The role of nuclear hormone receptors in cutaneous wound repair

Cell Biochemistry and Function

Volumn 33, Issue 1, 2015, Pages 1-13

  Rieger, Sandra ^a   Zhao, Hengguang ^b   Martin, Paige ^a   Abe, Koichiro ^c   Lisse, Thomas S ^a  

^a MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^b THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^c TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Hormones; Innervation; Keratinocytes; Nuclear receptors; Regeneration; Tissue repair; Vitamin D; Wound healing

Indexed keywords

ANDROGEN RECEPTOR; CELL NUCLEUS RECEPTOR; ESTROGEN RECEPTOR; GLUCOCORTICOID RECEPTOR; HORMONE RECEPTOR; NUCLEAR HORMONE RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; RETINOIC ACID; RETINOID X RECEPTOR; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR; CELL RECEPTOR;

ANGIOGENESIS; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL THERAPY; ENDOCRINE DISEASE; EPITHELIZATION; ESTROGEN ACTIVITY; ESTROGEN THERAPY; FIBROBLAST; HUMAN; INFLAMMATION; KERATINOCYTE; MARINE BIOLOGY; NONHUMAN; ORGANOGENESIS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; SKIN INJURY; STEM CELL NICHE; TISSUE REPAIR; WOUND CLOSURE; WOUND HEALING; ANIMAL; CHEMISTRY; CYTOLOGY; FUNCTIONS OF THE SKIN AND ITS APPENDAGES; METABOLISM; SKIN;

ANIMALS; HUMANS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SKIN; SKIN PHYSIOLOGICAL PHENOMENA; WOUND HEALING;

EID: 84921597106     PISSN: 02636484     EISSN: 10990844     Source Type: Journal    
DOI: 10.1002/cbf.3086     Document Type: Article

References (147)

1. Peck MD. Epidemiology of burns throughout the world. Part II: intentional burns in adults. Burns: ISBI 2012; 38: 630-637. doi:10.1016/j.burns.2011.12.028.
2. Luderer HF, Nazarian RM, Zhu ED, Demay MB. Ligand-dependent actions of the vitamin D receptor are required for activation of TGF-beta signaling during the inflammatory response to cutaneous injury. Endocrinology 2013; 154: 16-24. doi:10.1210/en.2012-1579.
3. Junker JP, Philip J, Kiwanuka E, Hackl F, Caterson EJ, Eriksson E. Assessing quality of healing in skin: review of available methods and devices. Wound Repair Regen: Official Publication of the Wound Healing Soc [and] Euro Tissue Repair Soc 2014; 22(Suppl 1): 2-10. DOI: 10.1111/wrr.12162
4. Clark RA. Biology of dermal wound repair. Dermatol Clin 1993; 11: 647-666.
5. Clark RA. Basics of cutaneous wound repair. J Dermatol Surg Oncol 1993; 19: 693-706.
6. Winkelmann RK. Cutaneous sensory nerves. Semin Dermatol 1988; 7: 236-268.
7. Mihara M. Regenerated cutaneous nerves in human epidermal and subepidermal regions. An electron microscopy study. Arch Dermatol Res 1984; 276: 115-122.
8. Paus R, Heinzelmann T, Robicsek S, Czarnetzki BM, Maurer M. Substance P stimulates murine epidermal keratinocyte proliferation and dermal mast cell degranulation in situ. Arch Dermatol Res 1995; 287: 500-502.
9. Sayedyahossein S, Nini L, Irvine TS, Dagnino L. Essential role of integrin-linked kinase in regulation of phagocytosis in keratinocytes. FASEB 2012; 26: 4218-4229. doi:10.1096/fj.12-207852.
10. Han C, Song Y, Xiao H, et al.. Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila. Neuron 2014; 81: 544-560. doi:10.1016/j.neuron.2013.11.021.
11. Wang XJ, Han G, Owens P, Siddiqui Y, Li AG. Role of TGF beta-mediated inflammation in cutaneous wound healing. J Investig Dermatol Symp Proc/Soc Investig Dermatol Inc [and] Euro Soc Dermatol Res 2006; 11: 112-117.
12. Arwert EN, Hoste E, Watt FM. Epithelial stem cells, wound healing and cancer. Nat Rev Cancer 2012; 12: 170-180. doi:10.1038/nrc3217.
