Endogenous retinoids in the hair follicle and sebaceous gland

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 1, 2012, Pages 222-229

  Everts, Helen B ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Hair follicle; Retinoic acid; Retinoid; Sebaceous gland; Stem cells; Synthesis

Indexed keywords

CELLULAR RETINOL BINDING PROTEIN 1; FATTY ACID BINDING PROTEIN; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOL; RETINOL PALMITATE;

ACNE; ALOPECIA AREATA; HAIR FOLLICLE; HOMEOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PSORIASIS; RETINOL INTOXICATION; REVIEW; SEBACEOUS GLAND;

ANIMALS; HAIR FOLLICLE; HUMANS; MICE; RECEPTORS, RETINOIC ACID; SEBACEOUS GLANDS; STEM CELLS; TRETINOIN; VITAMIN A DEFICIENCY;

EID: 83255194028     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2011.08.017     Document Type: Review

References (145)

1. S.B. Wolbach, and P.R. Howe Tissue changes following deprivation of fat-soluble A vitamin J. Exp. Med. 42 1925 753 777
2. C. Girard, O. Dereure, V. Blatiere, B. Guillot, and D. Bessis Vitamin A deficiency phrynoderma associated with chronic giardiasis Pediatr. Dermatol. 23 2006 346 349
3. M.A. Anzano, A.J. Lamb, and J.A. Olson Growth, appetite, sequence of pathological signs and survival following the induction of rapid, synchronous vitamin A deficiency in the rat J. Nutr. 109 1979 1419 1431
4. H.B. Everts, and C.D. Berdanier Nutrient-gene interactions in mitochondrial function: vitamin A needs are increased in BHE/Cdb rats IUBMB Life 53 2002 289 294
5. G. Ries, and R. Hess Retinol: safety considerations for its use in cosmetic products J. Toxicol., Cutaneous Ocul. Toxicol. 18 1999 169 185
6. M.Y.S. Shih, M.A. Kane, P. Zhou, C.L.E. Yen, R.S. Streeper, J.L. Napoli, and R.V. Farese Retinol esterification by DGAT1 is essential for retinoid homeostasis in murine skin J. Biol. Chem. 284 2009 4292 4299
7. T. Ruzicka, C. Sommerburg, G. Goerz, P. Kind, and H. Mensing Treatment of cutaneous lupus-erythematosus with acitretin and hydroxychloroquine Br. J. Dermatol. 127 1992 513 518
8. C.C. Zouboulis, S. Schagen, and T. Alestas The sebocyte culture: a model to study the pathophysiology of the sebaceous gland in sebostasis, seborrhoea and acne Arch. Dermatol. Res. 300 2008 397 413
9. K.R. Smith, and D.M. Thiboutot Sebaceous gland lipids: friend or foe? J. Lipid Res. 49 2008 271 281
10. S.B. Kurlandsky, M.V. Gamble, R. Ramakrishnan, and W.S. Blaner Plasma delivery of retinoic acid to tissues in the rat J. Biol. Chem. 270 1995 17850 17857
11. J.L. Napoli Physiological insights into all-trans-retinoic acid biosynthesis Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2011 10.1016/j.bbalip.2011.05.004
12. S. Kumar, L.L. Sandell, P.A. Trainer, F. Koentgen, and G. Duester Alcohol and aldehyde dehydrogenases: retinoid metabolic effects in mouse knockout models Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2011 10.1016/j.bbalip. 2011.04.004
13. W.S. Blaner, M.V. Gamble, S. Vogel, R. Piantedosi, J. Paik, and M.E. Gottesman Retinol-binding protein (RBP): essential physiologic functions J. Nutr. 132 2002 2979S S
14. R. Blomhoff, M.H. Green, J.B. Green, T. Berg, and K.R. Norum Vitamin-A metabolism - new perspectives on absorption, transport, and storage Physiol. Rev. 71 1991 951 990
15. R. Kawaguchi, J.M. Yu, J. Honda, J. Hu, J. Whitelegge, P.P. Ping, P. Wiita, D. Bok, and H. Sun A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A Science 315 2007 820 825
16. P.N. MacDonald, and D.E. Ong A lecithin:retinol acyltransferase activity in human and rat liver Biochem. Biophys. Res. Commun. 156 1988 157 163
17. J.L. Napoli Interactions of retinoid binding proteins and enzymes in retinoid metabolism Biochim. Biophys. Acta 1440 1999 139 162
