Russian Journal of Developmental Biology

, Volume 46, Issue 5, pp 237–245 | Cite as

Role of hormones in perinatal and early postnatal development: Possible contribution to programming/imprinting phenomena

  • V. I. GoudochnikovEmail author


In parallel to formulating the paradigm of developmental origins of health and disease (DOHaD), the search began on mechanisms of programming/imprinting in ontogeny. Some recent evidence has revealed the important role of glucocorticoids in such mechanisms. However, in the last decades numerous data have been accumulated on participation of other hormones in developmental bioregulation. In present article we analyse these data, as referred to melatonin, but also to neuroactive steroids, somatolactogens and related peptides: insulin-like growth factor of type I (IGF-I) and oxytocin, i.e. peptide regulators related to growth and lactation respectively. Special attention was devoted to the evidence of glucocorticoid interactions with some of these hormones.


melatonin neuroactive steroids somatolactogens insulin-like growth factor-I oxytocin 


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  1. Allen, D.B., Julius, J.R., Breen, T.J., and Attie, K.M., Treatment of glucocorticoid-induced growth suppression with growth hormone, J. Clin. Endocrinol. Metab., 1998, vol. 83, pp. 2824–2829.CrossRefPubMedGoogle Scholar
  2. Arumugam, R., Horowitz, E., Lu, D., et al., The interplay of prolactin and the glucocorticoids in the regulation of beta-cell gene expression, fatty acid oxidation, and glucose-stimulated insulin secretion: implications for carbohydrate metabolism in pregnancy, Endocrinology, 2008, vol. 149, pp. 5401–5414.PubMedCentralCrossRefPubMedGoogle Scholar
  3. Bagby, S.P., Developmental hypertension, nephrogenesis, and mother’s milk: programming the neonate, J. Am. Soc. Nephrol., 2007, vol. 18, pp. 1626–1629.CrossRefPubMedGoogle Scholar
  4. Bagnell, C.A., Steinetz, B.G., and Bartol, F.F., Milk-borne relaxin and the lactocrine hypothesis for maternal programming of neonatal tissues, Ann. N.Y. Acad. Sci., 2009, vol. 1160, pp. 152–157.CrossRefPubMedGoogle Scholar
  5. Bartol, F.F., Wiley, A.A., and Bagnell, C.A., Epigenetic programming of porcine endometrial function and the lactocrine hypothesis, Reprod. Dom. Anim., 2008, vol. 43, suppl. 2, pp. 273–279.CrossRefGoogle Scholar
  6. Bartol, F.F., Wiley, A.A., and Bagnell, C.A., Relaxin and maternal lactocrine programming of neonatal uterine development, Ann. N.Y. Acad. Sci., 2009, vol. 1160, pp. 158–163.CrossRefPubMedGoogle Scholar
  7. Braun, T., Li, S., Moss, T.J., et al., Maternal betamethasone administration reduces binucleate cell number and placental lactogen in sheep, J. Endocrinol., 2007, vol. 194, pp. 337–347.CrossRefPubMedGoogle Scholar
  8. Brummelte, S., Schmidt, K.L., Taves, M.D., et al., Elevated corticosterone levels in stomach milk, serum, and brain of male and female offspring after maternal corticosterone treatment in the rat, Develop. Neurobiol., 2010, vol. 70, pp. 714–725.CrossRefGoogle Scholar
  9. Brunton, P.J., Russell, J.A., and Douglas, A.J., Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation, J. Neuroendocrinol., 2008, vol. 20, pp. 764–776.CrossRefPubMedGoogle Scholar