13. Lu CP, Polak L, Rocha AS, et al. Identification of stem cell populations in sweat glands and ducts reveals roles in homeostasis and wound repair. Cell 2012; 150: 136-150. doi:10.1016/j.cell.2012.04.045.
14. Murphy PS, Evans GR. Advances in wound healing: a review of current wound healing products. Plast Surg Int J 2012; 2012: 190-436. DOI: 10.1155/2012/190436
15. Broadley KN, Aquino AM, Woodward SC, et al. Monospecific antibodies implicate basic fibroblast growth factor in normal wound repair. Lab Investig; J Tech Meth Pathol 1989; 61: 571-575.
16. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci U S A 1998; 95: 5672-5677.
17. Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature 2008; 453: 314-321. doi:10.1038/nature07039.
18. O'Toole EA. Extracellular matrix and keratinocyte migration. Clin Exp Dermatol 2001; 26: 525-530.
19. Mann J, Oakley F, Akiboye F, Elsharkawy A, Thorne AW, Mann DA. Regulation of myofibroblast transdifferentiation by DNA methylation and MeCP2: implications for wound healing and fibrogenesis. Cell Death Differ 2007; 14: 275-285. doi:10.1038/sj.cdd.4401979.
20. Engin C. Effects of calcitonin gene-related peptide on wound contraction in denervated and normal rat skin: a preliminary report. Plast Reconstr Surg 1998; 101: 1887-1890.
21. Tanaka T, Danno K, Ikai K, Imamura S. Effects of substance P and substance K on the growth of cultured keratinocytes. J Invest Dermatol 1988; 90: 399-401.
22. Cheret J, Lebonvallet N, Buhe V, Carre JL, Misery L, Le Gall-Ianotto C. Influence of sensory neuropeptides on human cutaneous wound healing process. J Dermatol Sci 2014; 74: 193-203. doi:10.1016/j.jdermsci.2014.02.001.
23. Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 2007; 179: 1311-1323. doi:10.1083/jcb.200704042.
24. Hinz B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 2007; 127: 526-537. doi:10.1038/sj.jid.5700613.
25. Hinz B, Gabbiani G. Fibrosis: recent advances in myofibroblast biology and new therapeutic perspectives. F1000 Biol Rports 2010; 2: 78. DOI: 10.3410/B2-78
26. Mangelsdorf DJ, Thummel C, Beato M, et al. The nuclear receptor superfamily: the second decade. Cell 1995; 83: 835-839.
27. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ. Nuclear receptors and lipid physiology: opening the X-files. Science 2001; 294: 1866-1870. doi:10.1126/science.294.5548.1866.
28. Kobayashi K, Sueyoshi T, Inoue K, Moore R, Negishi M. Cytoplasmic accumulation of the nuclear receptor CAR by a tetratricopeptide repeat protein in HepG2 cells. Mol Pharmacol 2003; 64: 1069-1075. doi:10.1124/mol.64.5.1069.
29. Margolis DJ, Knauss J, Bilker W. Hormone replacement therapy and prevention of pressure ulcers and venous leg ulcers. Lancet 2002; 359: 675-677. doi:10.1016/S0140-6736(02)07806-6.
30. Beer HD, Gassmann MG, Munz B, et al. Expression and function of keratinocyte growth factor and activin in skin morphogenesis and cutaneous wound repair. J Investig Dermatol Symp Proc/Soc Investig Dermatol Inc [and] Euro Soc Dermatol Res 2000; 5: 34-39. DOI: 10.1046/j.1087-0024.2000.00009.x
31. Beer HD, Fassler R, Werner S. Glucocorticoid-regulated gene expression during cutaneous wound repair. Vitam Horm 2000; 59: 217-239.
32. Brincat MP, Baron YM, Galea R. Estrogens and the skin. Climacteric: J Int Menop Soc 2005; 8: 110-123. doi:10.1080/13697130500118100.
33. Roth GS, Harman SM, Lamberg SI. Altered ovarian regulation of wound healing during aging. Proc Soc Exp Biol Med Soc Exp Biol Med 1981; 166: 17-23.
34. Calvin M, Dyson M, Rymer J, Young SR. The effects of ovarian hormone deficiency on wound contraction in a rat model. Br J Obstet Gynaecol 1998; 105: 223-227.
35. Ashcroft GS, Ashworth JJ. Potential role of estrogens in wound healing. Am J Clin Dermatol 2003; 4: 737-743.
36. Ashcroft GS, Mills SJ, Lei K, et al. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest 2003; 111: 1309-1318. doi:10.1172/JCI16288.
