Metabolism of melatonin and biological activity of intermediates of melatoninergic pathway in human skin cells

FASEB Journal

Volumn 27, Issue 7, 2013, Pages 2742-2755

  Kim, Tae Kang ^a   Kleszczynśki, Konrad ^b   Janjetovic, Zorica ^a   Sweatman, Trevor ^a   Lin, Zongtao ^a   Li, Wei ^a   Reiter, Russel J ^c   Fischer, Tobias W ^b   Slominski, Andrzej T ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF LÜBECK   (Germany)

^c Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

5 methoxytryptamine; 6 hydroxymelatonin; AFMK; Keratinocytes; Melanocytes

Indexed keywords

6 HYDROXYMELATONIN; CYTOKERATIN 10; CYTOKERATIN 14; KI 67 ANTIGEN; MELATONIN; N ACETYLSEROTONIN;

ARTICLE; CELL DIFFERENTIATION; EPIDERMIS; EX VIVO STUDY; FIBROBLAST; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORMONE METABOLISM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; KERATINOCYTE; MELANOCYTE; MELANOMA CELL; PRIORITY JOURNAL; SKIN CELL; UPREGULATION;

5-METHOXYTRYPTAMINE; 6-HYDROXYMELATONIN; AFMK; KERATINOCYTES; MELANOCYTES;

5-METHOXYTRYPTAMINE; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EPIDERMIS; FEMALE; FIBROBLASTS; HUMANS; KERATIN-10; KERATIN-14; KERATINOCYTES; KINETICS; KYNURAMINE; MELANOCYTES; MELANOMA; MELATONIN; METABOLIC NETWORKS AND PATHWAYS; SEROTONIN; SKIN; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SWINE;

EID: 84879654262     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-224691     Document Type: Article

References (66)

