Regulation of Retinoid-Mediated Signaling Involved in Skin Homeostasis by RAR and RXR Agonists/Antagonists in Mouse Skin

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Gericke, Janine ^a   Ittensohn, Jan ^a   Mihály, Johanna ^a,b   Álvarez, Susana ^c   Álvarez, Rosana ^c   Töröcsik, Dániel ^a   de Lera, Ángel R ^c   Rühl, Ralph ^a,b,d  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b Paprika Bioanalytics Bt   (Hungary)

^c UNIVERSITY OF VIGO   (Spain)

^d Apoptosis and Genomics Research Group of the Hungarian Academy of Science   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; MACROPHAGE DERIVED CHEMOKINE; PROTEIN INHIBITOR; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; RETINOIC ACID RECEPTOR ALPHA AGONIST; RETINOIC ACID RECEPTOR ALPHA ANTAGONIST; RETINOIC ACID RECEPTOR GAMMA; RETINOIC ACID RECEPTOR GAMMA AGONIST; RETINOIC ACID RECEPTOR GAMMA ANTAGONIST; RETINOID X RECEPTOR; RETINOID X RECEPTOR AGONIST; RETINOID X RECEPTOR ANTAGONIST; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AUTOREGULATION; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; CRABP2 GENE; CRYSTALLIZATION; CYP26A1 GENE; CYP26B1 GENE; EPIDERMIS CELL; FEMALE; GENE; GENE CONTROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOMODULATION; KRT4 GENE; MOUSE; NONHUMAN; PROTEIN METABOLISM; PROTEIN SYNTHESIS; RBP1 GENE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN; SKIN BIOPSY; SKINFOLD THICKNESS;

ANIMALS; CLUSTER ANALYSIS; EPIDERMIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOMEOSTASIS; MICE; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; RETINOIDS; SIGNAL TRANSDUCTION; SKIN; TRETINOIN;

EID: 84876526571     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062643     Document Type: Article

References (81)

1. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, et al. (1995) The nuclear receptor superfamily: the second decade. Cell 83: 835-839.
2. Chapellier B, Mark M, Messaddeq N, Calleja C, Warot X, et al. (2002) Physiological and retinoid-induced proliferations of epidermis basal keratinocytes are differently controlled. Embo J 21: 3402-3413.
3. Feng X, Peng ZH, Di W, Li XY, Rochette-Egly C, et al. (1997) 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: 59-71.
4. Pérez E, Bourguet W, Gronemeyer H, de Lera AR, (2012) Modulation of RXR function through ligand design. Biochim Biophys Acta 1821: 57-69.
5. Fisher GJ, Talwar HS, Xiao JH, Datta SC, Reddy AP, et al. (1994) Immunological identification and functional quantitation of retinoic acid and retinoid X receptor proteins in human skin. J Biol Chem 269: 20629-20635.
6. Elder JT, Astrom A, Pettersson U, Tavakkol A, Krust A, et al. (1992) Retinoic acid receptors and binding proteins in human skin. J Invest Dermatol 98: 36S-41S.
7. Elder JT, Fisher GJ, Zhang QY, Eisen D, Krust A, et al. (1991) Retinoic acid receptor gene expression in human skin. J Invest Dermatol 96: 425-433.
8. Dolle P, Ruberte E, Leroy P, Morriss-Kay G, Chambon P, (1990) Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110: 1133-1151.
9. Germain P, Chambon P, Eichele G, Evans RM, Lazar MA, et al. (2006) International Union of Pharmacology. LX. Retinoic acid receptors. Pharmacol Rev 58: 712-725.
10. Redfern CP, Todd C, (1992) Retinoic acid receptor expression in human skin keratinocytes and dermal fibroblasts in vitro. J Cell Sci 102 (Pt 1): 113-121.
11. Altucci L, Leibowitz MD, Ogilvie KM, de Lera AR, Gronemeyer H, (2007) RAR and RXR modulation in cancer and metabolic disease. Nat Rev Drug Discov 6: 793-810.
12. de Lera AR, Bourguet W, Altucci L, Gronemeyer H, (2007) Design of selective nuclear receptor modulators: RAR and RXR as a case study. Nat Rev Drug Discov 6: 811-820.
13. Allenby G, Bocquel MT, Saunders M, Kazmer S, Speck J, et al. (1993) Retinoic acid receptors and retinoid X receptors: interactions with endogenous retinoic acids. Proc Natl Acad Sci U S A 90: 30-34.
14. Allenby G, Janocha R, Kazmer S, Speck J, Grippo JF, et al. (1994) Binding of 9-cis-retinoic acid and all-trans-retinoic acid to retinoic acid receptors alpha, beta, and gamma. Retinoic acid receptor gamma binds all-trans-retinoic acid preferentially over 9-cis-retinoic acid. J Biol Chem 269: 16689-16695.
15. Rühl R, Garcia A, Schweigert FJ, Worm M, (2004) Modulation of cytokine production by low and high retinoid diets in ovalbumin-sensitized mice. Int J Vitam Nutr Res 74: 279-284.
16. Rühl R, (2007) Effects of dietary retinoids and carotenoids on immune development. Proc Nutr Soc 66: 458-469.
17. Rühl R, Hanel A, Garcia AL, Dahten A, Herz U, et al. (2007) Role of vitamin A elimination or supplementation diets during postnatal development on the allergic sensitisation in mice. Mol Nutr Food Res 51: 1173-1181.
18. Roos TC, Jugert FK, Merk HF, Bickers DR, (1998) Retinoid metabolism in the skin. Pharmacol Rev 50: 315-333.
19. Elias PM, (1987) Retinoid effects on the epidermis. Dermatologica 175Suppl 1: 28-36.
20. Elias PM, Fritsch PO, Lampe M, Williams ML, Brown BE, et al. (1981) Retinoid effects on epidermal structure, differentiation, and permeability. Lab Invest 44: 531-540.
21. Everts HB, King LE Jr, Sundberg JP, Ong DE, (2004) Hair cycle-specific immunolocalization of retinoic acid synthesizing enzymes Aldh1a2 and Aldh1a3 indicate complex regulation. J Invest Dermatol 123: 258-263.
22. Everts HB, Sundberg JP, King LE Jr, Ong DE, (2007) Immunolocalization of enzymes, binding proteins, and receptors sufficient for retinoic acid synthesis and signaling during the hair cycle. J Invest Dermatol 127: 1593-1604.
23. Saurat JH, (1999) Retinoids and psoriasis: novel issues in retinoid pharmacology and implications for psoriasis treatment. J Am Acad Dermatol 41: S2-6.
24. Mevorah B, Salomon D, Siegenthaler G, Hohl D, Meier ML, et al. (1996) Ichthyosiform dermatosis with superficial blister formation and peeling: evidence for a desmosomal anomaly and altered epidermal vitamin A metabolism. J Am Acad Dermatol 34: 379-385.
25. Mihály J, Gamlieli A, Worm M, Rühl R, (2011) Decreased retinoid concentration and retinoid signalling pathways in human atopic dermatitis. Exp Dermatol 20: 326-330.
26. Swann RT, Smith DE, Tramposch KM, Zusi FC (1996) Preparation and RARg-specific retinoid receptor transactivation of retinobenzoic acid derivatives. Eur Pat Appl EP 747347.
27. Zusi FC, Reczek PR, Ostrowski J (1998) Preparation of 5-substituted-1,1,3,3-tetramethyl-2-ketoindanes as retinoid-like compounds. PCT Int Appl WO 9847861.
28. Starrett JE, Tortolani DR, Mansuri MM, Meanwell NA (1996) Retinoid-like heterocycles: US5559248. US patents.