37. Cotsarelis G. Epithelial stem cells: a folliculocentric view. J Invest Dermatol 2006; 126: 1459-1468. doi:10.1038/sj.jid.5700376.
38. Ashcroft GS, Greenwell-Wild T, Horan MA, Wahl SM, Ferguson MW. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am J Pathol 1999; 155: 1137-1146. doi:10.1016/S0002-9440(10)65217-0.
39. Ashcroft GS, Dodsworth J, van Boxtel E, et al. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat Med 1997; 3: 1209-1215.
40. Ashcroft GS, Horan MA, Ferguson MW. Aging is associated with reduced deposition of specific extracellular matrix components, an upregulation of angiogenesis, and an altered inflammatory response in a murine incisional wound healing model. J Invest Dermatol 1997; 108: 430-437.
41. Ashcroft GS, Horan MA, Herrick SE, Tarnuzzer RW, Schultz GS, Ferguson MW. Age-related differences in the temporal and spatial regulation of matrix metalloproteinases (MMPs) in normal skin and acute cutaneous wounds of healthy humans. Cell Tissue Res 1997; 290: 581-591.
42. Ashcroft GS, Kielty CM, Horan MA, Ferguson MW. Age-related changes in the temporal and spatial distributions of fibrillin and elastin mRNAs and proteins in acute cutaneous wounds of healthy humans. J Pathol 1997; 183: 80-89. doi:10.1002/(SICI)1096-9896(199709)183:1<80::AID-PATH1104>3.0.CO;2-N.
43. Ashworth JJ, Smyth JV, Pendleton N, et al. The dinucleotide (CA) repeat polymorphism of estrogen receptor beta but not the dinucleotide (TA) repeat polymorphism of estrogen receptor alpha is associated with venous ulceration. J Steroid Biochem Mol Biol 2005; 97: 266-270. doi:10.1016/j.jsbmb.2005.05.012.
44. Strudwick X, Powell BC, Cowin AJ. Role of sex hormones in acute and chronic wound healing. Prim Intent 2006; 14: 35-38.
45. Kariya Y, Moriya T, Suzuki T, et al. Sex steroid hormone receptors in human skin appendage and its neoplasms. Endocr J 2005; 52: 317-325.
46. Emmerson E, Rando G, Meda C, Campbell L, Maggi A, Hardman MJ. Estrogen receptor-mediated signalling in female mice is locally activated in response to wounding. Mol Cell Endocrinol 2013; 375: 149-156. doi:10.1016/j.mce.2013.05.015.
47. Campbell L, Emmerson E, Davies F, et al. Estrogen promotes cutaneous wound healing via estrogen receptor beta independent of its antiinflammatory activities. J Exp Med 2010; 207: 1825-1833. doi:10.1084/jem.20100500.
48. Murashima A, Kishigami S, Thomson A, Yamada G. Androgens and mammalian male reproductive tract development. Biochim Biophys Acta 2014. doi:10.1016/j.bbagrm.2014.05.020.
49. Basaria S. Male hypogonadism. Lancet 2014; 383: 1250-1263. doi:10.1016/S0140-6736(13)61126-5.
50. Fimmel S, Zouboulis CC. Influence of physiological androgen levels on wound healing and immune status in men. Aging Male: ISSAM 2005; 8: 166-174. doi:10.1080/13685530500233847.
51. Ashcroft GS, Mills SJ, Ashworth JJ. Ageing and wound healing. Biogerontology 2002; 3: 337-345.
52. Ashcroft GS, Mills SJ. Androgen receptor-mediated inhibition of cutaneous wound healing. J Clin Invest 2002; 110: 615-624. doi:10.1172/JCI15704.
53. Gilliver SC, Ashworth JJ, Mills SJ, Hardman MJ, Ashcroft GS. Androgens modulate the inflammatory response during acute wound healing. J Cell Sci 2006; 119: 722-732. doi:10.1242/jcs.02786.
54. Gilliver SC, Ruckshanthi JP, Hardman MJ, Zeef LA, Ashcroft GS. 5Alpha-dihydrotestosterone (DHT) retards wound closure by inhibiting re-epithelialization. J Pathol 2009; 217: 73-82. doi:10.1002/path.2444.
55. Lai JJ, Lai KP, Chuang KH, et al. Monocyte/macrophage androgen receptor suppresses cutaneous wound healing in mice by enhancing local TNF-alpha expression. J Clin Invest 2009; 119: 3739-3751. doi:10.1172/JCI39335.