  10. Brunton, P.J., Resetting the dynamic range of hypothalamicpituitary-adrenal axis stress responses through pregnancy, J. Neuroendocrinol., 2010, vol. 2, pp. 1198–1213.CrossRefGoogle Scholar
  11. Casolini, P., Domenici, M.R., Cinque, C., et al., Maternal exposure to low levels of corticosterone during lactation protects the adult offspring against ischemic brain damage, J. Neurosci., 2007, vol. 27, pp. 7041–7046.CrossRefPubMedGoogle Scholar
  12. Chen, Y.-H., Xu, D.-X., Wang, J.-P., et al., Melatonin protects against lipopolysaccharide-induced intra-uterine fetal death and growth retardation in mice, J. Pineal Res., 2006, vol. 40, pp. 40–47.CrossRefPubMedGoogle Scholar
  13. Chen, Y.-C., Sheen, J.-M., Tiao, M.-M., et al., Roles of melatonin in fetal programming in compromised pregnancies, Int. J. Mol. Sci., 2013, vol. 14, pp. 5380–5401.PubMedCentralCrossRefPubMedGoogle Scholar
  14. Chiam, K., Tilley, W.D., Butler, L.M., and Bianco-Miotto, T., The dynamic and static modification of the epigenome by hormones: a role in the developmental origin of hormone related cancers, Biochim. Biophys. Acta, 2009, vol. 1795, pp. 104–109.PubMedGoogle Scholar
  15. Cianfarani, S., Germani, D., Rossi, L., et al., IGF-I and IGF-binding protein-1 are related to cortisol in human cord blood, Eur. J. Endocrinol., 1998, vol. 138, pp. 524–529.CrossRefPubMedGoogle Scholar
  16. Cisternas, C.D., Compagnucci, M.V., Conti, N.R., et al., Protective effect of maternal prenatal melatonin administration on rat pups born to mothers submitted to constant light during gestation, Braz. J. Med. Biol. Res., 2010, vol. 43, pp. 874–882.CrossRefPubMedGoogle Scholar
  17. Csaba, G. and Inczefi-Gonda, A., Breastmilk can mediate chemical imprinting: benzpyrene exposure during lactation reduces the thymic glucocorticoid receptor density of the offspring, Gen. Pharmacol., 1994, vol. 25, pp. 603–606.CrossRefPubMedGoogle Scholar
  18. Csaba, G., The biological basis and clinical significance of hormonal imprinting, an epigenetic process, Clin. Epigenet., 2011, vol. 2, pp. 187–196.CrossRefGoogle Scholar
  19. Darnaudery, M., Perez-Martin, M., Belizaire, G., et al., Insulin-like growth factor 1 reduces age-related disorders induced by prenatal stress in female rats, Neurobiol. Aging, 2006, vol. 27, pp. 119–127.CrossRefPubMedGoogle Scholar
  20. Davis, F.C., Melatonin: role in development, J. Biol. Rhythms, 1997, vol. 12, pp. 498–508.CrossRefPubMedGoogle Scholar
  21. Dong, F. and Ren, J., Insulin-like growth factors (IGFs) and IGF-binding proteins in nephrotic syndrome children on glucocorticoid, Pharmacol. Res., 2003, vol. 48, pp. 319–323.CrossRefPubMedGoogle Scholar
  22. Douglas, A.J., Johnstone, H.A., Wigger, A., et al., The role of endogenous opioids in neurohypophysial and hypothalamo-pituitary-adrenal axis hormone secretory responses to stress in pregnant rats, J. Endocrinol., 1998, vol. 158, pp. 285–293.CrossRefPubMedGoogle Scholar
  23. Fedotov, V.P. and Goudochnikov, V.I., The role of catecholamines in neurohumoral influences on cultured rat pituitary cells: high sensitivity in early postnatal development and interactions with glucocorticoid hormone, in 10. International Symposium on Chromaffin Cell Biology, Bergen, 1999, p. 180.Google Scholar
