A wound-induced keratin inhibits Src activity during keratinocyte migration and tissue repair

Journal of Cell Biology

Volumn 197, Issue 3, 2012, Pages 381-389

  Rotty, Jeremy D ^a,b   Coulombe, Pierre A ^a,b  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; CYTOKERATIN 6; KERATIN; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE; RECOMBINANT PROTEIN; STEROID RECEPTOR COACTIVATOR KINASE; UNCLASSIFIED DRUG; DETERGENT; KRT1 17 PROTEIN, MOUSE; KRT1-17 PROTEIN, MOUSE; OCTOXINOL; PROTEIN KINASE P60;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TISSUE REPAIR; WOUND; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE; CELL MOTION; CYTOLOGY; DRUG ANTAGONISM; EPIDERMIS; GENETICS; IMMUNOPRECIPITATION; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY; SKIN; WESTERN BLOTTING; WOUND HEALING;

ANIMALS; BLOTTING, WESTERN; CELL MOVEMENT; CELLS, CULTURED; DETERGENTS; EPIDERMIS; IMMUNOPRECIPITATION; KERATIN-6; KERATINOCYTES; KERATINS; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OCTOXYNOL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS PP60(C-SRC); SKIN; WOUND HEALING;

EID: 84862627407     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201107078     Document Type: Article

References (61)

