Cholesterol regulates melanogenesis in human epidermal melanocytes and melanoma cells

Experimental Dermatology

Volumn 18, Issue 8, 2009, Pages 680-688

  Schallreuter, Karin U ^a,b   Hasse, Sybille ^a,b   Rokos, Hartmut ^a,b   Chavan, Bhaven ^a   Shalbaf, Mohamed ^a   Spencer, Jennifer D ^a,b   Wood, John M ^a  

^a UNIVERSITY OF BRADFORD   (United Kingdom)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Cholesterol; HMG CoA reductase; LDL receptor; Melanogenesis

Indexed keywords

APOLIPOPROTEIN B100; CHOLESTEROL; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ESTROGEN RECEPTOR BETA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MELANIN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MONOPHENOL MONOOXYGENASE; TYROSINE 3 MONOOXYGENASE;

AMELANOTIC MELANOMA; ARTICLE; CELL LEVEL; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; KERATINOCYTE; MELANOCYTE; MELANOGENESIS; MELANOMA CELL; MELANOSOME; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN PIGMENTATION; WESTERN BLOTTING;

APOLIPOPROTEIN B-100; CELL LINE, TUMOR; CHOLESTEROL; CYCLIC AMP; EPIDERMIS; HUMANS; MELANOCYTES; MELANOMA; MODELS, BIOLOGICAL; PIGMENTATION; RECEPTORS, ESTROGEN; RECEPTORS, LDL; TIME FACTORS; VITAMIN D;

EID: 70449463450     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2009.00850.x     Document Type: Article

References (60)