56. Vermeulen A, Kaufman JM, Goemaere S, van Pottelberg I. Estradiol in elderly men. Aging Male: ISSAM 2002; 5: 98-102.
57. Chabab A, Sultan C, Fenart O, Descomps B. Stimulation of aromatase activity by dihydrotestosterone in human skin fibroblasts. J Steroid Biochem 1986; 25: 165-169.
58. Ashcroft GS, Horan MA, Ferguson MW. Aging alters the inflammatory and endothelial cell adhesion molecule profiles during human cutaneous wound healing. Lab Investig; J Tech Meth Pathol 1998; 78: 47-58.
59. Daly TJ, Weston WL. Retinoid effects on fibroblast proliferation and collagen synthesis in vitro and on fibrotic disease in vivo. J Am Acad Dermatol 1986; 15: 900-902.
60. Sundstrom A, Alfredsson L, Sjolin-Forsberg G, Gerden B, Bergman U, Jokinen J. Association of suicide attempts with acne and treatment with isotretinoin: retrospective Swedish cohort study. BMJ 2010; 341: c5812. doi:10.1136/bmj.c5812.
61. Lee DD, Stojadinovic O, Krzyzanowska A, Vouthounis C, Blumenberg M, Tomic-Canic M. Retinoid-responsive transcriptional changes in epidermal keratinocytes. J Cell Physiol 2009; 220: 427-439. doi:10.1002/jcp.21784.
62. Melnik BC. The role of transcription factor FoxO1 in the pathogenesis of acne vulgaris and the mode of isotretinoin action. Giornale italiano di dermatologia e venereologia: organo ufficiale, Societa italiana di dermatologia e sifilografia 2010; 145: 559-571.
63. Melnik BC. Is nuclear deficiency of FoxO1 due to increased growth factor/PI3K/Akt-signalling in acne vulgaris reversed by isotretinoin treatment? Br J Dermatol 2010; 162: 1398-1400. doi:10.1111/j.1365-2133.2010.09754.x.
64. Melnik BC. FoxO1-the key for the pathogenesis and therapy of acne? JDDG 2010; 8: 105-114. DOI: 10.1111/j.1610-0387.2010.07344.x
65. Ponugoti B, Xu F, Zhang C, Tian C, Pacios S, Graves DT. FOXO1 promotes wound healing through the up-regulation of TGF-beta1 and prevention of oxidative stress. J Cell Biol 2013; 203: 327-343. doi:10.1083/jcb.201305074.
66. Dingwall M, Marchildon F, Gunanayagam A, Louis CS, Wiper-Bergeron N. Retinoic acid-induced Smad3 expression is required for the induction of osteoblastogenesis of mesenchymal stem cells. Differ; Res Biol Divers 2011; 82: 57-65. doi:10.1016/j.diff.2011.05.003.
67. Glick AB, Flanders KC, Danielpour D, Yuspa SH, Sporn MB. Retinoic acid induces transforming growth factor-beta 2 in cultured keratinocytes and mouse epidermis. Cell Regul 1989; 1: 87-97.
68. Gunes Bilgili S, Calka O, Akdeniz N, Bayram I, Metin A. The effects of retinoids on secondary wound healing: biometrical and histopathological study in rats. J Dermatolog Treat 2013; 24: 283-289. doi:10.3109/09546634.2012.697985.
69. Gencoglan G, Tosun M, Gencoglan O. Isotretinoin-induced effects of mast cells on wound healing. JDD 2010; 9: 1207-1210.
70. Braungart E, Magdolen V, Degitz K. Retinoic acid upregulates the plasminogen activator system in human epidermal keratinocytes. J Invest Dermatol 2001; 116: 778-784. doi:10.1046/j.1523-1747.2001.01310.x.
71. Warner RL, Bhagavathula N, Nerusu K, et al. MDI 301, a nonirritating retinoid, improves abrasion wound healing in damaged/atrophic skin. Wound Repair Regen: Wound Heal Soc [and] Euro Tissue Repair Soc 2008; 16: 117-124. DOI: 10.1111/j.1524-475X.2007.00338.x
72. Bikle DD, Nemanic MK, Gee E, Elias P. 1, 25-Dihydroxyvitamin D3 production by human keratinocytes. Kinetics and regulation. J Clin Invest 1986; 78: 557-566. doi:10.1172/JCI112609.
