CIRCADIAN RHYTHM AND LIPID METABOLISM IN ANIMAL CELLS. PART II. INFLUENCE OF THE CIRCADIAN RHYTHM ON THE SKIN AND FAT TISSUES. DESYNCHRONIZES AND LIPID METABOLISM
Abstract
This review (consisting of 2 parts) deals with the subjects of nature, properties, organization and functioning of the circadian rhythm and its importance in the regulation of physiological processes. Molecular and genetic aspects of the biological clock and its interrelation with lipid metabolism are also considered. Metabolic circadian rhythms are among the most important processes in an organism. There is a direct relationship between synchronicity and the processes of regulation of synthesis, absorption and secretion of lipids. The connection is observed at several levels: biochemical, molecular and genetic. Particular attention is paid to the influence of the circadian rhythm on the functioning and structure of skin and fat tissues which, in its turn, have autonomous circadian oscillators. In this case, the watch genes regulate the activity of numerous tissue-specific genes, thereby translating the daily information into physiologically significant signals. Considerable part of the article is devoted to the issues of desynchronizes, its causes and consequences. Diurnal disorders caused by external or internal factors can lead to disruption of the organism’s regulatory systems, which represents the development of metabolic disorders and tissue damage, which, in turn, can lead to maladaptation of the organism.
About the Authors
O. S. Sobolevskaya
Vitebsk State Medical University
Belarus
Ph. D. (Biol.), Assistant Professor
Belarus
Ph. D. (Biol.), Assistant Professor
O. D. Myadelets
Vitebsk State Medical University
Belarus
D. Sc. (Med.), Professor, Head of the Department
Belarus
D. Sc. (Med.), Professor, Head of the Department
E. S. Pashinskaya
Vitebsk State Medical University
Belarus
Ph. D. (Biol.), Assistant Professor
Belarus
Ph. D. (Biol.), Assistant Professor
References
1. Lamia K., Storch K., Weitz C. Physiological significance of a peripheral tissue circadian clock. Proceedings of the National Academy of Sciences of the United States of America, 2008, vol. 105, pp. 15172–15177. doi: 10.1073/pnas.0806717105.
2. Le Fur I., Reinberg A., Lopez S., Morizot F., Mechkouri M., Tschachler E. Analysis of circadian and ultradian rhythms of skin surface properties of face and forearm of healthy women. The Journal of Investigative Dermatology, 2001, vol. 117, no. 3, pp. 718–724. doi: 10.1046/j.0022-202x.2001.01433.x.
3. Yosipovitch G., Xiong GL, Haus E., Sackett-Lundeen L., Ashkenazi I., Maibach HI Time-dependent variations of the skin barrier function in humans: transepidermal water loss, stratum corneum hydration, skin surface pH, and skin temperature. The Journal of Investigative Dermatology, 1998, vol. 110, pp. 20–23. doi: 10.1046/j.1523-1747.1998.00069.x.
4. Luber A., Ensanyat S., Zeichner J. Therapeutic implications of the circadian clock on skin function. Journal of Drugs in Dermatology, 2014, vol. 13, pp. 130–134.
5. Van Someren E. Mechanisms and functions of coupling between sleep and temperature rhythms. Progress in Brain Research, 2006, vol. 153, pp. 309–324. doi: 10.1016/S0079-6123(06)53018-3.
6. Verschoore M., Poncet M., Krebs B., Ortonne J. Circadian variations in the number of actively secreting sebaceous follicles and androgen circadian rhythms. Chronobiology International, 1993, vol. 10, pp. 349–359.
7. Matsui M. Biological Rhythms in the Skin. International Journal of Molecular Sciences, 2016, vol. 17, no. 6, p. 801.
8. Pershing L., Corlett J., Lambert L., Poncelet C. Circadian activity of topical 0.05 % betamethasone dipropionate in human skin in vivo. The Journal of Investigative Dermatology, 1994, vol. 102, pp. 734–739.
9. Geyfman M., Andersen B. How the skin can tell time. The Journal of Investigative Dermatology, 2009, vol. 129, no. 5, pp. 1063–1066.
10. Desotelle J., Wilking M., Ahmad N. The circadian control of skin and cutaneous photodamage. Photochemistry and Photobiology, 2012, vol. 88, no. 5, pp. 1037–1047. doi: 10.1111/j.1751-1097.2012.01099.x.
11. Bjarnason G., Jordan R., Wood P., Li Q., Lincoln D., Sothern R., Hrushesky W., Ben-David Y. Circadian expression of clock genes in human oral mucosa and skin: association with specific cell-cycle phases. The American Journal of Pathology, 2001, vol. 158, no. 5, pp. 1793–1801. doi: 10.1016/S0002-9440(10)64135-1.