  24. Fedotov, V.P., Gudoshnikov, V.I., Komolov, I.S., and Abramova, V.V., Secretory activity of lactotrophs and its regulation by hypothalamic hormones in primary pituitary cell cultures from rats of different ages, Bull. Exp. Biol. Med. (Moscow), 1992, vol. 113, pp. 536–539.CrossRefGoogle Scholar
  25. Ferreira, D.S., Amaral, F.G., Mesquita, C.C., et al., Maternal melatonin programs the daily pattern of energy metabolism in adult offspring, PLoS ONE, 2012, vol. 7, Article e38795.PubMedCentralCrossRefPubMedGoogle Scholar
  26. Fowden, A.L., Giussani, D.A., and Forhead, A.J., Intrauterine programming of physiological systems: causes and consequences, Physiology, 2006, vol. 21, pp. 29–37.CrossRefPubMedGoogle Scholar
  27. Fowden, A.L. and Forhead, A.J., Hormones as epigenetic signals in developmental programming, Exp. Physiol., 2009, vol. 94, pp. 607–625.CrossRefPubMedGoogle Scholar
  28. Freemark, M., Regulation of maternal metabolism by pituitary and placental hormones: roles in fetal development and metabolic programming, Horm. Res., 2006, vol. 65, suppl. 3, pp. 41–49.CrossRefPubMedGoogle Scholar
  29. Gaal, A. and Csaba, G., Effect of retinoid (vitamin A or retinoic acid) treatment (hormonal imprinting) through breastmilk on the glucocorticoid receptor and estrogen receptor binding capacity of the adult rat offspring, Hum. Exp. Toxicol., 1998, vol. 17, pp. 560–563.CrossRefPubMedGoogle Scholar
  30. Gallou-Kabani, C., Vige, A., and Junien, C., Lifelong circadian and epigenetic drifts in metabolic syndrome, Epigenetics, 2007, vol. 2, pp. 137–146.CrossRefPubMedGoogle Scholar
  31. Gicquel, C. and Le Bouc, Y., Hormonal regulation of fetal growth, Horm. Res., 2006, vol. 65, suppl. 3, pp. 28–33.CrossRefPubMedGoogle Scholar
  32. Gitto, E., Pellegrino, S., Gitto, P., et al., Oxidative stress of the newborn in the preand postnatal period and the clinical utility of melatonin, J. Pineal Res., 2009, vol. 46, pp. 128–139.CrossRefPubMedGoogle Scholar
  33. Gluckman, P.D. and Pinal, C.S., Regulation of fetal growth by the somatotrophic axis, J. Nutr., 2003, vol. 133, pp. 1741S–1746S.Google Scholar
  34. Gluckman, P.D., Hanson, M.A., Buklijas, T., et al., Epigenetic mechanisms that underpin metabolic and cardiovascular diseases, Nature Rev. Endocrinol., 2009, vol. 5, pp. 401–408.CrossRefGoogle Scholar
  35. Gluckman, P.D., Hanson, M.A., and Buklijas, T., A conceptual framework for the developmental origins of health and disease, J. Dev. Orig. Health Dis., 2010, vol. 1, pp. 6–18.CrossRefPubMedGoogle Scholar
  36. Godfrey, K.M. and Barker, D.J.P., Fetal programming and adult health, Public Health Nutr., 2001, vol. 4, pp. 611–624.CrossRefPubMedGoogle Scholar
  37. Godfrey, K.M., Lillycrop, K.A., Burdge, G.C., et al., Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease, Pediatr. Res., 2007, vol. 61, pp. 5R–10R.CrossRefPubMedGoogle Scholar
  38. Goudochnikov, V.I., Relationship between stored and secreted growth hormone and prolactin in primary cultures of pituitary cells obtained from neonatal, prepubertal and adult rats, in 10. Reuniao Anual da FESBE, Serra Negra, 1995, p. 373.Google Scholar
  39. Goudochnikov, V.I., Pathogeny of glucocorticoid-induced growth retardation, evaluated in experimental studies using laboratory animals and cell cultures as models, NewsLab (Sao Paulo), 1997, no. 22, pp. 90–100.Google Scholar
