Delayed cutaneous wound healing and aberrant expression of hair follicle stem cell markers in mice selectively lacking ctip2 in epidermis

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Liang, Xiaobo ^a   Bhattacharya, Shreya ^a   Bajaj, Gaurav ^a   Guha, Gunjan ^a   Wang, Zhixing ^a   Jang, Hyo Sang ^a   Leid, Mark ^a   Indra, Arup Kumar ^a,b   Ganguli Indra, Gitali ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CD133 ANTIGEN; CD34 ANTIGEN; CELL MARKER; CELL PROTEIN; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; CYTOKERATIN 15; CYTOKERATIN 8; LEUCINE RICH REPEAT AND IMMUNOGLOBULIN LIKE DOMAIN PROTEIN 1; NUCLEAR FACTOR OF ACTIVATED T CELL CYTOPLASMIC 1; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; UVOMORULIN; ACTIN; BCL11B PROTEIN, MOUSE; CADHERIN; PHALLOIDIN; REPRESSOR PROTEIN; RETINOIC ACID; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ADHESION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DERMIS; EPIDERMIS; EPITHELIZATION; EXTRACELLULAR MATRIX; GRANULATION TISSUE; HAIR FOLLICLE; HISTOLOGY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; SKINFOLD THICKNESS; STEM CELL; WOUND HEALING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; NEWBORN; PATHOLOGY; SKIN; TRANSGENIC MOUSE;

ACTINS; ANIMALS; ANIMALS, NEWBORN; CADHERINS; CELL DIFFERENTIATION; CELL MOVEMENT; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHALLOIDINE; REPRESSOR PROTEINS; SKIN; STEM CELLS; TRETINOIN; TUMOR SUPPRESSOR PROTEINS; WOUND HEALING;

EID: 84863115864     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029999     Document Type: Article

References (83)

1. Baranowsky A, Mokkapati S, Bechtel M, Krugel J, Miosge N, et al. (2010) Impaired wound healing in mice lacking the basement membrane protein nidogen 1. Matrix Biol 29: 15-21.
2. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M, (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601.
3. Gurtner GC, Werner S, Barrandon Y, Longaker MT, (2008) Wound repair and regeneration. Nature 453: 314-321.
4. Werner S, Grose R, (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83: 835-870.
5. Ito M, Liu Y, Yang Z, Nguyen J, Liang F, et al. (2005) Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 11: 1351-1354.
6. Myers SR, Leigh IM, Navsaria H, (2007) Epidermal repair results from activation of follicular and epidermal progenitor keratinocytes mediated by a growth factor cascade. Wound Repair Regen 15: 693-701.
7. Hudson LG, Newkirk KM, Chandler HL, Choi C, Fossey SL, et al. (2009) Cutaneous wound reepithelialization is compromised in mice lacking functional Slug (Snai2). J Dermatol Sci 56: 19-26.
8. Martin P, (1997) Wound healing-aiming for perfect skin regeneration. Science 276: 75-81.
9. Santoro MM, Gaudino G, (2005) Cellular and molecular facets of keratinocyte reepithelization during wound healing. Exp Cell Res 304: 274-286.
10. Alt-Holland A, Shamis Y, Riley KN, DesRochers TM, Fusenig NE, et al. (2008) E-cadherin suppression directs cytoskeletal rearrangement and intraepithelial tumor cell migration in 3D human skin equivalents. J Invest Dermatol 128: 2498-2507.
11. Koizumi M, Matsuzaki T, Ihara S, (2005) Expression of P-cadherin distinct from that of E-cadherin in re-epithelialization in neonatal rat skin. Dev Growth Differ 47: 75-85.
12. Singer AJ, Clark RA, (1999) Cutaneous wound healing. N Engl J Med 341: 738-746.
13. Fuchs E, (1995) Keratins and the skin. Annu Rev Cell Dev Biol 11: 123-153.
14. Patel GK, Wilson CH, Harding KG, Finlay AY, Bowden PE, (2006) Numerous keratinocyte subtypes involved in wound re-epithelialization. J Invest Dermatol 126: 497-502.
15. Paladini RD, Coulombe PA, (1998) Directed expression of keratin 16 to the progenitor basal cells of transgenic mouse skin delays skin maturation. J Cell Biol 142: 1035-1051.
16. Wawersik MJ, Mazzalupo S, Nguyen D, Coulombe PA, (2001) Increased levels of keratin 16 alter epithelialization potential of mouse skin keratinocytes in vivo and ex vivo. Mol Biol Cell 12: 3439-3450.
