Effects of long-term exposure to light or darkness and return to normal light-dark cycle on serum melatonin levels in rats
Long-term exposure to light/darkness on melatonin
Abstract
Increasing evidence suggests that the presence of constant light or darkness have diverse effects on circadian physiology. The aim of this study is to explore serum levels of melatonin upon return to a normal light-dark cycle (LDC) in rats exposed to constant light (LL) or darkness (DD). Results showed the different profiles of melatonin levels after exposure to LL or DD. Similarly, the restoration of the LDC (12L:12D) modified the endogenous melatonin levels. In the LL group, serum melatonin remained at levels similar to control values, and when normal LDC was restored, melatonin levels of the rats decreased but without significant difference compared to control. In the DD group, serum melatonin increased significantly (22%), and upon switching to normal LDC, serum melatonin level was significantly decreased compared to constant dark condition. Even 15 days later, a significant 76% drop in serum melatonin level was still observed in LDC condition. The results suggested that prolonged exposure to LL or DD, especially to DD, had profound effects on the serum melatonin. LL has little influence and this result can be explained by the potential compensation of extrapineal melatonin generated by other tissues and organs.
References
2. Kuhlman SJ, Michon Craig L, Duffy JF (2018) Introduction to chronobiology. Cold Spring Harb. Perspect. Biol. 10 (9): pii: a033613. doi: 10.1101/cshperspect.a033613.
3. Daan S, Aschoff J (1982) Circadian contribution to survival. Vertebrate Circadian System, eds Aschoff J, Daan S, Groos G (Springer, Berlín), pp 305-321.
4. Czeisler CA, Wright Jr KP (1999) Influence of light on circadian rhythmicity in humans. Regulation of Sleep and Circadian Rhythms, eds Turek FW, Zee PC (Dekker, New York), pp 149-180.
5. Lewy AJ, Wehr TA, Goodwin FK, Newsome DA, Markey SP (1980) Light suppresses melatonin secretion in humans. Science 210: 1267-1269.
6. Sinhasane SV, Joshi BN (1997) Melatonin and exposure to constant light/darkness affects ovarian follicular kinetics and estrous cycle in Indian desert gerbil Meriones hurrianae. Gen. Comp. Endocrinol. 108: 352-357.
7. Dauchy RT, Dauchy EM, Hanifin JP, Gauthreaux SL, Mao L, Belancio VP, Ooms TG, Dupepe LM, Jablonski MR, Warfield B, Wren MA, Brainard GC, Hill SM, Blask DE (2013) Effects of spectral transmittance through standard laboratory cages on circadian metabolism and physiology in nude rats. J. Am. Assoc. Lab. Anim. Sci. 52: 146–156.
8. González MM (2018) Dim light at night and constant darkness: Two frequently used lighting conditions that jeopardize the health and well-being of laboratory rodents. Front. Neurol. 9: 609. https://doi.org/10.3389/fneur.2018.00609
9. Martino E, Bambini G, Vaudagna G, Breccia M, Baschieri L (1985) Effects of continuous light and dark exposure on hypothalamic thyrotropin-releasing hormone in rats. J. Endocrinol. Invest. 8: 31-33.
10. Olatunji-Bello II, Sofola OA (2001) Effect of continuous light and darkness exposures on the pituitary-gonadal axis and thyroid activity in male rats. Afr. J. Biomed. Res. 4: 119-122.
11. Nir I, Hirschmann N (1982) Effect of constant light and darkness on pituitary and serum gonadotropin and sex hormone levels of parturient rats. J. Neural. Transm. 55: 157-168.
12. González MM, Aston-Jones G (2008) Light deprivation damages monoamine neurons and produces a depressive behavioral phenotype in rats. Proc. Natl. Acad. Sci. USA 105: 4898–4903.
13. Monje FJ, Cabatic M, Divisch I, Kim E-J, Herkner KR, Binder BR, Pollak DD (2011) Constant darkness induces IL-6-dependent depression-like behavior through the NF-B signaling pathway. J. Neurosci. 31 (25): 9075–9083.