18. S.B. Kurlandsky, J.H. Xiao, E.A. Duell, J.J. Voorhees, and G.J. Fisher Biological activity of all-trans retinol requires metabolic conversion to all-trans retinoic acid and is mediated through activation of nuclear retinoid receptors in human keratinocytes J. Biol. Chem. 269 1994 32821 32827
19. T. Matsuura, and A.C. Ross Regulation of hepatic lecithin: retinol acyltransferase activity by retinoic acid Arch. Biochem. Biophys. 301 1993 221 227
20. S.B. Kurlandsky, E.A. Duell, S. Kang, J.J. Voorhees, and G.J. Fisher Auto-regulation of retinoic acid biosynthesis through regulation of retinol esterification in human keratinocytes J. Biol. Chem. 271 1996 15346 15352
21. A.C. Ross Retinoid production and catabolism: role of diet in regulating retinol esterification and retinoic acid oxidation J. Nutr. 133 2003 291S 296S
22. B.N. Rexer, and D.E. Ong A novel short-chain alcohol dehydrogenase from rats with retinol dehydrogenase activity, cyclically expressed in uterine epithelium Biol. Reprod. 67 2002 1555 1564
23. N.G. Markova, A. Pinkas-Sarafova, N. Karaman-Jurukovska, V. Jurukovski, and M. Simon Expression pattern and biochemical characteristics of a major epidermal retinol dehydrogenase Mol. Genet. Metab. 78 2003 119 135
24. H.B. Everts, J.P. Sundberg, L.E. King Jr., and D.E. Ong Immunolocalization of enzymes, binding proteins, and receptors sufficient for retinoic acid synthesis and signaling during the hair cycle J. Investig. Dermatol. 127 2007 1593 1604
25. K. Niederreither, V. Subbarayan, P. Dolle, and P. Chambon Embryonic retinoic acid synthesis is essential for early mouse post-implantation development Nat. Genet. 21 1999 444 448
26. V. Dupe, N. Matt, J.M. Garnier, P. Chambon, M. Mark, and N.B. Ghyselinck A newborn lethal defect due to inactivation of retinaldehyde dehydrogenase type 3 is prevented by maternal retinoic acid treatment Proc. Natl. Acad. Sci. U. S. A. 100 2003 14036 14041
27. D. Dong, S.E. Ruuska, D.J. Levinthal, and N. Noy Distinct roles for cellular retinoic acid-binding proteins I and II in regulating signaling by retinoic acid J. Biol. Chem. 274 1999 23695 23698
28. A.S. Budhu, and N. Noy Direct channeling of retinoic acid between cellular retinoic acid-binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid-induced growth arrest Mol. Cell. Biol. 22 2002 2632 2641
29. R.J. Sessler, and N. Noy A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II Mol. Cell 18 2005 343 353
30. R.A. Bucco, W.L. Zheng, J.T. Davis, E. Sierra-Rivera, K.G. Osteen, A.K. Chaudhary, and D.E. Ong Cellular retinoic acid-binding protein (II) presence in rat uterine epithelial cells correlates with their synthesis of retinoic acid Biochemistry 36 1997 4009 4014
31. W.L. Zheng, R.A. Bucco, E. Sierra-Rievera, K.G. Osteen, M.H. Melner, and D.E. Ong Synthesis of retinoic acid by rat ovarian cells that express cellular retinoic acid-binding protein-II Biol. Reprod. 60 1999 110 114
32. H.B. Everts, J.P. Sundberg, and D.E. Ong Immunolocalization of retinoic acid biosynthesis systems in selected sites in rat Exp. Cell Res. 308 2005 309 319
33. T.T. Schug, D.C. Berry, N.S. Shaw, S.N. Travis, and N. Noy Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors Cell 129 2007 723 733
34. M. Rieck, W. Meissner, S. Ries, S. Mueller-Brusselbach, and R. Muller Ligand-mediated regulation of peroxisome proliferator-activated receptor (PPAR) beta/delta: a comparative analysis of PPAR-selective agonists and all-trans retinoic acid Mol. Pharmacol. 74 2008 1269 1277
35. M.G. Borland, J.E. Foreman, E.E. Girroir, R. Zolfaghari, A.K. Sharma, S. Amin, F.J. Gonzalez, A.C. Ross, and J.M. Peters Ligand activation of peroxisome proliferator-activated receptor-beta/delta inhibits cell proliferation in human HaCaT keratinocytes Mol. Pharmacol. 74 2008 1429 1442
