DOI QR코드

DOI QR Code

Endotoxin-induced inflammation disturbs melatonin secretion in ewe

  • Herman, Andrzej Przemyslaw (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Wojtulewicz, Karolina (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Bochenek, Joanna (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Krawczynska, Agata (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Antushevich, Hanna (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Pawlina, Bartosz (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Zielinska-Gorska, Marlena (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Herman, Anna (Faculty of Cosmetology, The Academy of Cosmetics and Health Care) ;
  • Romanowicz, Katarzyna (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences) ;
  • Tomaszewska-Zaremba, Dorota (The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences)
  • 투고 : 2017.03.13
  • 심사 : 2017.06.05
  • 발행 : 2017.12.01

초록

Objective: The study examined the effect of intravenous administration of bacterial endotoxin-lipopolysaccharide (LPS) -on the nocturnal secretion of melatonin and on the expression of enzymes of the melatonin biosynthetic pathway in the pineal gland of ewes, taking into account two different photoperiodic conditions: short-night (SN; n = 12) and long-night (LN; n = 12). Methods: In both experiments, animals (n = 12) were randomly divided into two groups: control (n = 6) and LPS-treated (n = 6) one. Two hours after sunset, animals received an injection of LPS or saline. Blood samples were collected starting one hour after sunset and continuing for 3 hours after the treatment. The ewes were euthanized 3 hours after LPS/saline treatment. The concentration of hormones in plasma was assayed by radioimmunoassay. In the pineal gland, the content of serotonin and its metabolite was determined by HPLC; whereas the expression of examined genes and protein was assayed using real-time polymerase chain reaction and Western Blot, respectively. Results: Endotoxin administration lowered (p<0.05) levels of circulating melatonin in animals from LN photoperiod only during the first hour after treatment, while in ewes from SN photoperiod only in the third hour after the injection. Inflammation more substantially suppressed biosynthesis of melatonin in ewes from SN photoperiod, which were also characterised by lower (p<0.05) cortisol concentrations after LPS treatment compared with animals from LN photoperiod. In the pineal gland of ewes subjected to SN photoperiod, LPS reduced (p<0.05) serotonin content and the expression of melatonin biosynthetic pathway enzymes, such as tryptophan hydroxylase and arylalkylamine-N-acetyltransferase. Pineal activity may be disturbed by circulating LPS and proinflammatory cytokines because the expression of mRNAs encoding their corresponding receptors was determined in this gland. Conclusion: The present study showed that peripheral inflammation reduces the secretion of melatonin, but this effect may be influenced by the photoperiod.

