Skip to main content
Log in

Absence of Photoperiodism and Digestive Enzymes in Rats: The Role of Age and the Endogenous Melatonin Level

  • Published:
Advances in Gerontology Aims and scope Submit manuscript

Abstract

The effect of the prolonged absence of a photoperiodic signal (constant lighting and constant darkness) on changes in the activity of digestive enzymes in the late postnatal ontogenesis of rats is studied. Age-related alterations were characterized by a change in enzyme activity, as well as a redistribution of the functional activity between the amylo- and lipolytic links and the upper (pancreas) and lower (small intestine) divisions of the gastrointestinal tract. It was shown that, with age, the enzyme activity was affected both by an absence of photoperiodism and by a melatonin level associated with the light regime. Age-related changes characterizing “aging” of the digestive system were observed later under light deprivation conditions than with standard illumination and especially constant illumination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Vinogradova, I.A., Ilyukha, V.A., Fedorova, A.S., et al., Age-related changes in physical performance and some biochemical parameters of rat muscles affected by light modes and pineal gland preparations, Usp. Gerontol., 2007, vol. 20, no. 1, pp. 66–73.

    Google Scholar 

  2. Drozdova, G.A. and Fekson, E.G., Determination of amylase activity in biological fluids, Lab. Delo, 1981, no. 3, pp. 138–139.

  3. Nikolaevskaya, V.R., An experimental study of the milk protein digestion in postnatal ontogenesis, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow, 1979.

  4. Svechkina, E.B., Tyutyunnik, N.N., and Vinogradova, I.A., The influence of light modes, melatonin and epithalon on the activity of pancreatic and intestinal amylases in rats of different ages, Usp. Gerontol., 2006, no. 19, pp. 66–71.

  5. Ugolev, A.M., Evolyutsiya pishchevareniya i printsipy evolyutsii funktsii: elementy sovremennogo funktsionalizma (Evolution of Digestion and Principles of Evolution of Functions: Elements of Modern Functionalism), Leningrad: Nauka, 1985.

  6. Ugolev, A.M. and Chernyakhovskaya, M.Yu., Determination of the final stages of triglyceride hydrolysis, in Issledovanie pishchevaritel’nogo apparata u cheloveka (Analysis of Human Digestive Tract), Leningrad: Nauka, 1969.

  7. Hochachka, P.W. and Somero, G.N., Strategies of Biochemical Adaptation, Philadelphia: Saunders, 1973.

    Google Scholar 

  8. Eticheskaya ekspertiza biomeditsinskikh issledovanii: Prakticheskie rekomendatsii (Ethical Expertise of Biomedical Studies: Practical Recommendations), Belousov, Yu.B., Ed., Moscow: Ross. O-vo Klin. Issled., 2005.

    Google Scholar 

  9. Acuña-Castroviejo, D., Escames, G., Venegas, C., et al., Extrapineal melatonin: sources, regulation, and potential functions, Cell. Mol. Life Sci., 2014, vol. 71, no. 16, pp. 2997–3025.

  10. Alonso-Vale, M.I., Andreotti, S., Borges-Silva, C.N., et al., Intermittent and rhythmic exposure to melatonin in primary cultured adipocytes enhances the insulin and dexamethasone effects on leptin expression, J. Pineal Res., 2006, vol. 41, no. 1, pp. 28–34.

    Article  CAS  PubMed  Google Scholar 

  11. Alonso-Vale, M.I., Andreotti, S., Peres, S.B., et al., Melatonin enhances leptin expression by rat adipocytes in the presence of insulin, Am. J. Physiol. Endocrinol. Metab., 2005, vol. 288, no. 4, pp. E805–E812.

    Article  CAS  PubMed  Google Scholar 

  12. Alonso-Vale, M.I., Anhe, G.F., Borges-Silva, C., et al., Pinealectomy alters adipose tissue adaptability to fasting in rats, Metabolism, 2004, vol. 53, no. 4, pp. 500–506.

    Article  CAS  PubMed  Google Scholar 

  13. Anhe, G.F., Caperuto, L.C., Pereira-Da-Silva, M., et al., In vivo activation of insulin receptor tyrosine kinase by melatonin in the rat hypothalamus, J. Neurochem., 2004, vol. 90, no. 3, pp. 559–566.