36. P.D. Fiorella, and J.L. Napoli Microsomal retinoic acid metabolism. Effects of cellular retinoic acid-binding protein (type I) and C18-hydroxylation as an initial step J. Biol. Chem. 269 1994 10538 10544
37. J.F. Boylan, and L.J. Gudas The level of Crabp-I expression influences the amounts and types of all-trans-retinoic acid metabolites in F9 teratocarcinoma stem-cells J. Biol. Chem. 267 1992 21486 21491
38. A.C. Chen, K. Yu, M.A. Lane, and L.J. Gudas Homozygous deletion of the CRABPI gene in AB1 embryonic stem cells results in increased CRABPII gene expression and decreased intracellular retinoic acid concentration Arch. Biochem. Biophys. 411 2003 159 173
39. J.M. Baron, R. Heise, W.S. Blaner, M. Neis, S. Joussen, A. Dreuw, Y. Marquardt, J.H. Saurat, H.F. Merk, D.R. Bickers, and F.K. Jugert Retinoic acid and its 4-oxo metabolites are functionally active in human skin cells in vitro J. Investig. Dermatol. 125 2005 143 153
40. K. Niederreither, S. Abu-Abed, B. Schuhbaur, M. Petkovich, P. Chambon, and P. Dolle Genetic evidence that oxidative derivatives of retinoic acid are not involved in retinoid signaling during mouse development Nat. Genet. 31 2002 84 88
41. O. Sorg, C. Tran, P. Carraux, D. Grand, C. Barraclough, J.-F. Arrighi, P. Descombes, V. Piguet, and J.-H. Saurat Metabolism and biological activities of topical 4-oxoretinoids in mouse skin J. Investig. Dermatol. 128 2008 999 1008
42. M. Petkovich, N.J. Brand, A. Krust, and P. Chambon A human retinoic acid receptor which belongs to the family of nuclear receptors Nature 330 1987 444 450
43. P. Chambon A decade of molecular biology of retinoic acid receptors FASEB J. 10 1996 940 954
44. J.E. Balmer, and R. Blomhoff Gene expression regulation by retinoic acid J. Lipid Res. 43 2002 1773 1808
45. D.J. Mangelsdorf, E.S. Ong, J.A. Dyck, and R.M. Evans Nuclear receptor that identifies a novel retinoic acid response pathway Nature 345 1990 224 229
46. R.A. Heyman, D.J. Mangelsdorf, J.A. Dyck, R.B. Stein, G. Eichele, R.M. Evans, and C. Thaller 9-cis retinoic acid is a high-affinity ligand for the retinoid-X receptor Cell 68 1992 397 406
47. C. Calleja, N. Messaddeq, B. Chapellier, H.Y. Yang, W. Krezel, M. Li, D. Metzger, B. Mascrez, K. Ohta, H. Kagechika, Y. Endo, M. Mark, N.B. Ghyselinck, and P. Chambon Genetic and pharmacological evidence that a retinoic acid cannot be the RXR-activating ligand in mouse epidermis keratinocytes Genes Dev. 20 2006 1525 1538
48. J. Lengqvist, A.M. de Urquiza, A.C. Bergman, T.M. Willson, J. Sjovall, T. Perlmann, and W.J. Griffiths Polyunsaturated fatty acids including docosahexaenoic and arachidonic acid bind to the retinoid X receptor alpha ligand-binding domain Mol. Cell. Proteomics 3 2004 692 703
49. A.M. de Urquiza, S.Y. Liu, M. Sjoberg, R.H. Zetterstrom, W. Griffiths, J. Sjovall, and T. Perlmann Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain Science 290 2000 2140 2144
50. A.C. Ross Retinol esterification by rat-liver microsomes - evidence for a fatty acyl coenzyme-A-retinol acyltransferase J Biol. Chem. 257 1982 2453 2459
51. S.M. O'Byrne, N. Wongsiriroj, J. Libien, S. Vogel, I.J. Goldberg, W. Baehr, K. Palczewski, and W.S. Blaner Retinoid absorption and storage is impaired in mice lacking lecithin: retinol acyltransferase (LRAT) J. Biol. Chem. 280 2005 35647 35657
52. M.D. Orland, K. Anwar, D. Cromley, C.H. Chu, L.P. Chen, J.T. Billheimer, M.M. Hussain, and D. Cheng Acyl coenzyme A dependent retinol esterification by acyl coenzyme A: diacylglycerol acyltransferase 1 Biochim. Biophys. Acta 1737 2005 76 82
53. C.L.E. Yen, M. Monetti, B.J. Burri, and R.V. Farese The triacylglycerol synthesis enzyme DGAT1 also catalyzes the synthesis of diacylglycerols, waxes, and retinyl esters J. Lipid Res. 46 2005 1502 1511