1. Tan, D. X., Manchester, L. C., Hardeland, R., Lopez-Burillo, S., Mayo, J. C., Sainz, R. M., and Reiter, R. J. (2003) Melatonin: a hormone, a tissue factor, an autocoid, a paracoid, and an antioxidant vitamin. J. Pineal Res. 34, 75-78
2. Hardeland, R., Cardinali, D. P., Srinivasan, V., Spence, D. W., Brown, G. M., and Pandi-Perumal, S. R. (2011) Melatonin - a pleiotropic, orchestrating regulator molecule. Prog. Neurobiol. 93, 350-384
3. Reiter, R. J., Tan, D. X., and Fuentes-Broto, L. (2010) Melatonin: a multitasking molecule. Prog. Brain Res. 181, 127-151
4. Stehle, J. H., Saade, A., Rawashdeh, O., Ackermann, K., Jilg, A., Sebesteny, T., and Maronde, E. (2011) A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function, and chronobiological diseases. J. Pineal Res. 51, 17-43
5. Iriti, M., Varoni, E. M., and Vitalini, S. (2010) Melatonin in traditional Mediterranean diets. J. Pineal Res. 49, 101-105
6. Slominski, A., Tobin, D. J., Zmijewski, M. A., Wortsman, J., and Paus, R. (2008) Melatonin in the skin: synthesis, metabolism and functions. Trends Endocrinol. Metab. 19, 17-24
7. Slominski, R. M., Reiter, R. J., Schlabritz-Loutsevitch, N., Ostrom, R. S., and Slominski, A. T. (2012) Melatonin membrane receptors in peripheral tissues: distribution and functions. Mol. Cell. Endocrinol. 351, 152-166
8. Reiter, R. J. (1991) Pineal melatonin: cell biology of its synthesis and of its physiological interactions. Endocr. Rev. 12, 151-180
9. Dubocovich, M. L., Delagrange, P., Krause, D. N., Sugden, D., Cardinali, D. P., and Olcese, J. (2010) International Union of Basic and Clinical Pharmacology. LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors. Pharmacol. Rev. 62, 343-380
10. Lanoix, D., Lacasse, A. A., Reiter, R. J., and Vaillancourt, C. (2012) Melatonin: the smart killer: the human trophoblast as a model. Mol. Cell. Endocrinol. 348, 1-11
11. Jockers, R., Maurice, P., Boutin, J. A., and Delagrange, P. (2008) Melatonin receptors, heterodimerization, signal transduction and binding sites: what's new? Br. J. Pharmacol. 154, 1182-1195 (Pubitemid 351992057)
12. Tan, D. X., Manchester, L. C., Burkhardt, S., Sainz, R. M., Mayo, J. C., Kohen, R., Shohami, E., Huo, Y. S., Hardeland, R., and Reiter, R. J. (2001) N1-acetyl-N2-formyl-5-methoxykynuramine, a biogenic amine and melatonin metabolite, functions as a potent antioxidant. FASEB J. 15, 2294-2296
13. Luchetti, F., Canonico, B., Betti, M., Arcangeletti, M., Pilolli, F., Piroddi, M., Canesi, L., Papa, S., and Galli, F. (2010) Melatonin signaling and cell protection function. FASEB J. 24, 3603-3624
14. Semak, I., Naumova, M., Korik, E., Terekhovich, V., Wortsman, J., and Slominski, A. (2005) A novel metabolic pathway of melatonin: oxidation by cytochrome c. Biochemistry 44, 9300-9307 (Pubitemid 40934380)
15. Nosjean, O., Ferro, M., Coge, F., Beauverger, P., Henlin, J. M., Lefoulon, F., Fauchere, J. L., Delagrange, P., Canet, E., and Boutin, J. A. (2000) Identification of the melatonin-binding site MT3 as the quinone reductase 2. J. Biol. Chem. 275, 31311-31317
16. Fischer, T. W., Slominski, A., Zmijewski, M. A., Reiter, R. J., and Paus, R. (2008) Melatonin as a major skin protectant: from free radical scavenging to DNA damage repair. Exp. Dermatol. 17, 713-730
17. Slominski, A., Wortsman, J., and Tobin, D. J. (2005) The cutaneous serotoninergic/melatoninergic system: securing a place under the sun. FASEB J. 19, 176-194 (Pubitemid 40189259)