73. Bikle DD, Nemanic MK, Whitney JO, Elias PW. Neonatal human foreskin keratinocytes produce 1, 25-dihydroxyvitamin D3. Biochemistry 1986; 25: 1545-1548.
74. Bouillon R, Carmeliet G, Verlinden L, et al. Vitamin D and human health: lessons from vitamin D receptor null mice. Endocr Rev 2008; 29: 726-776. doi:10.1210/er.2008-0004.
75. Christakos S, Hewison M, Gardner DG, et al. Vitamin D: beyond bone. Ann N Y Acad Sci 2013; 1287: 45-58. doi:10.1111/nyas.12129.
76. Lisse TS, Chun RF, Rieger S, Adams JS, Hewison M. Vitamin D activation of functionally distinct regulatory miRNAs in primary human osteoblasts. J Bone Miner Res: J Amer Soc Bone Miner Res 2013; 28: 1478-1488. doi:10.1002/jbmr.1882.
77. Lisse TS, Adams JS, Hewison M. Vitamin D and microRNAs in bone. Crit Rev Eukaryot Gene Expr 2013; 23: 195-214.
78. Demay MB, MacDonald PN, Skorija K, Dowd DR, Cianferotti L, Cox M. Role of the vitamin D receptor in hair follicle biology. J Steroid Biochem Mol Biol 2007; 103: 344-346. doi:10.1016/j.jsbmb.2006.12.036.
79. Oda Y, Sihlbom C, Chalkley RJ, et al. Two distinct coactivators, DRIP/mediator and SRC/p160, are differentially involved in vitamin D receptor transactivation during keratinocyte differentiation. Mol Endocrinol 2003; 17: 2329-2339. doi:10.1210/me.2003-0063.
80. Oda Y, Uchida Y, Moradian S, Crumrine D, Elias PM, Bikle DD. Vitamin D receptor and coactivators SRC2 and 3 regulate epidermis-specific sphingolipid production and permeability barrier formation. J Invest Dermatol 2009; 129: 1367-1378. doi:10.1038/jid.2008.380.
81. Lisse TS, Saini V, Zhao H, Luderer HF, Gori F, Demay MB. The vitamin D receptor is required for activation of cWnt and Hedgehog signaling in keratinocytes. Mol Endocrinol 2014; 28(10): 1698-1706. me20141043. DOI: 10.1210/me.2014-1043.
82. Li YC, Pirro AE, Amling M, et al. Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci U S A 1997; 94: 9831-9835.
83. Feldman D, Chen T, Cone C, et al. Vitamin D resistant rickets with alopecia: cultured skin fibroblasts exhibit defective cytoplasmic receptors and unresponsiveness to 1, 25(OH)2D3. J Clin Endocrinol Metab 1982; 55: 1020-1022. doi:10.1210/jcem-55-5-1020.
84. Hewison M, Rut AR, Kristjansson K, et al. Tissue resistance to 1, 25-dihydroxyvitamin D without a mutation of the vitamin D receptor gene. Clin Endocrinol (Oxf) 1993; 39: 663-670.
85. Chen H, Hewison M, Adams JS. Functional characterization of heterogeneous nuclear ribonuclear protein C1/C2 in vitamin D resistance: a novel response element-binding protein. J Biol Chem 2006; 281: 39114-39120. doi:10.1074/jbc.M608006200.
86. Lisse TS, Liu T, Irmler M, et al. Gene targeting by the vitamin D response element binding protein reveals a role for vitamin D in osteoblast mTOR signaling. FASEB 2011; 25: 937-947. doi:10.1096/fj.10-172577.
87. Lisse TS, Hewison M, Adams JS. Hormone response element binding proteins: novel regulators of vitamin D and estrogen signaling. Steroids 2011; 76: 331-339. doi:10.1016/j.steroids.2011.01.002.
88. Lisse TS, Chen H, Nanes MS, Hewison M, Adams JS. Vitamin D response element binding protein. In Vitamin D. Elsevier Academic Press: San Diego, USA, 2011; 251-271.
89. Reichrath J, Classen UG, Meineke V, et al. Immunoreactivity of six monoclonal antibodies directed against 1, 25-dihydroxyvitamin-D3 receptors in human skin. Histochem J 2000; 32: 625-629.