54. N. Wongsiriroj, R. Piantedosi, K. Palczewski, I.J. Goldberg, T.P. Johnston, E. Li, and W.S. Blaner The molecular basis of retinoid absorption - a genetic dissection J. Biol. Chem. 283 2008 13510 13519
55. D.E. Ong, P.N. MacDonald, and A.M. Gubitosi Esterification of retinol in rat liver. Possible participation by cellular retinol-binding protein and cellular retinol-binding protein II J. Biol. Chem. 263 1988 5789 5796
56. F.M. Herr, and D.E. Ong Differential interaction of lecithin-retinol acyltransferase with cellular retinol binding proteins Biochemistry 31 1992 6748 6755
57. E.P. Lorie, H. Li, A. Vahlquist, and H. Torma The involvement of cytochrome p450 (CYP) 26 in the retinoic acid metabolism of human epidermal keratinocytes Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 1791 2009 220 228
58. G. Duester Genetic dissection of retinoid dehydrogenases Chem. Biol. Interact. 130 2001 469 480
59. A. Molotkov, X. Fan, and G. Duester Excessive vitamin A toxicity in mice genetically deficient in either alcohol dehydrogenase Adh1 or Adh3 Eur. J. Biochem. 269 2002 2607 2612
60. X. Fan, A. Molotkov, S. Manabe, C.M. Donmoyer, L. Deltour, M.H. Foglio, A.E. Cuenca, W.S. Blaner, S.A. Lipton, and G. Duester Targeted disruption of Aldh1a1 (Raldh1) provides evidence for a complex mechanism of retinoic acid synthesis in the developing retina Mol. Cell. Biol. 23 2003 4637 4648
61. A. Molotkov, and G. Duester Genetic evidence that retinaldehyde dehydrogenase Raldh1 (Aldh1a1) functions downstream of alcohol dehydrogenase Adh1 in metabolism of retinol to retinoic acid J. Biol. Chem. 278 2003 36085 36090
62. L. Deltour, M.H. Foglio, and G. Duester Impaired retinol utilization in Adh4 alcohol dehydrogenase mutant mice Dev. Genet. 25 1999 1 10
63. L. Deltour, M.H. Foglio, and G. Duester Metabolic deficiencies in alcohol dehydrogenase Adh1, Adh3, and Adh4 null mutant mice. Overlapping roles of Adh1 and Adh4 in ethanol clearance and metabolism of retinol to retinoic acid J. Biol. Chem. 274 1999 16796 16801
64. R.J. Haselbeck, H.L. Ang, and G. Duester Class IV alcohol/retinol dehydrogenase localization in epidermal basal layer: potential site of retinoic acid synthesis during skin development Dev. Dyn. 208 1997 447 453
65. D.M. Jenkinson, H.Y. Elder, I. Montgomery, and V.A. Moss Comparative studies of the ultrastructure of the sebaceous gland Tissue Cell 17 1985 683 698
66. A.J. Thody, and S. Shuster Control and function of sebaceous glands Physiol. Rev. 69 1989 383 416
67. A. Tosti Comparison of histodynamics of sebaceous glands and epidermis in man - microanatomic and morphometric study J. Investig. Dermatol. 62 1974 147 152
68. A. Wrobel, H. Seltmann, S. Fimmel, K. Muller-Decker, M. Tsukada, B. Bogdanoff, N. Mandt, U. Blume-Peytavi, C.E. Orfanos, and C.C. Zouboulis Differentiation and apoptosis in human immortalized sebocytes J. Investig. Dermatol. 120 2003 175 181
69. M.R. Schneider, R. Schmidt-Ullrich, and R. Paus The hair follicle as a dynamic miniorgan Curr. Biol. 19 2009 R132 R142
70. Y. Amoh, K. Katsuoka, and R.M. Hoffman The advantages of hair follicle pluripotent stem cells over embryonic stem cells and induced pluripotent stem cells for regenerative medicine J. Dermatol. Sci. 60 2010 131 137
71. G. Cotsarelis, T.T. Sun, and R.M. Lavker Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis Cell 61 1990 1329 1337
72. R.J. Morris, Y. Liu, L. Marles, Z. Yang, C. Trempus, S. Li, J.S. Lin, J.A. Sawicki, and G. Cotsarelis Capturing and profiling adult hair follicle stem cells Nat. Biotechnol. 22 2004 411 417
73. T. Tumbar, G. Guasch, V. Greco, C. Blanpain, W.E. Lowry, M. Rendl, and E. Fuchs Defining the epithelial stem cell niche in skin Science 303 2004 359 363
74. G. Cotsarelis Epithelial stem cells: a folliculocentric view J. Investig. Dermatol. 126 2006 1459 1468
75. V. Jaks, M. Kasper, and R. Toftgard The hair follicle-a stem cell zoo Exp. Cell Res. 316 2010 1422 1428
