Augmenting Endogenous Wnt Signaling Improves Skin Wound Healing

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Whyte, Jemima L ^a   Smith, Andrew A ^a   Liu, Bo ^a   Manzano, Wilfred R ^a   Evans, Nick D ^a,c   Dhamdhere, Girija R ^a   Fang, Mark Y ^a,d   Chang, Howard Y ^a,b   Oro, Anthony E ^a   Helms, Jill A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; AXIN 2; BETA GALACTOSIDASE; LIPOSOMAL WNT3A PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WOUND HEALING PROMOTING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG FORMULATION; EPITHELIZATION; FIBROBLAST; GENETIC MODEL; HAIR FOLLICLE; HAIR GROWTH; HISTOLOGY; LIPOSOMAL DELIVERY; MALE; MOUSE; NONHUMAN; PROTEIN FUNCTION; REPORTER GENE; SIGNAL TRANSDUCTION; SKIN WOUND HEALING; WOUND; WOUND HEALING;

ANIMALS; AXIN PROTEIN; BETA-GALACTOSIDASE; EAR, EXTERNAL; EPIDERMIS; GENE EXPRESSION; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; LIPOSOMES; MICE; MICE, TRANSGENIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKIN; TIME FACTORS; WNT SIGNALING PATHWAY; WNT3A PROTEIN; WOUND HEALING;

EID: 84885810577     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076883     Document Type: Article

References (48)

