Targeted skin overexpression of the mineralocorticoid receptor in mice causes epidermal atrophy, premature skin barrier formation, eye abnormalities, and alopecia

American Journal of Pathology

Volumn 171, Issue 3, 2007, Pages 846-860

  Marie, Yannis Sainte ^a   Toulon, Antoine ^a   Paus, Ralf ^b   Maubec, Eve ^c   Cherfa, Aicha ^a   Grossin, Maggy ^d   Descamps, Vincent ^c   Clemessy, Maud ^e   Gasc, Jean Marie ^e   Peuchmaur, Michel ^f   Glick, Adam ^g   Farman, Nicolette ^a,e   Jaisser, Frederic ^a  

^a INSERM   (France)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c BICHAT HOSPITAL   (France)

^d HÔPITAL LOUIS MOURIER   (France)

^e l'alimentation et l'Environnement   (France)

^f HÔPITAL ROBERT DEBRÉ   (France)

^g PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; KERATIN; MINERALOCORTICOID RECEPTOR;

ALOPECIA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIRTH; CONTROLLED STUDY; DEATH; DYSTROPHY; EMBRYO; EPIDERMIS; EYE MALFORMATION; EYE MOVEMENT; FEMALE; FOOT PAD; GENE OVEREXPRESSION; HAIR FOLLICLE; HUMAN; HUMAN TISSUE; KERATINOCYTE; MORTALITY; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN ATROPHY; SWEAT GLAND; TRANSGENIC MOUSE; VIBRISSA;

EID: 34548844449     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.060991     Document Type: Article

References (63)