14. Reiter RJ (1993) The melatonin rhythm-both clock and calendar. Experientia 49: 654-664.
15. Arendt J (1988) Melatonin. Clin. Endocrinol. 29: 205-229.
16. Reiter RJ, Tan DX, Fuentes-Broto L (2010) Melatonin: a multitasking molecule. Prog. Brain. Res. 181: 127-151.
17. Poeggeler B (1993) Melatonin and the light-dark zeitgeber in vertebrates, invertebrates and unicellular organisms. Experientia 49: 611-613.
18. Pandi-Perumal SR, Srinivasan V, Maestroni GJM, Cardinali DP, Poeggeler B, Hardeland R (2006) Melatonin: Nature’s most versatile biological signal? FEBS J. 273: 2813-2838.
19. Tan, DX, Hardeland R, Manchester LC, Paredes SD, Korkmaz A, Sainz RM, Mayo JC, Fuentes-Broto L, Reiter RJ (2010) The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol. Rev. 85: 607-623.
20. Weil ZM, Borniger JC, Cisse YM, Abi Salloum BA, Nelson RJ (2015) Neuroendocrine control of photoperiodic changes in immune function. Front. Neuroendocrinol. 37: 108-118.
21. Schwartz MD, Wotus C, Liu T, Friesen WO, Borjigin J, Oda GA, de la Iglesia HO (2009) Dissociation of circadian and light inhibition of melatonin release through forced desynchronization in the rat. Proc. Natl. Acad. Sci. USA 106: 17540-17545.
22. Xu G, Dean J, Liu T, Tian F, Borjigin J (2018) Chronic circadian advance shifts abolish melatonin secretion for days in rats. Neurobiol. Sleep Circad. Rhythms 5: 78–83. doi: 10.1016/j.nbscr.2018.02.002.
23. Cardinali DP, Pévet P (1998) Basic aspects of melatonin action. Sleep Med. Rev. 2: 175-190.
24. Huether G (1993) The contribution of extrapineal sites of melatonin synthesis to circulating melatonin levels in higher vertebrates. Experientia 49 (8): 665-670. doi: 10.1007/BF01923948.
25. Kvetnoy I (1999) Extrapineal melatonin: location and role within diffuse neuroendocrine system. Histochem. J. 31: 1–12.
26. Acuña-Castroviejo D, Escames G, Venegas C, Diaz-Casado ME, Lima-Cabello E, Lopez LC, Rosales-Corral S, Tan DX, Reiter RJ (2014) Extrapineal melatonin: sources, regulation, and potential functions. Cell Mol. Life Sci. 71: 2997-3025.
27. Tan DX, Xu B, Zhou X, Reiter RJ (2018) Pineal calcification, melatonin production, aging, associated health consequences and rejuvenation of the pineal gland. Molecules 23 (2): pii: E301. doi: 10.3390/molecules23020301.
28. Lynch HJ, Rivest RW, Ronsheim PM, Wurtman RJ (1981) Light intensity and the control of melatonin secretion in rats. Neuroendocrinol. 33 (3): 181-185. doi: 10.1159/000123226
29. Wideman CH, Murphy HM (2009) Constant light induces alterations in melatonin levels, food intake, feed efficiency, visceral adiposity, and circadian rhythms in rats. Nutr. Neurosci. 12 (5): 233-240. doi: 10.1179/147683009X423436.
30. Escribano BM, Moreno A, Tasset I, Tunez I (2014) Impact of light/dark cycle patterns on oxidative stress in an adriamycin-induced nephropathy model in rats. PLoS ONE 9 (5): e97713. doi:10.1371/journal.pone.0097713.
31. Baydaş G, Erçel E, Canatan H, Dönder E, Akyol A (2001) Effect of melatonin on oxidative status of rat brain, liver and kidney tissues under constant light exposure. Cell Biochem. Funct. 19: 37-41.
32. Berbets АМ, Barbe AМ, Yuzko OМ (2019) Constant light exposure terminates pregnancy in rats with pineal gland dysfunction, low melatonin level and pro-inflammatory response. Melatonin Res. 2 (4): 9-24. doi: 10.32794/mr11250038.
33. Farhadi N, Gharghani M, Farhadi Z (2016) Effects of long-term light, darkness and oral administration of melatonin on serum levels of melatonin. Biomed. J. 39: 81-84.