29. Starrett JE, Tortolani DR, Mansuri MM, Meanwell NA (1998) Heterocyclic-substituted naphthalenyl retinobenzoic acid derivatives: US5849923. US patents.
30. Alvarez S, Alvarez R, Khanwalkar H, Germain P, Lemaire G, et al. (2009) Retinoid receptor subtype-selective modulators through synthetic modifications of RARgamma agonists. Bioorg Med Chem 17: 4345-4359.
31. Tsang KY, Sinha S, Liu X, Bhat S, Chandarardna RAS (2007) Disubstituted chalcone oximes having RARg retinoid receptor antagonist activities. US 7,253,319 B2.
32. Tsang KY, Sinha S, Liu XB, Bath S, Chandraratna RAS (2005) Disubstituted chalcone oximes having RARg retinoid receptor antagonist activity. US 2005/0165095.
33. Bourguet W, de Lera AR, Gronemeyer H, (2010) Inverse agonists and antagonists of retinoid receptors. Methods Enzymol 485: 161-195.
34. Nahoum V, Perez E, Germain P, Rodriguez-Barrios F, Manzo F, et al. (2007) Modulators of the structural dynamics of the retinoid X receptor to reveal receptor function. Proc Natl Acad Sci U S A 104: 17323-17328.
35. Calleja C, Messaddeq N, Chapellier B, Yang H, Krezel W, et al. (2006) Genetic and pharmacological evidence that a retinoic acid cannot be the RXR-activating ligand in mouse epidermis keratinocytes. Genes Dev 20: 1525-1538.
36. Rühl R, (2006) Method to determine 4-oxo-retinoic acids, retinoic acids and retinol in serum and cell extracts by liquid chromatography/diode-array detection atmospheric pressure chemical ionisation tandem mass spectrometry. Rapid Commun Mass Spectrom 20: 2497-2504.
37. Cheepala SB, Syed Z, Trutschl M, Cvek U, Clifford JL, (2007) Retinoids and skin: microarrays shed new light on chemopreventive action of all-trans retinoic acid. Mol Carcinog 46: 634-639.
38. Fisher GJ, Voorhees JJ, (1996) Molecular mechanisms of retinoid actions in skin. Faseb J 10: 1002-1013.
39. Roelandt T, Thys B, Heughebaert C, De Vroede A, De Paepe K, et al. (2009) LEKTI-1 in sickness and in health. Int J Cosmet Sci 31: 247-254.
40. Brattsand M, Stefansson K, Lundh C, Haasum Y, Egelrud T, (2005) A proteolytic cascade of kallikreins in the stratum corneum. J Invest Dermatol 124: 198-203.
41. Caubet C, Jonca N, Brattsand M, Guerrin M, Bernard D, et al. (2004) Degradation of corneodesmosome proteins by two serine proteases of the kallikrein family, SCTE/KLK5/hK5 and SCCE/KLK7/hK7. J Invest Dermatol 122: 1235-1244.
42. Lee DD, Stojadinovic O, Krzyzanowska A, Vouthounis C, Blumenberg M, et al. (2009) Retinoid-responsive transcriptional changes in epidermal keratinocytes. J Cell Physiol 220: 427-439.
43. Yoshimura K, Uchida G, Okazaki M, Kitano Y, Harii K, (2003) Differential expression of heparin-binding EGF-like growth factor (HB-EGF) mRNA in normal human keratinocytes induced by a variety of natural and synthetic retinoids. Exp Dermatol 12Suppl 2: 28-34.
44. Weiss RA, Eichner R, Sun TT, (1984) Monoclonal antibody analysis of keratin expression in epidermal diseases: a 48- and 56-kdalton keratin as molecular markers for hyperproliferative keratinocytes. J Cell Biol 98: 1397-1406.
45. Romanowska M, al Yacoub N, Seidel H, Donandt S, Gerken H, et al. (2008) PPARdelta enhances keratinocyte proliferation in psoriasis and induces heparin-binding EGF-like growth factor. J Invest Dermatol 128: 110-124.
46. Romanowska M, Reilly L, Palmer CN, Gustafsson MC, Foerster J, (2010) Activation of PPARbeta/delta causes a psoriasis-like skin disease in vivo. PLoS One 5: e9701.
47. Michalik L, Desvergne B, Tan NS, Basu-Modak S, Escher P, et al. (2001) Impaired skin wound healing in peroxisome proliferator-activated receptor (PPAR)alpha and PPARbeta mutant mice. J Cell Biol 154: 799-814.
48. Tan NS, Michalik L, Desvergne B, Wahli W, (2005) Multiple expression control mechanisms of peroxisome proliferator-activated receptors and their target genes. J Steroid Biochem Mol Biol 93: 99-105.
49. Proksch E, Brandner JM, Jensen JM, (2008) The skin: an indispensable barrier. Exp Dermatol 17: 1063-1072.
50. Akiyama M, (2011) The roles of ABCA12 in keratinocyte differentiation and lipid barrier formation in the epidermis. Dermatoendocrinol 3: 107-112.
51. Jennemann R, Sandhoff R, Langbein L, Kaden S, Rothermel U, et al. (2007) Integrity and barrier function of the epidermis critically depend on glucosylceramide synthesis. J Biol Chem 282: 3083-3094.
52. Holleran WM, Takagi Y, Uchida Y, (2006) Epidermal sphingolipids: metabolism, function, and roles in skin disorders. FEBS Lett 580: 5456-5466.
53. Harris IR, Farrell AM, Grunfeld C, Holleran WM, Elias PM, et al. (1997) Permeability barrier disruption coordinately regulates mRNA levels for key enzymes of cholesterol, fatty acid, and ceramide synthesis in the epidermis. J Invest Dermatol 109: 783-787.
54. Mao C, Xu R, Szulc ZM, Bielawski J, Becker KP, et al. (2003) Cloning and characterization of a mouse endoplasmic reticulum alkaline ceramidase: an enzyme that preferentially regulates metabolism of very long chain ceramides. J Biol Chem 278: 31184-31191.