1. Marks D B, Marks A D, Smith C M, Walker J. Oxygen Metabolism and Toxicity. Basic Medical Biochemistry 1996, 327-340. In, ed, Baltimore, Williams & Wilkin
2. Brown M S, Goldstein J L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89:331-340.
3. Schürer N Y, Plewig G, Elias P M. Stratum corneum lipid function. Dermatologica 1991, 183:77-94.
4. Menon G K, Grayson S, Elias P M. Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry. J Invest Dermatol 1985, 84:508-512.
5. Landmann L. The epidermal permeability barrier. Anat Embryol (Berl) 1988, 178:1-13.
6. Thiboutot D, Jabara S, McAllister J M. Human skin is a steroidogenic tissue: steroidogenic enzymes and cofactors are expressed in epidermis, normal sebocytes, and an immortalized sebocyte cell line (SEB-1). J Invest Dermatol 2003, 120:905-914.
7. Chen W, Thiboutot D, Zouboulis C C. Cutaneous androgen metabolism: basic research and clinical perspectives. J Invest Dermatol 2002, 119:992-1007.
8. Slominski A, Wortsman J. Neuroendocrinology of the skin. Endocr Rev 2000, 21:457-487.
9. Slominski A, Ermak G, Mihm M. ACTH receptor, CYP11A1, CYP17 and CYP21A2 genes are expressed in skin. J Clin Endocrinol Metab 1996, 81:2746-2749.
10. Slominski A, Zjawiony J, Wortsman J. A novel pathway for sequential transformation of 7-dehydrocholesterol and expression of the P450scc system in mammalian skin. Eur J Biochem 2004, 271:4178-4188.
11. Thornton M J, Taylor A H, Mulligan K. Oestrogen receptor beta is the predominant oestrogen receptor in human scalp skin. Exp Dermatol 2003, 12:181-190.
12. Kippenberger S, Loitsch S, Solano F, Bernd A, Kaufmann R. Quantification of tyrosinase, TRP-1, and Trp-2 transcripts in human melanocytes by reverse transcriptase-competitive multiplex PCR--regulation by steroid hormones. J Invest Dermatol 1998, 110:364-367.
13. Slominski A, Zbytek B, Szczesniewski A. CRH stimulation of corticosteroids production in melanocytes is mediated by ACTH. Am J Physiol Endocrinol Metab 2005, 288:E701-E706.
14. Jee S H, Lee S Y, Chiu H C, Chang C C, Chen T J. Effects of estrogen and estrogen receptor in normal human melanocytes. Biochem Biophys Res Commun 1994, 199:1407-1412.
15. McLeod S D, Ranson M, Mason R S. Effects of estrogens on human melanocytes in vitro. J Steroid Biochem Mol Biol 1994, 49:9-14.
16. Schallreuter K U, Kothari S, Chavan B, Spencer J D. Regulation of melanogenesis - controversies and new concepts. Exp Dermatol 2008, 17:395-404.
17. Slominski A, Zbytek B, Zmijewski M. Corticotropin releasing hormone and the skin. Front Biosci 2006, 11:2230-2248.
18. Lazaroff M, Patankar S, Yoon S O, Chikaraishi D M. The cyclic AMP response element directs tyrosine hydroxylase expression in catecholaminergic central and peripheral nervous system cell lines from transgenic mice. J Biol Chem 1995, 270:21579-21589.
19. Price E R, Horstmann M A, Wells A G. alpha-Melanocyte-stimulating hormone signaling regulates expression of microphthalmia, a gene deficient in Waardenburg syndrome. J Biol Chem 1998, 273:33042-33047.
20. Hirayama K, Shimoji M, Swick L, Meyer A, Kapatos G. Characterization of GTP cyclohydrolase I gene expression in the human neuroblastoma SKN-BE(2)M17: enhanced transcription in response to cAMP is conferred by the proximal promoter. J Neurochem 2001, 79:576-587.
21. Spencer J D, Schallreuter K U. Regulation of pigmentation in human epidermal melanocytes by functional high-affinity beta melanocyte-stimulating hormone/melanocortin-4 receptor signaling. Endocrinology 2009, 150.
22. Marles L K, Peters E M, Tobin D J, Hibberts N A, Schallreuter K U. Tyrosine hydroxylase isoenzyme I is present in human melanosomes: a possible novel function in pigmentation. Exp Dermatol 2003, 12:61-70.
23. Brooks A R, Blackhart B D, Haubold K, Levy-Wilson B. Characterization of tissue-specific enhancer elements in the second intron of the human apolipoprotein B gene. J Biol Chem 1991, 266:7848-7859.
24. Brooks A R, Levy-Wilson B. Hepatocyte nuclear factor 1 and C/EBP are essential for the activity of the human apolipoprotein B gene second-intron enhancer. Mol Cell Biol 1992, 12:1134-1148.
25. Hasse S, Kothari S, Rokos H, Kauser S, Schürer N Y, Schallreuter K U. In vivo and in vitro evidence for autocrine DCoH/HNF-1alpha transcription of albumin in the human epidermis. Exp Dermatol 2005, 14:182-187.
26. Pittelkow M, Shipley J. Serum-free culture of normal human melanocytes: growth kinetics and growth factor requirements. J Cell Physiol 1989, 140:565-576.
27. Seiji M, Fitzpatrick T B, Birbeck M S. The melanosome: a distinctive subcellular particle of mammalian melanocytes and the site of melanogenesis. J Invest Dermatol 1961, 36:243-252.
28. Kiistala U, Mustakallio K. Dermo-epidermal separation with suction. Electron microscopic and histochemical study of initial events of blistering on human skin. J Invest Dermatol 1967, 48:466-477.
29. Schallreuter K U, Gibbons N C, Elwary S M, Parkin S M, Wood J M. Calcium-activated butyrylcholinesterase in human skin protects acetylcholinesterase against suicide inhibition by neurotoxic organophosphates. Biochem Biophys Res Commun 2007, 355:1069-1074.
30. Kalb V F, Bernlohr R W. A new spectrophotometric assay for protein in cell extracts. Anal Biochem 1977, 82:362-371.