    Article  CAS  PubMed  Google Scholar 

  14. Anisimov, V.N., Light pollution, reproductive function and cancer risk, Neuroendocrinol. Lett., 2006, vol. 27, no. 1–2, pp. 35–52.

  15. Anisimov, V.N., Pliss, G.B., Iogannsen, M.G., et al., Spontaneous tumors in outbred LIO rats, J. Exp. Clin. Cancer Res., 1989, vol. 8, no. 4, pp. 254–262.

    Google Scholar 

  16. Arendt, J., Melatonin: characteristics, concerns, and prospects, J. Biol. Rhythms, 2005, vol. 20, no. 4, pp. 291–303.

    Article  CAS  PubMed  Google Scholar 

  17. Bahr, I., Muhlbauer, E., Schucht, H., et al., Melatonin stimulates glucagon secretion in vitro and in vivo, J. Pineal Res., 2011, vol. 50, no. 3, pp. 336–344.

    Article  CAS  PubMed  Google Scholar 

  18. Brydon, L., Petit, L., Delagrange, P., et al., Functional expression of MT2 (Mel1b) melatonin receptors in human PAZ6 adipocytes, Endocrinology, 2001, vol. 142, no. 10, pp. 4264–4271.

    Article  CAS  PubMed  Google Scholar 

  19. Bubenik, G.A., Gastrointestinal melatonin: localization, function, and clinical relevance, Dig. Dis. Sci., 2002, vol. 47, no. 10, pp. 2336–2348.

    Article  CAS  PubMed  Google Scholar 

  20. Bubenik, G.A., Localization of melatonin in the digestive tract of the rat. Effect of maturation, diurnal variation, melatonin treatment and pinealectomy, Hormone Res., 1980, vol. 12, no. 6, pp. 313–323.

    Article  CAS  PubMed  Google Scholar 

  21. Bubenik, G.A., Therapeutic perspectives of gastrointestinal melatonin, in The Melatonin: From Molecules to Therapy, Pandi-Perumal, S.R. and Cardinali, D.P., Eds., New York, Nova Science, 2006.

    Google Scholar 

  22. Bubenik, G.A., Thirty four years since the discovery of gastrointestinal melatonin, J. Physiol. Pharmacol., 2008, vol. 59, no. 2, pp. 33–51.

    PubMed  Google Scholar 

  23. Bubenik, G.A., Pang, S.F., Cockshut, J.R., et al., Circadian variation of portal, arterial and venous blood levels of melatonin in pigs and its relationship to food intake and sleep, J. Pineal Res., 2000, vol. 28, no. 1, pp. 9–15.

    Article  CAS  PubMed  Google Scholar 

  24. Chen, C., Fichna, J., Bashashati, M., et al., Distribution, function and physiological role of melatonin in the lower gut, World J. Gastroenterol., 2011, vol. 17, no. 34, pp. 3888–3898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Diaz, B. and Blazquez, E., Effect of pinealectomy on plasma glucose, insulin and glucagon levels in the rat, Horm. Metab. Res., 1986, vol. 18, no. 4, pp. 225–229.

    Article  CAS  PubMed  Google Scholar 

  26. Drago, F., Macauda, S., and Salehi, S., Small doses of melatonin increase intestinal motility in rats, Dig. Dis. Sci., 2002, vol. 47, no. 9, pp. 1969–1974.

    Article  CAS  PubMed  Google Scholar 

  27. Eckel-Mahan, K. and Sassone-Corsi, P., Metabolism and the circadian clock converge, Physiol. Rev., 2013, vol. 93, no. 1, pp. 107–135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Helander, H.F., Ultrastructure and function of gastric mucoid and zymogen cells in the rat during development, Gastroenterology, 1969, vol. 56, no. 1, pp. 53–70.

    Article  CAS  PubMed  Google Scholar 

  29. Huether, G., Hajak, G., Reimer, A., et al., The metabolic fate of infused L-tryptophan in men: possible clinical implications of the accumulation of circulating tryptophan and tryptophan metabolites, Psychopharmacology, 1992, vol. 106, no. 4, pp. 422–432.

