Bone morphogenetic protein signaling suppresses wound-induced skin repair by inhibiting keratinocyte proliferation and migration

Journal of Investigative Dermatology

Volumn 134, Issue 3, 2014, Pages 827-837

  Lewis, Christopher J ^a   Mardaryev, Andrei N ^a   Poterlowicz, Krzysztof ^a   Sharova, Tatyana Y ^b   Aziz, Ahmar ^b   Sharpe, David T ^a   Botchkareva, Natalia V ^a   Sharov, Andrey A ^b  

^a UNIVERSITY OF BRADFORD   (United Kingdom)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; CYTOKERATIN 14; CYTOKERATIN 14 PROMOTER PROTEIN; CYTOKERATIN 16; CYTOKERATIN 17; MYOSIN VA; SMAD1 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; NOGGIN; OSTEOGENIC PROTEIN 1; SMAD5 PROTEIN; SMAD8 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETAL ORGANIZATION; EX VIVO STUDY; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; MICROARRAY ANALYSIS; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN EPITHELIUM; TRANSGENIC MOUSE; WILD TYPE; WOUND HEALING; CELL MOTILITY; EPIDERMIS; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; PROMOTER REGION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SKIN INJURY;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; EPIDERMIS; HUMANS; KERATIN-14; KERATINOCYTES; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; WOUND HEALING;

EID: 84894066757     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2013.419     Document Type: Article

References (93)

