ISSN 0564-3783  



Main page
Contacts
Themes
Archive  
Themes
Subscription
Information to authors
Editorial board
Mobile version


In Ukrainian

Export citations
UNIMARC
BibTeX
RIS





Changes in the inflammation state of white adipose tissue in rats with diet-induced obesity at different modes of melatonin administration

Kalmukova O., Yurchenko A., Savchuk A., Dzerzhynsky M.

 




SUMMARY. The effects of various modes (morning and evening) of melatonin (30 mg/kg/day for 7 weeks) administration on the inflammatory process in visceral white adipose tissue (presence of macrophages forming structures similar to the crown-like structures around adipocytes; the level of fibrosis and the mast cells number in white adipose tissue; the content of proinflammatory (IL-1β, IL-8, tumor necrosis factor α, interferon γ) and anti-inflammatory (IL-4, IL-10) cytokines in blood serum) in rats with diet-induced obesity was investigated. After the administration of melatonin, obese rats demonstrated the decrease of macrophages and mast cells number in white adipose tissue, with a notable reduction of collagen fiber content (fibrosis) and adipocyte cell area. Evening administration of melatonin (one hour before light-off) showed greater efficacy compared to morning (one hour after light-on). In addition, serum of obese rats which received melatonin had increased levels of anti-inflammatory cytokines, while pro-inflammatory on the contrary decreased. This indicates about manifestation of the anti-inflammatory properties of melatonin in the context of the obesity development and is a theoretical precondition for further consideration of the possibility to use it in the obesity treatment.

Key words: high calorie obesity, inflammation, chronobiology, melatonin, cytokines, fibrosis, mast cells, adipocytes

Tsitologiya i Genetika 2020, vol. 54, no. 1, pp. 50-61

  • Educational and scientific centre Institute of Biology and Medicine Taras Shevchenko National University of Kyiv 64/13, Volodymyrska St., 01601 Kyiv, Ukraine

E-mail: olesiakalmukova28 gmail.com

Kalmukova O., Yurchenko A., Savchuk A., Dzerzhynsky M. Changes in the inflammation state of white adipose tissue in rats with diet-induced obesity at different modes of melatonin administration, Tsitol Genet., 2020, vol. 54, no. 1, pp. 50-61.

In "Cytology and Genetics":
O. O. Kalmukova, A. V. Yurchenko, A. M. Savchuk & M. E. Dzerzhynsky Changes in the Inflammatory Status in White Adipose Tissue of Rats with Diet-Induced Obesity at Different Regimens of Melatonin Administration, Cytol Genet., 2020, vol. 54, no. 1, pp. 3847
DOI: 10.3103/S0095452720010077


References

1. Caër, C., Rouault, C., Le Roy, T., Poitou, C., Aron-Wisnewsky, J., Torcivia, A., Bichet, J., Clément, K., Guerre-Millo, M. and Andre, S. Immune cell-derived cytokines contribute to obesity-related inflammation, fibrogenesis and metabolic deregulation in human adipose tissue, Sci. Rep., 2017, vol. 7, no. 3000, pp. 111.

2. Rodríguez, A., Ezquerro, S., Méndez-Giménez, L., Becerril, S. and Frühbeck, G., Revisiting the adipocyte: a model for integration of cytokine signaling in the regulation of energy metabolism, Am. J. Physiol.Endocrinol. Metab., 2015, vol. 309, no. 8, pp. E691E714.

3. Kang, Y.E., Kim, J.M., Joung, K.H., Lee, J.H., You, B.R., Choi, M.J., Ryu, M.J., Ko, Y.B., Lee, J., Ku, B.J., Shong, M., Lee, K.H., and Kim, H.J., The roles of adipokines, proinflammatory cytokines, and adipose tissue macrophages in obesity-associated insulin resistance in modest obesity and early metabolic dysfunction, PLoS One, 2016, vol. 11, no. 4. e0154003.

4. Żelechowska, P., Agier, J., Kozłowska, E., and Brzezińska-Błaszczyk, E., Mast cells participate in chronic low-grade inflammation within adipose tissue, Obesity Rev., 2018, vol. 19, no 5, pp. 686697.

5. Apostolopoulos, V., de Courten, M. P., Stojanovska, L., Blatch, G. L., Tangalakis, K. and de Courten, B., The complex immunological and inflammatory network of adipose tissue in obesity, Mol. Nutr. Food Res., 2016, vol. 60, no. 1, pp. 4357.