    Article  Google Scholar 

  30. Huether, G., Messner, M., Rodenbeck, A., and Hardeland, R., Effect of continuous melatonin infusions on steady-state plasma melatonin levels in rats under near physiological conditions, J. Pineal Res., 1998, vol. 24, no. 3, pp. 146–151.

    Article  CAS  PubMed  Google Scholar 

  31. Huether, G., Poegeller, G., Reinier, R., and George, A., Effect of tryptophan administration on circulating melatonin levels in chicks and rats: evidence for stimulation of melatonin synthesis and release in the gastrointestinal tract, Life Sci., 1992, vol. 51, no. 12, pp. 945–953.

    Article  CAS  PubMed  Google Scholar 

  32. Jaworek, J., Nawrot-Porabka, K., Leja-Szpak, A., et al., Melatonin as modulator of pancreatic enzyme secretion and pancreatoprotector, J. Physiol. Pharmacol., 2007, vol. 58, no. 6, pp. 65–80.

    PubMed  Google Scholar 

  33. Konturek, S.J., Konturek, P.C., Brzozowska, I., et al., Localization and biological activities of melatonin in intact and diseased gastrointestinal tract (GIT), J. Physiol. Pharmacol., 2007, vol. 58, no. 3, pp. 381–405.

    CAS  PubMed  Google Scholar 

  34. Lee, P.P.N., Hong, G.X., and Pang, S.F., Melatonin in the gastrointestinal tract, in Role of Melatonin and Pineal Peptides in Neuroimmunomodulation, Fraschini, F. and Reiter, R.J., Eds., New York: Plenum, 1991.

    Google Scholar 

  35. Lima, F.B., Machado, U.F., Bartol, I., et al., Pinealectomy causes glucose intolerance and decreases adipose cell responsiveness to insulin in rats, Am. J. Physiol., 1998, vol. 275, no. 6, pp. 934–941.

    Google Scholar 

  36. Mendez, N., Abarzua-Catalan, L., Vilches, N., et al., Timed maternal melatonin treatment reverses circadian disruption of the fetal adrenal clock imposed by exposure to constant light, PLoS One, 2012, vol. 7, no. 8, p. e42713.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Messner, M., Hueiher, G., Lorf, T., et al., Presence of melatonin in the human hepatobiliary-gastroineslinal tract, Life Sci., 2001, vol. 69, no. 5, pp. 543–551.

    Article  CAS  PubMed  Google Scholar 

  38. Mustonen, A.-M., Nieminen, P., and Härinen, H., Effects of continuous light and melatonin treatment on energy metabolism of the rat, J. Endocrinol. Invest., 2002, vol. 25, no. 8, pp. 716–723.

    Article  CAS  PubMed  Google Scholar 

  39. Nogueira, T.C., Lellis-Santos, C., Jesus, D.S., et al., Absence of melatonin induces night-time hepatic insulin resistance and increased gluconeogenesis due to stimulation of nocturnal unfolded protein response, Endocrinology, 2011, vol. 152, no. 4, pp. 1253–1263.

    Article  CAS  PubMed  Google Scholar 

  40. Ozaki, Y. and Lynch, H.J., Presence of melatonin in plasma and urine of pineal-ectomized rats, Endocrinology, 1976, vol. 99, no. 2, pp. 641–644.

    Article  CAS  PubMed  Google Scholar 

  41. Picinato, M.C., Haber, E.P., Carpinelli, A.R., et al., Daily rhythm of glucose-induced insulin secretion by isolated islets from intact and pine-alectomized rat, J. Pineal Res., 2002, vol. 33, no. 3, pp. 172–177.

    Article  CAS  PubMed  Google Scholar 

  42. Plano, S.A., Casiraghi, L.P., García Moro, P., et al., Circadian and metabolic effects of light: implications in weight homeostasis and health, Front. Neurol., 2017, vol. 19, no. 8, p. 558.

    Article  Google Scholar 

  43. Popović, B., Velimirović, M., Stojković, T., et al., The influence of ageing on the extrapineal melatonin synthetic pathway, Exp. Gerontol., 2018, vol. 110, pp. 151–157.

