Transcriptional control of skin reepithelialization

Journal of Dermatological Science

Volumn 73, Issue 1, 2014, Pages 3-9

  Bellavia, Gabriella ^a   Fasanaro, Pasquale ^a   Melchionna, Roberta ^a   Capogrossi, Maurizio C ^a   Napolitano, Monica ^a  

^a LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Skin; Transcription factor; Wound healing

Indexed keywords

ANDROGEN RECEPTOR; BETA CATENIN; CCAAT ENHANCER BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; ESTROGEN RECEPTOR; GLUCOCORTICOID RECEPTOR; GRAINY HEAD 3; MYC PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PROTEIN C JUN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD7 PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR HOXA3; TRANSCRIPTION FACTOR HOXB13; TRANSCRIPTION FACTOR HOXD3; TRANSCRIPTION FACTOR JUNB; UNCLASSIFIED DRUG;

CELL MIGRATION; CELL PROLIFERATION; ENZYME ACTIVITY; EPITHELIZATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; UPREGULATION; WOUND CLOSURE; WOUND HEALING;

SKIN; TRANSCRIPTION FACTOR; WOUND HEALING;

ANIMALS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; RE-EPITHELIALIZATION; SKIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84890127742     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2013.08.007     Document Type: Review

References (68)

1. Shaw T.J., Martin P. Wound repair at a glance. J Cell Sci 2009, 122:3209-3213.
2. Kondo T., Ishida Y. Molecular pathology of wound healing. Forensic Sci Int 2010, 203:93-98.
3. Baum C.L., Arpey C.J. Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg 2005, 31:674-686. (discussion 86).
4. Bahou W.F., Gnatenko D.V. Platelet transcriptome: the application of microarray analysis to platelets. Semin Thromb Hemost 2004, 30:473-484.
5. Kim M.H., Liu W., Borjesson D.L., Curry F.R., Miller L.S., Cheung A.L., et al. Dynamics of neutrophil infiltration during cutaneous wound healing and infection using fluorescence imaging. J Invest Dermatol 2008, 128:1812-1820.
6. Schafer M., Werner S. Oxidative stress in normal and impaired wound repair. Pharmacol Res 2008, 58:165-171.
7. Reinke J.M., Sorg H. Wound repair and regeneration. Eur Surg Res 2012, 49:35-43.
8. Abe R., Donnelly S.C., Peng T., Bucala R., Metz C.N. Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol 2001, 166:7556-7562.
9. Schafer M., Werner S. Transcriptional control of wound repair. Annu Rev Cell Dev Biol 2007, 23:69-92.
10. Farnham P.J. Insights from genomic profiling of transcription factors. Nat Rev Genet 2009, 10:605-616.
11. Schiller M., Javelaud D., Mauviel A. TGF-beta-induced SMAD signaling and gene regulation: consequences for extracellular matrix remodeling and wound healing. J Dermatol Sci 2004, 35:83-92.
12. Faler B.J., Macsata R.A., Plummer D., Mishra L., Sidawy A.N. Transforming growth factor-beta and wound healing. Perspect Vasc Surg Endovasc Ther 2006, 18:55-62.
13. Ashcroft G.S., Yang X., Glick A.B., Weinstein M., Letterio J.L., Mizel D.E., et al. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1999, 1:260-266.
14. Sumiyoshi K., Nakao A., Setoguchi Y., Okumura K., Ogawa H. Exogenous Smad3 accelerates wound healing in a rabbit dermal ulcer model. J Invest Dermatol 2004, 123:229-236.
15. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev 2005, 19:2783-2810.
16. Hosokawa R., Urata M.M., Ito Y., Bringas P., Chai Y. Functional significance of Smad2 in regulating basal keratinocyte migration during wound healing. J Invest Dermatol 2005, 125:1302-1309.
17. Owens P., Engelking E., Han G., Haeger S.M., Wang X.J. Epidermal Smad4 deletion results in aberrant wound healing. Am J Pathol 2010, 176:122-133.
18. Yang L., Li W., Wang S., Wang L., Li Y., Yang X., et al. Smad4 disruption accelerates keratinocyte reepithelialization in murine cutaneous wound repair. Histochem Cell Biol 2012, 138:573-582.
19. Han G., Li F., Ten Dijke P., Wang X.J. Temporal Smad7 transgene induction in mouse epidermis accelerates skin wound healing. Am J Pathol 2011, 179:1768-1779.
20. Myster D.L., Bonnette P.C., Duronio R.J. A role for the DP subunit of the E2F transcription factor in axis determination during Drosophila oogenesis. Development 2000, 127:3249-3261.
21. D'Souza S.J., Vespa A., Murkherjee S., Maher A., Pajak A., Dagnino L. E2F-1 is essential for normal epidermal wound repair. J Biol Chem 2002, 277:10626-10632.