90. Pillai S, Bikle DD. Epidermal vitamin D metabolism, function, and regulation. Adv Lipid Res 1991; 24: 321-341.
91. Bikle DD. Vitamin D regulated keratinocyte differentiation. J Cell Biochem 2004; 92: 436-444. DOI: 10.1002/jcb.20095
92. Bikle DD, Chang S, Crumrine D, et al. Mice lacking 25OHD 1alpha-hydroxylase demonstrate decreased epidermal differentiation and barrier function. J Steroid Biochem Mol Biol 2004; 89-90: 347-353. doi:10.1016/j.jsbmb.2004.03.113.
93. Bollag WB. Differentiation of human keratinocytes requires the vitamin d receptor and its coactivators. J Invest Dermatol 2007; 127: 748-750. doi:10.1038/sj.jid.5700692.
94. Liu PT, Stenger S, Li H, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006; 311: 1770-1773. doi:10.1126/science.1123933.
95. Schauber J, Gallo RL. Expanding the roles of antimicrobial peptides in skin: alarming and arming keratinocytes. J Invest Dermatol 2007; 127: 510-512. doi:10.1038/sj.jid.5700761.
96. Schauber J, Dorschner RA, Coda AB, et al. Injury enhances TLR2 function and antimicrobial peptide expression through a vitamin D-dependent mechanism. J Clin Invest 2007; 117: 803-811. doi:10.1172/JCI30142.
97. Chun RF, Liu PT, Modlin RL, Adams JS, Hewison M. Impact of vitamin D on immune function: lessons learned from genome-wide analysis. Front Physiol 2014; 5: 151. doi:10.3389/fphys.2014.00151.
98. Hewison M. Antibacterial effects of vitamin D. Nat Rev Endocrinol 2011; 7: 337-345. doi:10.1038/nrendo.2010.226.
99. Xie Z, Komuves L, Yu QC, et al. Lack of the vitamin D receptor is associated with reduced epidermal differentiation and hair follicle growth. J Invest Dermatol 2002; 118: 11-16. doi:10.1046/j.1523-1747.2002.01644.x.
100. Teichert A, Elalieh H, Bikle D. Disruption of the hedgehog signaling pathway contributes to the hair follicle cycling deficiency in Vdr knockout mice. J Cell Physiol 2010; 225: 482-489. doi:10.1002/jcp.22227.
101. Teichert AE, Elalieh H, Elias PM, Welsh J, Bikle DD. Overexpression of hedgehog signaling is associated with epidermal tumor formation in vitamin D receptor-null mice. J Invest Dermatol 2011; 131: 2289-2297. doi:10.1038/jid.2011.196.
102. Meindl S, Rot A, Hoetzenecker W, Kato S, Cross HS, Elbe-Burger A. Vitamin D receptor ablation alters skin architecture and homeostasis of dendritic epidermal T cells. Br J Dermatol 2005; 152: 231-241. doi:10.1111/j.1365-2133.2005.06392.x.
103. Cianferotti L, Cox M, Skorija K, Demay MB. Vitamin D receptor is essential for normal keratinocyte stem cell function. Proc Natl Acad Sci U S A 2007; 104: 9428-9433. doi:10.1073/pnas.0702884104.
104. Ito M, Liu Y, Yang Z, et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 2005; 11: 1351-1354. doi:10.1038/nm1328.
105. Ito M, Cotsarelis G. Is the hair follicle necessary for normal wound healing? J Invest Dermatol 2008; 128: 1059-1061. doi:10.1038/jid.2008.86.
106. Langton AK, Herrick SE, Headon DJ. An extended epidermal response heals cutaneous wounds in the absence of a hair follicle stem cell contribution. J Invest Dermatol 2008; 128: 1311-1318. doi:10.1038/sj.jid.5701178.
107. Zhang JZ, Maruyama K, Ono I, Kaneko F. Production and secretion of platelet-derived growth factor AB by cultured human keratinocytes: regulatory effects of phorbol 12-myristate 13-acetate, etretinate, 1, 25-dihydroxyvitamin D3, and several cytokines. J Dermatol 1995; 22: 305-309.
108. Kong J, Grando SA, Li YC. Regulation of IL-1 family cytokines IL-1alpha, IL-1 receptor antagonist, and IL-18 by 1, 25-dihydroxyvitamin D3 in primary keratinocytes. J Immunol 2006; 176: 3780-3787.
109. Ding N, Yu RT, Subramaniam N, et al. A vitamin D receptor/SMAD genomic circuit gates hepatic fibrotic response. Cell 2013; 153: 601-613. doi:10.1016/j.cell.2013.03.028.