18. Facciola, G., Hidestrand, M., von Bahr, C., and Tybring, G. (2001) Cytochrome P450 isoforms involved in melatonin metabolism in human liver microsomes. Eur. J. Clin. Pharmacol. 56, 881-888 (Pubitemid 33788564)
19. Semak, I., Korik, E., Antonova, M., Wortsman, J., and Slominski, A. (2008) Metabolism of melatonin by cytochrome P450s in rat liver mitochondria and microsomes. J. Pineal. Res. 45, 515-523
20. Grace, M. S., Cahill, G. M., and Besharse, J. C. (1991) Melatonin deacetylation: retinal vertebrate class distribution and Xenopus laevis tissue distribution. Brain Res. 559, 56-63
21. Rogawski, M. A., Roth, R. H., and Aghajanian, G. K. (1979) Melatonin: deacetylation to 5-methoxytryptamine by liver but not brain aryl acylamidase. J. Neurochem. 32, 1219-1226 (Pubitemid 9156789)
22. Hirata, F., Hayaishi, O., Tokuyama, T., and Seno, S. (1974) In vitro and in vivo formation of two new metabolites of melatonin. J. Biol. Chem. 249, 1311-1313
23. Hardeland, R., Reiter, R. J., Poeggeler, B., and Tan, D. X. (1993) The significance of the metabolism of the neurohormone melatonin: antioxidative protection and formation of bioactive substances. Neurosci. Biobehav. Rev. 17, 347-357 (Pubitemid 23306320)
24. Tan, D. X., Manchester, L. C., Terron, M. P., Flores, L. J., and Reiter, R. J. (2007) One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J. Pineal Res. 42, 28-42 (Pubitemid 44924323)
25. Fischer, T. W., Sweatman, T. W., Semak, I., Sayre, R. M., Wortsman, J., and Slominski, A. (2006) Constitutive and UV-induced metabolism of melatonin in keratinocytes and cell-free systems. FASEB J. 20, 1564-1566
26. Slominski, A. T., Zmijewski, M. A., Skobowiat, C., Zbytek, B., Slominski, R. M., and Steketee, J. D. (2012) Sensing the environment: regulation of local and global homeostasis by the skin's neuroendocrine system. Adv. Anat. Embryol. Cell. Biol. 212, 1-115
27. Slominski, A., and Wortsman, J. (2000) Neuroendocrinology of the skin. Endocr. Rev. 21, 457-487
28. Slominski, A., Wortsman, J., Tuckey, R. C., and Paus, R. (2007) Differential expression of HPA axis homolog in the skin. Mol. Cell. Endocrinol. 265-266, 143-149 (Pubitemid 46273958)
29. Slominski, A., Fischer, T. W., Zmijewski, M. A., Wortsman, J., Semak, I., Zbytek, B., Slominski, R. M., and Tobin, D. J. (2005) On the role of melatonin in skin physiology and pathology. Endocrine 27, 137-148
30. Fischer, T. W., Slominski, A., Tobin, D. J., and Paus, R. (2008) Melatonin and the hair follicle. J. Pineal Res. 44, 1-15 (Pubitemid 350231105)
31. Slominski, A., Baker, J., Rosano, T. G., Guisti, L. W., Ermak, G., Grande, M., and Gaudet, S. J. (1996) Metabolism of serotonin to N-acetylserotonin, melatonin, and 5-methoxytryptamine in hamster skin culture. J. Biol. Chem. 271, 12281-12286
32. Slominski, A., Pisarchik, A., Semak, I., Sweatman, T., Wortsman, J., Szczesniewski, A., Slugocki, G., McNulty, J., Kauser, S., Tobin, D. J., Jing, C., and Johansson, O. (2002) Serotoninergic and melatoninergic systems are fully expressed in human skin. FASEB J. 16, 896-898
33. Slominski, A., Pisarchik, A., Johansson, O., Jing, C., Semak, I., Slugocki, G., and Wortsman, J. (2003) Tryptophan hydroxylase expression in human skin cells. Biochim. Biophys. Acta 1639, 80-86 (Pubitemid 38366211)
34. Slominski, A., Pisarchik, A., Semak, I., Sweatman, T., Szczesniewski, A., and Wortsman, J. (2002) Serotoninergic system in hamster skin. J. Invest. Dermatol. 119, 934-942 (Pubitemid 35340921)
35. Slominski, A., Pisarchik, A., Zbytek, B., Tobin, D. J., Kauser, S., and Wortsman, J. (2003) Functional activity of serotoninergic and melatoninergic systems expressed in the skin. J. Cell. Physiol. 196, 144-153 (Pubitemid 36676452)