1. Blanpain C, Fuchs E: Epidermal stem cells of the skin. Annu Rev Cell Dev Biol 2006, 22:339-373
2. Schmidt-Ullrich R, Paus R: Molecular principles of hair follicle induction and morphogenesis. Bioessays 2005, 27:247-261
3. Stenn KS, Paus R: Controls of hair follicle cycling. Physiol Rev 2001, 81:449-494
4. Alonso LC, Rosenfield RL: Molecular genetic and endocrine mechanisms of hair growth. Horm Res 2003, 60:1-13
5. Calléja C, Messaddeq N, Chapellier B, Yang H, Krezel W, Li M, Metzger D, Mascrez B, Ohta K, Kagechika H, Endo Y, Mark M, Ghyselinck NB, Chambon P: Genetic and pharmacological evidence that a retinoic acid cannot be the RXR-activating ligand in mouse epidermis keratinocytes. Genes Dev 2006, 20:1525-1538
6. Icre G, Wahli W, Michalik L: Functions of the peroxisome proliferator-activated receptor (PPAR) α and β in skin homeostasis, epithelial repair, and morphogenesis. J Investig Dermatol Symp Proc 2006, 11:30-35
7. Ohnemus U, Uenalan M, Inzunza J, Gustafsson JA, Paus R: The hair follicle as an estrogen target and source. Endocr Rev 2006, 27:677-706
8. Bikle DD, Elalieh H, Chang S, Xie Z, Sundberg JP: Development and progression of alopecia in the vitamin D receptor null mouse. J Cell Physiol 2006, 207:340-353
9. Radoja N, Stojadinovic O, Waseem A, Tomic-Canic M, Milisavljevic V, Teebor S, Blumenberg M: Thyroid hormones and gamma interferon specifically increase K15 keratin gene transcription. Mol Cell Biol 2004, 24:3168-3179
10. Lu NZ, Wardell SE, Burnstein KL, Defranco D, Fuller PJ, Giguere V, Hochberg RB, McKay L, Renoir JM, Weigel NL, Wilson EM, McDonnell DP, Cidlowski JA: International Union of Pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. Pharmacol Rev 2006, 58:782-797
11. Safer JD, Crawford TM, Holick MF: Topical thyroid hormone accelerates wound healing in mice. Endocrinology 2005, 146:4425-4430
12. Pèrez A, Chen TC, Turner A, Raab R, Bhawan J, Poche P, Holick MF: Efficacy and safety of topical calcitriol (1,25-dihydroxyvitamin d3) for the treatment of psoriasis. Br J Dermatol 1996, 134:238-246
13. Schäcke H, Docke WD, Asadullah K: Mechanisms involved in the side effects of glucocorticoids. Pharmacol Ther 2002, 96:23-43
14. Farman N, Rafestin-Oblin ME: Multiple aspects of mineralocorticoid selectivity. Am J Physiol 2001, 280:F181-F192
15. Kenouch S, Lombes M, Delahaye F, Eugene E, Bonvalet JP, Farman N: Human skin as target for aldosterone: coexpression of mineralocorticoid receptors and 11 β-hydroxysteroid dehydrogenase. J Clin Endocrinol Metab 1994, 79:1334-1341
16. Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, Mangelsdorf DJ: Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 2006, 126:789-799
17. Lotufo PA, Chae CU, Ajani UA, Hennekens CH, Manson JE: Male pattern baldness and coronary heart disease: the Physicians' Health Study. Arch Intern Med 2000, 160:165-171
18. Matilainen VA, Makinen PK, Keinanen-Kiukaanniemi SM: Early onset of androgenetic alopecia associated with early severe coronary heart disease: a population-based, case-control study. J Cardiovasc Risk 2001, 8:147-151
19. Moghetti P, Tosi F, Tosti A, Negri C, Misciali C, Perrone F, Caputo M, Muggeo M, Castello R: Comparison of spironolactone, flutamide, and finasteride efficacy in the treatment of hirsutism: a randomized, double blind, placebo-controlled trial. J Clin Endocrinol Metab 2000, 85:89-94
20. Sinclair R: Chronic telogen effluvium: a study of 5 patients over 7 years. J Am Acad Dermatol 2005, 52:12-16
21. Rossier BC, Pradervand S, Schild L, Hummler E: Epithelial sodium channel and the control of sodium balance: interaction between genetic and environmental factors. Annu Rev Physiol 2002, 64:877-897
22. Brouard M, Casado M, Djelidi S, Barrandon Y, Farman N: Epithelial sodium channel in human epidermal keratinocytes: expression of its subunits and relation to sodium transport and differentiation. J Cell Sci 1999, 112:3343-3352
23. Roudier-Pujol C, Rochat A, Escoubet B, Eugene E, Barrandon Y, Bonvalet JP, Farman N: Differential expression of epithelial sodium channel subunit mRNAs in rat skin. J Cell Sci 1996, 109:379-385