1. Martin P, (1997) Wound healing-aiming for perfect skin regeneration. Science 276: 75-81.
2. DasGupta R, Fuchs E, (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126: 4557-4568.
3. Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, et al. (2003) Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A 100: 3299-3304.
4. Merrill BJ, Gat U, DasGupta R, Fuchs E, (2001) Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev 15: 1688-1705.
5. Osorio KM, Lilja KC, Tumbar T, (2011) Runx1 modulates adult hair follicle stem cell emergence and maintenance from distinct embryonic skin compartments. J Cell Biol 193: 235-250.
6. Sadelain M, Papapetrou EP, Bushman FD, (2012) Safe harbours for the integration of new DNA in the human genome. Nat Rev Cancer 12: 51-58.
7. Al Alam D, Green M, Tabatabai Irani R, Parsa S, Danopoulos S, et al. (2011) Contrasting expression of canonical Wnt signaling reporters TOPGAL, BATGAL and Axin2(LacZ) during murine lung development and repair. PLoS ONE 6: e23139.
8. Chua AW, Ma D, Gan SU, Fu Z, Han HC, et al. (2011) The role of R-spondin2 in keratinocyte proliferation and epidermal thickening in keloid scarring. J Invest Dermatol 131: 644-654.
9. Darby IA, Bisucci T, Hewitson TD, MacLellan DG, (1997) Apoptosis is increased in a model of diabetes-impaired wound healing in genetically diabetic mice. Int J Biochem Cell Biol 29: 191-200.
10. Telgenhoff D, Shroot B, (2005) Cellular senescence mechanisms in chronic wound healing. Cell Death Differ 12: 695-698.
11. Nguyen H, Merrill BJ, Polak L, Nikolova M, Rendl M, et al. (2009) Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat Genet 41: 1068-1075.
12. Snippert HJ, Haegebarth A, Kasper M, Jaks V, van Es JH, et al. (2010) Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 327: 1385-1389.
13. Levy V, Lindon C, Zheng Y, Harfe BD, Morgan BA, (2007) Epidermal stem cells arise from the hair follicle after wounding. FASEB J 21: 1358-1366.
14. Ito M, Yang Z, Andl T, Cui C, Kim N, et al. (2007) Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447: 316-320.
15. Stoick-Cooper CL, Weidinger G, Riehle KJ, Hubbert C, Major MB, et al. (2007) Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134: 479-489.
16. Chang J, Siebert JW, Schendel SA, Press BH, Longaker MT, (1995) Scarless wound healing: implications for the aesthetic surgeon. Aesthetic Plast Surg 19: 237-241.
17. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, et al. (2002) Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 22: 1184-1193.
18. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, et al. (2002) Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22: 1172-1183.
19. Kabashima K, Sakabe J, Yoshiki R, Tabata Y, Kohno K, et al. (2010) Involvement of Wnt signaling in dermal fibroblasts. Am J Pathol 176: 721-732.
20. Plikus MV, Mayer JA, de la Cruz D, Baker RE, Maini PK, et al. (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451: 340-344.
21. Chan EF, Gat U, McNiff JM, Fuchs E, (1999) A common human skin tumour is caused by activating mutations in beta-catenin. Nat Genet 21: 410-413.
22. Kishimoto J, Burgeson RE, Morgan BA, (2000) Wnt signaling maintains the hair-inducing activity of the dermal papilla. Genes Dev 14: 1181-1185.
23. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, et al. (2004) Defining the epithelial stem cell niche in skin. Science 303: 359-363.
24. Oro AE, Higgins K, (2003) Hair cycle regulation of Hedgehog signal reception. Dev Biol 255: 238-248.
25. Ansell DM, Kloepper JE, Thomason HA, Paus R, Hardman MJ, (2011) Exploring the "hair growth-wound healing connection": anagen phase promotes wound re-epithelialization. J Invest Dermatol 131: 518-528.
26. Ksander GA, Vistnes LM, Rose EH, (1977) Excisional wound biomechanics, skin tension lines, and elastic contraction. Plast Reconstr Surg 59: 398-406.
27. Ouhtit A, Muller HK, Davis DW, Ullrich SE, McConkey D, et al. (2000) Temporal events in skin injury and the early adaptive responses in ultraviolet-irradiated mouse skin. Am J Pathol 156: 201-207.
28. Behrens J, Jerchow BA, Wurtele M, Grimm J, Asbrand C, et al. (1998) Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280: 596-599.
29. Minear S, Leucht P, Jiang J, Liu B, Zeng A, et al. (2010) Wnt proteins promote bone regeneration. Sci Transl Med 2: 29ra30.
30. Zhao L, Rooker SM, Morrell N, Leucht P, Simanovskii D, et al. (2009) Controlling the in vivo activity of Wnt liposomes. Methods Enzymol 465: 331-347.
31. Clark RAF, Henson PM (1988) The Molecular and cellular biology of wound repair. New York: Plenum Press. xxii, 597 p. p.
32. Seifert AW, Kiama SG, Seifert MG, Goheen JR, Palmer TM, et al. (2012) Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489: 561-565.
33. Tanaka EM (2012) Regenerative biology: Skin, heal thyself. Nature 489.
34. Seifert AW, Monaghan JR, Voss SR, Maden M, (2012) Skin regeneration in adult axolotls: a blueprint for scar-free healing in vertebrates. PLoS ONE 7: e32875.
35. Grinnell F, (1994) Fibroblasts, myofibroblasts, and wound contraction. J Cell Biol 124: 401-404.
36. Sumiyoshi K, Nakao A, Setoguchi Y, Okumura K, Ogawa H, (2004) Exogenous Smad3 accelerates wound healing in a rabbit dermal ulcer model. J Invest Dermatol 123: 229-236.
37. Langton AK, Herrick SE, Headon DJ, (2008) An extended epidermal response heals cutaneous wounds in the absence of a hair follicle stem cell contribution. J Invest Dermatol 128: 1311-1318.
38. Aber C, Jimenez J, Kirsner RS, (2011) Hair and wound healing: anagen gets an "A". J Invest Dermatol 131: 278.
39. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E, (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118: 635-648.
40. Liu B, Yu HM, Hsu W, (2007) Craniosynostosis caused by Axin2 deficiency is mediated through distinct functions of beta-catenin in proliferation and differentiation. Dev Biol 301: 298-308.
41. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E, (2008) NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132: 299-310.
42. Chen D, Jarrell A, Guo C, Lang R, Atit R, (2012) Dermal beta-catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation. Development 139: 1522-1533.
43. Lo Celso C, Prowse DM, Watt FM, (2004) Transient activation of beta-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 131: 1787-1799.
44. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM, (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115: 97-105.
45. Helms JA, Kim CH, Eichele G, Thaller C, (1996) Retinoic acid signaling is required during early chick limb development. Development 122: 1385-1394.
46. Hu D, Marcucio RS, Helms JA, (2003) A zone of frontonasal ectoderm regulates patterning and growth in the face. Development 130: 1749-1758.
47. Helms JA, Cordero D, Tapadia MD, (2005) New insights into craniofacial morphogenesis. Development 132: 851-861.
48. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.