36. Fischer, T. W., Kleszczynski, K., Hardkop, L. H., Kruse, N., and Zillikens, D. (2012) Melatonin enhances antioxidative enzyme gene expression (CAT, GPx, SOD), prevents their UVR-induced depletion, and protects against the formation of DNA damage (8-hydroxy-2=-deoxyguanosine) in ex vivo human skin. J. Pineal Res 23171152
37. Kleszczynski, K., Hardkop, L. H., and Fischer, T. W. (2011) Differential effects of melatonin as a broad range UV-damage preventive dermato-endocrine regulator. Dermato-endocrinology 3, 27-31
38. Slominski, A., Tobin, D. J., Shibahara, S., and Wortsman, J. (2004) Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 84, 1155-1228 (Pubitemid 39287950)
39. Slominski, A., Wortsman, J., Plonka, P. M., Schallreuter, K. U., Paus, R., and Tobin, D. J. (2005) Hair follicle pigmentation. J. Invest. Dermatol. 124, 13-21 (Pubitemid 40100943)
40. Kleszczynski, K., and Fischer, T. W. (2012) Development of a short-term human full-thickness skin organ culture model in vitro under serum-free conditions. Arch. Dermatol. Res. 304, 579-587
41. Slominski, A., Zbytek, B., and Slominski, R. (2009) Inhibitors of melanogenesis increase toxicity of cyclophosphamide and lymphocytes against melanoma cells. Int. J. Cancer 124, 1470-1477
42. 2 is a noncalcemic analog of vitamin D with potent antiproliferative and prodifferentiation activities in normal and malignant cells. Am. J. Physiol. Cell Physiol. 300, C526-C541
43. Slominski, A. T., Li, W., Bhattacharya, S. K., Smith, R. A., Johnson, P. L., Chen, J., Nelson, K. E., Tuckey, R. C., Miller, D., Jiao, Y., Gu, W., and Postlethwaite, A. E. (2011) Vitamin D analogs 17,20S(OH)2pD and 17,20R(OH)2pD are noncalcemic and exhibit antifibrotic activity. J. Invest. Dermatol. 131, 1167-1169
44. Slominski, A. T., Kim, T.-K., Shehabi, H. Z., Semak, I., Tang, E. K. Y., Nguyen, M. N., Benson, H. A. E., Korik, E., Janjetovic, Z., Chen, J., Yates, C. R., Postlethwaite, A., Li, W., and Tuckey, R. C. (2012) In vivo evidence for a novel pathway of vitamin D3 metabolism initiated by P450scc and modified by CYP27B1. FASEB J. 26, 3901-3915
45. 3, novel P450scc product, stimulates differentiation and inhibits proliferation and NF-κB activity in human keratinocytes. J. Cell. Physiol. 223, 36-48
46. Slominski, A. T., Kim, T. K., Chen, J., Nguyen, M. N., Li, W., Yates, C. R., Sweatman, T., Janjetovic, Z., and Tuckey, R. C. (2012) Cytochrome P450scc-dependent metabolism of 7-dehydrocholesterol in placenta and epidermal keratinocytes. Int. J. Biochem. Cell Biol. 44, 2003-2018
47. Schoop, V. M., Mirancea, N., and Fusenig, N. E. (1999) Epidermal organization and differentiation of HaCaT keratinocytes in organotypic coculture with human dermal fibroblasts. J. Invest. Dermatol. 112, 343-353 (Pubitemid 29125112)
48. Hardeland, R., Tan, D. X., and Reiter, R. J. (2009) Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J. Pineal Res. 47, 109-126
49. 2-formyl-5- methoxykynuramine/N1-acetyl-5-methoxy-kynuramine formation from melatonin in mice. J. Pineal Res. 49, 106-114
50. Slominski, A., Semak, I., Pisarchik, A., Sweatman, T., Szczesniewski, A., and Wortsman, J. (2002) Conversion of L-tryptophan to serotonin and melatonin in human melanoma cells. FEBS Lett. 511, 102-106 (Pubitemid 34127831)
51. Slominski, A., Pisarchik, A., Semak, I., Sweatman, T., and Wortsman, J. (2003) Characterization of the serotoninergic system in the C57BL/6 mouse skin. Eur. J. Biochem. 270, 3335-3344 (Pubitemid 37011627)