12. Ndiaye M., Nihal M., Wood G., Ahmad N. Skin, reactive oxygen species, and circadian clocks. Antioxidants & Redox Signaling, 2014, vol. 20, pp. 2982–2996. doi: 10.1089/ars.2013.5645.
13. Srinivasan V., Pandi-Perumal S., Brzezinski A., Bhatnagar K., Cardinali D. Melatonin, immune function and cancer. Recent patents on endocrine, metabolic, and immune drug discovery еndocrine, metabolic & immune drug discovery, 2011, vol. 5, pp. 109–123.
14. Abbaszadeh A., Haddadi G., Haddadi Z. Melatonin role in ameliorating radiation-induced skin damage: from theory to practice (a review of literature). Journal of Biomedical Physics & Engineering, 2017, vol. 7, no. 2, pp. 127–134.
15. Kostiuk N., Zhigulina V., Belyakova M. Effect of melatonin on lipid barrier in rats’ skin. American Journal of Biochemistry, 2012, vol. 2, no. 5, pp. 67–73. doi: 10.5923/j.ajb.20120205.04.
16. Wakatsuki A., Okatani Y., Ikenoue N., Kaneda C., Fukaya T. Effects of short-term melatonin administration on lipoprotein metabolism in normolipidemic postmenopausal women. Maturitas, 2001, vol. 38 (2), pp. 171–177.
17. Sandu C., Liu T., Malan A., Challet E., Pevet P., Felder-Schmittbuhl M. Circadian clocks in rat skin and dermal fibroblasts: differential effects of aging, temperature and melatonin. Cellular and Molecular Life Sciences, 2015, vol. 72, pp. 2237–2248. doi: 10.1007/s00018-014-1809-7.
18. Janich P., Toufighi K., Solanas G., Luis N., Minkwitz S., Serrano L., Lehner B., Benitah S. A. Human epidermal stem cell function is regulated by circadian oscillations Cell. Stem Cell, 2013, vol. 13, pp. 745–753. doi: 10.1016/j.stem.2013.09.004.
19. Sporl R., Korge S., Jurchott K., Wunderskirchner М. Kruppel-like factor 9 is a circadian transcription factor in human epidermis that controls proliferation of keratinocytes. Proceedings of the National Academy of Sciences of the United States of America, 2012, vol. 109, no. 27, pp. 10903–10908. doi: 10,1073/pnas.1118641109.
20. Fonseca-Alaniz M., Takada J., Alonso-Vale M., Lima F. Adipose tissue as an endocrine organ: from theory to practice. Jornal de Pediatria, 2007, vol. 83, no. 5, pp. s192−s203. doi: 10, 2223/JPED.1709.
21. Poglio S., Galvani S., Bour S., André M., Prunet-Marcassus B., Pénicaud L., Casteilla L., Cousin B. Adipose tissue sensitivity to radiation exposure. The American Journal of Pathology, 2009, vol. 174, no. 1, pp. 44−53. doi: 10.2353/ajpath. 2009.080505.
22. Tereshina E. V. Age-related dysfunction of adipose tissue. Gerontologiya i Geriatriya [Gerontology and Geriatrics], 2005, no. 5, pp. 98−101.
23. Unger R., Clark G., Scherer P., Orci L. Lipid homeostasis, lipotoxicity and the metabolic syndrome. Biochimica et Biophysica Acta, 2010, vol. 1801, pp. 209–214. doi: 10.1016/j.bbalip.2009.10.006.
24. Shostak A., Meyer-Kovac J., Oster H. Circadian regulation of lipid mobilization in white adipose tissues. Diabetes, 2013, vol. 62, pp. 2195–2203.
25. Dallmann R., Viola A., Tarokh L., Cajochen C., Brown S. The human circadian metabolome. Proceedings of the National Academy of Sciences of the United States of America, 2012, vol. 109, pp. 2625–2629. doi: 10,1073/pnas.1114410109.
26. Paschos G., Ibrahim S., Song W., Kunieda T., Grant G., Reyes T., Bradfield C., Vaughan C., Eiden M., Masoodi M. Obesity in mice with adipocytespecific deletion of clock component. Nature Medicine, 2012, vol. 18, pp. 1768–1777. doi: 10.1038/nm.2979.
27. Green C., Takahashi J., Bass J. The meter of metabolism. Cell, 2008, vol. 134, pp. 728–742. doi: 10.1016/j.cell.2008.08.022.