  40. Goudochnikov, V.I., Glucocorticoid programming: prenatal or perinatal?, J. Dev. Orig. Health Dis., 2009, vol. 1, suppl. 1, pp. S182–S183.Google Scholar
  41. Goudochnikov, V.I. and Dalmora, S.L., Age-related peculiarities and tissue-specific mechanisms of growth-regulatory hormonal effects, in 23. Encontro Anual de Ciencias Fisiologicas do Rio Grande do Sul, Santa Maria, 1994, p. 16.Google Scholar
  42. Goudochnikov, V.I., Mamayeva, T.V., and Fedotov, V.P., Study on the control of growth hormone secretion in early postnatal development by means of rat pituitary cell cultures, Medicina (Buenos Aires), 1996, vol. 56, pp. 613–614.Google Scholar
  43. Groer, M.W., Davis, M.W., and Hemphill, J., Postpartum stress: current concepts and the possible protective role of breast-feeding, J. Obstet. Gynecol. Neonatal Nurs., 2002, vol. 31, pp. 411–417.CrossRefPubMedGoogle Scholar
  44. Gudoshnikov, V.I. and Fedotov, V.P., Increased sensitivity of neonatal rat pituitary cells to bromocriptine and melatonin, Bull. Exp. Biol. Med. (Moscow), 1993a, vol. 115, pp. 202–204.CrossRefGoogle Scholar
  45. Gudoshnikov, V.I. and Fedotov, V.P., The heightened sensitivity of hypophyseal cells of neonatal rats to corticosteroids, Neurosci. Behav. Physiol. (New York), 1993b, vol. 23, pp. 107–111.CrossRefGoogle Scholar
  46. Gudoshnikov, V.I., Mamaeva, T.V., and Fedotov, V.P., Effect of steroid hormones and noradrenalin on the growth hormone secretion by the primary cultures of pituitary gland cells of rats of different age, Probl. Endokrinol., 1994, vol. 40, no. 1, pp. 39–41.Google Scholar
  47. Gunn, B.G., Brown, A.R., Lambert, J.J., and Belelli, D., Neurosteroids and GABAA receptor interactions: a focus on stress, Front. NeuroSci., 2011, vol. 5, Article 131.Google Scholar
  48. Hardeland, R., Melatonin, non-coding RNAs, messenger RNA stability and epigenetics: evidence, hints, gaps and perspectives, Int. J. Mol. Sci., 2014, vol. 15, pp. 18221–18252.PubMedCentralCrossRefPubMedGoogle Scholar
  49. Harris, A. and Seckl, J., Glucocorticoids, prenatal stress and the programming of disease, Horm Behav., 2011, vol. 59, pp. 279–289.CrossRefPubMedGoogle Scholar
  50. Heinrichs, M., Neumann, I., and Ehlert, U., Lactation and stress: protective effects of breast-feeding in humans, Stress, 2002, vol. 5, pp. 195–203.CrossRefPubMedGoogle Scholar
  51. Hill, D.J., Strain, A.J., and Milner, R.D.G., Growth factors in embryogenesis, Oxford Rev. Reprod. Biol., 1987, vol. 9, pp. 398–455.Google Scholar
  52. Hill, P.D., Chatterton, R.T., and Aldag, J.C., Neuroendocrine responses to stressors in lactating and nonlactating mammals: a literature review, Biol. Res. Nursing, 2003, vol. 5, pp. 79–86.CrossRefGoogle Scholar
  53. Hirst, J.J., Walker, D.W., Yawno, T., and Palliser, H.K., Stress in pregnancy: a role for neuroactive steroids in protecting the fetal and neonatal brain, Dev. NeuroSci., 2009, vol. 31, pp. 363–377.CrossRefPubMedGoogle Scholar
  54. Hokken-Koelega, A.C.S., Stijnen, T., de Muinck Keizer Schrama, S.M., et al., Levels of growth hormone, insulin-like growth factor-I (IGF-I) and -II, IGF-binding protein-1 and -3, and cortisol in prednisone-treated children with growth retardation after renal transplantation, J. Clin. Endocrinol. Metab., 1993, vol. 77, pp. 932–938.PubMedGoogle Scholar