    Article  CAS  PubMed  Google Scholar 

  44. Prunet-Marcassus, B., Desbazeille, M., Bros, A., et al., Melatonin reduces body weight gain in Sprague Dawley rats with diet-induced obesity, Endocrinology, 2003, vol. 144, no. 12, pp. 5347–5352.

    Article  CAS  PubMed  Google Scholar 

  45. Rasmussen, D.D., Boldt, B.M., Wilkinson, C.W., et al., Daily melatonin administration at middle age suppresses male rat visceral fat, plasma leptin, and plasma insulin to youthful levels, Endocrinology, 1999, vol. 140, no. 2, pp. 1009–1012.

    Article  CAS  PubMed  Google Scholar 

  46. Rodríguez, V., Mellado, C., Alvarez, E., et al., Effect of pineal ectomy on liver insulin and glucagon receptor concentrations in the rat, J. Pineal Res., 1989, vol. 6, no. 1, pp. 77–88.

    Article  PubMed  Google Scholar 

  47. Sánchez, S., Paredes, S.D., Martín, M.I., et al., Effect of tryptophan administration on circulating levels of melatonin and phagocytic activity, J. Appl. Biomed., 2004, vol. 2, pp. 169–177.

    Article  Google Scholar 

  48. Sanchez-Hidalgo, M., Alarcon de la Lastra, C., Carrascosa-Salmoral, M.P., et al., Age-related changes in melatonin synthesis in rat extrapineal tissues, Exp. Gerontol., 2009, vol. 44, no. 5, pp. 328–334.

    Article  CAS  PubMed  Google Scholar 

  49. Simonneax, V. and Ribelayga, C., Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters, Pharmacol. Rev., 2003, vol. 55, no. 2, pp. 325–395.

    Article  CAS  Google Scholar 

  50. Tan, D., Chen, L., Poeggler, B., and Reiter, R., Melatonin: a potent endogenous hydroxyl radical scavenger, Endocrinol. J., 2007, vol. 1, pp. 57–60.

    Google Scholar 

  51. Tan, D.-X., Manchester, L.C., Hardeland, R., et al., Melatonin: a hormone, a tissue factor, an autocoid, a paracoid, and an antioxidant vitamin, J. Pineal Res., 2003, vol. 34, no. 1, pp. 75–78.

    Article  CAS  PubMed  Google Scholar 

  52. Tapia-Osorio, A., Salgado-Delgado, R., Angeles-Castellanos, M., and Escobar, C., Disruption of circadian rhythms due to chronic constant light leads to depressive and anxiety-like behaviors in the rat, Behav. Brain. Res., 2013, vol. 252, pp. 1–9.

    Article  PubMed  Google Scholar 

  53. The Gastrointestinal System: Gastrointestinal, Nutritional and Hepatobiliary Physiology, Dordrecht: Springer-Verlag, 2014.

  54. Thor, P.J., Krolczyk, G., Gil, K., et al., Melatonin and serotonin effects on gastrointestinal motility, J. Physiol. Pharmacol., 2007, vol. 58, no. 6, pp. 97–103.

    PubMed  Google Scholar 

  55. Wolden-Hanson, T., Mitton, D.R., McCants, R.L., et al., Daily melatonin administration to middle-aged male rats suppresses body weight, intraabdominal adiposity, and plasma leptin and insulin independent of food intake and total body fat, Endocrinology, 2000, vol. 141, no. 2, pp. 487–497.

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to E.B. Svechkina for technical assistance in the collection of material.

Funding

This study was supported from the federal budget for implementing the state assignment for the Karelian Research Center of the Russian Academy of Sciences (topic no. 0218-2019-0073).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. A. Khizhkin.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by V. Mittova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khizhkin, E.A., Ilyukha, V.A., Vinogradova, I.A. et al. Absence of Photoperiodism and Digestive Enzymes in Rats: The Role of Age and the Endogenous Melatonin Level. Adv Gerontol 9, 402–410 (2019). https://doi.org/10.1134/S2079057019040106

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079057019040106

Keywords:

Navigation