키워드

참고문헌

  1. Ko CH, Takahashi JS. Molecular components of the mammalian circadian clock. Hum Mol Genet 2006;15:R271-7. https://doi.org/10.1093/hmg/ddl207
  2. Schomerus C, Korf HW. Mechanisms regulating melatonin synthesis in the mammalian pineal organ. Ann NY Acad Sci 2005;1057:372-83. https://doi.org/10.1196/annals.1356.028
  3. Reiter RJ. The melatonin rhythm: both a clock and a calendar. Experientia 1993;49:654-64. https://doi.org/10.1007/BF01923947
  4. Piesiewicz A, Kedzierska U, Adamska I, et al. Pineal arylalkylamine N-acetyltransferase (Aanat) gene expression as a target of inflammatory mediators in the chicken. Gen Comp Endocrinol 2012;179:143-51. https://doi.org/10.1016/j.ygcen.2012.08.013
  5. Skwarlo-Sonta K, Majewski P, Markowska M, Oblap R, Olszanska B. Bidirectional communication between the pineal gland and the immune system. Can J Physiol Pharmacol 2003;81:342-9. https://doi.org/10.1139/y03-026
  6. Bochenek J, Skipor A, Kowalewska M, Herman AP. The Toll-like receptors mRNA expression profile in the pineal gland of sheep during long and short days. J Anim Feed Sci 2015;24:208-15. https://doi.org/10.22358/jafs/65626/2015
  7. Fraser S, Cowen P, Franklin M, Franey C, Arendt J. Direct radioimmunoassay for melatonin in plasma. Clin Chem 1983;29:396-7.
  8. Kokot F, Stupnicki R. Radioimmunological and radiocompetitive methods in clinical use. 2nd ed. (in Polish) Warsaw, Poland: PZWL; 1985.
  9. Rasmussen R. Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K, editors. Rapid cycle Real-Time PCR methods and applications. Berlin, Germany: Springer-Verlag; 2001. p. 21-34.
  10. Carrillo-Vico A, Lardone PJ, Alvarez-Sanchez N, Rodriguez-Rodriguez A, Guerrero JM. Melatonin: buffering the immune system. Int J Mol Sci 2013;14:8638-83. https://doi.org/10.3390/ijms14048638
  11. Radogna M, Ghibelli L. Melatonin: A pleiotropic molecule regulating inflammation. Biochem Pharmacol 2010;80:1844-52. https://doi.org/10.1016/j.bcp.2010.07.041
  12. Herman AP, Bochenek J, Skipor J, et al. Interleukin-1${\beta}$ modulates melatonin secretion in ovine pineal gland: ex vivo study. BioMed Res Int 2015;2015:526464.
  13. Herman AP, Bochenek J, Krol K, et al. Central interleukin-1${\beta}$ suppresses the nocturnal secretion of melatonin. Med Inflam 2016;2016:2589483.
  14. Fernandes PA, Cecon E, Markus RP, Ferreira ZS. Effect of TNF-alpha on the melatonin synthetic pathway in the rat pineal gland: basis for a ‘feedback' of the immune response on circadian timing. J Pineal Res 2006;41:344-50. https://doi.org/10.1111/j.1600-079X.2006.00373.x
  15. Tsai SY, McNulty JA. Interleukin-$1{\beta}$ expression in the pineal gland of the rats. J Pineal Res 1999;27:42-8. https://doi.org/10.1111/j.1600-079X.1999.tb00595.x
  16. da Silveira Cruz-Machado S, Pinato L, Tamura EK, Carvalho-Sousa CE, Markus RP. Glia-pinealocyte network: the paracrine modulation of melatonin synthesis by tumor necrosis factor (TNF). PLoS ONE 2012;7:e40142. https://doi.org/10.1371/journal.pone.0040142
  17. Skipor J, Szczepkowska A, Kowalewska M, Herman AP, Lisiewski P. Profile of toll-like receptor mRNA expression in the choroid plexus in adult ewes. Acta Vet Hung 2015;63:69-78. https://doi.org/10.1556/AVet.2014.027
  18. Banks WA. Anorectic effects of circulating cytokines: role of the vascular blood-brain barrier. Nutrition 2001;17:434-7. https://doi.org/10.1016/S0899-9007(01)00507-X
  19. O'Connor JC, Lawson MA, Andre C, et al. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatr 2009;14:511-22. https://doi.org/10.1038/sj.mp.4002148
  20. Laviano A, Cangiano C, Fava A, et al. Peripherally injected IL-1 induces anorexia and increases brain tryptophan concentrations. Adv Exp Med Biol 1999;467:105-8.
  21. Martini, Meites J. Neurochemical aspects of hypothalamic function. New York and London: Academic Press; 1970.
  22. Von Euler US, Heller H. Invertebrate hormones: tissue hormones. 1st Edition, Academic Press; 2013.
  23. Sugden LA, Sugden D, Klein DC. Alpha 1-adrenoceptor activation elevates cytosolic calcium in rat pinealocytes by increasing net influx. J Biol Chem 1987:262;741-5.
  24. Coon SL, Roseboom PH, Baler R, et al. Pineal serotonin N-acetyltransferase: expression cloning and molecular analysis. Science 1995;270:1681-3. https://doi.org/10.1126/science.270.5242.1681
  25. Kim TD, Kim JS, Kim JH, et al. Rhythmic serotonin N-acetyltransferase mRNA degradation is essential for the maintenance of its circadian oscillation. Mol Cel Biol 2005;25:3232-46. https://doi.org/10.1128/MCB.25.8.3232-3246.2005
  26. Battaglia DF, Bowen JM, Krasa HB, et al. Endotoxin inhibits the reproductive neuroendocrine axis while stimulating adrenal steroids: a simultaneous view from hypophyseal portal and peripheral blood. Endocrinology 1997;138:4273-81. https://doi.org/10.1210/endo.138.10.5449
  27. Herman AP, Krawczynska A, Bochenek J, et al. The effect of rivastigmine on the LPS-induced suppression of GnRH/LH secretion during the follicular phase of the estrous cycle in ewes. Anim Reprod Sci 2013;138: 203-12. https://doi.org/10.1016/j.anireprosci.2013.03.005
  28. Troiani ME, Reiter RJ, Vaughan MK, Oakins S, Vaughan GM. Swimming depresses nighttime melatonin content without changing Nacetyltransferase activity in the rat pineal gland. Neuroendocrinology 1988;47:55-60. https://doi.org/10.1159/000124891
  29. Stankov BM, Kanchev LN. Influence of acute stress on the pineal activity during day and night time. Acta Physiol Pol 1989;40:117-25.
  30. Kellner M, Yassouridis A, Manz B, et al. Corticotropin-releasing hormone inhibits melatonin secretion in healthy volunteers - a potential link to low-melatonin syndrome in depression?" Neuroendocrinology 1997;65:284-90. https://doi.org/10.1159/000127186
  31. Touitou Y, Bogdan A, Auzeby A, Touitou C. Activity of melatonin and other pineal indoles on the in vitro synthesis of cortisol, cortisone, and adrenal androgens. J Pineal Res 1989;6:341-50. https://doi.org/10.1111/j.1600-079X.1989.tb00430.x
  32. Del Rey A, Chrousos G, Besedovsky H. The hypothalamus-pituitaryadrenal axis, Volume 7 (NeuroImmune Biology). 1st Edition. Oxford, UK: Elsevier Science; 2008.
  33. Król K, Tomaszewska-Zaremba D, Herman AP. Photoperiod-dependent effect of inflammation on nocturnal gene expression of proinflammatory cytokines and their receptors in pars tuberalis of ewe. J Anim Feed Sci 2016;25:3-11. https://doi.org/10.22358/jafs/65581/2016

피인용 문헌

  1. Immune-pineal axis - acute inflammatory responses coordinate melatonin synthesis by pinealocytes and phagocytes pp.00071188, 2018, https://doi.org/10.1111/bph.14083
  2. of ewe during different photoperiodic conditions pp.1918-1825, 2018, https://doi.org/10.1139/cjas-2017-0121
  3. Brain-derived neurotrophic factor (BDNF) affects somatotrophic axis activity in sheep vol.30, pp.4, 2017, https://doi.org/10.22358/jafs/143353/2021
  4. Effect of Lipopolysaccharide-Induced Inflammatory Challenge on β-Glucuronidase Activity and the Concentration of Quercetin and Its Metabolites in the Choroid Plexus, Blood Plasma and Cerebrospina vol.22, pp.13, 2017, https://doi.org/10.3390/ijms22137122