6. Cinti, S., Mitchell, G., Barbatelli, G., Murano, I., Ceresi, E., Faloia, E., Wang, S., Fortier, M., Green-berg, A., and Obin, M., Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans, J. Lipid. Res., 2005, vol. 46, pp. 23472355.

7. Jiang, C, Qu, A., Matsubara, T., Chanturiya, T., Jou, W., Gavrilova, O., Shah, Y, and Gonzalez, F.J., Disruption of hypoxia-inducible factor 1 in adipocytes improves insulin sensitivity and decreases adiposity in high-fat diet-fed mice, Diabetes, 2011, vol. 60, no. 10, pp. 24842495.

8. Zhou, Y., Yu, X., Chen, H., Sjberg, S., Roux, J., Zhang, L., Ivoulsou, A., Bensaid, F., Liu, C, Liu, J., Tordjman, J., Clement, K., Lee, C, Hotamisligil, G., Libby, P., and Shi, G., Leptin deficiency shifts mast cells toward anti-inflammatory actions and protects mice from obesity and diabetes by polarizing M2 macrophages, Cell Metab., 2015, vol. 22, no. 6, pp. 10451058.

9. Altintas M., Azad A., Nayer B., Contreras, G., Zaias, J., Faul, C., Reiser, J., and Nayer, A., Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice, Lipid Res., 2011, vol. 52, pp. 480488.

10. Toniato, E., Frydas, I., Robuffo, I., Ronconi, G., Caraffa, A.L., Kritas, S., and Conti, P., Activation and inhibition of adaptive immune response mediated by mast cells, Biol. Reg. Horn.Agents, 2017, vol. 31, no. 3, pp. 543548.

11. Daryabor, G., Kabelitz, D., and Kalantar, K., An update on immune dysregulation in obesity-related insulin resistance, Scand. J. Immun., 2019, vol. 89, no. 4, pp. e12747e12763.

12. Tordjman, S., Chokron, S., Delorme, R., Charrier, A., Bellissant, E., Jaafari, N., and Fougerou, C., Melato-nin: pharmacology, functions and therapeutic benefits, Curr. Neuropharm., 2017, vol. 15, no. 3, pp. 434443.

13. Hardeland, R., Cardinali, D.P., Srinivasan, V., Spence, D.W., Brown, G.M., and Pandi-Perumal, S.R., MelatoninaA pleiotropic, orchestrating regulator molecule, Progr. Neurobiol., 2011, vol. 93, no. 3, pp. 350384.

14. Amaral, F.G.D. and Cipolla-Neto, J., A brief review about melatonin, a pineal hormone, Arch. Endocrinol. Metab., 2018, vol. 62, no. 4, pp. 472479.

15. Reina, M. and Martínez, A., A new free radical scavenging cascade involving melatonin and three of its metabolites (OHM, AFMK and AMK), Comp. Theor. Chem., 2018, vol. 1123, pp. 111118.

16. Cardinali, D.P., Hardeland, R., Inflammaging, metabolic syndrome and melatonin: a call for treatment studies, Neuroendocrinology, 2017, vol. 104, no. 4, pp. 382397.

17. Calvo, J.R., Gonzalez-Yanes, C., and Maldonado, M.D., The role of melatonin in the cells of the innate immunity: a review, Pineal Res., 2013, vol. 55, no. 2, pp. 103120.

18. Laitinen, J.T., Castren, E., Vakkuri, O., and Saavedra, J.M., Diurnal rhythm of melatonin binding in the rat suprachiasmatic nucleus, Endocrinology, 1989, vol. 124, no. 3, pp. 15851587.

19. Acufia-Castroviejo, D., Reiter, R. J., Menendez-Pelaez, A., Pablos, M. I. and Burgos, A. Characterization of high-affinity melatonin binding sites in purified cell nuclei of rat liver, Pineal Res., 1994, vol. 16, no. 2, pp. 100112.

20. Gerdin, M.J., Masana, M.I., Rivera-Bermüdez, M.A., Hudson, R.L., Earnest, D.J., Gillette, M.U., and Dubocovich, M.L., Melatonin desensitizes endogenous MT2 melatonin receptors in the rat suprachiasmatic nucleus: relevance for defining the periods of sensitivity of the mammalian circadian clock to melatonin, FASEB J., 2004, vol. 18, no. 14, pp. 16461656.