110. Usategui A, Criado G, Del Rey MJ, Fare R, Pablos JL. Topical vitamin D analogue calcipotriol reduces skin fibrosis in experimental scleroderma. Arch Dermatol Res 2014. doi:10.1007/s00403-014-1466-6.
111. Lagishetty V, Misharin AV, Liu NQ, et al. Vitamin D deficiency in mice impairs colonic antibacterial activity and predisposes to colitis. Endocrinology 2010; 151: 2423-2432. doi:10.1210/en.2010-0089.
112. Jiang YJ, Kim P, Lu YF, Feingold KR. PPARgamma activators stimulate aquaporin 3 expression in keratinocytes/epidermis. Exp Dermatol 2011; 20: 595-599. doi:10.1111/j.1600-0625.2011.01269.x.
113. Elizondo RA, Yin Z, Lu X, Watsky MA. Effect of vitamin D receptor knockout on cornea epithelium wound healing and tight junctions. Invest Ophthalmol Vis Sci 2014. doi:10.1167/iovs.13-13553.
114. Michalik L, Wahli W. Involvement of PPAR nuclear receptors in tissue injury and wound repair. J Clin Invest 2006; 116: 598-606. doi:10.1172/JCI27958.
115. Rosenfield RL, Kentsis A, Deplewski D, Ciletti N. Rat preputial sebocyte differentiation involves peroxisome proliferator-activated receptors. J Invest Dermatol 1999; 112: 226-232. doi:10.1046/j.1523-1747.1999.00487.x.
116. Makrantonaki E, Zouboulis CC. Testosterone metabolism to 5alpha-dihydrotestosterone and synthesis of sebaceous lipids is regulated by the peroxisome proliferator-activated receptor ligand linoleic acid in human sebocytes. Br J Dermatol 2007; 156: 428-432. doi:10.1111/j.1365-2133.2006.07671.x.
117. Michalik L, Desvergne B, Tan NS, et al. Impaired skin wound healing in peroxisome proliferator-activated receptor (PPAR)alpha and PPARbeta mutant mice. J Cell Biol 2001; 154: 799-814. doi:10.1083/jcb.200011148.
118. Tan NS, Michalik L, Desvergne B, Wahli W. Peroxisome proliferator-activated receptor-beta as a target for wound healing drugs. Expert Opin Ther Targets 2004; 8: 39-48. doi:10.1517/14728222.8.1.39.
119. Tan NS, Michalik L, Di-Poi N, Desvergne B, Wahli W. Critical roles of the nuclear receptor PPARbeta (peroxisome-proliferator-activated receptor beta) in skin wound healing. Biochem Soc Trans 2004; 32: 97-102. doi:10.1042/.
120. Tan NS, Michalik L, Di-Poi N, et al. Essential role of Smad3 in the inhibition of inflammation-induced PPARbeta/delta expression. EMBO J 2004; 23: 4211-4221. doi:10.1038/sj.emboj.7600437.
121. Di-Poi N, Tan NS, Michalik L, Wahli W, Desvergne B. Antiapoptotic role of PPARbeta in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol Cell 2002; 10: 721-733.
122. Sha W, Thompson K, South J, Baron M, Leask A. Loss of PPARgamma expression by fibroblasts enhances dermal wound closure. Fibrogenesis Tissue Repair 2012; 5: 5. doi:10.1186/1755-1536-5-5.
123. Bienert GP, Chaumont F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochimica et Biophysica Acta 2014; 1840(5): 1596-1604. doi:10.1016/j.bbagen.2013.09.017.
124. Hara M, Ma T, Verkman AS. Selectively reduced glycerol in skin of aquaporin-3-deficient mice may account for impaired skin hydration, elasticity, and barrier recovery. J Biol Chem 2002; 277: 46616-46621. doi:10.1074/jbc.M209003200.
125. Loo AE, Ho R, Halliwell B. Mechanism of hydrogen peroxide-induced keratinocyte migration in a scratch-wound model. Free Radic Biol Med 2011; 51: 884-892. doi:10.1016/j.freeradbiomed.2011.06.001.
126. Schacke H, Docke WD, Asadullah K. Mechanisms involved in the side effects of glucocorticoids. Pharmacol Ther 2002; 96: 23-43.
127. Quax RA, Manenschijn L, Koper JW, et al. Glucocorticoid sensitivity in health and disease. Nat Rev Endocrinol 2013; 9: 670-686. doi:10.1038/nrendo.2013.183.