17. Safer JD, Crawford TM, Holick MF, (2005) Topical thyroid hormone accelerates wound healing in mice. Endocrinology 146: 4425-4430.
18. Wojcik SM, Bundman DS, Roop DR, (2000) Delayed wound healing in keratin 6a knockout mice. Mol Cell Biol 20: 5248-5255.
19. Wojcik SM, Longley MA, Roop DR, (2001) Discovery of a novel murine keratin 6 (K6) isoform explains the absence of hair and nail defects in mice deficient for K6a and K6b. J Cell Biol 154: 619-630.
20. Hosokawa R, Urata MM, Ito Y, Bringas P Jr, Chai Y, (2005) Functional significance of Smad2 in regulating basal keratinocyte migration during wound healing. J Invest Dermatol 125: 1302-1309.
21. Casanova ML, Bravo A, Martinez-Palacio J, Fernandez-Acenero MJ, Villanueva C, et al. (2004) Epidermal abnormalities and increased malignancy of skin tumors in human epidermal keratin 8-expressing transgenic mice. FASEB J 18: 1556-1558.
22. Porter RM, Lunny DP, Ogden PH, Morley SM, McLean WH, et al. (2000) K15 expression implies lateral differentiation within stratified epithelial basal cells. Lab Invest 80: 1701-1710.
23. Waseem A, Dogan B, Tidman N, Alam Y, Purkis P, et al. (1999) Keratin 15 expression in stratified epithelia: downregulation in activated keratinocytes. J Invest Dermatol 112: 362-369.
24. Jensen KB, Watt FM, (2006) Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc Natl Acad Sci U S A 103: 11958-11963.
25. Morasso MI, Tomic-Canic M, (2005) Epidermal stem cells: the cradle of epidermal determination, differentiation and wound healing. Biol Cell 97: 173-183.
26. Watt FM, (2000) Epidermal stem cells as targets for gene transfer. Hum Gene Ther 11: 2261-2266.
27. Watt FM, Lo Celso C, Silva-Vargas V, (2006) Epidermal stem cells: an update. Curr Opin Genet Dev 16: 518-524.
28. Fuchs E, (2007) Scratching the surface of skin development. Nature 445: 834-842.
29. Ansell DM, Kloepper JE, Thomason HA, Paus R, Hardman MJ, (2010) Exploring the "hair growth-wound healing connection": anagen phase promotes wound re-epithelialization. J Invest Dermatol 131: 518-528.
30. Levy V, Lindon C, Harfe BD, Morgan BA, (2005) Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell 9: 855-861.
31. Driskell RR, Clavel C, Rendl M, Watt FM, (2011) Hair follicle dermal papilla cells at a glance. J Cell Sci 124: 1179-1182.
32. Giangreco A, Jensen KB, Takai Y, Miyoshi J, Watt FM, (2009) Necl2 regulates epidermal adhesion and wound repair. Development 136: 3505-3514.
33. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E, (2008) NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132: 299-310.
34. Ito Y, Hamazaki TS, Ohnuma K, Tamaki K, Asashima M, et al. (2007) Isolation of murine hair-inducing cells using the cell surface marker prominin-1/CD133. J Invest Dermatol 127: 1052-1060.
35. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, et al. (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 40: 1291-1299.
36. Jensen KB, Collins CA, Nascimento E, Tan DW, Frye M, et al. (2009) Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 4: 427-439.
37. Trempus CS, Morris RJ, Ehinger M, Elmore A, Bortner CD, et al. (2007) CD34 expression by hair follicle stem cells is required for skin tumor development in mice. Cancer Res 67: 4173-4181.
38. Driskell RR, Giangreco A, Jensen KB, Mulder KW, Watt FM, (2009) Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 136: 2815-2823.
39. Guo A, Jahoda CA, (2009) An improved method of human keratinocyte culture from skin explants: cell expansion is linked to markers of activated progenitor cells. Exp Dermatol 18: 720-726.
40. Avram D, Fields A, Pretty On Top K, Nevrivy DJ, Ishmael JE, et al. (2000) Isolation of a novel family of C(2)H(2) zinc finger proteins implicated in transcriptional repression mediated by chicken ovalbumin upstream promoter transcription factor (COUP-TF) orphan nuclear receptors. J Biol Chem 275: 10315-10322.
41. Avram D, Fields A, Senawong T, Topark-Ngarm A, Leid M, (2002) COUP-TF (chicken ovalbumin upstream promoter transcription factor)-interacting protein 1 (CTIP1) is a sequence-specific DNA binding protein. Biochem J 368: 555-563.