21. Dallmann, R., Brown, S.A., and Gachon, F., Chronopharmacology: new insights and therapeutic implications, Ann. Rev. Pharmacol. Toxicol., 2014, vol. 54, pp. 339361.

22. McKenna, H., van der Horst, G.T., Reiss, I., and Martin, D., Clinical chronobiology: a timely consideration in critical care medicine, Crit. Care, 2018, vol. 22, no. 124, pp. 110.

23. Dyar, K.A. and Eckel-Mahan, K.L., Circadian metabolomics in time and space, Front. Neurosci., 2017, vol. 11, no. 369, pp. 110.

24. Shen, X.H., Tang, Q.Y., Huang, J., and Cai, W., Vitamin E regulates adipocytokine expression in a rat model of dietary-induced obesity, Exp. Biol. Med., 2010, vol. 235, no. 1, pp. 4751.

25. Halenova, T., Raksha, N., Vovk, T., Savchuk, O., Ostapchenko, L., Prylutskyy, Y., Kyzyma, O., Ritter, U., and Scharff, P., Effect of C60 fullerene nanoparticles on the diet-induced obesity in rats, Int. J. Obesity, 2018, vol. 42, pp.19871998.

26. Kalmukova, O., Pustovalov, A., Vareniuk, I., and Dzerzhynsky, M., Effect of melatonin different time administration on the development of diet-induced obesity in rats, Bull. Taras Shevchenko Nat. Univ. KyivProbl.Physiol. Func. Regul., 2018, vol. 23, no. 2, pp. 2027.

27. Suvarna, K., Layton, C., Bancroft, J.D., editors. Bancrofts theory and practice of histological techniques. 7th ed. Churchill Livingstone Elsevier; 2013. 654 p.

28. Mishra, N.S., Wanjari, S.P., Parwani, R.N., Wanjari, P.V., and Kaothalker, S.P., Assessment of collagen and elastic fibres in various stages of oral sub-mucous fibrosis using Massons trichrome, Verhoeff vangieson and picrosirius staining under light and polarizing microscopy, J. Dent. Spec., 2015, vol. 3, no. 2, pp. 1705.

29. Spencer, M., Unal, R., Zhu, B., Rasouli, N., McGehee, R.E., Jr., Peterson, C.A., and Kern, P.A., Adipose tissue extracellular matrix and vascular abnormalities in obesity and insulin resistance, J. Clin. Endocrinol. Metab., 2011, vol. 96, no. 12, pp. E1990E1998.

30. Altintas, M.M., Azad, A., Nayer, B., Contreras, G., Zaias, J., Faul, C., Reiser, J., and Nayer, A., Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice, J. Lipid Res., 2011, vol. 52, no. 3, pp. 480488.

31. Crowther, J.R., The ELISA Guidebook, Totowa, New Jersey: Humana Press Inc., 2001.

32. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding, Anal. Biochem., 1976, vol. 72, nos. 12, pp. 248254.

33. Martinez-Santibacez, G., Nien-Kai Lumeng, C., Macrophages and the regulation of adipose tissue remodeling, Ann. Rev. Nutr., 2014, vol. 34, pp. 5776.

34. Wu, J., Boström, P., Sparks, L.M., Ye, L., Choi, J.H., Giang, A.H., Khandekar, M., Virtanen, K., Nuutila, P., Schaart, G., Huang, K., Tu, H., Lichtenbelt, W., Hoeks, J., Enerback, S., Schrauwen, P., and Spiegelman, B., Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human, Cell, 2012, vol. 150, no. 2, pp. 366376.

35. Harms, M., Seale, P., Brown and beige fat: development, function and therapeutic potential, Nat. Med., 2013, vol. 19, no. 10, pp. 12521263.

36. Jin, J.X., Lee, S., Taweechaipaisankul, A., Kim, G.A., and Lee, B.C., Melatonin regulates lipid metabolism in porcine oocytes, J. Pineal Res., 2017, vol. 62, no. 2. e12388.

37. Choe, S.S., Huh, J.Y., Hwang, I.J., Kim, J.I., and Kim, J.B., Adipose tissue remodeling: its role in energy metabolism and metabolic disorders, Front. Endocrinol., 2016, vol. 7, no. 30, pp. 116.