52. Fischer, T. W., Zmijewski, M. A., Zbytek, B., Sweatman, T. W., Slominski, R. M., Wortsman, J., and Slominski, A. (2006) Oncostatic effects of the indole melatonin and expression of its cytosolic and nuclear receptors in cultured human melanoma cell lines. Int. J. Oncol. 29, 665-672
53. Slominski, A., and Pruski, D. (1993) Melatonin inhibits proliferation and melanogenesis in rodent melanoma cells. Exp. Cell Res. 206, 189-294
54. Yu, H. S., and Reiter, R. J. (1993) Melatonin Biosynthesis, Physiological Effects, and Clinical Implications, CRC Press, Boca Raton
55. Hipler, U. C., Fischer, T. W., and Elsner, P. (2003) HaCaT cell proliferation influenced by melatonin. Skin Pharmacol. Appl. Skin Physiol. 16, 379-385 (Pubitemid 37256073)
56. Kobayashi, H., Kromminga, A., Dunlop, T. W., Tychsen, B., Conrad, F., Suzuki, N., Memezawa, A., Bettermann, A., Aiba, S., Carlberg, C., and Paus, R. (2005) A role of melatonin in neuroectodermal-mesodermal interactions: the hair follicle synthesizes melatonin and expresses functional melatonin receptors. FASEB J. 19, 1710-1712 (Pubitemid 41429538)
57. Fischer, T. W., Zbytek, B., Sayre, R. M., Apostolov, E. O., Basnakian, A. G., Sweatman, T. W., Wortsman, J., Elsner, P., and Slominski, A. (2006) Melatonin increases survival of HaCaT keratinocytes by suppressing UV-induced apoptosis. J. Pineal Res. 40, 18-26
58. Schallreuter, K. U., Bahadoran, P., Picardo, M., Slominski, A., Elassiuty, Y. E., Kemp, E. H., Giachino, C., Liu, J. B., Luiten, R. M., Lambe, T., Le Poole, I. C., Dammak, I., Onay, H., Zmijewski, M. A., Dell'Anna, M. L., Zeegers, M. P., Cornall, R. J., Paus, R., Ortonne, J. P., and Westerhof, W. (2008) Vitiligo pathogenesis: autoimmune disease, genetic defect, excessive reactive oxygen species, calcium imbalance, or what else? Exp Dermatol 17, 139-140; discussion 141-160
59. Slominski, A., Paus, R., and Bomirski, A. (1989) Hypothesis: possible role for the melatonin receptor in vitiligo: discussion paper. J. R. Soc. Med. 82, 539-541 (Pubitemid 19211413)
60. Moll, R., Divo, M., and Langbein, L. (2008) The human keratins: biology and pathology. Histochem. Cell Biol. 129, 705-733
61. Omary, M. B., Coulombe, P. A., and McLean, W. H. (2004) Intermediate filament proteins and their associated diseases. N. Engl. J. Med. 351, 2087-2100 (Pubitemid 39482502)
62. Vassar, R., Coulombe, P. A., Degenstein, L., Albers, K., and Fuchs, E. (1991) Mutant keratin expression in transgenic mice causes marked abnormalities resembling a human genetic skin disease. Cell 64, 365-380 (Pubitemid 121001261)
63. Slominski, A., Chassalevris, N., Mazurkiewicz, J., Maurer, M., and Paus, R. (1994) Murine skin as a target for melatonin bioregulation. Exp. Dermatol. 3, 45-50 (Pubitemid 24160578)
64. Elias, P. M., Menon, G., Wetzel, B. K., and Williams, J. J. (2010) Barrier requirements as the evolutionary "driver" of epidermal pigmentation in humans. Am. J. Hum. Biol. 22, 526-537
65. Fischer, T. W., Zmijewski, M. A., Wortsman, J., and Slominski, A. (2008) Melatonin maintains mitochondrial membrane potential and attenuates activation of initiator (casp-9) and effector caspases (casp-3/casp-7) and PARP in UVR-exposed HaCaT keratinocytes. J. Pineal Res. 44, 397-407 (Pubitemid 351533524)
66. Kleszczynski, K., Tukaj, S., Kruse, N., Zillikens, D., and Fischer, T. W. (2013) Melatonin prevents ultraviolet radiation-induced alterations in plasma membrane potential and intracellular pH in human keratinocytes. J. Pineal Res. 54, 89-99 Muskuloskeletal and Skin Diseases/National Institutes of Health