76. V. Horsley, D. O'Carroll, R. Tooze, Y. Ohinata, M. Saitou, T. Obukhanych, M. Nussenzweig, A. Tarakhovsky, and E. Fuchs Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland Cell 126 2006 597 609
77. K.B. Jensen, C.A. Collins, E. Nascimento, D.W. Tan, M. Frye, S. Itami, and F.M. Watt Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis Cell Stem Cell 4 2009 427 439
78. U.B. Jensen, X. Yan, C. Triel, S.H. Woo, R. Christensen, and D.M. Owens A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus J. Cell Sci. 121 2008 609 617
79. J.G.W. Nijhof, K.M. Braun, A. Giangreco, C. van Pelt, H. Kawamoto, R.L. Boyd, R. Willemze, L.H.F. Mullenders, F.M. Watt, F.R. de Gruijl, and W. van Ewijk The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells Development 133 2006 3027 3037
80. H.J. Snippert, A. Haegebarth, M. Kasper, V. Jaks, J.H. van Es, N. Barker, M. van de Wetering, M. van den Born, H. Begthel, R.G. Vries, D.E. Stange, R. Toftgard, and H. Clevers Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin Science 327 2010 1385 1389
81. V. Jaks, N. Barker, M. Kasper, J.H. Van Es, H.J. Snippert, H. Clevers, and R. Toftgard Lgr5 marks cycling, yet long-lived, hair follicle stem cells Nat. Genet. 40 2008 1291 1299
82. M. Ito, K. Kizawa, K. Hamada, and G. Cotsarelis Hair follicle stem cells in the lower bulge form the secondary germ, a biochemically distinct but functionally equivalent progenitor cell population, at the termination of catagen Differentiation 72 2004 548 557
83. E. Legue, and J.F. Nicolas Hair follicle renewal: organization of stem cells in the matrix and the role of stereotyped lineages and behaviors Development 132 2005 4143 4154
84. F.M. Watt, and K.B. Jensen Epidermal stem cell diversity and quiescence Embo Mol. Med. 1 2009 260 267
85. D.J. Kim, K. Kataoka, D. Rao, K. Kiguchi, G. Cotsarelis, and J. DiGiovanni Targeted disruption of Stat3 reveals a major role for follicular stem cells in skin tumor initiation Cancer Res. 69 2009 7587 7594
86. M. Li, A.K. Indra, X. Warot, J. Brocard, N. Messaddeq, S. Kato, D. Metzger, and P. Chambon Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis Nature 407 2000 633 636
87. M. Li, H. Chiba, X. Warot, N. Messaddeq, C. Gerard, P. Chambon, and D. Metzger RXR alpha ablation in skin keratinocytes results in alopecia and epidermal alterations Development 128 2001 675 688
88. Y.C. Li, A.E. Pirro, M. Amling, G. Delling, R. Baroni, R. Bronson, and M.B. DeMay Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia Proc. Nat. Acad. Sci. U. S. A. 94 1997 9831 9835
89. D.D. Bikle, H. Elalieh, S. Chang, Z. Xie, and J.P. Sundberg Development and progression of alopecia in the vitamin D receptor null mouse J. Cell. Physiol. 207 2006 340 353
90. X. Cao, S.L. Teitelbaum, H.J. Zhu, L. Zhang, X. Feng, and F.P. Ross Competition for a unique response element mediates retinoic acid inhibition of vitamin D3-stimulated transcription J. Biol. Chem. 271 1996 20650 20654
91. F.K. Jugert, T.C. Roos, I. Notzon, and H.F. Merk Vitamin D3 and its synthetic analogue secocholestra-trien-1,2, 24-triol influence the metabolism and the isomerization of retinoic acid in human keratinocytes Skin Pharmacol. Appl. Skin Physiol. 11 1998 161 165
92. N.J. Koszewski, J. Herberth, and H.H. Malluche Retinoic acid receptor gamma 2 interactions with vitamin D response elements J. Steroid Bioch. Mol. Biol. 120 2010 200 207
93. Y. Sakai, and M.B. Demay Evaluation of keratinocyte proliferation and differentiation in vitamin D receptor knockout mice Endocrinology 141 2000 2043 2049
94. K. Foitzik, T. Spexard, M. Nakamura, U. Halsner, and R. Paus Towards dissecting the pathogenesis of retinoid-induced hair loss: all-trans retinoic acid induces premature hair follicle regression (catagen) by upregulation of transforming growth factor-beta 2 in the dermal papilla J. Investig. Dermatol. 124 2005 1119 1126