1. Altun-Gultekin, Z.F., and J.A. Wagner. 1996. Src, ras, and rac mediate the migratory response elicited by NGF and PMA in PC12 cells. J. Neurosci. Res. 44: 308-327. http://dx.doi.org/10.1002/(SICI)1097-4547(19960515)44:4< 308::AID-JNR2>3.0.CO;2-G
2. Ayli, E.E., W. Li, T.T. Brown, A. Witkiewicz, R. Elenitsas, and J.T. Seykora. 2008. Activation of Src-family tyrosine kinases in hyperproliferative epidermal disorders. J. Cutan. Pathol. 35:273-277. http://dx.doi.org/10.1111/j.1600-0560.2007.00807.x
3. Behrens, J., L. Vakaet, R. Friis, E. Winterhager, F. Van Roy, M.M. Mareel, and W. Birchmeier. 1993. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/betacatenin complex in cells transformed with a temperature-sensitive v-SRC gene. J. Cell Biol. 120:757-766. http://dx.doi.org/10.1083/jcb.120.3.757
4. Berg, K.D., R.M. Tamas, A. Riemann, L.L. Niels-Christiansen, G.H. Hansen, and E. Michael Danielsen. 2009. Caveolae in fibroblast-like synoviocytes: Static structures associated with vimentin-based intermediate filaments. Histochem. Cell Biol. 131:103-114. http://dx.doi.org/10.1007/s00418-008-0475-y
5. Bernot, K.M., P.A. Coulombe, and K.M. McGowan. 2002. Keratin 16 expression defines a subset of epithelial cells during skin morphogenesis and the hair cycle. J. Invest. Dermatol. 119:1137-1149. http://dx.doi.org/10.1046/j.1523-1747.2002.19518.x
6. Bernot, K.M., P.A. Coulombe, and P. Wong. 2004. Skin: An ideal model system to study keratin genes and proteins. Methods Cell Biol. 78:453-487. http://dx.doi.org/10.1016/S0091-679X(04)78016-4
7. Bernot, K.M., C.H. Lee, and P.A. Coulombe. 2005. A small surface hydrophobic stripe in the coiled-coil domain of type I keratins mediates tetramer stability. J. Cell Biol. 168:965-974. http://dx.doi.org/10.1083/jcb.200408116
8. Bild, A.H., G. Yao, J.T. Chang, Q. Wang, A. Potti, D. Chasse, M.B. Joshi, D. Harpole, J.M. Lancaster, A. Berchuck, et al. 2006. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature. 439:353-357. http://dx.doi.org/10.1038/nature04296
9. Brennan, D., S. Peltonen, A. Dowling, W. Medhat, K.J. Green, J.K. Wahl III, F. Del Galdo, and M.G. Mahoney. 2011. A role for caveolin-1 in desmoglein binding and desmosome dynamics. Oncogene.
10. Caruso, J.A., and P.M. Stemmer. 2011. Proteomic profiling of lipid rafts in a human breast cancer model of tumorigenic progression. Clin. Exp. Metastasis. 28:529-540. http://dx.doi.org/10.1007/s10585-011-9389-5
11. Cooper, J.A., K.L. Gould, C.A. Cartwright, and T. Hunter. 1986. Tyr527 is phosphorylated in pp60c-src: Implications for regulation. Science. 231:1431-1434. http://dx.doi.org/10.1126/science.2420005
12. Coulombe, P.A., and P. Wong. 2004. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat. Cell Biol. 6:699-706. http://dx.doi.org/10.1038/ncb0804-699
13. Dauer, D.J., B. Ferraro, L. Song, B. Yu, L. Mora, R. Buettner, S. Enkemann, R. Jove, and E.B. Haura. 2005. Stat3 regulates genes common to both wound healing and cancer. Oncogene. 24:3397-3408. http://dx.doi.org/10.1038/sj.onc.1208469
14. Delva, E., J.M. Jennings, C.C. Calkins, M.D. Kottke, V. Faundez, and A.P. Kowalczyk. 2008. Pemphigus vulgaris IgG-induced desmoglein-3 endocytosis and desmosomal disassembly are mediated by a clathrinand dynamin-independent mechanism. J. Biol. Chem. 283:18303-18313. http://dx.doi.org/10.1074/jbc.M710046200
15. DePianto, D., M.L. Kerns, A.A. Dlugosz, and P.A. Coulombe. 2010. Keratin 17 promotes epithelial proliferation and tumor growth by polarizing the immune response in skin. Nat. Genet. 42:910-914. http://dx.doi.org/10.1038/ng.665
16. Djalilian, A.R., D. McGaughey, S. Patel, E.Y. Seo, C. Yang, J. Cheng, M. Tomic, S. Sinha, A. Ishida-Yamamoto, and J.A. Segre. 2006. Connexin 26 regulates epidermal barrier and wound remodeling and promotes psoriasiform response. J. Clin. Invest. 116:1243-1253. http://dx.doi.org/10.1172/JCI27186
17. Dvorak, H.F. 1986. Tumors: Wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315:1650-1659. http://dx.doi.org/10.1056/NEJM198612253152606
18. Fincham, V.J., and M.C. Frame. 1998. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J. 17:81-92. http://dx.doi.org/10.1093/emboj/17.1.81
19. Frame, M.C., V.J. Fincham, N.O. Carragher, and J.A. Wyke. 2002. v-Src's hold over actin and cell adhesions. Nat. Rev. Mol. Cell Biol. 3:233-245. http://dx.doi.org/10.1038/nrm779
20. Gao, C.Y., M.A. Stepp, R. Fariss, and P. Zelenka. 2004. Cdk5 regulates activation and localization of Src during corneal epithelial wound closure. J. Cell Sci. 117:4089-4098. http://dx.doi.org/10.1242/jcs.01271
21. Gaudry, C.A., H.L. Palka, R.L. Dusek, A.C. Huen, M.J. Khandekar, L.G. Hudson, and K.J. Green. 2001. Tyrosine-phosphorylated plakoglobin is associated with desmogleins but not desmoplakin after epidermal growth factor receptor activation. J. Biol. Chem. 276:24871-24880. http://dx.doi.org/10.1074/jbc.M102731200