42. Golonzhka O, Leid M, Indra G, Indra AK, (2007) Expression of COUP-TF-interacting protein 2 (CTIP2) in mouse skin during development and in adulthood. Gene Expr Patterns 7: 754-760.
43. Leid M, Ishmael JE, Avram D, Shepherd D, Fraulob V, et al. (2004) CTIP1 and CTIP2 are differentially expressed during mouse embryogenesis. Gene Expr Patterns 4: 733-739.
44. Golonzhka O, Liang X, Messaddeq N, Bornert JM, Campbell AL, et al. (2009) Dual role of COUP-TF-interacting protein 2 in epidermal homeostasis and permeability barrier formation. J Invest Dermatol 129: 1459-1470.
45. Ganguli-Indra G, Liang X, Hyter S, Leid M, Hanifin J, et al. (2009) Expression of COUP-TF-interacting protein 2 (CTIP2) in human atopic dermatitis and allergic contact dermatitis skin. Exp Dermatol 18: 994-996.
46. Ganguli-Indra G, Wasylyk C, Liang X, Millon R, Leid M, et al. (2009) CTIP2 expression in human head and neck squamous cell carcinoma is linked to poorly differentiated tumor status. PLoS ONE 4: e5367.
47. 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: 799-810.
48. Liang CC, Park AY, Guan JL, (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2: 329-333.
49. Florin L, Knebel J, Zigrino P, Vonderstrass B, Mauch C, et al. (2006) Delayed wound healing and epidermal hyperproliferation in mice lacking JunB in the skin. J Invest Dermatol 126: 902-911.
50. Foitzik K, Lindner G, Mueller-Roever S, Maurer M, Botchkareva N, et al. (2000) Control of murine hair follicle regression (catagen) by TGF-beta1 in vivo. FASEB J 14: 752-760.
51. Mecklenburg L, Tobin DJ, Muller-Rover S, Handjiski B, Wendt G, et al. (2000) Active hair growth (anagen) is associated with angiogenesis. J Invest Dermatol 114: 909-916.
52. Slominski A, Paus R, (1993) Melanogenesis is coupled to murine anagen: toward new concepts for the role of melanocytes and the regulation of melanogenesis in hair growth. J Invest Dermatol 101: 90S-97S.
53. Slominski A, Wortsman J, Plonka PM, Schallreuter KU, Paus R, et al. (2005) Hair follicle pigmentation. J Invest Dermatol 124: 13-21.
54. Muller-Rover S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, et al. (2001) A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117: 3-15.
55. Ganguli G, Abecassis J, Wasylyk B, (2000) MDM2 induces hyperplasia and premalignant lesions when expressed in the basal layer of the epidermis. EMBO J 19: 5135-5147.
56. Wang Z, Coleman DJ, Bajaj G, Liang X, Ganguli-Indra G, et al. (2011) RXRalpha ablation in epidermal keratinocytes enhances UVR-induced DNA damage, apoptosis, and proliferation of keratinocytes and melanocytes. J Invest Dermatol 131: 177-187.
57. Hardy MM, Blomme EA, Lisowski A, Chinn KS, Jones A, et al. (2003) Selective cyclooxygenase-2 inhibition does not alter keratinocyte wound responses in the mouse epidermis after abrasion. J Pharmacol Exp Ther 304: 959-967.
58. Kanazawa S, Fujiwara T, Matsuzaki S, Shingaki K, Taniguchi M, et al. (2010) bFGF regulates PI3-kinase-Rac1-JNK pathway and promotes fibroblast migration in wound healing. PLoS One 5: e12228.
59. Schreier T, Degen E, Baschong W, (1993) Fibroblast migration and proliferation during in vitro wound healing. A quantitative comparison between various growth factors and a low molecular weight blood dialysate used in the clinic to normalize impaired wound healing. Res Exp Med (Berl) 193: 195-205.
60. Dassule HR, Lewis P, Bei M, Maas R, McMahon AP, (2000) Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127: 4775-4785.
61. Indra AK, Warot X, Brocard J, Bornert JM, Xiao JH, et al. (1999) Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res 27: 4324-4327.
62. Semenova E, Koegel H, Hasse S, Klatte JE, Slonimsky E, et al. (2008) Overexpression of mIGF-1 in keratinocytes improves wound healing and accelerates hair follicle formation and cycling in mice. Am J Pathol 173: 1295-1310.