95. C.M. Metallo, L. Ji, J.J. De Pablo, and S.P. Palecek Retinoic acid and bone morphogenetic protein signaling synergize to efficiently direct epithelial differentiation of human embryonic stem cells Stem Cells 26 2008 372 380
96. G. Bilousova, J.A. Chen, and D.R. Roop Differentiation of mouse induced pluripotent stem cells into a multipotent keratinocyte lineage J. Investig. Dermatol. 131 2011 857 864
97. M. Saitou, S. Sugai, T. Tanaka, K. Shimouchi, E. Fuchs, S. Narumiya, and A. Kakizuka Inhibition of skin development by targeted expression of a dominant-negative retinole acid receptor Nature 374 1995 159 162
98. S. Imakado, J.R. Bickenbach, D.S. Bundman, J.A. Rothnagel, P.S. Attar, X.J. Wang, V.R. Walczak, S. Wisniewski, J. Pote, J.S. Gordon, R.A. Heyman, R.M. Evans, and D.R. Roop Targeting expression of a dominant-negative retinoic acid receptor mutant in the epidermis of transgenic mice results in loss of barrier function Genes Dev. 9 1995 317 329
99. P.S. Attar, P.W. Wertz, M. McArthur, S. Imakado, J.R. Bickenbach, and D.R. Roop Inhibition of retinoid signaling in transgenic mice alters lipid processing and disrupts epidermal barrier function Mol. Endocrinol. 11 1997 792 800
100. X. Feng, Z.H. Peng, W. Di, X.Y. Li, C. RochetteEgly, P. Chambon, J.J. Voorhees, and J.H. Xiao Suprabasal expression of a dominant-negative RXR alpha mutant in transgenic mouse epidermis impairs regulation of gene transcription and basal keratinocyte proliferation by RAR-selective retinoids Genes Dev. 11 1997 59 71
101. B. Chapellier, M. Mark, N. Messaddeq, C. Calleja, X. Warot, J. Brocard, C. Gerard, M. Li, D. Metzger, N.B. Ghyselinck, and P. Chambon Physiological and retinoid-induced proliferations of epidermis basal keratinocytes are differently controlled EMBO J. 21 2002 3402 3413
102. N.B. Ghyselinck, V. Dupe, A. Dierich, N. Messaddeq, J.M. Garnier, C. Rochette-Egly, P. Chambon, and M. Mark Role of the retinoic acid receptor beta (RARbeta) during mouse development Int. J. Dev. Biol. 41 1997 425 447
103. J. Reichrath, M. Mittmann, J. Kamradt, and S.M. Muller Expression of retinoid-X receptors (- alpha,-beta,-gamma) and retinoic acid receptors (- alpha,-beta,-gamma) in normal human skin: an immunohistological evaluation Histochem. J. 29 1997 127 133
104. N. Billoni, B. Gautier, Y.F. Mahe, and B.A. Bernard Expression of retinoid nuclear receptor superfamily members in human hair follicles and its implication in hair growth Acta Derm. Venereol. 77 1997 350 355
105. J.P. Viallet, and D. Dhouailly Retinoic acid and mouse skin morphogenesis.1. Expression pattern of retinoic acid receptor genes during hair vibrissa follicle, plantar, and nasal gland development J. Investig. Dermatol. 103 1994 116 121
106. H.C. Tsou, S.P. Si, X.H. Lee, A. Gonzalezserva, and M. Peacocke A beta-2rare-Lacz transgene identifies retinoic acid-mediated transcriptional activation in distinct cutaneous sites Exp. Cell Res. 214 1994 27 34
107. H.B. Everts, L.E. King Jr., J.P. Sundberg, and D.E. Ong Hair cycle-specific immunolocalization of retinoic acid synthesizing enzymes Aldh1a2 and Aldh1a3 indicate complex regulation J. Investig. Dermatol. 123 2004 258 263
108. J. Rossant, R. Zirngibl, D. Cado, M. Shago, and V. Giguere Expression of a retinoic acid response element-hsplacz transgene defines specific domains of transcriptional activity during mouse embryogenesis Genes Dev. 5 1991 1333 1344
109. D.M. Ansell, J.E. Kloepper, H.A. Thomason, R. Paus, and M.J. Hardman Exploring the "hair growth-wound healing connection": anagen phase promotes wound re-epithelialization J. Investig. Dermatol. 131 2011 518 528