22. Leonard W.J., O'Shea J.J. Jaks and STATs: biological implications. Annu Rev Immunol 1998, 16:293-322.
23. Sano S., Itami S., Takeda K., Tarutani M., Yamaguchi Y., Miura H., et al. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J 1999, 18:4657-4668.
24. Melchionna R., Bellavia G., Romani M., Straino S., Germani A., di Carlo A., et al. C/EBPγ regulates wound repair and EGF receptor signaling. J Invest Dermatol 2012, 132:1908-1917.
25. Sano S., Chan K.S., di Giovanni J. Impact of Stat3 activation upon skin biology: a dichotomy of its role between homeostasis and diseases. J Dermatol Sci 2008, 50:1-14.
26. Kachgal S., Mace K.A., Boudreau N.J. The dual roles of homeobox genes in vascularization and wound healing. Cell Adh Migr 2012, 6:457-470.
27. Mace K.A., Hansen S.L., Myers C., Young D.M., Boudreau N. HOXA3 induces cell migration in endothelial and epithelial cells promoting angiogenesis and wound repair. J Cell Sci 2005, 118:2567-2577.
28. Hansen S.L., Myers C.A., Charboneau A., Young D.M., Boudreau N. HoxD3 accelerates wound healing in diabetic mice. Am J Pathol 2003, 163:2421-2431.
29. Mack J.A., Maytin E.V. Persistent inflammation and angiogenesis during wound healing in K14-directed Hoxb13 transgenic mice. J Invest Dermatol 2010, 130:856-865.
30. Mack J.A., Abramson S.R., Ben Y., Coffin J.C., Rothrock J.K., Maytin E.V., et al. Hoxb13 knockout adult skin exhibits high levels of hyaluronan and enhanced wound healing. FASEB J 2003, 17:1352-1354.
31. Ashcroft G.S., Mills S.J. Androgen receptor-mediated inhibition of cutaneous wound healing. J Clin Invest 2002, 110:615-624.
32. Toraldo G., Bhasin S., Bakhit M., Guo W., Serra C., Safer J.D., et al. Topical androgen antagonism promotes cutaneous wound healing without systemic androgen deprivation by blocking beta-catenin nuclear translocation and cross-talk with TGF-beta signaling in keratinocytes. Wound Repair Regen 2012, 20:61-73.
33. Gilliver S.C., Ruckshanthi J.P., Hardman M.J., Zeef L.A., Ashcroft G.S. 5alpha-dihydrotestosterone (DHT) retards wound closure by inhibiting re-epithelialization. J Pathol 2009, 217:73-82.
34. Ashcroft G.S., Greenwell-Wild T., Horan M.A., Wahl S.M., Ferguson M.W. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am J Pathol 1999, 155:1137-1146.
35. Campbell L., Emmerson E., Davies F., Gilliver S.C., Krust A., Chambon P., et al. Estrogen promotes cutaneous wound healing via estrogen receptor beta independent of its antiinflammatory activities. J Exp Med 2010, 207:1825-1833.
36. Ashcroft G.S., Dodsworth J., van Boxtel E., Tarnuzzer R.W., Horan M.A., Schultz G.S., et al. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat Med 1997, 3:1209-1215.
37. Gilliver S.C., Emmerson E., Campbell L., Chambon P., Hardman M.J., Ashcroft G.S. 17beta-estradiol inhibits wound healing in male mice via estrogen receptor-alpha. Am J Pathol 2010, 176:2707-2721.
38. Sanchis A., Alba L., Latorre V., Sevilla L.M., Perez P. Keratinocyte-targeted overexpression of the glucocorticoid receptor delays cutaneous wound healing. PLoS One 2012, 7:e29701.
39. Grose R., Werner S., Kessler D., Tuckermann J., Huggel K., Durka S., et al. A role for endogenous glucocorticoids in wound repair. EMBO Rep 2002, 3:575-582.
40. Michalik L., Feige J.N., Gelman L., Pedrazzini T., Keller H., Desvergne B., et al. Selective expression of a dominant-negative form of peroxisome proliferator-activated receptor in keratinocytes leads to impaired epidermal healing. Mol Endocrinol 2005, 19:2335-2348.
41. Michalik L., Desvergne B., Tan N.S., Basu-Modak S., Escher P., Rieusset J., et al. Impaired skin wound healing in peroxisome proliferator-activated receptor (PPAR)alpha and PPARbeta mutant mice. J Cell Biol 2001, 154:799-814.
42. Michalik L., Wahli W. Involvement of PPAR nuclear receptors in tissue injury and wound repair. J Clin Invest 2006, 116:598-606.
43. Michalik L., Wahli W. Peroxisome proliferator-activated receptors (PPARs) in skin health, repair and disease. Biochim Biophys Acta 2007, 1771:991-998.
44. Wang S., Samakovlis C. Grainy head and its target genes in epithelial morphogenesis and wound healing. Curr Top Dev Biol 2012, 98:35-63.
45. Mace K.A., Pearson J.C., McGinnis W. An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 2005, 308:381-385.