128. Issa LL, Leong GM, Barry JB, Sutherland RL, Eisman JA. Glucocorticoid receptor-interacting protein-1 and receptor-associated coactivator-3 differentially interact with the vitamin D receptor (VDR) and regulate VDR-retinoid X receptor transcriptional cross-talk. Endocrinology 2001; 142: 1606-1615. doi:10.1210/endo.142.4.8068.
129. Ragan C, Grokoest AW, Boots RH. Effect of adrenocorticotrophic hormone on rheumatoid arthritis. Am J Med 1949; 7: 741-750.
130. Wang AS, Armstrong EJ, Armstrong AW. Corticosteroids and wound healing: clinical considerations in the perioperative period. Am J Surg 2013; 206: 410-417. doi:10.1016/j.amjsurg.2012.11.018.
131. Tiganescu A, Hupe M, Uchida Y, Mauro T, Elias PM, Holleran WM. Increased glucocorticoid activation during mouse skin wound healing. J Endocrinol 2014; 221: 51-61. doi:10.1530/JOE-13-0420.
132. Grose R, Werner S, Kessler D, et al. A role for endogenous glucocorticoids in wound repair. EMBO Rep 2002; 3: 575-582. doi:10.1093/embo-reports/kvf119.
133. Lindstedt E, Sandblom P. Wound healing in man: tensile strength of healing wounds in some patient groups. Ann Surg 1975; 181: 842-846.
134. El Roz A, Bard JM, Huvelin JM, Nazih H. LXR agonists and ABCG1-dependent cholesterol efflux in MCF-7 breast cancer cells: relation to proliferation and apoptosis. Anticancer Res 2012; 32: 3007-3013.
135. Sticozzi C, Pecorelli A, Belmonte G, Valacchi G. Cigarette smoke affects ABCAl expression via liver X receptor nuclear translocation in human keratinocytes. Int J Mol Sci 2010; 11: 3375-3386. doi:10.3390/ijms11093375.
136. Jiang YJ, Kim P, Elias PM, Feingold KR. LXR and PPAR activators stimulate cholesterol sulfotransferase type 2 isoform 1b in human keratinocytes. J Lipid Res 2005; 46: 2657-2666. doi:10.1194/jlr.M500235-JLR200.
137. Walczak R, Joseph SB, Laffitte BA, Castrillo A, Pei L, Tontonoz P. Transcription of the vascular endothelial growth factor gene in macrophages is regulated by liver X receptors. J Biol Chem 2004; 279: 9905-9911. doi:10.1074/jbc.M310587200.
138. Spits H, Artis D, Colonna M, et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nat Rev Immunol 2013; 13: 145-149. doi:10.1038/nri3365.
139. Serafini N, Klein Wolterink RG, Satoh-Takayama N, et al. Gata3 drives development of RORgammat+group 3 innate lymphoid cells. J Exp Med 2014; 211: 199-208. doi:10.1084/jem.20131038.
140. Romera-Hernandez M, Aparicio-Domingo P, Cupedo T. Damage control: RORgammat+innate lymphoid cells in tissue regeneration. Curr Opin Immunol 2013; 25: 156-160. doi:10.1016/j.coi.2013.01.007.
141. Aujla SJ, Chan YR, Zheng M, et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 2008; 14: 275-281. doi:10.1038/nm1710.
142. Ouyang W. Distinct roles of IL-22 in human psoriasis and inflammatory bowel disease. Cytokine Growth Factor Rev 2010; 21: 435-441. doi:10.1016/j.cytogfr.2010.10.007.
143. McGee HM, Schmidt BA, Booth CJ, et al. IL-22 promotes fibroblast-mediated wound repair in the skin. J Invest Dermatol 2013; 133: 1321-1329. doi:10.1038/jid.2012.463.
144. Zhao Y, Bruemmer D. NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology. Arterioscler Thromb Vasc Biol 2010; 30: 1535-1541. doi:10.1161/ATVBAHA.109.191163.
145. Niu G, Ye T, Qin L, et al. Orphan nuclear receptor TR3/Nur77 improves wound healing by upregulating the expression of integrin beta4. FASEB 2014. doi:10.1096/fj.14-257550.
146. Grose R, Werner S. An aPPARently protective mechanism for keratinocytes in wounded skin. Trends Mol Med 2002; 8: 149-151.
147. Hubner G, Brauchle M, Smola H, Madlener M, Fassler R, Werner S. Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine 1996; 8: 548-556. doi:10.1006/cyto.1996.0074.