22. Geisbrecht, B.V., S. Bouyain, and M. Pop. 2006. An optimized system for expression and purification of secreted bacterial proteins. Protein Expr. Purif. 46:23-32. http://dx.doi.org/10.1016/j.pep.2005.09.003
23. Goto, M., H. Sumiyoshi, T. Sakai, R. Fässler, S. Ohashi, E. Adachi, H. Yoshioka, and S. Fujiwara. 2006. Elimination of epiplakin by gene targeting results in acceleration of keratinocyte migration in mice. Mol. Cell. Biol. 26: 548-558. http://dx.doi.org/10.1128/MCB.26.2.548-558.2006
24. Guarino, M. 2010. Src signaling in cancer invasion. J. Cell. Physiol. 223: 14-26.
25. Hall, C.L., L.A. Lange, D.A. Prober, S. Zhang, and E.A. Turley. 1996. pp60(c-src) is required for cell locomotion regulated by the hyaluronanreceptor RHAMM. Oncogene. 13:2213-2224.
26. Hanke, J.H., J.P. Gardner, R.L. Dow, P.S. Changelian, W.H. Brissette, E.J. Weringer, B.A. Pollok, and P.A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271:695-701. http://dx.doi.org/10.1074/jbc.271.2.695
27. Kasper, M., V. Jaks, A. Are, A. Bergström, A. Schwäger, N. Barker, and R. Toftgård. 2011. Wounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytes. Proc. Natl. Acad. Sci. USA. 108:4099-4104. http://dx.doi.org/10.1073/pnas.1014489108
28. Kawabuchi, M., Y. Satomi, T. Takao, Y. Shimonishi, S. Nada, K. Nagai, A. Tarakhovsky, and M. Okada. 2000. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature. 404:999-1003. http://dx.doi.org/10.1038/35010121
29. Kerns, M.L., D. DePianto, A.T. Dinkova-Kostova, P. Talalay, and P.A. Coulombe. 2007. Reprogramming of keratin biosynthesis by sulforaphane restores skin integrity in epidermolysis bullosa simplex. Proc. Natl. Acad. Sci. USA. 104:14460-14465. http://dx.doi.org/10.1073/pnas.0706486104
30. Kim, S., P. Wong, and P.A. Coulombe. 2006. A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature. 441:362-365. http://dx.doi.org/10.1038/nature04659
31. Kim, S., J. Kellner, C.H. Lee, and P.A. Coulombe. 2007. Interaction between the keratin cytoskeleton and eEF1Bgamma affects protein synthesis in epithelial cells. Nat. Struct. Mol. Biol. 14:982-983. http://dx.doi.org/10.1038/nsmb1301
32. Larcher, F., C. Bauluz, M. Díaz-Guerra, M. Quintanilla, C.J. Conti, C. Ballestín, and J.L. Jorcano. 1992. Aberrant expression of the simple epithelial type II keratin 8 by mouse skin carcinomas but not papillomas. Mol. Carcinog. 6:112-121. http://dx.doi.org/10.1002/mc.2940060206
33. Lee, C.H., and P.A. Coulombe. 2009. Self-organization of keratin intermediate filaments into cross-linked networks. J. Cell Biol. 186:409-421. http://dx.doi.org/10.1083/jcb.200810196
34. Lloyd, C., Q.C. Yu, J. Cheng, K. Turksen, L. Degenstein, E. Hutton, and E. Fuchs. 1995. The basal keratin network of stratified squamous epithelia: Defining K15 function in the absence of K14. J. Cell Biol. 129:1329-1344. http://dx.doi.org/10.1083/jcb.129.5.1329
35. Mansbridge, J.N., and A.M. Knapp. 1987. Changes in keratinocyte maturation during wound healing. J. Invest. Dermatol. 89:253-263. http://dx.doi.org/10.1111/1523-1747.ep12471216
36. Martin, P. 1997. Wound healing-aiming for perfect skin regeneration. Science. 276:75-81. http://dx.doi.org/10.1126/science.276.5309.75
37. Mazzalupo, S., M.J. Wawersik, and P.A. Coulombe. 2002. An ex vivo assay to assess the potential of skin keratinocytes for wound epithelialization. J. Invest. Dermatol. 118:866-870. http://dx.doi.org/10.1046/j.1523-1747.2002.01736.x
38. McGowan, K.M., and P.A. Coulombe. 1998. Onset of keratin 17 expression coincides with the definition of major epithelial lineages during skin development. J. Cell Biol. 143:469-486. http://dx.doi.org/10.1083/jcb.143.2.469
39. McGowan, K.M., X. Tong, E. Colucci-Guyon, F. Langa, C. Babinet, and P.A. Coulombe. 2002. Keratin 17 null mice exhibit age- and strain-dependent alopecia. Genes Dev. 16:1412-1422. http://dx.doi.org/10.1101/gad.979502
40. Miravet, S., J. Piedra, J. Castaño, I. Raurell, C. Francí, M. Duñach, and A. García de Herreros. 2003. Tyrosine phosphorylation of plakoglobin causes contrary effects on its association with desmosomes and adherens junction components and modulates beta-catenin-mediated transcription. Mol. Cell. Biol. 23:7391-7402. http://dx.doi.org/10.1128/MCB.23.20.7391-7402.2003
41. Moll, R., R. Krepler, and W.W. Franke. 1983. Complex cytokeratin polypeptide patterns observed in certain human carcinomas. Differentiation. 23:256-269. http://dx.doi.org/10.1111/j.1432-0436.1982.tb01291.x
42. Oneyama, C., T. Hikita, K. Enya, M.W. Dobenecker, K. Saito, S. Nada, A. Tarakhovsky, and M. Okada. 2008. The lipid raft-anchored adaptor protein Cbp controls the oncogenic potential of c-Src. Mol. Cell. 30:426-436. http://dx.doi.org/10.1016/j.molcel.2008.03.026
