Proc. Natl. Acad. Sci. USA 83: 7698–7702.
   PubMedGoogle Scholar
• Rudel, T., and G. M. Bokoch 1997. Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276: 1571–1574.
   PubMed Web of Science ®Google Scholar
• Schlesinger, T. Unpublished observations.
   Google Scholar
• Siow, Y. L., G. B. Kalmar, J. S. Sanghera, T. Tai, S. S. Oh, and S. L. Pelech 1997. Identification of two essential phosphorylated threonine residues in the catalytic domain of Mekk1. Indirect activation by Pak3 and protein kinase C. J. Biol. Chem. 272: 7586–7594.
   PubMedGoogle Scholar
• Smith, A., F. Ramos-Morales, A. Ashworth, and M. Collins 1997. A role for JNK/SAPK in proliferation, but not apoptosis, of IL-3-dependent cells. Curr. Biol. 7: 893–896.
   PubMedGoogle Scholar
• Sumimoto, S.-I., T. Heike, S.-I. Kanazashi, N. Shintaku, E.-Y. Jung, D. Hata, K. Katamura, and M. Mayumi 1994. Involvement of LFA-1/intracellular adhesion molecule-1-dependent cell adhesion in CD40-mediated inhibition of human B lymphoma cell death induced by surface IgM crosslinking. J. Immunol. 153: 2488–2496.
   PubMed Web of Science ®Google Scholar
• Toyoshima, F., T. Moriguchi, and E. Nishida 1997. Fas induces cytoplasmic apoptotic responses and activation of the MKK7-JNK/SAPK and MKK6-p38 pathways independent of CPP32-like proteases. J. Cell Biol. 139: 1005–1015.
   PubMed Web of Science ®Google Scholar
• Tsubata, T., J. Wu, and T. Honjo 1993. B-cell apoptosis induced by antigen receptor crosslinking is blocked by a T-cell signal through CD40. Nature 364: 645–648.
   PubMed Web of Science ®Google Scholar
• Verheij, M., R. Bose, X. H. Lin, B. Yao, W. D. Jarvis, S. Grant, M. J. Birrer, E. Szabo, L. I. Zon, J. M. Kyriakis, A. Haimovitz-Friedman, Z. Fuks, and R. N. Kolesnick 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380: 75–79.
   PubMed Web of Science ®Google Scholar
• Wang, X., N. G. Zelenski, J. Yang, J. Sakai, M. S. Brown, and J. L. Goldstein 1996. Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. EMBO J. 15: 1012–1020.
   PubMed Web of Science ®Google Scholar
• Widmann, C., W. Dolci, and B. Thorens 1995. Agonist-induced internalization and recycling of the glucagon-like peptide-1 receptor in transfected fibroblasts and in insulinomas. Biochem. J. 310: 203–214.
   PubMedGoogle Scholar
• Widmann, C., P. Gerwins, N. Lassignal Johnson, and G. L. Johnson. MEKK1 and MEKK4 activate CPP32-like caspases, but differ in their ability to induce apoptosis. Submitted for publication.
   Google Scholar
• Widmann, C., N. Lassignal Johnson, A. M. Gardner, R. J. Smith, and G. L. Johnson 1997. Potentiation of apoptosis by low dose stress stimuli in cells expressing activated MEK kinase 1. Oncogene 15: 2439–2447.
   PubMed Web of Science ®Google Scholar
• Xia, Z., M. Dickens, J. Raingeaud, R. J. Davis, and M. E. Greenberg 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326–1331.
   PubMed Web of Science ®Google Scholar
• Xu, S., D. J. Robbins, L. B. Christerson, J. M. English, C. A. Vanderbilt, and M. H. Cobb 1996. Cloning of rat MEK kinase 1 cDNA reveals an endogenous membrane-associated 195-kDa protein with a large regulatory domain. Proc. Natl. Acad. Sci. USA 93: 5291–5295.
   PubMedGoogle Scholar
• Yang, X., R. Khosravi-Far, H. Y. Chang, and D. Baltimore 1997. Daax, a novel Fas-binding protein that activates JNK and apoptosis. Cell 89: 1067–1076.
   PubMed Web of Science ®Google Scholar
• Zha, J., H. Harada, E. Yang, J. Jockel, and S. J. Korsmeyer 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not Bcl-XL. Cell 87: 619–628.
   PubMed Web of Science ®Google Scholar
• Zhou, Q., S. Snipas, K. Orth, M. Muzio, V. M. Dixit, and G. S. Salvesen 1997. Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J. Biol. Chem. 272: 7797–7800.
   PubMedGoogle Scholar