A role for MEK kinase 1 in TGF-β/activin-induced epithelium movement and embryonic eyelid closure

EMBO Journal

Volumn 22, Issue 17, 2003, Pages 4443-4454

  Zhang, Lin ^a   Wang, Wei ^a   Hayashi, Yasuhito ^a   Jester, James V ^b   Birk, David E ^c   Gao, Min ^d   Liu, Chia Yang ^e   Kao, Winston W Y ^a   Karin, Michael ^d   Xia, Ying ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Actin stress fiber; Activin signaling; Embryonic eyelid closure; Epithelial cell migration; MEKK1 JNK pathway; TGF

Indexed keywords

ACTIN; ACTIVIN; F ACTIN; MEK KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE; SMAD4 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CONTACT; CELL CULTURE; CELL MIGRATION; CELL MOTION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; EPITHELIUM; EYELID; EYELID CLOSURE; FETUS; GENETIC CONSERVATION; KERATINOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN POLYMORPHISM; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STRESS FIBER;

ACTINS; ACTIVINS; ANIMALS; BASE SEQUENCE; CELL MOVEMENT; DNA; DROSOPHILA; ENZYME ACTIVATION; EPITHELIUM; EVOLUTION; EYELIDS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KERATINOCYTES; MAP KINASE KINASE KINASE 1; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MAMMALIA;

EID: 0042237016     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg440     Document Type: Article

References (41)