1. Ahmed MI, Mardaryev AN, Lewis CJ et al. (2011) MicroRNA-21 is an important downstream component of BMP signalling in epidermal keratinocytes. J Cell Sci 124:3399-4044
2. Allard J, Mogilner A (2013) Traveling waves in actin dynamics and cell motility. Curr Opin Cell Biol 25:107-155
3. Andl T, Ahn K, Kairo A et al. (2004) Epithelial BMPR1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development 131:2257-688
4. Ashcroft GS, Yang X, Glick AB et al. (1999) Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1:260-66
5. Barrientos S, Stojadinovic O, Golinko MS et al. (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16:585-6011
6. Blanpain C, Fuchs E (2006) Epidermal stem cells of the skin. Annu Rev Cell Dev Biol 22:339-733
7. Blanpain C, Lowry WE, Geoghegan A et al. (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118:635-488
8. Botchkarev VA, Botchkareva NV, Nakamura M et al. (2001) NOGGIN is required for induction of hair follicle growth phase in postnatal skin. FASEB J 15:2205-144
9. Botchkarev VA, Botchkareva NV, Roth W et al. (1999) NOGGIN is a mesenchymally derived stimulator of hair-follicle induction. Nat Cell Biol 1:158-644
10. Botchkarev VA, Sharov AA (2004) BMP signaling in the control of skin development and hair follicle growth. Differentiation 72:512-266
11. Cao TT, Chang W, Masters SE et al. (2004) Myosin-Va binds to and mechanochemically couples microtubules to actin filaments. Mole Biol Cell 15:151-611
12. Cotsarelis G (2006) Epithelial stem cells: a folliculocentric view. J Invest Dermatol 126:1459-688
13. Coulombe PA (1997) Towards a molecular definition of keratinocyte activation after acute injury to stratified epithelia. Biochem Biophys Res Commun 236:231-88
14. D'Souza SJ, Pajak A, Balazsi K et al. (2001) Ca2-and BMP-6 signaling regulate E2F during epidermal keratinocyte differentiation. J Biol Chem 276:23531-88
15. Driscoll MK, McCann C, Kopace R et al. (2012) Cell shape dynamics: from waves to migration. PLoS Comput Biol 8:e10023922
16. Drozdoff V, Wall NA, Pledger WJ (1994) Expression and growth inhibitory effect of decapentaplegic Vg-related protein 6: evidence for a regulatory role in keratinocyte differentiation. Proc Natl Acad Sci USA 91:5528-322
17. Eppinga RD, Peng IF, Lin JL et al. (2008) Opposite effects of overexpressed myosin Va or heavy meromyosin Va on vesicle distribution, cytoskeleton organization, and cell motility in nonmuscle cells. Cell Motil Cytoskeleton 65:197-2155
18. Falanga V (1993) Growth factors and wound healing. J Dermatol Surg Oncol 19:711-44
19. Fessing MY, Atoyan R, Shander B et al. (2010) BMP signaling induces cell-typespecific changes in gene expression programs of human keratinocytes and fibroblasts. J Invest Dermatol 130:398-4044
20. Firat-Karalar EN, Welch MD (2011) New mechanisms and functions of actin nucleation. Curr Opin Cell Biol 23:4-133
21. Flanders KC, Major CD, Arabshahi A et al. (2003) Interference with transforming growth factor-beta/ Smad3 signaling results in accelerated healing of wounds in previously irradiated skin. Am J Pathol 163:2247-577
22. Fletcher DA, Mullins RD (2010) Cell mechanics and the cytoskeleton. Nature 463:485-922
23. Fuchs E (2008) Skin stem cells: rising to the surface. J Cell Biol 180:273-844
24. Fuentealba LC, Eivers E, Ikeda A et al. (2007) Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131:980-933
25. Hosokawa R, Urata MM, Ito Y et al. (2005) Functional significance of Smad2 in regulating basal keratinocyte migration during wound healing. J Invest Dermatol 125:1302-99
26. Hsu YC, Pasolli HA, Fuchs E (2011) Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144:92-1055
27. Hwang EA, Lee HB, Tark KC (2001) Comparison of bone morphogenetic protein receptors expression in the fetal and adult skin. Yonsei Med J 42:581-66
28. Ito M, Cotsarelis G (2008) Is the hair follicle necessary for normal wound healing? J Invest Dermatol 128:1059-611
29. Ito M, Liu Y, Yang Z et al. (2005) Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 11:1351-44
30. Jamora C, DasGupta R, Kocieniewski P et al. (2003) Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422:317-222
31. Kaiser S, Schirmacher P, Philipp A et al. (1998) Induction of bone morphogenetic protein-6 in skin wounds. Delayed reepitheliazation and scar formation in BMP-6 overexpressing transgenic mice. J Invest Dermatol 111:1145-522
32. Kandyba E, Leung Y, Chen YB et al. (2013) Competitive balance of intrabulge BMP/Wnt signaling reveals a robust gene network ruling stem cell homeostasis and cyclic activation. Proc Natl Acad Sci USA 110:1351-66
33. Kasper M, Jaks V, Are A et al. (2011) Wounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytes. Proc Natl Acad Sci USA 108:4099-1044