  55. Horton, Th., Ray, S.L., and Stetson, M.H., Maternal transfer of photoperiodic information in Siberian hamsters. III. Melatonin injections program postnatal reproductive development expressed in constant light, Biol. Reprod., 1989, vol. 40, pp. 34–39.CrossRefGoogle Scholar
  56. Ingulli, E., Singh, A., Moazami, S., and Tejani, A., Prednisone inhibits the efficacy of recombinant human growth hormone in pediatric renal transplant recipients, Kidney Int., 1993, vol. 44, suppl. 43, pp. 65–S70.Google Scholar
  57. Jahnke, G., Marr, M., Myers, C., et al., Maternal and developmental toxicity evaluation of melatonin administered orally to pregnant Sprague–Dawley rats, Toxicol. Sci., 1999, vol. 50, pp. 271–279.CrossRefPubMedGoogle Scholar
  58. Kennaway, D.J., Melatonin and development: physiology and pharmacology, Semin. Perinatol., 2000, vol. 24, pp. 258–266.CrossRefPubMedGoogle Scholar
  59. Kennaway, D.J., Programming of the fetal suprachiasmatic nucleus and subsequent adult rhythmicity, Trends Endocrinol. Metab., 2002, vol. 13, pp. 398–402.CrossRefPubMedGoogle Scholar
  60. Kim, M.-J., Kim, H.K., Kim, B.-S., and Yim, S.-V., Melatonin increases cell proliferation in the dentate gyrus of maternally separated rats, J. Pineal Res., 2004, vol. 37, pp. 193–197.CrossRefPubMedGoogle Scholar
  61. Korkmaz, A., Rosales-Corral, S., and Reiter, R.J., Gene regulation by melatonin linked to epigenetic phenomena, Gene, 2012, vol. 503, pp. 1–11.CrossRefPubMedGoogle Scholar
  62. Kwon, K.J., Kim, J.N., Kim, M.K., et al., Melatonin synergistically increases resveratrol-induced heme oxygenase-1 expression through the inhibition of ubiquitindependent proteasome pathway: a possible role in neuroprotection, J. Pineal Res., 2011, vol. 50, pp. 110–123.PubMedGoogle Scholar
  63. Langley-Evans, S.C., Developmental programming of health and disease, Proc. Nutr. Soc., 2006, vol. 65, pp. 97–105.PubMedCentralCrossRefPubMedGoogle Scholar
  64. Lee, P.R., Brady, D.L., Shapiro, R.A., et al., Prenatal stress generates deficits in rat social behavior: reversal by oxytocin, Brain Res., 2007, vol. 1156, pp. 152–167.PubMedCentralCrossRefPubMedGoogle Scholar
  65. Lupu, F., Terwilliger, J.D., Lee, K., et al., Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth, Dev. Biol., 2001, vol. 229, pp. 141–162.CrossRefPubMedGoogle Scholar
  66. Matsuzuka, T., Sakamoto, N., Ozawa, M., et al., Alleviation of maternal hyperthermia-induced early embryonic death by administration of melatonin to mice, J. Pineal Res., 2005, vol. 39, pp. 217–223.CrossRefPubMedGoogle Scholar
  67. Mauras, N., Growth hormone therapy in the glucocorticosteroid-dependent child: metabolic and linear growth effects, Horm. Res., 2001, vol. 56, no. Suppl. 1, pp. 13–18.CrossRefPubMedGoogle Scholar
  68. McArthur, S., Siddique, Z.L., Christian, H.C., et al., Perinatal glucocorticoid treatment disrupts the hypothalamolactotroph axis in adult female, but not male, rats, Endocrinology, 2006, vol. 147, pp. 1904–1915.CrossRefPubMedGoogle Scholar
  69. Meaney, M.J., Szyf, M., and Seckl, J.R., Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health, Trends Mol. Med., 2007, vol. 13, pp. 269–277.CrossRefPubMedGoogle Scholar