34. Arendt J, Aulinas A. Physiology of the Pineal Gland and Melatonin. [Updated 2022 Oct 30]. In: Feingold KR, Anawalt B, Blackman MR, et al., editors. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc.; 2000-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK550972/
35. Tan DX, Reiter RJ, Zimmerman S, Hardeland R (2023) Melatonin: both a messenger of darkness and a participant in the cellular actions of non-visible solar radiation of near infrared light. Biology (Basel) 12 (1): 89. doi: 10.3390/biology12010089.
36. Tchekalarova J, Stoyanova T, Nenchovska Z, Ivanova N, Atanasova D, Atanasova M, Georgieva K (2019) Effect of endurance training on diurnal rhythms of superoxide dismutase activity, glutathione and lipid peroxidation in plasma of pinealectomized rats. Neurosci. Lett. 716: 134637. doi: 10.1016/j.neulet.2019.134637.
37. Ibrahim DS (2017) Neuroprotective effect of Cucumis melo Var. flexuosus leaf extract on the brains of rats with streptozotocin-induced diabetes. Metab. Brain Dis. 32: 69-75.
38. Honma S, Kanematsu N, Katsuno Y, Homna K (1996) Persistence of circadian oscillation while locomotor activity and plasma melatonin levels became aperiodic under prolonged continuous light in the rat. Neurosci. Lett. 216: 49-52.
39. Fukuhara C, Aguzzi J, Bullock N, Tosini G (2005) Effect of long-term exposure to constant dim light on the circadian system of rats. Neurosignals 14: 117-125.
40. Pablos MI, Agapito MT, Recio JM, Pérez-Gallardo L, Córdova MD, Mori JO (1993) Effect of iron and estrogen on melatonin secretion by the chicken pineal gland. Neurosci. Lett. 159: 211-214.
41. Tomás-Zapico C, Coto-Montes A, Martínez-Fraga J, Rodríguez-Colunga MJ, Tolivia D (2003) Effects of continuous light exposure on antioxidant enzymes, porphyric enzymes and cellular damage in the Harderian gland of the Syrian hamster. J. Pineal Res. 34: 60-68.
42. Mochizuki M, Kuwabara T, Gery I (1988) Effects of continuous light exposure on the rat retina and pineal gland. Graefes Arch. Clin. Exp. Ophthalmol. 226: 346-352.
43. Gerasimov AV, Logvinov SV, Kostyuchenko VP (2010) Morphological changes in the pineal gland of rats under conditions of long-term exposure to bright light. Bull. Exp. Biol. Med. 150: 86-88.
44. Logvinov SV, Gerasimov AV, Kostiuchenko VP (2004) Ultrastructure of the pinealocytes in rats exposed to light and radiation. Morfologia 125: 71-75.
45. González MM, Aston-Jones G (2006) Circadian regulation of arousal: Role of the noradrenergic locus coeruleus system and light exposure. Sleep 29: 1327-1336.
46. Arendt J (2012) Biological rhythms during residence in polar regions. Chronobiol. Int. 29: 379-394.
47. Rosenthal, NE, Sack DA, Gillin JC, Lewy AJ, Goodwin FK, Davenport Y, Mueller PS, Newsome DA, Wehr TA (1984) Seasonal affective disorder. A description of the syndrome and preliminary findings with light therapy. Arch. Gen. Psychiatry. 41: 72-80.
48. Rosen LN, Targum SD, Terman M, Bryant MJ, Hoffman H, Kasper SF, Hamovit JR, Docherty JP, Welch B, Rosenthal NE (1990) Prevalence of seasonal affective disorder at four latitudes. Psychiatry Res. 31: 131–144.
49. López-González MA, Guerrero JM, Delgado F (1997) Presence of the pineal hormone melatonin in rat cochlea: its variations with lighting conditions. Neurosci. Lett. 238: 81-83.
50. Ayhan IC, Toyran N, Gundogan UN (2012) Exposure to continuous darkness leads to atypical symptoms of seasonal affective disorder in rats. Turk J. Med. Sci. 40: 271-277.
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