28. Turek F., Joshu C., Kohsaka A., Lin E., Ivanova G., McDearmon E., Laposky A., Losee-Olson S., Easton A., Jensen D. Obesity and metabolic syndrome in circadian Clock mutant mice. Science, 2005, vol. 308 (5724), pp. 1043–1045. doi: 10.1126/ science.1108750.
29. Grimaldi B., Bellet M., Katada S., Astarita G., Hirayama J., Amin R., Granneman J., Piomelli D., Leff T., Sassone-Corsi P. PER2 controls lipid metabolism by direct regulation of PPARg. Cell Metabolism, 2010, vol. 12, no. 5, pp. 509–520. doi: 10.1016/j.cmet.2010.10.005.
30. Yang X., Downes M., Yu R., Bookout A., He W., Straume M., Mangelsdorf D., Evans R. Nuclear receptor expression links the circadian clock to metabolism. Cell, 2006, vol. 126, pp. 801–810. doi: 10.1016/j.cell.2006.06.050.
31. Guo B., Chatterjee S., Li L., Kim J., Lee J., Yechoor V., Minze L., Hsueh W., Ma K. The clock gene, brain and muscle Arnt-like 1, regulates adipogenesis via Wnt signaling pathway. FASEB Journal: Official Publication of the Federation of Ame rican Societies for Experimental Biology, 2012, vol. 26, pp. 3453–3463. doi: 10.1096/fj.12-205781.
32. Delezie J., Dumont S., Dardente H., Oudart H., Gruchez-Cassiau A., Klosen P., Teboul M., Delaunay F., Puvet P., Challet E. The nuclear receptor REV-ERBα is required for the daily balance of carbohydrate and lipid metabolism. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 2012, vol. 26, pp. 3321–3335. doi: 10.1096/fj.12-208751.
33. Gimble J., Floyd Z. Fat circadian biology. Journal of Applied Physiology, 2009, vol. 107, pp. 1629–1637. doi: 10, 1152/ japplphysiol.00090.2009.
34. Cho H., Zhao X., Hatori M., Yu R., Barish G., Lam M., Chong L., DiTacchio L., Atkins A., Glass C. Regulation of cir ca-dian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature, 2012, vol. 485, pp. 123–127. doi: 10,1038/nature11048.
35. Kumar N., Solt L., Wang Y., Rogers P., Bhattacharyya G., Kamenecka T., Stayrook K., Crumbley C., Floyd Z., Gimble J., Griffin P., Burris T. Regulation of adipogenesis by natural and synthetic REV-ERB ligands. Endocrinology, 2010, vol. 151, pp. 3015–3025. doi: 10,1210/en.2009-0800.
36. Solt L. A., Wang Y., Banerjee S. Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature, 2002, vol. 485 (7396), pp. 62–68. doi: 10,1038/nature11030.
37. Nadol’nik L. I. Stress and thyroid gland. Biomeditsinskaya khimiya [Biomedical Chemistry], 2010, vol. 56, no. 4, pp. 443–456 (in Russian).
38. Khnychenko L. K. Sapronov N. S. Stress and its role in the development of pathological processes. Obzory po klinicheskoy farma kologii i lekarstvennoy terapii [Reviews of Clinical Pharmacology and Drug Therapy], 2003, vol. 2, no. 3, pp. 2–15 (in Russian).
39. Knutson K., Spiegel K., Penev P., Van Cauter E. The metabolic consequences of sleep deprivation. Sleep Medicine Reviews, 2007, vol. 11, pp. 163–178. doi: 10.1016/j.smrv.2007.01.002.
40. Knutson K., Van Cauter E. Associations between sleep loss and increased risk of obesity and diabetes. Annals of the New York Academy of Sciences, 2008, vol. 1129, pp. 287–304. doi: 10.1196/annals.1417.033.
41. Ramsey K., Marcheva B., Kohsaka A., Bass J. The clockwork of metabolism. Annual Review of Nutrition, 2007, vol. 27, pp. 219–240. doi: 10, 1146/annurev.nutr.27.061406.093546.
42. Straif K., Baan R., Grosse Y., Secretan B., Ghissassi F., Bouvard V., Altieri A., Benbrahim-Tallaa L., Cogliano V. Carcinogenicity of shift-work, painting, and fire-fighting. Lancet Oncology, 2007, vol. 8, pp. 1065–1066.
43. Gangwisch J., Malaspina D., Boden-Albala B., Heymsfield S. Inadequate sleep as a risk factor for obesity: analyses of the NHANES I. Sleep, 2005, vol. 28, pp. 1289–1296.
44. Spiegel K., Leproult R., Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet, 1999, vol. 354, pp. 1435–1439. doi: 10.1016/S0140-6736(99)01376-8.