110. J.P. Viallet, and D. Dhouailly Retinoic acid and mouse skin morphogenesis.2. Role of epidermal competence in hair glandular metaplasia Dev. Biol. 166 1994 277 288
111. C.M. Chuong, S.A. Ting, R.B. Widelitz, and Y.S. Lee Mechanism of skin morphogenesis 2. retinoic acid modulates axis orientation and phenotypes of skin appendages Development 115 1992 839 852
112. M.T. Flowers, C.M. Paton, S.M. O'Byrne, K. Schiesser, J.A. Dawson, W.S. Blaner, C. Kendziorski, and J.M. Ntambi Metabolic changes in skin caused by Scd1 deficiency: a focus on retinol metabolism PLoS One 6 2011
113. L.E. King, K.J. McElwee, J.P. Sundberg, and A. Alopecia Dermatologic immunity B.J. Nickoloff, F.O. Nestle, Curr Dir Autoimmun 2008 Basel, Karger 280 312
114. ab2J): a new allele and a model for scarring alopecia Am. J. Pathol. 156 2000 2067 2075
115. P. Karnik, Z. Tekeste, T.S. McCormick, A.C. Gilliam, V.H. Price, K.D. Cooper, and P. Mirmirani Hair follicle stem cell-specific PPARg deletion causes scarring alopecia J. Investig. Dermatol. 129 2009 1243 1257
116. M.J. Harries, K.C. Meyer, and R. Paus Hair loss as a result of cutaneous autoimmunity: frontiers in the immunopathogenesis of primary cicatricial alopecia Autoimmun. Rev. 8 2009 478 483
117. K.J. McElwee, R. Hoffmann, P. Freyschmidt-Paul, E. Wenzel, S. Kissling, J.P. Sundberg, and M. Zoller Resistance to alopecia areata in C3H/HeJ mice is associated with increased expression of regulatory cytokines and a failure to recruit CD4+ and CD8+ cells J. Investig. Dermatol. 119 2002 1426 1433
118. K.J. McElwee, E.M. Spiers, and R.F. Oliver In vivo depletion of CD8+ T cells restores hair growth in the DEBR model for alopecia areata Br. J. Dermatol. 135 1996 211 217
119. A. Gilhar, M. Landau, B. Assy, R. Shalaginov, S. Serafimovich, and R.S. Kalish Mediation of alopecia areata by cooperation between CD4(+) and CD8(+) T lymphocytes - transfer to human scalp explants on Prkd(cscid) mice Arch. Dermatol. 138 2002 916 922
120. R. Paus, N. Ito, M. Takigawa, and T. Ito The hair follicle and immune privilege J. Investig. Dermatol. Symp. Proc. 8 2003 188 194
121. A. Gilhar, Y. Kam, B. Assy, and R.S. Kalish Alopecia areata induced in C3H/HeJ mice by interferon-gamma: evidence for loss of immune privilege J. Investig. Dermatol. 124 2005 288 289
122. T. Ito, N. Ito, M. Saatoff, H. Hashizume, H. Fukamizu, B.J. Nickoloff, M. Takigawa, and R. Paus Maintenance of hair follicle immune privilege is linked to prevention of NK cell attack J. Investig. Dermatol. 128 2008 1196 1206
123. G. Stuttgen Historical perspectives of tretinoin J. Am. Acad. Dermatol. 15 1986 735 740
124. D. Thiboutot, H. Gollnick, V. Bettoli, B. Dreno, S.W. Kang, J.J. Leyden, A.R. Shalita, V. Lozada, D. Berson, A. Finlay, C.L. Goh, M.I. Herane, A. Kaminsky, R. Kubba, A. Layton, Y. Miyachi, M. Perez, J.P. Martin, M. Ramos-e-Silva, J.A. See, N. Shear, and J. Wolf New insights into the management of acne: an update from the global alliance to improve outcomes in acne group J. Am. Acad. Dermatol. 60 2009 S1 S50
125. G. Tzimas, and H. Nau The role of metabolism and toxicokinetics in retinoid teratogenesis Curr. Pharm. Des. 7 2001 803 831
126. M. Landthaler, J. Kummermehr, A. Wagner, and G. Plewig Inhibitory effects of 13-cis retinoic acid on human sebaceous glands Arch. Dermatol. Res. 269 1980 297 309
127. C.C. Zouboulis, B.P. Korge, D. Mischke, and C.E. Orfanos Altered proliferation, synthetic activity, and differentiation of cultured human sebocytes in the absence of vitamin-A and their modulation by synthetic retinoids J. Investig. Dermatol. 101 1993 628 633
128. C.C. Zouboulis, B. Korge, H. Akamatsu, L.Q. Xia, S. Schiller, H. Gollnick, and C.E. Orfanos Effects of 13-cis-retinoic acid, all-trans-retinoic acid, and acitretin on the proliferation, lipid-synthesis and keratin expression of cultured human sebocytes in vitro J. Investig. Dermatol. 96 1991 792 797