  70. Mehls, O., Tonshoff, B., Kovacs, G., et al., Interaction between glucocorticoids and growth hormone, Acta Paediatr. Suppl., 1993, vol. 388, pp. 77–82.PubMedGoogle Scholar
  71. Morley-Fletcher, S., Mairesse, J., Soumier, A., et al., Chronic agomelatine treatment corrects behavioral, cellular, and biochemical abnormalities induced by prenatal stress in rats, Psychopharmacology, 2011, vol. 217, pp. 301–313.CrossRefPubMedGoogle Scholar
  72. Mosier, H.D., Jr. and Jansons, R.A., Increase in pulsatile secretion of growth hormone during failure of catch-up growth following glucocorticoid-induced growth inhibition, Proc. Soc. Exp. Biol. Med., 1985, vol. 178, pp. 457–461.CrossRefPubMedGoogle Scholar
  73. de Moura, E.G., Lisboa, P.C., and Passos, M.C.F., Neonatal programming of neuroimmunomodulation: role of adipocytokines and neuropeptides, Neuroimmunomodulation, 2008, vol. 15, pp. 176–188.CrossRefPubMedGoogle Scholar
  74. Nogami, H. and Tachibana, T., Dexamethasone induces advanced growth hormone expression in the fetal rat pituitary gland in vivo, Endocrinology, 1993, vol. 132, pp. 517–523.PubMedGoogle Scholar
  75. Ortoft, G., Gronbaek, H., and Oxlund, H., Growth hormone administration can improve growth in glucocorticoid-injected rats without affecting the lymphocytopenic effect of the glucocorticoid, Growth Hormone IGF Res., 1998, vol. 8, pp. 251–264.CrossRefGoogle Scholar
  76. Ortoft, G., Andreassen, T.T., and Oxlund, H., Growth hormone can reverse glucocorticoid-induced low bone turnover on cortical but not on cancellous bone surfaces in adult Wistar rats, Bone, 2005, vol. 36, pp. 123–133.CrossRefPubMedGoogle Scholar
  77. Oxenkrug, G.F., Requintina, P.J., and Juwiler, A., Ontogenetic effects of MAO-A inhibition on rat pineal N-acetylserotonin and melatonin during the first month of neonatal life, Hum. Psychopharmacol., 2000, vol. 15, pp. 589–593.CrossRefPubMedGoogle Scholar
  78. Patchev, V.K., Montkowski, A., Rouskova, D., et al., Neonatal treatment of rats with the neuroactive steroid tetrahydrodeoxycorticosterone (THDOC) abolishes the behavioral and neuroendocrine consequences of adverse early life events, J. Clin. Invest., 1997, vol. 99, pp. 962–966.PubMedCentralCrossRefPubMedGoogle Scholar
  79. Plagemann, A., 'Fetal programming and functional teratogenesis': on epigenetic mechanisms and prevention of perinatally acquired lasting health risks, J. Perinat. Med., 2004, vol. 32, pp. 297–305.CrossRefPubMedGoogle Scholar
  80. Richter, H.G., Hansell, J.A., Raut, S., and Giussani, D.A., Melatonin improves placental efficiency and birth weight and increases the placental expression of antioxidant enzymes in undernourished pregnancy, J. Pineal Res., 2009, vol. 46, pp. 357–364.CrossRefPubMedGoogle Scholar
  81. Rivkees, S.A., Danon, M., and Herrin, J., Prednisone dose limitation of growth hormone treatment of steroidinduced growth failure, J. Pediatr., 1994, vol. 125, pp. 322–325.CrossRefPubMedGoogle Scholar
  82. Robson, H., Siebler, T., Shalet, S.M., and Williams, G.R., Interactions between GH, IGF-I, glucocorticoids, and thyroid hormones during skeletal growth, Pediatr. Res., 2002, vol. 52, pp. 137–147.CrossRefPubMedGoogle Scholar