38. Sadashiv, S.T., Paul, B.N., Kumar, S., Chandra, A., Dhananjai, S., and Negi, M.P., Over expression of resistin in adipose tissue of the obese induces insulin resistance, World J. Diabetes, 2012, vol. 3, no. 7, pp. 135141.

39. Jialal, I., Adams-Huet, B., and Devaraj, S., Factors that promote macrophage homing to adipose tissue in metabolic syndrome, J. Diabetes Complicat., 2016, vol. 30, no. 8, pp. 14341436.

40. Sun, K., Tordjman, J., Cliiment, K., and Scherer, P.E., Fibrosis and adipose tissue dysfunction, Cell Metab., 2013, vol. 18, no. 4, pp. 470477.

41. Herro, R., Croft, M., The control of tissue fibrosis by the inflammatory molecule LIGHT (TNF Super-family member 14), Pharmacol. Res., 2016, vol. 104, pp. 151155.

42. Halenova, T., Roslova, N., Vareniuk, I., Dzerzhyn-sky, M., Savchuk, O., Ostapchenko, L., Prylutskyy, Y., Ritter, U., and Scharff, P., Hepatoprotective effect of orally applied water-soluble pristine C60 fullerene against CCL-induced acute liver injury in rats, RSC Adv., 2016, vol. 6, no. 102, pp. 100046100055.

43. Liu, J., Clough, S.J., Hutchinson, A J., Adamah-Biassi, E.B., Popovska-Gorevski, M. and Dubocovich, M.L., MT1 and MT2 melatonin receptors: a therapeutic perspective, Ann. Rev. Pharmacol. Toxicol., 2016, vol. 56, pp. 361383.

44. Cano Barquilla, P., Pagano, E.S., Jiménez-Ortega, V., Fernández-Mateos, P., Esquifmo, A.I., and Cardinali, D.P., Melatonin normalizes clinical and biochemical parameters of mild inflammation in diet-induced metabolic syndrome in rats, J. Pineal Res., 2014, vol. 57, no. 3, pp. 280290.

45. Alamdari, N.M., Mahdavi, R., Roshanravan, N., Yaghin, N.L., Ostadrahimi, A.R, and Faramarzi, E., A double-blind, placebo-controlled trial related to the effects of melatonin on oxidative stress and inflammatory parameters of obese women, Horm. Metab. Res., 2015, vol. 47, no. 7, pp. 504508.

46. Agil, A., Reiter, R.J., Jiménez-Aranda, A., Ibán-Arias, R., Navarro-Alarcyn, M., Marchal, J.A., Adem, A., and Fernández-Vázquez, G., Melatonin ameliorates low-grade inflammation and oxidative stress in young Zucker diabetic fatty rats, J. Pineal Res., 2013, vol. 54, no. 4, pp. 381388.

47. Favero, G., Stacchiotti, A., Castrezzati, S., Bonomini, F., Albanese, M., Rezzani, R., and Rodella, L.F., Melatonin reduces obesity and restores adipokine patterns and metabolism in obese (ob/ob) mice, Nutr. Res., 2015, vol. 35, no. 10, pp. 891900.

48. Tamtaji, O.R., Mobini, M., Reiter, R.J., Azami, A., Gholami, M.S., and Asemi, Z., Melatonin, a toll-like receptor inhibitor: current status and future perspectives, J. Cell. Physiol., 2019, vol. 234, no. 6, pp. 77887795.

49. Askenase, P.W., Itakura, A., Leite-de-Moraes, M.C., Lisbonne, M., Roongapinun, S., Goldstein, D.R., and Szczepanik, M., TLR-dependent IL-4 production by invariant Vα+14+ Jαl8+ NKT cells to initiate contact sensitivity in vivo, J. Immunol., 2005, vol. 175, no. 10, pp. 63906401.

50. Hardeland, R., Opposite effects of melatonin in different systems and under different conditions, Curr. Top. Biochem. Res., 2016, vol. 17, pp. 5769.

51. Carrillo-Vico, A., Lardone, P., Álvarez-Sánchez, N., Rodríguez-Rodríguez, A., and Guerrero, J., Melatonin: buffering the immune system, Int. J. Mol. Sci., 2013, vol. 14, no. 4, pp. 86388683.

52. Hardeland, R., Melatonin and inflammationstory of a double-edged blade, J. Pineal Res., 2018, vol. 65, no. 4, e12525.

Copyright© ICBGE 2002-2021 Coded & Designed by Volodymyr Duplij Modified 22.06.21