129. T. Sato, N. Imai, N. Akimoto, T. Sakiguchi, K. Kitamura, and A. Ito Epidermal growth factor and 1 alpha,25-dihydroxyvitamin D-3 suppress lipogenesis in hamster sebaceous gland cells in vitro J. Investig. Dermatol. 117 2001 965 970
130. E.C. Gomez Differential effect of 13-cis-retinoic acid and an aromatic retinoid (Ro-10-9359) on the sebaceous glands of the hamster flank organ J. Investig. Dermatol. 76 1981 68 69
131. M. Tsukada, M. Schroder, T.C. Roos, R.A. Chandraratna, U. Reichert, H.F. Merk, C.E. Orfanos, and C.C. Zouboulis 13-cis retinoic acid exerts its specific activity on human sebocytes through selective intracellular isomerization to all-trans retinoic acid and binding to retinoid acid receptors J. Investig. Dermatol. 115 2000 321 327
132. M.J. Kim, N. Ciletti, S. Michel, U. Reichert, and R.L. Rosenfield The role of specific retinoid receptors in sebocyte growth and differentiation in culture J. Investig. Dermatol. 114 2000 349 353
133. A.M. Nelson, K.L. Gilliland, Z.Y. Cong, and D.M. Thiboutot 13-cis retinoic acid induces apoptosis and cell cycle arrest in human SEB-1 sebocytes J. Investig. Dermatol. 126 2006 2178 2189
134. A.M. Nelson, W. Zhao, K.L. Gilliland, A.L. Zaenglein, W.L. Liu, and D.M. Thiboutot Isotretinoin temporally regulates distinct sets of genes in patient skin J. Investig. Dermatol. 129 2009 1038 1042
135. T. Karlsson, A. Vahlquist, N. Kedishvili, and H. Torma 13-cis-Retinoic acid competitively inhibits 3 alpha-hydroxysteroid oxidation by retinol dehydrogenase RoDH-4: a mechanism for its anti-androgenic effects in sebaceous glands? Biochem. Biophys. Res. Commun. 303 2003 273 278
136. B.C. Melnik, G. Schmitz, and C.C. Zouboulis Anti-acne agents attenuate FGFR2 signal transduction in acne J. Investig. Dermatol. 129 2009 1868 1877
137. A.M. Nelson, W. Zhao, K.L. Gilliland, A.L. Zaenglein, W.L. Liu, and D.M. Thiboutot Neutrophil gelatinase-associated lipocalin mediates 13-cis retinoic acid-induced apoptosis of human sebaceous gland cells J. Clin. Investig. 118 2008 1468 1478
138. E. Papakonstantinou, A.J. Aletras, E. Glass, P. Tsogas, A. Dionyssopoulos, J. Adjaye, S. Fimmel, P. Gouvousis, R. Herwig, H. Lehrach, C.C. Zouboulis, and G. Karakiulakis Matrix metalloproteinases of epithelial origin in facial sebum of patients with acne and their regulation by isotretinoin J. Investig. Dermatol. 125 2005 673 684
139. J.M. Dufour, M.N. Vo, N. Bhattacharya, J. Okita, R. Okita, and K.H. Kim Peroxisorne proliferators disrupt retinoic acid receptor alpha signaling in the testis Biol. Reprod. 68 2003 1215 1224
140. M.J. Kim, D. Deplewski, N. Ciletti, S. Michel, U. Reichert, and R.L. Rosenfield Limited cooperation between peroxisome proliferator-activated receptors and retinoid X receptor agonists in sebocyte growth and development Mol. Genet. Metab. 74 2001 362 369
141. W.C. Chen, C.C. Yang, H.M. Sheu, H. Seltmann, and C.C. Zouboulis Expression of peroxisome proliferator-activated receptor and CCAAT/enhancer binding protein transcription factors in cultured human sebocytes J. Investig. Dermatol. 121 2003 441 447
142. C.A. Collins, and F.M. Watt Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for beta-catenin and Notch signalling Dev. Biol. 324 2008 55 67
143. M. Theodosiou, V. Laudet, and M. Schubert From carrot to clinic: an overview of the retinoic acid signaling pathway Cell. Mol. Life Sci. 67 2010 1423 1445
144. J.J. Thiele, S.U. Weber, and L. Packer Sebaceous gland secretion is a major physiologic route of vitamin E delivery to skin J. Investig. Dermatol. 113 1999 1006 1010
145. C. Kramer, H. Seltmann, M. Seifert, W. Tilgen, C.C. Zouboulis, and J. Reichrath Characterization of the vitamin D endocrine system in human sebocytes in vitro J. Steroid Bioch. Mol. Biol. 113 2009 9 16