55. Fullerton A, Serup J, (1997) Characterization of irritant patch test reactions to topical D vitamins and all-trans retinoic acid in comparison with sodium lauryl sulphate. Evaluation by clinical scoring and multiparametric non-invasive measuring techniques. Br J Dermatol 137: 234-240.
56. Attar PS, Wertz PW, McArthur M, Imakado S, Bickenbach JR, et al. (1997) Inhibition of retinoid signaling in transgenic mice alters lipid processing and disrupts epidermal barrier function. Mol Endocrinol 11: 792-800.
57. Li M, Chiba H, Warot X, Messaddeq N, Gerard C, et al. (2001) RXR-alpha ablation in skin keratinocytes results in alopecia and epidermal alterations. Development 128: 675-688.
58. Li M, Indra AK, Warot X, Brocard J, Messaddeq N, et al. (2000) Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis. Nature 407: 633-636.
59. Stücker M, Hoffmann M, Altmeyer P, (2002) Instrumental evaluation of retinoid-induced skin irritation. Skin Res Technol 8: 133-140.
60. Stephensen CB, (2001) Vitamin A, infection, and immune function. Annu Rev Nutr 21: 167-192.
61. Stephensen CB, Rasooly R, Jiang X, Ceddia MA, Weaver CT, et al. (2002) Vitamin A enhances in vitro Th2 development via retinoid X receptor pathway. J Immunol 168: 4495-4503.
62. Dawson HD, Collins G, Pyle R, Key M, Taub DD, (2008) The Retinoic Acid Receptor-alpha mediates human T-cell activation and Th2 cytokine and chemokine production. BMC Immunol 9: 16.
63. Iwata M, Eshima Y, Kagechika H, (2003) Retinoic acids exert direct effects on T cells to suppress Th1 development and enhance Th2 development via retinoic acid receptors. Int Immunol 15: 1017-1025.
64. Imai T, Nagira M, Takagi S, Kakizaki M, Nishimura M, et al. (1999) Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int Immunol 11: 81-88.
65. Bonecchi R, Bianchi G, Bordignon PP, D'Ambrosio D, Lang R, et al. (1998) Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J Exp Med 187: 129-134.
66. Sallusto F, Mackay CR, Lanzavecchia A, (1997) Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science 277: 2005-2007.
67. Dulkys Y, Schramm G, Kimmig D, Knoss S, Weyergraf A, et al. (2001) Detection of mRNA for eotaxin-2 and eotaxin-3 in human dermal fibroblasts and their distinct activation profile on human eosinophils. J Invest Dermatol 116: 498-505.
68. Menzies-Gow A, Ying S, Sabroe I, Stubbs VL, Soler D, et al. (2002) Eotaxin (CCL11) and eotaxin-2 (CCL24) induce recruitment of eosinophils, basophils, neutrophils, and macrophages as well as features of early- and late-phase allergic reactions following cutaneous injection in human atopic and nonatopic volunteers. J Immunol 169: 2712-2718.
69. Sabroe I, Hartnell A, Jopling LA, Bel S, Ponath PD, et al. (1999) Differential regulation of eosinophil chemokine signaling via CCR3 and non-CCR3 pathways. J Immunol 162: 2946-2955.
70. Balmer JE, Blomhoff R, (2002) Gene expression regulation by retinoic acid. J Lipid Res 43: 1773-1808.
71. Virtanen M, Torma H, Vahlquist A, (2000) Keratin 4 upregulation by retinoic acid in vivo: a sensitive marker for retinoid bioactivity in human epidermis. J Invest Dermatol 114: 487-493.
72. Goyette P, Feng Chen C, Wang W, Seguin F, Lohnes D, (2000) Characterization of retinoic acid receptor-deficient keratinocytes. J Biol Chem 275: 16497-16505.
73. Schug TT, Berry DC, Shaw NS, Travis SN, Noy N, (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129: 723-733.
74. Goodman DS, (1984) Overview of current knowledge of metabolism of vitamin A and carotenoids. J Natl Cancer Inst 73: 1375-1379.
75. Chai X, Zhai Y, Napoli JL, (1997) cDNA cloning and characterization of a cis-retinol/3alpha-hydroxysterol short-chain dehydrogenase. J Biol Chem 272: 33125-33131.
76. Kiefer C, Hessel S, Lampert JM, Vogt K, Lederer MO, et al. (2001) Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J Biol Chem. 276: 14110-14116.
77. Tan NS, Michalik L, Noy N, Yasmin R, Pacot C, et al. (2001) Critical roles of PPAR beta/delta in keratinocyte response to inflammation. Genes Dev 15: 3263-3277.
78. Shaw N, Elholm M, Noy N, (2003) Retinoic acid is a high affinity selective ligand for the peroxisome proliferator-activated receptor beta/delta. J Biol Chem 278: 41589-41592.
79. Perlmann T, Jansson L, (1995) A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and NURR1. Genes Dev 9: 769-782.
80. Volakakis N, Joodmardi E, Perlmann T, (2009) NR4A orphan nuclear receptors influence retinoic acid and docosahexaenoic acid signaling via up-regulation of fatty acid binding protein 5. Biochem Biophys Res Commun 390: 1186-1191.
81. Haider AS, Lowes MA, Suarez-Farinas M, Zaba LC, Cardinale I, et al. (2008) Cellular genomic maps help dissect pathology in human skin disease. J Invest Dermatol 128: 606-615.