45. Laposky A., Easton A., Dugovic C., Walisser J., Bradfield C., Turek F. Deletion of the mammalian circadian clock gene BMAL1/Mop3 alters baseline sleep architecture and the response to sleep deprivation. Sleep, 2005, vol. 28, pp. 395–409.
46. Taheri S., Lin L., Austin D., Young T., Mignot E. Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Medicine, 2013, vol. 1, no. 3, pp. E62. doi: 10.1371/journal.pmed.0010062.
47. Colles S., Dixon J., O’Brien P. Night eating syndrome and nocturnal snacking: association with obesity, binge eating and psychological distress. International Journal of Obesity, 2007, vol. 31, pp. 1722–1730. doi: 10.1038/sj.ijo.0803664.
48. Shoelson S., Herrero L., Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology, 2007, vol. 132, pp. 2169–2180.
49. Marcheva B., Ramsey K., Affinati A., Bass J. Clock genes and metabolic disease. Journal of Applied Physiology, 2009, vol. 107, no. 5, pp. 1638–1646. doi: 10,1152 / japplphysiol.00698.
50. Rudic R., McNamara P., Curtis A., Boston R., Panda S., Hogenesch J., Fitzgerald G. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biology, 2004, vol. 2, pp. e377. doi: 10.1371/journal.pbio.0020377.
51. Nakahata Y., Sahar S., Astarita G., Kaluzova M., Sassone-Corsi P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science, 2009, vol. 324, pp. 654–657. doi: 10,1126/science.1170803.
52. Revollo J., Korner A., Mills K., Satoh A., Wang T., Garten A., Dasgupta B., Sasaki Y., Wolberger C., Townsend R., Milbrandt J., Kiess W., Imai S. Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metabolism, 2007, vol. 6, pp. 363–375. doi: 10,1016/j.cmet.2007.09.003.
53. Galman C., Angelin B., Rudling M. Bile acid synthesis in humans has a rapid diurnal variation that is asynchronous with cholesterol synthesis. Gastroenterology, 2005, vol. 129, pp. 1445–1453. doi: 10,1053/j.gastro.2005.09.009.
54. Duez H., van der Veen J., Duhem C., Pourcet B., Touvier T., Fontaine C., Derudas B., Bauge E., Havinga R., Bloks V., Wolters H., van der Sluijs F., Vennstrom B., Kuipers F., Staels B. Regulation of bile acid synthesis by the nuclear receptor Rev-erbalpha. Gastroenterology, 2008, vol. 135, pp. 689–698. doi: 10,1053/j.gastro.2008.05.035.
55. Le Martelot G., Claudel T., Gatfield D., Schaad O., Kornmann B., Sasso G., Moschetta A., Schibler U. REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biology, 2009, vol. 7, pp. e1000181. doi: 10,1053/j. gastro.2008.05.035.
56. Marcheva B., Ramsey K., Affinati A., Bass J. Clock genes and metabolic disease. Journal of Applied Physiology, 2009, vol. 107, no. 5, pp. 1638–1646. doi: 10,1152/japplphysiol.00698.2009.
57. Knutson K., Curiel T., Salazar L., Disis M. Immunologic principles and immunotherapeutic approaches in ovarian cancer. Hematology/Oncology Clinics of North America, 2003, vol. 17, pp. 1051–1073.
58. Durgan D., Young M. The cardiomyocyte circadian clock: emerging roles in health and disease. Circulation Research, 2010, vol. 106, no. 4, pp. 647–658. doi: 10,1161/CIRCRESAHA.109.209957.
59. He Y., Jones C., Fujiki N., Xu Y., Guo B., Holder J., Rossner M., Nishino S., Fu Y. The transcriptional repressor DEC2 regulates sleep length in mammals. Science, 2009, vol. 325, pp. 866–870. doi: 10.1126/science.1174443.
60. Young M., Razeghi P., Cedars A., Guthrie P., Taegtmeyer H. Intrinsic diurnal variations in cardiac metabolism and contractile function. Circulation Research, 2001, vol. 89, pp. 1199–1208.
61. Stavinoha M., RaySpellicy J., Hart-Sailors M., Mersmann H., Bray M., Young M. Diurnal variations in the responsiveness of cardiac and skeletal muscle to fatty acids. American Journal of Physiology, 2004, vol. 287, pp. E878–E887. doi: 10,1152/ajpendo.00189.2004.
62. Imeri L., Opp M. How (and why) the immune system makes us sleep. Nature Reviews. Neuroscience, 2009, vol. 10, pp. 199–210. doi: 10.1038/nrn2576.