34. Kobielak K, Pasolli HA, Alonso L et al. (2003) Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J Cell Biol 163:609-233
35. Kobielak K, Stokes N, de la Cruz J et al. (2007) Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proc Natl Acad Sci USA 104:10063-88
36. Krause C, Guzman A, Knaus P (2011) NOGGIN. Int J Biochem Cell Biol 43: 478-811
37. Kulessa H, Turk G, Hogan BL (2000) Inhibition of BMP signaling affects growth and differentiation in the anagen hair follicle. EMBO J 19:6664-744
38. Kurosaka S, Kashina A (2008) Cell biology of embryonic migration. Birth Defects Res C Embryo Today 84:102-222
39. Lan L, Han H, Zuo H et al. (2010) Upregulation of myosin Va by Snail is involved in cancer cell migration and metastasis. Int J Cancer 126:53-644
40. 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 128:1311-88
41. Lengsfeld AM, Low I, Wieland T et al. (1974) Interaction of phalloidin with actin. Proc Natl Acad Sci USA 71:2803-77
42. Levy V, Lindon C, Zheng Y et al. (2007) Epidermal stem cells arise from the hair follicle after wounding. FASEB J 21:1358-666
43. Li J, Chen J, Kirsner R (2007) Pathophysiology of acute wound healing. Clin Dermatol 25:9-188
44. Lichti U, Anders J, Yuspa SH (2008) Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat Protoc 3:799-8100
45. Lu CP, Polak L, Rocha AS et al. (2012) Identification of stem cell populations in sweat glands and ducts reveals roles in homeostasis and wound repair. Cell 150:136-500
46. Mardaryev AN, Ahmed MI, Vlahov NV et al. (2010) Micro-RNA-31 controls hair cycle-associated changes in gene expression programs of the skin and hair follicle. FASEB J 24:3869-811
47. Mardaryev AN, Meier N, Poterlowicz K et al. (2011) Lhx2 differentially regulates Sox9, Tcf4 and Lgr5 in hair follicle stem cells to promote epidermal regeneration after injury. Development 138:4843-522
48. Mathura JR Jr., Jafari N, Chang JT et al. (2000) Bone morphogenetic proteins-22 and -4: negative growth regulators in adult retinal pigmented epithelium. Invest Ophthalmol Vis Sci 41:592-6000
49. Mazzalupo S, Wawersik MJ, Coulombe PA (2002) An ex vivo assay to assess the potential of skin keratinocytes for wound epithelialization. J Invest Dermatol 118:866-700
50. Mazzalupo S, Wong P, Martin P et al. (2003) Role for keratins 6 and 17 during wound closure in embryonic mouse skin. Dev Dyn 226:356-655
51. McDonnell MA, Law BK, Serra R et al. (2001) Antagonistic effects of TGFbeta1 and BMP-6 on skin keratinocyte differentiation. Exp Cell Res 263:265-733
52. McGowan KM, Coulombe PA (1998) Onset of keratin 17 expression coincides with the definition of major epithelial lineages during skin development. J Cell Biol 143:469-866
53. Merlo S, Frasca G, Canonico PL et al. (2009) Differential involvement of estrogen receptor alpha and estrogen receptor beta in the healing promoting effect of estrogen in human keratinocytes. J Endocrinol 200:189-977
54. Meyer M, Muller AK, Yang J et al. (2012) FGF receptors 1 and 2 are key regulators of keratinocyte migration in vitro and in wounded skin. J Cell Sci 125:5690-7011
55. Ming Kwan K, Li AG, Wang XJ et al. (2004) Essential roles of BMPR-IA signaling in differentiation and growth of hair follicles and in skin tumorigenesis. Genesis 39:10-255
56. Miyazono K, Kamiya Y, Morikawa M (2010) Bone morphogenetic protein receptors and signal transduction. J Biochem 147:35-511
57. Moll R, Divo M, Langbein L (2008) The human keratins: biology and pathology. Histochem Cell Biol 129:705-333
58. Munz B, Smola H, Engelhardt F et al. (1999) Overexpression of activin A in the skin of transgenic mice reveals new activities of activin in epidermal morphogenesis, dermal fibrosis and wound repair. EMBO J 18:5205-155
59. Paladini RD, Takahashi K, Bravo NS et al. (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 132:381-977
60. Pardali K, Kowanetz M, Heldin CH et al. (2005) Smad pathway-specific transcriptional regulation of the cell cycle inhibitor p21(WAF1/Cip1). J Cell Physiol 204:260-722
61. Park GT, Morasso MI (2002) Bone morphogenetic protein-2 (BMP-2) transactivates Dlx3 through Smad1 and Smad4: alternative mode for Dlx33 induction in mouse keratinocytes. Nucleic Acids Res 30:515-222
62. Park HY, Wu C, Yaar M et al. (2009) Role of BMP-4 and its signaling pathways in cultured human melanocytes. Int J Cell Biol 2009:7504822
63. Patel GK, Wilson CH, Harding KG et al. (2006) Numerous keratinocyte subtypes involved in wound re-epithelialization. J Invest Dermatol 126:497-5022
64. Plikus MV, Mayer JA, de la Cruz D et al. (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451: 340-44
