A role for the mitogen-activated protein kinase kinase kinase 1 in epithelial wound healing

Molecular Biology of the Cell

Volumn 17, Issue 8, 2006, Pages 3446-3455

  Deng, Maoxian ^a   Chen, Wei Li ^a,b   Takatori, Atsushi ^a   Peng, Zhimin ^a   Zhang, Lin ^a,c   Mongan, Maureen ^a   Parthasarathy, Ranjani ^a   Sartor, Maureen ^a   Miller, Marian ^a   Yang, Jianhua ^d   Su, Bing ^d   Kao, Winston W Y ^a   Xia, Ying ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MYELOPID; NEUTRALIZING ANTIBODY; PLASMINOGEN ACTIVATOR INHIBITOR 1; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CELL MIGRATION; CONTROLLED STUDY; CORNEA INJURY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; EPIDERMIS; EPITHELIUM; EPITHELIZATION; EXTRACELLULAR MATRIX; EYELID; FETUS DEVELOPMENT; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMAN; HUMAN CELL; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN INJURY; WOUND CLOSURE; WOUND HEALING;

ACTIVINS; ANIMALS; ANIMALS, NEWBORN; CELL MOVEMENT; CORNEA; ENZYME ACTIVATION; EPIDERMIS; EPITHELIAL CELLS; EPITHELIUM; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KERATINOCYTES; MAP KINASE KINASE KINASE 1; MICE; MICE, INBRED C57BL; SKIN; WOUND HEALING;

EID: 33746652899     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-02-0102     Document Type: Article

References (40)