63. Mauch C, Zamek J, Abety AN, Grimberg G, Fox JW, et al. Accelerated wound repair in ADAM-9 knockout animals. J Invest Dermatol 130: 2120-2130.
64. Hirobe T, (1983) Proliferation of epidermal melanocytes during the healing of skin wounds in newborn mice. J Exp Zool 227: 423-431.
65. Hirobe T, (1988) Genetic factors controlling the proliferative activity of mouse epidermal melanocytes during the healing of skin wounds. Genetics 120: 551-558.
66. Slominski A, Tobin DJ, Shibahara S, Wortsman J, (2004) Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev 84: 1155-1228.
67. Bigliardi-Qi M, Gaveriaux-Ruff C, Zhou H, Hell C, Bady P, et al. (2006) Deletion of delta-opioid receptor in mice alters skin differentiation and delays wound healing. Differentiation 74: 174-185.
68. Gerritsen MJ, Elbers ME, de Jong EM, van de Kerkhof PC, (1997) Recruitment of cycling epidermal cells and expression of filaggrin, involucrin and tenascin in the margin of the active psoriatic plaque, in the uninvolved skin of psoriatic patients and in the normal healthy skin. J Dermatol Sci 14: 179-188.
69. Leigh IM, Navsaria H, Purkis PE, McKay IA, Bowden PE, et al. (1995) Keratins (K16 and K17) as markers of keratinocyte hyperproliferation in psoriasis in vivo and in vitro. Br J Dermatol 133: 501-511.
70. Tokumaru S, Higashiyama S, Endo T, Nakagawa T, Miyagawa JI, et al. (2000) Ectodomain shedding of epidermal growth factor receptor ligands is required for keratinocyte migration in cutaneous wound healing. J Cell Biol 151: 209-220.
71. Fitsialos G, Chassot AA, Turchi L, Dayem MA, LeBrigand K, et al. (2007) Transcriptional signature of epidermal keratinocytes subjected to in vitro scratch wounding reveals selective roles for ERK1/2, p38, and phosphatidylinositol 3-kinase signaling pathways. J Biol Chem 282: 15090-15102.
72. Grose R, Hutter C, Bloch W, Thorey I, Watt FM, et al. (2002) A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 129: 2303-2315.
73. Usui ML, Underwood RA, Mansbridge JN, Muffley LA, Carter WG, et al. (2005) Morphological evidence for the role of suprabasal keratinocytes in wound reepithelialization. Wound Repair Regen 13: 468-479.
74. Werner S, Munz B, (2000) Suppression of keratin 15 expression by transforming growth factor beta in vitro and by cutaneous injury in vivo. Exp Cell Res 254: 80-90.
75. Chu YW, Seftor EA, Romer LH, Hendrix MJ, (1996) Experimental coexpression of vimentin and keratin intermediate filaments in human melanoma cells augments motility. Am J Pathol 148: 63-69.
76. Gilbert S, Loranger A, Daigle N, Marceau N, (2001) Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J Cell Biol 154: 763-773.
77. Kazerounian S, Uitto J, Aho S, (2002) Unique role for the periplakin tail in intermediate filament association: specific binding to keratin 8 and vimentin. Exp Dermatol 11: 428-438.
78. Denton CP, Khan K, Hoyles RK, Shiwen X, Leoni P, et al. (2009) Inducible lineage-specific deletion of TbetaRII in fibroblasts defines a pivotal regulatory role during adult skin wound healing. J Invest Dermatol 129: 194-204.
79. Yamaguchi R, Takami Y, Yamaguchi Y, Shimazaki S, (2007) Bone marrow-derived myofibroblasts recruited to the upper dermis appear beneath regenerating epidermis after deep dermal burn injury. Wound Repair Regen 15: 87-93.
80. Pedroso DC, Tellechea A, Moura L, Fidalgo-Carvalho I, Duarte J, et al. (2007) Improved survival, vascular differentiation and wound healing potential of stem cells co-cultured with endothelial cells. PLoS One 6: e16114.
81. Segatto O, Anastasi S, Alema S, (2011) Regulation of epidermal growth factor receptor signalling by inducible feedback inhibitors. J Cell Sci 124: 1785-1793.
82. Sibilia M, Kroismayr R, Lichtenberger BM, Natarajan A, Hecking M, et al. (2007) The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75: 770-787.
83. Repertinger SK, Campagnaro E, Fuhrman J, El-Abaseri T, Yuspa SH, et al. (2004) EGFR enhances early healing after cutaneous incisional wounding. J Invest Dermatol 123: 982-989.