43. Osmanagic-Myers, S., and G. Wiche. 2004. Plectin-RACK1 (receptor for activated C kinase 1) scaffolding: A novel mechanism to regulate protein kinase C activity. J. Biol. Chem. 279:18701-18710. http://dx.doi.org/10.1074/jbc.M312382200
44. Osmanagic-Myers, S., M. Gregor, G. Walko, G. Burgstaller, S. Reipert, and G. Wiche. 2006. Plectin-controlled keratin cytoarchitecture affects MAP kinases involved in cellular stress response and migration. J. Cell Biol. 174:557-568. http://dx.doi.org/10.1083/jcb.200605172
45. Paladini, R.D., K. Takahashi, N.S. Bravo, and P.A. Coulombe. 1996. Onset of re-epithelialization after skin injury correlates with a reorganization of keratin filaments in wound edge keratinocytes: Defining a potential role for keratin 16. J. Cell Biol. 132:381-397. http://dx.doi.org/10.1083/jcb.132.3.381
46. Rouabhia, M., L. Germain, F. Bélanger, R. Guignard, and F.A. Auger. 1992. Optimization of murine keratinocyte culture for the production of graftable epidermal sheets. J. Dermatol. 19:325-334.
47. Seeliger, M.A., M. Young, M.N. Henderson, P. Pellicena, D.S. King, A.M. Falick, and J. Kuriyan. 2005. High yield bacterial expression of active c-Abl and c-Src tyrosine kinases. Protein Sci. 14:3135-3139. http://dx.doi.org/10.1110/ps.051750905
48. South, A.P., H. Wan, M.G. Stone, P.J. Dopping-Hepenstal, P.E. Purkis, J.F. Marshall, I.M. Leigh, R.A. Eady, I.R. Hart, and J.A. McGrath. 2003. Lack of plakophilin 1 increases keratinocyte migration and reduces desmosome stability. J. Cell Sci. 116:3303-3314. http://dx.doi.org/10.1242/jcs.00636
49. Stefansson, I.M., H.B. Salvesen, and L.A. Akslen. 2006. Loss of p63 and cytokeratin 5/6 expression is associated with more aggressive tumors in endometrial carcinoma patients. Int. J. Cancer. 118:1227-1233. http://dx.doi.org/10.1002/ijc.21415
50. Strickland, J.E., D.A. Greenhalgh, A. Koceva-Chyla, H. Hennings, C. Restrepo, M. Balaschak, and S.H. Yuspa. 1988. Development of murine epidermal cell lines which contain an activated rasHa oncogene and form papillomas in skin grafts on athymic nude mouse hosts. Cancer Res. 48: 165-169.
51. Tachibana, H., Y. Inoue, T. Kanehisa, and Y. Fukami. 1988. Local similarity in the amino acid sequence between the non-catalytic region of Rous sarcoma virus oncogene product p60v-src and intermediate filament proteins. J. Biochem. 104:869-872.
52. Takahashi, K., J. Folmer, and P.A. Coulombe. 1994. Increased expression of keratin 16 causes anomalies in cytoarchitecture and keratinization in transgenic mouse skin. J. Cell Biol. 127:505-520. http://dx.doi.org/10.1083/jcb.127.2.505
53. Takahashi, K., B. Yan, K. Yamanishi, S. Imamura, and P.A. Coulombe. 1998. The two functional keratin 6 genes of mouse are differentially regulated and evolved independently from their human orthologs. Genomics. 53:170-183. http://dx.doi.org/10.1006/geno.1998.5476
54. Todorović, V., B.V. Desai, M.J. Patterson, E.V. Amargo, A.D. Dubash, T. Yin, J.C. Jones, and K.J. Green. 2010. Plakoglobin regulates cell motility through Rho- and fibronectin-dependent Src signaling. J. Cell Sci. 123:3576-3586. http://dx.doi.org/10.1242/jcs.070391
55. Tong, X., and P.A. Coulombe. 2006. Keratin 17 modulates hair follicle cycling in a TNFalpha-dependent fashion. Genes Dev. 20:1353-1364. http://dx.doi.org/10.1101/gad.1387406
56. Wong, P., and P.A. Coulombe. 2003. Loss of keratin 6 (K6) proteins reveals a function for intermediate filaments during wound repair. J. Cell Biol. 163:327-337. http://dx.doi.org/10.1083/jcb.200305032
57. Wong, P., E. Colucci-Guyon, K. Takahashi, C. Gu, C. Babinet, and P.A. Coulombe. 2000. Introducing a null mutation in the mouse K6α and K6β genes reveals their essential structural role in the oral mucosa. J. Cell Biol. 150:921-928. http://dx.doi.org/10.1083/jcb.150.4.921
58. Wong, S.Y., and J.F. Reiter. 2011. Wounding mobilizes hair follicle stem cells to form tumors. Proc. Natl. Acad. Sci. USA. 108:4093-4098. http://dx.doi.org/10.1073/pnas.1013098108
59. Xian, W., M.P. Rosenberg, and J. DiGiovanni. 1997. Activation of erbB2 and c-src in phorbol ester-treated mouse epidermis: Possible role in mouse skin tumor promotion. Oncogene. 14:1435-1444. http://dx.doi.org/10.1038/sj.onc.1200980
60. Xu, W., S.C. Harrison, and M.J. Eck. 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 385:595-602. http://dx.doi.org/10.1038/385595a0
61. Yin, T., S. Getsios, R. Caldelari, A.P. Kowalczyk, E.J. Müller, J.C. Jones, and K.J. Green. 2005. Plakoglobin suppresses keratinocyte motility through both cell-cell adhesion-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. USA. 102:5420-5425. http://dx.doi.org/10.1073/pnas.0501676102