1. Ashrafi, S.H., Atassi, B., Erickson, R. and Sabet, T. (1993) Migration of epithelium during phenytoin-dependent gingival overgrowth in mice. Scanning Microsc., 7, 1247-1253.
2. Bakin, A.V., Tomlinson, A.K., Bhowmick, N.A., Moses, H.L. and Arteaga, C.L. (2000) Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J. Biol. Chem., 275, 36803-36810.
3. Beck, P.L., Rosenberg, I.M., Xavier, R.J., Koh, T., Wong, J.F. and Podolsky, D.K. (2003) transforming growth factor-beta mediates intestinal healing and susceptibility to injury in vitro and in vivo through epithelial cells. Am. J. Pathol., 162, 597-608.
4. Berkowitz, E.A. et al. (1996) Characterization of the mouse transforming growth factor alpha gene: its expression during eyelid development and in waved 1 tissues. Cell Growth Differ., 7, 1271-1282.
5. Birk, D.E. and Mayne, R. (1997) Localization of collagen types I, III and V during tendon development. Changes in collagen types I and III are correlated with changes in fibril diameter. Eur. J. Cell Biol., 72, 352-361.
6. Christerson, L.B., Gallagher, E., Vanderbilt, C.A., Whitehurst, A.W., Wells, C., Kazempour, R., Sternweis, P.C. and Cobb, M.H. (2002) p115 Rho GTPase activating protein interacts with MEKK1. J. Cell Physiol., 192, 200-208.
7. Davis, R.J. (2000) Signal transduction by the JNK group of MAP kinases. Cell, 103, 239-252.
8. Findlater, G.S., McDougall, R.D. and Kaufman, M.H. (1993) Eyelid development, fusion and subsequent reopening in the mouse. J. Anat., 183, 121-129.
9. Gibson, E.M., Henson, E.S., Villanueva, J. and Gibson, S.B. (2002) MEK kinase 1 induces mitochondrial permeability transition leading to apoptosis independent of cytochrome c release. J. Biol. Chem., 277, 10573-10580.
10. Glise, B. and Noselli, S. (1997) Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev., 11, 1738-1747.
11. Han, Z., Boyle, D.L., Chang, L., Bennett, B., Karin, M., Yang, L., Manning, A.M. and Firestein, G.S. (2001) c-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J. Clin. Invest, 108, 73-81.
12. Harris, M.J. and Juriloff, D.M. (1986) Eyelid development and fusion induced by cortisone treatment in mutant, lidgap-Miller, fetal mice. A scanning electron microscope study. J. Embryol. Exp. Morphol., 91, 1-18.
13. Henkemeyer, M., Orioli, D., Henderson, J.T., Saxton, T.M., Roder, J., Pawson, T. and Klein, R. (1996) Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell, 86, 35-46.
14. Hibi, M., Lin, A., Smeal, T., Minden, A. and Karin, M. (1993) Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev., 7, 2135-2148.
15. Hocevar, B.A., Brown, T.L. and Howe, P.H. (1999) TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J., 18, 1345-1356.
16. Jacinto, A., Woolner, S. and Martin, P. (2002) Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev. Cell, 3, 9-19.
17. Karin, M. (1996) The regulation of AP-1 activity by mitogen-activated protein kinases. Phil. Trans. R. Soc. Lond. B Biol. Sci., 351, 127-134.
18. Kim, K.Y., Jeong, S.Y., Won, J., Ryu, P.D. and Nam, M.J. (2001) Induction of angiogenesis by expression of soluble type II transforming growth factor-beta receptor in mouse hepatoma. J. Biol. Chem., 276, 38781-38786.
19. Kuan, C.Y., Yang, D.D., Samanta Roy, D.R., Davis, R.J., Rakic, P. and Flavell, R.A. (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron, 22, 667-676.
20. Kultz, D., Madhany, S. and Burg, M.B. (1998) Hyperosmolality causes growth arrest of murine kidney cells. Induction of GADD45 and GADD153 by osmosensing via stress-activated protein kinase 2. J. Biol. Chem., 273, 13645-13651.
21. Li, G., Gustafson-Brown, C., Hanks, S.K., Nason, K., Arbeit, J.M., Pogliano, K., Wisdom, R.M. and Johnson, R.S. (2003) c-Jun is essential for organization of the epidermal leading edge. Dev. Cell, 4, 865-877.
22. 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.
23. Liu, C.Y., Zhu, G., Westerhausen-Larson, A., Converse, R., Kao, C.W., Sun, T.T. and Kao, W.W. (1993) Cornea-specific expression of K12 keratin during mouse development. Curr. Eye Res., 12, 963-974.
24. Minamino, T., Yujiri, T., Terada, N., Taffet, G.E., Michael, L.H., Johnson, G.L. and Schneider, M.D. (2002) MEKK1 is essential for cardiac hypertrophy and dysfunction induced by Gq. Proc. Natl Acad. Sci. USA, 99, 3866-3871.
25. Morrison, S.J., White, P.M., Zock, C., and Anderson, D.J. (1999) Prospective identification, isolation by flow cytometry and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell, 96, 737-749.
26. Nobes, C.D. and Hall, A. (1999) Rho GTPases control polarity, protrusion and adhesion during cell movement. J. Cell Biol., 144, 1235-1244.
27. Petroll, W.M., Ma, L., Jester, J.V., Cavanagh, H.D. and Bean, J. (2001) Organization of junctional proteins in proliferating cat corneal endothelium during wound healing. Cornea, 20, 73-80.
28. Rouabhia, M., Germain, L., Belanger, F., Guignard, R. and Auger, F.A. (1992) Optimization of murine keratinocyte culture for the production of graftable epidermal sheets. J. Dermatol., 19, 325-334.
29. Sluss, H.K., and Davis, R.J. (1997) Embryonic morphogenesis signaling pathway mediated by JNK targets the transcripfion factor JUN and the TGF-beta homologue Decapentaplegic. J. Cell. Biochem., 67, 1-12.
30. Sluss, H.K., Han, Z., Barrett, T., Davis, R.J. and Ip, Y.T. (1996) A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev., 10, 2745-2758.
31. Tao, L., Wadsworth, S., Mercer, J., Mueller, C., Lynn, K., Siekierka, J. and August, A. (2002) Opposing roles of serine/threonine kinases MEKK1 and LOK in regulating the CD28 responsive element in T-cells. Biochem. J., 363, 175-182.
32. 2-terminal kinase). Eur. J. Biochem., 244, 587-595.
33. Vassalli, A., Matzuk, M.M., Gardner, H.A., Lee, K.F. and Jaenisch, R. (1994). Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev., 8, 414-427.
34. Vuong, H., Patterson, T., Shapiro, P., Kalvakolanu, D.V., Wu, R., Ma, W.Y., Dong, Z., Kleeberger, S.R. and Reddy, S.P. (2000). Phorbol ester-induced expression of airway squamous cell differentiation marker, SPRR1B, is regulated by protein kinase Cdelta/Ras/MEKK1/MKK1-dependent/AP-1 signal transduction pathway. J. Biol. Chem., 275, 32250-32259.
35. Wu, Z., Wu, J., Jacinto, E. and Karin, M. (1997). Molecular cloning and characterization of human JNKK2, a novel Jun NH2-terminal kinase-specific kinase. Mol. Cell. Biol., 17, 7407-7416.
36. Xia, Y., Wu, Z., Su, B., Murray, B. and Karin, M. (1998). JNKK1 organizes a MAP kinase module through specific and sequential interactions with upstream and downstream components mediated by its amino-terminal extension. Genes Dev., 12, 3369-3381.
37. Xia, Y., Makris, C., Su, B., Li, E., Yang, J., Nemerow, G.R. and Karin, M. (2000). MEK kinase 1 is critically required for c-Jun N-terminal kinase activation by proinflammatory stimuli and growth factor-induced cell migration. Proc. Natl Acad. Sci. USA, 97, 5243-5248.
38. Yan, M., Dai, T., Deak, J.C., Kyriakis, J.M., Zon, L.I., Woodgett, J.R. and Templeton, D.J. (1994). Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1. Nature, 372, 798-800.
39. 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.
40. Yujiri, T. et al. (2000). MEK kinase 1 gene disruption alters cell migration and c-Jun NH2-terminal kinase regulation but does not cause a measurable defect in NF-kappa B activation. Proc. Natl Acad. Sci. USA, 97, 7272-7277.
41. Zenz, R., Scheuch, H., Martin, P., Frank, C., Eferl, R., Kenner, L., Sibilia, M. and Wagner, E.F. (2003). c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev. Cell, 4, 879-889.