65. Reymann AC, Boujemaa-Paterski R, Martiel JL et al. (2012) Actin network architecture can determine myosin motor activity. Science 336:1310-44
66. Schafer M, Werner S (2007) Transcriptional control of wound repair. Annu Rev Cell Dev Biol 23:69-922
67. Sharov AA, Fessing M, Atoyan R et al. (2005) Bone morphogenetic protein (BMP) signaling controls hair pigmentation by means of crosstalk with the melanocortin receptor-1 pathway. Proc Natl Acad Sci U S A 102:93-88
68. Sharov AA, Mardaryev AN, Sharova TY et al. (2009) Bone morphogenetic protein antagonist noggin promotes skin tumorigenesis via stimulation of the Wnt and Shh signaling pathways. Am J Pathol 175:1303-144
69. Sharov AA, Sharova TY, Mardaryev AN et al. (2006) Bone morphogenetic protein signaling regulates the size of hair follicles and modulates the expression of cell cycle-associated genes. Proc Natl Acad Sci USA 103:18166-711
70. Sharov AA, Weiner L, Sharova TY et al. (2003) NOGGIN overexpression inhibits eyelid opening by altering epidermal apoptosis and differentiation. EMBO J 22:2992-30033
71. Shaw TJ, Martin P (2009) Wound repair at a glance. J Cell Sci 122:3209-133
72. Singh SK, Abbas WA, Tobin DJ (2012) Bone morphogenetic proteins differentially regulate pigmentation in human skin cells. J Cell Sci 125: 4306-199
73. Singhatanadgit W, Mordan N, Salih V et al. (2008) Changes in bone morphogenetic protein receptor-IB localisation regulate osteogenic responses of human bone cells to bone morphogenetic protein-2. Int J Biochem Cell Biol 40:2854-644
74. Sloane JA, Vartanian TK (2007) Myosin Va controls oligodendrocyte morphogenesis and myelination. J Neurosci 27:11366-755
75. Taylor G, Lehrer MS, Jensen PJ et al. (2000) Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102: 451-611
76. Tomic-Canic M, Komine M, Freedberg IM et al. (1998) Epidermal signal transduction and transcription factor activation in activated keratinocytes. J Dermatol Sci 17:167-811
77. Tomikawa K, Yamamoto T, Shiomi N et al. (2012) Smad2 decelerates reepithelialization during gingival wound healing. J Dent Res 91:764-700
78. Tsuboi R, Sato C, Shi CM et al. (1992) Stimulation of keratinocyte migration by growth factors. J Dermatol 19:652-33
79. Walsh DW, Godson C, Brazil DP et al. (2010) Extracellular BMP-antagonist regulation in development and disease: tied up in knots. Trends Cell Biol 20:244-566
80. Wang FS, Wolenski JS, Cheney RE et al. (1996) Function of myosin-V in filopodial extension of neuronal growth cones. Science 273:660-33
81. Wankell M, Munz B, Hubner G et al. (2001) Impaired wound healing in transgenic mice overexpressing the activin antagonist follistatin in the epidermis. EMBO J 20:5361-722
82. Wawersik M, Coulombe PA (2000) Forced expression of keratin 16 alters the adhesion, differentiation, and migration of mouse skin keratinocytes. Mol Biol Cell 11:3315-277
83. Wawersik MJ, Mazzalupo S, Nguyen D et al. (2001) Increased levels of keratin 16 alter epithelialization potential of mouse skin keratinocytes in vivo and ex vivo. Mol Biol Cell 12:3439-500
84. Wong SY, Reiter JF (2011) Wounding mobilizes hair follicle stem cells to form tumors. Proc Natl Acad Sci USA 108:4093-88
85. Wong VW, Sorkin M, Glotzbach JP et al. (2011) Surgical approaches to create murine models of human wound healing. J Biomed Biotechnol 2011:9696188
86. Wulf E, Deboben A, Bautz FA et al. (1979) Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci USA 76:4498-5022
87. Yaar M, Wu C, Park HY et al. (2006) Bone morphogenetic protein-4, a novel modulator of melanogenesis. J Biol Chem 281:25307-144
88. Yang L, Li W, Wang S et al. (2012) Smad4 disruption accelerates keratinocyte reepithelialization in murine cutaneous wound repair. Histochem Cell Biol 138:573-822
89. Yin T, Getsios S, Caldelari R et al. (2005) Plakoglobin suppresses keratinocyte motility through both cell-cell adhesion-dependent and -independent mechanisms. Proc Natl Acad Sci USA 102:5420-55
90. Yu X, Espinoza-Lewis RA, Sun C et al. (2010) Overexpression of constitutively active BMP-receptor-IB in mouse skin causes an ichthyosis-vulgaris-like disease. Cell Tissue Res 342:401-100
91. Yuhki M, Yamada M, Kawano M et al. (2004) BMPR1A signaling is necessary for hair follicle cycling and hair shaft differentiation in mice. Development 131:1825-333
92. Zhang J, He XC, Tong WG et al. (2006) Bone morphogenetic protein signaling inhibits hair follicle anagen induction by restricting epithelial stem/ progenitor cell activation and expansion. Stem Cells 24:2826-399
93. Zimmerman LB, De Jesus-Escobar JM, Harland RM (1996) The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86:599-6066 Diseases