24. Mauro T, Guitard M, Behne M, Oda Y, Crumrine D, Komuves L, Rassner U, Elias PM, Hummler E: The ENaC channel is required for normal epidermal differentiation. J Invest Dermatol 2002, 118:589-594
25. Leyvraz C, Charles RP, Rubera I, Guitard M, Rotman S, Breiden B, Sandhoff K, Hummler E: The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J Cell Biol 2005, 170:487-496
26. Ouvrard-Pascaud A, Sainte-Marie Y, Benitah JP, Perrier R, Soukaseum C, Cat AN, Royer A, Le Quang K, Charpentier F, Demolombe S, Mechta-Grigoriou F, Beggah AT, Maison-Blanche P, Oblin ME, Delcayre C, Fishman GI, Farman N, Escoubet B, Jaisser F: Conditional mineralocorticoid receptor expression in the heart leads to life-threatening arrhythmias. Circulation 2005, 111:3025-3033
27. Diamond I, Owolabi T, Marco M, Lam C, Glick A: Conditional gene expression in the epidermis of transgenic mice using the tetracycline-regulated transactivators tTA and rTA linked to the keratin 5 promoter. J Invest Dermatol 2000, 115:788-794
28. Saadi-Kheddouci S, Berrebi D, Romagnolo B, Cluzeaud F, Peuchmaur M, Kahn A, Vandewalle A, Perret C: Early development of polycystic kidney disease in transgenic mice expressing an activated mutant of the β-catenin gene. Oncogene 2001, 20:5972-5981
29. Gomez-Sanchez CE, de Rodriguez AF, Romero DG, Estess J, Warden MP, Gomez-Sanchez MT, Gomez-Sanchez EP: Development of a panel of monoclonal antibodies against the mineralocorticoid receptor. Endocrinology 2006, 147:1343-1348
30. Hardman MJ, Sisi P, Banbury DN, Byrne C: Patterned acquisition of skin barrier function during development. Development 1998, 125:1541-1552
31. Müller-Röver S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, McKay IA, Stenn KS, Paus R: A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 2001, 117:3-15
32. Tuckermann JP, Reichardt HM, Arribas R, Richter KH, Schutz G, Angel P: The DNA binding-independent function of the glucocorticoid receptor mediates repression of AP-1-dependent genes in skin. J Cell Biol 1999, 147:1365-1370
33. Lu J, Goldstein KM, Chen P, Huang S, Gelbert LM, Nagpal S: Transcriptional profiling of keratinocytes reveals a vitamin D-regulated epidermal differentiation network. J Invest Dermatol 2005, 124:778-785
34. Magerl M, Tobin DJ, Muller-Rover S, Hagen E, Lindner G, McKay IA, Paus R: Patterns of proliferation and apoptosis during murine hair follicle morphogenesis. J Invest Dermatol 2001, 116:947-955
35. Paus R, Stenn KS, Link RE: Telogen skin contains an inhibitor of hair growth. Br J Dermatol 1990, 122:777-784
36. Cascallana JL, Bravo A, Donet E, Leis H, Lara MF, Paramio JM, Jorcano JL, Perez P: Ectoderm-targeted overexpression of the glucocorticoid receptor induces hypohidrotic ectodermal dysplasia. Endocrinology 2005, 146:2629-2638
37. Cascallana JL, Bravo A, Page A, Budunova I, Slaga TJ, Jorcano JL, Perez P: Disruption of eyelid and cornea development by targeted overexpression of the glucocorticoid receptor. Int J Dev Biol 2003, 47:59-64
38. Pérez P, Page A, Bravo A, Del Rio M, Gimenez-Conti I, Budunova I, Slaga TJ, Jorcano JL: Altered skin development and impaired proliferative and inflammatory responses in transgenic mice overexpressing the glucocorticoid receptor. FASEB J 2001, 15:2030-2032
39. Priolo M, Lagana C: Ectodermal dysplasias: a new clinical-genetic classification. J Med Genet 2001, 38:579-585
40. Kellendonk C, Tronche F, Reichardt HM, Schutz G: Mutagenesis of the glucocorticoid receptor in mice. J Steroid Biochem Mol Biol 1999, 69:253-259
41. Li M, Chiba H, Warot X, Messaddeq N, Gerard C, Chambon P, Metzger D: RXR-alpha ablation in skin keratinocytes results in alopecia and epidermal alterations. Development 2001, 128:675-688
42. Li YC, Pirro AE, Amling M, Delling G, Baron R, Branson R, Demay MB: Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci USA 1997, 94:9831-9835