46. Ting S.B., Caddy J., Hislop N., Wilanowski T., Auden A., Zhao L.L., et al. A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 2005, 308:411-413.
47. Boglev Y., Wilanowski T., Caddy J., Parekh V., Auden A., Darido C., et al. The unique and cooperative roles of the Grainy head-like transcription factors in epidermal development reflect unexpected target gene specificity. Dev Biol 2011, 349:512-522.
48. Cheon S.S., Wei Q., Gurung A., Youn A., Bright T., Poon R., et al. Beta-catenin regulates wound size and mediates the effect of TGF-beta in cutaneous healing. FASEB J 2006, 20:692-701.
49. Cheon S.S., Cheah A.Y., Turley S., Nadesan P., Poon R., Clevers H., et al. Beta-catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci U S A 2002, 99:6973-6978.
50. Angel P., Szabowski A., Schorpp-Kistner M. Function and regulation of AP-1 subunits in skin physiology and pathology. Oncogene 2001, 20:2413-2423.
51. Li G., Gustafson-Brown C., Hanks S.K., Nason K., Arbeit J.M., Pogliano K., et al. c-Jun is essential for organization of the epidermal leading edge. Dev Cell 2003, 4:865-877.
52. Zenz R., Scheuch H., Martin P., Frank C., Eferl R., Kenner L., et al. c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev Cell 2003, 4:879-889.
53. Giles N., Rea S., Beer T., Wood F.M., Fear M.W. A peptide inhibitor of c-Jun promotes wound healing in a mouse full-thickness burn model. Wound Repair Regen 2008, 16:58-64.
54. Florin L., Knebel J., Zigrino P., Vonderstrass B., Mauch C., Schorpp-Kistner M., et al. Delayed wound healing and epidermal hyperproliferation in mice lacking JunB in the skin. J Invest Dermatol 2006, 126:902-911.
55. Yates S., Rayner T.E. Transcription factor activation in response to cutaneous injury: role of AP-1 in reepithelialization. Wound Repair Regen 2002, 10:5-15.
56. Ramet M., Lanot R., Zachary D., Manfruelli P. JNK signaling pathway is required for efficient wound healing in Drosophila. Dev Biol 2002, 241:145-156.
57. Zanet J., Pibre S., Jacquet C., Ramirez A., de Alborán I.M., Gandarillas A. Endogenous Myc controls mammalian epidermal cell size, hyperproliferation, endoreplication and stem cell amplification. J Cell Sci 2005, 118:1693-1704.
58. Waikel R.L., Kawachi Y., Waikel P.A., Wang X.J., Roop D.R. Deregulated expression of c-Myc depletes epidermal stem cells. Nat Genet 2001 June, 28:165-168.
59. Bryant M., Drew G.M., Houston P., Hissey P., Campbell C.J., Braddock M. Tissue repair with a therapeutic transcription factor. Hum Gene Ther 2000, 11:2143-2158.
60. Wu M., Melichian D.S., de la Garza M., Gruner K., Bhattacharyya S., Barr L., et al. Essential roles for early growth response transcription factor Egr-1 in tissue fibrosis and wound healing. Am J Pathol 2009, 175:1041-1055.
61. Grose R., Harris B.S., Cooper L., Topilko P., Martin P. Immediate early genes krox-24 and krox-20 are rapidly up-regulated after wounding in the embryonic and adult mouse. Dev Dyn 2002, 223:371-378.
62. Nerlov C. C/EBPs: recipients of extracellular signals through proteome modulation. Curr Opin Cell Biol 2008, 20:180-185.
63. Lopez R.G., Garcia-Silva S., Moore S.J., Bereshchenko O., Martinez-Cruz A.B., Ermakova O., et al. C/EBPalpha and beta couple interfollicular keratinocyte proliferation arrest to commitment and terminal differentiation. Nat Cell Biol 2009, 11:1181-1190.
64. Tan N.S., Michalik L., Di-Poi N., Ng C.Y., Mermod N., Roberts A.B., et al. Essential role of Smad3 in the inhibition of inflammation-induced PPARbeta/delta expression. EMBO J 2004, 23:4211-4221.
65. Ashcroft G.S., Mills S.J., Flanders K.C., Lyakh L.A., Anzano M.A., Gilliver S.C., et al. Role of Smad3 in the hormonal modulation of in vivo wound healing responses. Wound Repair Regen 2003, 11:468-473.
66. Aarenstrup L., Flindt E.N., Otkjaer K., Kirkegaard M., Andersen J.S., Kristiansen K. HDAC activity is required for p65/RelA-dependent repression of PPARdelta-mediated transactivation in human keratinocytes. J Invest Dermatol 2008, 128:1095-1106.
67. Lam A.P., Gottardi C.J. Beta-catenin signaling: a novel mediator of fibrosis and potential therapeutic target. Curr Opin Reumatol 2011, 23:562-567.
68. Stojadinovic O., Brem H., Vouthounis C., Lee B., Fallon J., Stallcup M., et al. Molecular pathogenesis of chronic wounds: the role of beta-catenin and c-myc in the inhibition of epithelialization and wound healing. Am J Pathol 2005, 167:59-69.