31. Peiretti E, Dessi S, Putzolu M, Fossarello M. Hyperexpression of low-density lipoprotein receptors and hydroxy-methylglutaryl-coenzyme A-reductase in human pinguecula and primary pterygium. Invest Ophthalmol Vis Sci 2004, 45:3982-3985.
32. Whittaker J R. Changes in melanogenesis during the dedifferentiation of chick retinal pigment cells in cell culture. Dev Biol 1963, 53:99-127.
33. Weerheim A, Ponec M. Determination of stratum corneum lipid profile by tape stripping in combination with high-performance thin-layer chromatography. Arch Dermatol Res 2001, 293:191-199.
34. Ponec M, te Pas M F, Havekes L, Boonstra J, Mommaas A M, Vermeer B J. LDL receptors in keratinocytes. J Invest Dermatol 1992, 98:50S-56S.
35. Williams M L, Mommaas-Kienhuis A M, Rutherford S L, Grayson S, Vermeer B J, Elias P M. Free sterol metabolism and low density lipoprotein receptor expression as differentiation markers of cultured human keratinocytes. J Cell Physiol 1987, 132:428-440.
36. te Pas M F, Lombardi P, Havekes L M, Boonstra J, Ponec M. Regulation of low-density lipoprotein receptor expression during keratinocyte differentiation. J Invest Dermatol 1991, 97:334-339.
37. Ponec M, Havekes L, Kempenaar J. Calcium-mediated regulation of the low density lipoprotein receptor and intracellular cholesterol synthesis in human epidermal keratinocytes. J Cell Physiol 1985, 125:98-106.
38. Harris I R, Siefken W, Beck-Oldach K, Brandt M, Wittern K P, Pollet D. Comparison of activities dependent on glutathione S-transferase and cytochrome P-450 IA1 in cultured keratinocytes and reconstructed epidermal models. Skin Pharmacol Appl Skin Physiol 2002, 15(Suppl. 1):59-67.
39. Elias P M. Epidermal lipids, barrier function, and desquamation. J Invest Dermatol 1983, 80(Suppl.):44s-49s.
40. Miranda M, Amicarelli F, Bonfigli A, Botti D, Zarivi O, Poma A. Changes of lipo-melanosome membrane leakage versus pH, charge and composition. Melanoma Res 1991, 1:195-200.
41. Rozanowska M, Korytowski W, Rozanowski B. Photoreactivity of aged human RPE melanosomes: a comparison with lipofuscin. Invest Ophthalmol Vis Sci 2002, 43:2088-2096.
42. Vedralova E, Duchon J. Comparison of lipids between tumor and normal hamster melanosomes. Neoplasma 1983, 30:317-321.
43. Haberberger R V, Pfeil U, Lips K S, Kummer W. Expression of the high affinity-choline transporter, CHT1, in the neuronal and non-neuronal cholinergic system of human and rat skin. J Invest Dermatol 2002, 119:943-948.
44. Thornton M J. The biological actions of estrogens on skin. Exp Dermatol 2002, 11:487-502.
45. Thornton M J. Oestrogen functions in skin and skin appendages. Expert Opin Ther Targets 2005, 9:617-629.
46. Schallreuter K U, Bahadoran P, Picardo M. Vitiligo pathogenesis: autoimmune disease, genetic defect, excessive reactive oxygen species, calcium imbalance, or what else?. Exp Dermatology 2007, 17:139-160.
47. Ranson M, Posen S, Mason R S. Human melanocytes as a target tissue for hormones: in vitro studies with 1 alpha-25, dihydroxyvitamin D3, alpha-melanocyte stimulating hormone, and beta-estradiol. J Invest Dermatol 1988, 91:593-598.
48. Cui R, Widlund H R, Feige E. Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell 2007, 128:853-864.
49. Pietras R J, Levin E R, Szego C M. Estrogen receptors and cell signaling. Science 2005, 310:51-53. Author reply -3
50. Fuse N, Yasumoto K, Suzuki H, Takahashi K, Shibahara S. Identification of a melanocyte-type promoter of the microphthalmia-associated transcription factor gene. Biochem Biophys Res Commun 1996, 219:702-707.
51. Bentley-Phillips B, Bayles M A. Cutaneous reactions to topical application of hydroquinone. Results of a 6-year investigation. S Afr Med J 1975, 49:1391-1395.
52. Serova L I, Filipenko M, Schilt N, Veerasirikul M, Sabban E L. Estrogen-triggered activation of GTP cyclohydrolase 1 gene expression: role of estrogen receptor subtypes and interaction with cyclic AMP. Neuroscience 2006, 140:1253-1263.
53. Schallreuter K U, Wood J M. The importance of L-phenylalanine transport and its autocrine turnover to L-tyrosine for melanogenesis in human epidermal melanocytes. Biochem Biophys Res Commun 1999, 262:423-428.
54. Wood J M, Schallreuter-Wood K U, Lindsey N J, Callaghan S, Gardner M L. A specific tetrahydrobiopterin binding domain on tyrosinase controls melanogenesis. Biochem Biophys Res Commun 1995, 206:480-485.
55. Wood J M, Chavan B, Hafeez I, Schallreuter K U. Regulation of tyrosinase by tetrahydropteridines and H2O2. Biochem Biophys Res Commun 2004, 325:1412-1417.
56. Schallreuter K U, Wood J M, Pittelkow M R. Regulation of melanin biosynthesis in the human epidermis by tetrahydrobiopterin. Science 1994, 263:1444-1446.
57. Citron B A, Davis M D, Milstien S. Identify of 4a carbinolamine dehydratase, a component of the phenylalanine hydroxylase system, and DCoH a transregulator of homeodomain proteins. Proc Natl Acad Sci U S A 1992, 89:11891-11894.
58. Hauer C R, Rebrin I, Thöny B. Phenylalanine hydroxylase-stimulating protein/pterin-4-alpha-carbinolamine dehydratase from rat and liver. Purification, characterisation and complete amino acid sequence. J Biol Chem 1993, 268:4828-4831.
59. Schallreuter K U, Kothari S, Hasse S. In situ and in vitro evidence for DCoH/HNF-1 alpha transcription of tyrosinase in human skin melanocytes. Biochem Biophys Res Commun 2003, 301:610-616.
60. Stryer L. Biochemistry 1988, New York, W.H. Freeman and Company