43. Xie Z, Komuves L, Yu QC, Elalieh H, Ng DC, Leary C, Chang S, Crumrine D, Yoshizawa T, Kato S, Bikle DD: Lack of the vitamin D receptor is associated with reduced epidermal differentiation and hair follicle growth. J Invest Dermatol 2002, 118:11-16
44. Sharov AA, Weiner L, Sharova TY, Siebenhaar F, Atoyan R, Reginato AM, McNamara CA, Funa K, Gilchrest BA, Brissette JL, Botchkarev VA: Noggin overexpression inhibits eyelid opening by altering epidermal apoptosis and differentiation. EMBO J 2003, 22:2992-3003
45. Xia Y, Kao WW: The signaling pathways in tissue morphogenesis: a lesson from mice with eye-open at birth phenotype. Biochem Pharmacol 2004, 68:997-1001
46. + metabolism. Proc Natl Acad Sci USA 1998, 95:9424-9429
47. Sundberg JP, Peters EM, Paus R: Analysis of hair follicles in mutant laboratory mice. J Investig Dermatol Symp Proc 2005, 10:264-270
48. Lopez GN, Webb P, Shinsako JH, Baxter JD, Greene GL, Kushner PJ: Titration by estrogen receptor activation function-2 of targets that are downstream from coactivators. MoI Endocrinol 1999, 13:897-909
49. Aszterbaum M, Feingold KR, Menon GK, Williams ML: Glucocorticoids accelerate fetal maturation of the epidermal permeability barrier in the rat. J Clin Invest 1993, 91:2703-2708
50. Kömüves LG, Hanley K, Jiang Y, Elias PM, Williams ML, Feingold KR: Ligands and activators of nuclear hormone receptors regulate epidermal differentiation during fetal rat skin development. J Invest Dermatol 1998, 111:429-433
51. Hanley K, Rassner U, Elias PM, Williams ML, Feingold KR: Epidermal barrier ontogenesis: maturation in serum-free media and acceleration by glucocorticoids and thyroid hormone but not selected growth factors. J Invest Dermatol 1996, 106:404-411
52. Ito N, Ito T, Kromminga A, Bettermann A, Takigawa M, Kees F, Straub RH, Paus R: Human hair follicles display a functional equivalent of the hypothalamic-pituitary-adrenal axis and synthesize cortisol. FASEB J 2005, 19:1332-1334
53. Slominski A, Wortsman J: Neuroendocrinology of the skin. Endocr Rev 2000, 21:457-487
54. Slominski A, Wortsman J, Kohn L, Ain KB, Venkataraman GM, Pisarchik A, Chung JH, Giuliani C, Thornton M, Slugocki G, Tobin DJ: Expression of hypothalamic-pituitary-thyroid axis related genes in the human skin. J Invest Dermatol 2002, 119:1449-1455
55. Slominski A, Wortsman J, Luger T, Paus R, Solomon S: Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. Physiol Rev 2000, 80:979-1020
56. Slominski A, Gomez-Sanchez CE, Foecking MF, Wortsman J: Metabolism of progesterone to DOC, corticosterone and 18OHDOC in cultured human melanoma cells. FEBS Lett 1999, 455:364-366
57. Slominski A, Gomez-Sanchez CE, Foecking MF, Wortsman J: Active steroidogenesis in the normal rat skin. Biochim Biophys Acta 2000, 1474:1-4
58. Slominski A, Wortsman J, Foecking MF, Shackleton C, Gomez-Sanchez C, Szczesniewski A: Gas chromatography/mass spectrometry characterization of corticosteroid metabolism in human immortalized keratinocytes. J Invest Dermatol 2002, 118:310-315
59. Slominski A, Zbytek B, Semak I, Sweatman T, Wortsman J: CRH stimulates POMC activity and corticosterone production in dermal fibroblasts. J Neuroimmunol 2005, 162:97-102
60. Slominski A, Zbytek B, Szczesniewski A, Semak I, Kaminski J, Sweatman T, Wortsman J: CRH stimulation of corticosteroids production in melanocytes is mediated by ACTH. Am J Physiol Endocrinol Metab 2005, 288:E701-E706
61. Deppe CE, Heering PJ, Viengchareun S, Grabensee B, Farman N, Lombes M: Cyclosporine a and FK506 inhibit transcriptional activity of the human mineralocorticoid receptor: a cell-based model to investigate partial aldosterone resistance in kidney transplantation. Endocrinology 2002, 143:1932-1941
62. Yamamoto S, Kato R: Hair growth-stimulating effects of cyclosporin A and FK506, potent immunosuppressants. J Dermatol Sci 1994, 7(Suppl):S47-S54
63. Gafter-Gvili A, Sredni B, Gal R, Gafter U, Kalechman Y: Cyclosporin A-induced hair growth in mice is associated with inhibition of calcineurin-dependent activation of NFAT in follicular keratinocytes. Am J Physiol Cell Physiol 2003, 284:C1593-C1603