63. Krueger J. The role of cytokines in sleep regulation. Current Pharmaceutical Design, 2008, vol. 14, pp. 3408–3416.
64. Hotamisligil G., Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nature Reviews. Immuno logy, 2008, vol. 8, pp. 923–934. doi: 10,1038/nri2449.
65. Graham C., Cook M., Gerkovich M., Sastre A. Examination of the melatonin hypothesis in women exposed at night to EMF or bright light. Environmental Health Perspectives, 2001, vol. 109, pp. 501–507.
66. Wojtovicz M., Jakiel G. Melatonin and its role in human reproduction. Ginekologia Polska, 2002, vol. 73, no. 12, pp. 1217–1231.
67. Giammanco S., Ernandes M., La Guardia M. Effects of environmental lighting and tryptophan devoid diet on the rat vaginal cycle. Archives of Physiology and Biochemistry, 1997, vol. 105, no. 5, pp. 445–449. doi: 10,1076/apab.105.5.445.3287.
68. Dai H., Zhang L., Cao M., Song F., Zheng H., Zhu X., Wei Q., Zhang W., Chen K. The role of polymorphisms in circadian pathway genes in breast tumorigenesis. Breast Cancer Research and Treatment, 2011, vol. 127, pp. 531–540. doi: 10.1007/s10549-010-1231-2.
69. Zhu Y., Stevens R., Hoffman A., Fitzgerald L., Kwon E., Ostrander E., Davis S., Zheng T., Stanford J. Testing the circadian gene hypothesis in prostate cancer: a population-based case-control study. Cancer Research, 2009, vol. 69, pp. 9315– 9322. doi: 10,1158 / 0008-5472.CAN-09-0648.
70. Roe O., Anderssen E., Helge E., Pettersen C., Olsen K., Sandeck H., Haaverstad R., Lundgren S., Larsson E. Genome-wide profile of pleural mesothelioma versus parietal and visceral pleura: the emerging gene portrait of the mesothelioma phenotype. PLoS One, 2009, vol. 4, p. 6554. doi: 10,1371/journal.pone.0006554.
71. Filipski E., Subramanian P., Carrière J., Guettier C., Barbason H., Lévi F. Circadian disruption accelerates liver carcinogenesis in mice. Mutation Research, 2009, vol. 680, pp. 95–105. doi: 10.1016/j.mrgentox.2009.10.002.
72. Adaskevich V. P. Acne vulgar and pink. N. Novgorod, NGMA, 2003. 195 p. (in Russian).
73. Kozin V. M. Psoriasis (questions of pathogenesis, clinic, therapy). Vitebsk, VGMU, 2007. 227 p. (in Russian).
74. Myadelets O. D., Adaskevich V. P. Morphofunctional dermatology. Moscow, Medlit, 2006. 752 p. (in Russian).
75. Povaliy T. M. Quantitative analysis of cholesterol of epidermal keratinocyte membranes in psoriasis. Vestnik Dermatologii i Venerologii [Bulletin of Dermatology and Venereology], 1997, no. 1, pp. 4–6 (in Russian).
76. Ernandes E. I., Margolina A. A., Petrukhina A. O. Lipid barrier of skin and cosmetics. Moscow, KLAVEL’, 2005. 400 p. (in Russian).
77. Boehncke W-H., Boehncke S., Schön M. Managing comorbid disease in patients with psoriasis. BMJ, 2010, vol. 340, pp. 200–203. doi: 10.1136/bmj.b5666.
78. Christofers E. Comorbidities in psoriasis. Journal of the European Academy of Dermatology and Venereology, 2006, vol. 20, iss. s2, pp. 52–55. doi:10.1111/j.1468-3083.2006.01773.x.
79. Zouboulis C. Isotretinoin revisited : pluripotent effects on human sebaceous gland cells. Journal of Investigative Dermatology, 2006, vol. 126, pp. 2154–2156. doi: 10,1038/sj.jid.5700418.
80. Zykova O. S., Sobolevskaya I. S., Myadelets O. D., Grushin V. N. Morphological features of the distribution of free cholesterol in the epidermis in psoriasis. Vestnik Vitebskogo Gosudarstvennogo Meditsinskogo Universiteta [Bulletin of Vi-tebsk State Medical University], 2012, vol. 11, no. 1, s. 42–47. (in Russian).
81. Sobolevskaya I. S. Some morphometric parameters of lipid-accumulating and lipid-synthesizing structures of human skin. Vestnik Vitebskogo Gosudarstvennogo Meditsinskogo Universiteta [Bulletin of Vitebsk State Medical University], 2012, vol. 11, no. 2, pp. 41–51. (in Russian).
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