1. Albo, D., Berger, D. H., Vogel, J., and Tuszynski, G. P. (1999). Thrombospondin-1 and transforming growth factor beta-1 upregulate plasminogen activator inhibitor type 1 in pancreatic cancer. J. Gastrointest. Surg. 3, 411-417.
2. Ashcroft, G. S., et al. (1999). Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1, 260-266.
3. Bamberger, C., Scharer, A., Antsiferova, M., Tychsen, B., Pankow, S., Muller, M., Rulicke, T., Paus, R., and Werner, S. (2005). Activin controls skin morphogenesis and wound repair predominantly via stromal cells and in a concentration-dependent manner via keratinocytes. Am. J. Pathol. 167, 733-747.
4. Bosch, M., Serras, F., Martin-Blanco, E., and Baguna, J. (2005). JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev. Biol. 280, 73-86.
5. Chan, J. C., Duszczyszyn, D. A., Castellino, F. J., and Ploplis, V. A. (2001). Accelerated skin wound healing in plasminogen activator inhibitor-1-deficient mice. Am. J. Pathol. 159, 1681-1688.
6. Chen, C. C., Mo, F. E., and Lau, L. F. (2001a). The angiogenic factor Cyr61 activates a genetic program for wound healing in human skin fibroblasts. J. Biol. Chem. 276, 47329-47337.
7. Chen, N., Nomura, M., She, Q. B., Ma, W. Y., Bode, A. M., Wang, L., Flavell, R. A., and Dong, Z. (2001b). Suppression of skin tumorigenesis in c-Jun NH(2)-terminal kinase-2-deficient mice. Cancer Res. 61, 3908-3912.
8. Chiquet-Ehrismann, R. (1995). Tenascins, a growing family of extracellular matrix proteins. Experientia 51, 853-862.
9. Dallas, S. L., Rosser, J. L., Mundy, G. R., and Bonewald, L. F. (2002). Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J. Biol. Chem. 277, 21352-21360.
10. Dawson, R. A., Goberdhan, N. J., Freedlander, E., and MacNeil, S. (1996). Influence of extracellular matrix proteins on human keratinocyte attachment, proliferation and transfer to a dermal wound model. Burns 22, 93-100.
11. Dudoit, S., and Fridlyand, J. (2002). A prediction-based resampling method for estimating the number of clusters in a dataset. Genome Biol. 3, RESEARCH0036.
12. Engers, R., Springer, E., Michiels, P., Collard, J. G., and Gabbert, H. E. (2001). Rac affects invasion of human renal cell carcinomas by up-regulating tissue inhibitor of metalloproteinases (TIMP)-1 and TIMP-2 expression. J. Biol. Chem. 276, 41889-41897.
13. Feijen, A., Goumans, M. J., and van den Eijnden-van Raaij, A. J. (1994). Expression of activin subunits, activin receptors and follistatin in postimplantation mouse embryos suggests specific developmental functions for different activins. Development 120, 3621-3637.
14. 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.
15. 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.
16. Hubner, G., Hu, Q., Smola, H., and Werner, S. (1996). Strong induction of activin expression after injury suggests an important role of activin in wound repair. Dev. Biol. 173, 490-498.
17. Keeton, M. R., Curriden, S. A., van Zonneveld, A. J., and Loskutoff, D. J. (1991). Identification of regulatory sequences in the type 1 plasminogen activator inhibitor gene responsive to transforming growth factor beta. J. Biol. Chem. 266, 23048-23052.
18. Koivukangas, V., Oikarinen, A., Risteli, J., Haukipuro, K. (2005). Effect of jaundice and its resolution on wound re-epithelization, skin collagen synthesis, and serum collagen propeptide levels in patients with neoplastic pancreaticobiliary obstruction. J. Surg. Res. 124, 237-243.
19. Li, F., Goncalves, J., Faughnan, K., Steiner, M. G., Pagan-Charry, I., Esposito, D., Chin, B., Providence, K. M., Higgins, P. J., and Staiano-Coico, L. (2000). Targeted inhibition of wound-induced PAI-1 expression alters migration and differentiation in human epidermal keratinocytes. Exp. Cell Res. 258, 245-253.
20. Liang, Q., Wiese, R. J., Bueno, O. F., Dai, Y. S., Markham, B. E., and Molkentin, J. D. (2001). The transcription factor gata4 is activated by extracellular signal-regulated kinase 1- and 2-mediated phosphorylation of serine 105 in cardiomyocytes. Mol. Cell. Biol. 21, 7460-7469.
21. 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.
22. Madlener, M. (1998). Differential expression of matrix metalloproteinases and their physiological inhibitors in acute murine skin wounds. Arch. Dermatol. Res. 290 (Suppl.) S24-S29.
23. Providence, K. M., and Higgins, P. J. (2004). PAI-1 expression is required for epithelial cell migration in two distinct phases of in vitro wound repair. J. Cell Physiol. 200, 297-308.
24. Ramet, M., Lanot, R., Zachary, D., and Manfruelli, P. (2002). JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 241, 145-156.
25. Reiner, A., Yekutieli, D., and Benjamini, Y. (2003). Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19, 368-375.
26. Roth, J. J., Sung, J. J., Granick, M. S., Solomon, M. P., Longaker, M. T., Rothman, V. L., Nicosia, R. F., and Tuszynski, G. P. (1999). Thrombospondin 1 and its specific cysteine-serine-valine-threonine-cysteine-clycine receptor in fetal wounds. Ann. Plast. Surg. 42, 553-563.
27. 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.
28. Schlesinger, T. K., Fanger, G. R., Yujiri, T., and Johnson, G. L. (1998). The TAO of MEKK. Front. Biosci. 3, 1181-1186.
29. Schrewe, H., Gendron-Maguire, M., Harbison, M. L., and Gridley, T. (1994). Mice homozygous for a null mutation of activin beta B are viable and fertile. Mech. Dev. 47, 43-51.
30. Setoguchi, Y., Jaffe, H. A., Danel, C., and Crystal, R. G. (1994). Ex vivo and in vivo gene transfer to the skin using replication-deficient recombinant adenovirus vectors. J. Investig. Dermatol. 102, 415-421.
31. Uno, K., Hayashi, H., Kuroki, M., Uchida, H., Yamauchi, Y., Kuroki, M., and Oshima, K. (2004). Thrombospondin-1 accelerates wound healing of corneal epithelia. Biochem. Blophys. Res. Commun. 315, 928-934.
32. 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.
33. Wankell, M., Munz, B., Hubner, G., Hans, W., Wolf, E., Goppelt, A., and Werner, S. (2001). Impaired wound healing in transgenic mice overexpressing the activin antagonist follistatin in the epidermis. EMBO J. 20, 5361-5372.
34. Werner, S., and Grose, R. (2003). Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83, 835-870.
35. Wolfinger, R. D., Gibson, G., Wolfinger, E. D., Bennett, L., Hamadeh, H., Bushel, P., Afshari, C., and Paules, R. S. (2001). Assessing gene significance from cDNA microarray expression data via mixed models. J. Comput. Biol. 8, 625-637.
36. 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.
37. 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.
38. Yujiri, T., Ware, M., Widmann, C., Oyer, R., Russell, D., Chan, E., Zaitsu, Y., Clarke, P., Tyler, K., Oka, Y., 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.
39. Zhang, L., Deng, M., Parthasarathy, R., Wang, L., Mongan, M., Molkentin, J. D., Zheng, Y., and Xia, Y. (2005). MEKK1 transduces activin signals in keratinocytes to induce actin stress fiber formation and migration. Mol. Cell Biol. 25, 60-65.
40. Zhang, L., Wang, W., Hayashi, Y., Jester, J. V., Birk, D. E., Gao, M., Liu, C. Y., Kao, W. W., Karin, M., and Xia, Y. (2003). A role for MEK kinase 1 in TGF-beta/activin-induced epithelium movement and embryonic eyelid closure. EMBO J. 22, 4443-4454.