  83. Root, A.W., Bongiovanni, A.M., and Eberlein, W.R., Studies of the secretion and metabolic effects of human growth hormone in children with glucocorticoid-induced growth retardation, J. Pediatr., 1969, vol. 75, pp. 826–832.CrossRefPubMedGoogle Scholar
  84. Savino, F., Liguori, S.A., Fissore, M.F., and Oggero, R., Breast milk hormones and their protective effect on obesity, Int. J. Pediat. Endocr., 2009, Article ID 327505.Google Scholar
  85. Sawano, S., Arimura, A., Schally, A.V., et al., Neonatal corticoid administration: effects upon adult pituitary growth hormone and hypothalamic growth hormone-releasing hormone activity, Acta Endocrinol. (Copenh.), 1969, vol. 61, pp. 57–67.Google Scholar
  86. Schack-Nielsen, L. and Michaelsen, K.F., Advances in our understanding of the biology of human milk and its effects on the offspring, J. Nutr., 2007, vol. 137, pp. 503S–510S.PubMedGoogle Scholar
  87. Siebler, T., Robson, H., Shalet, S.M., and Williams, G.R., Glucocorticoids, thyroid hormone and growth hormone interactions: implications for the growth plate, Horm. Res., 2001, vol. 56, no. Suppl. 1, pp. 7–12.CrossRefPubMedGoogle Scholar
  88. Simon, D., Lucidarme, N., Prieur, A.M., et al., Treatment of growth failure in juvenile chronic arthritis, Horm. Res., 2002, vol. 58, suppl. 1, pp. 28–32.CrossRefPubMedGoogle Scholar
  89. Soyka, L.F. and Crawford, J.D., Antagonism by cortisone of the linear growth induced in hypopituitary patients and hypophysectomized rats by human growth hormone, J. Clin. Endocrinol., 1965, vol. 25, pp. 469–475.CrossRefGoogle Scholar
  90. Thakkar, B.P., Zala, V.M., and Ramachandran, A.V., Simultaneous melatonin administration effectively deprograms the negative influence of neonatal hypothyroidism on immature follicles but not on mature follicles and body and ovarian weights, J. Endocrinol. Metab., 2011, vol. 1, pp. 220–226.Google Scholar
  91. Tomas, F.M., The anti-catabolic efficacy of insulin-like growth factor-I is enhanced by its early administration to rats receiving dexamethasone, J. Endocrinol., 1998, vol. 157, pp. 89–97.CrossRefPubMedGoogle Scholar
  92. Torres-Farfan, C., Valenzuela, F.J., Germain, A.M., et al., Maternal melatonin stimulates growth and prevents maturation of the capuchin monkey fetal adrenal gland, J. Pineal Res., 2006, vol. 41, pp. 58–66.CrossRefPubMedGoogle Scholar
  93. Ugrumov, M.V., Developing brain as an endocrine organ: a paradoxical reality, Neurochem. Res., 2010, vol. 35, pp. 837–850.CrossRefPubMedGoogle Scholar
  94. Valtonen, M., Kangas, A.-P., Voutilainen, M., and Ericksson, L., Diurnal rhythm of melatonin in young calves and intake of melatonin in milk, J. Animal Sci., 2003, vol. 77, pp. 149–154.Google Scholar
  95. Varcoe, T.J., Wight, N., Voultsios, A., et al., Chronic phase shifts of the photoperiod throughout pregnancy programs glucose intolerance and insulin resistance in the rat, PLoS ONE, 2011, vol. 6, Article ID 327505.Google Scholar
  96. Vilela, F.C. and Giusti-Paiva, A., Glucocorticoids disrupt neuroendocrine and behavioral responses during lactation, Endocrinology, 2011, vol. 152, pp. 4838–4845.CrossRefPubMedGoogle Scholar
  97. Waldhauser, F., Ehrhart, B., and Forster, E., Clinical aspects of the melatonin action: impact of development, aging, and puberty, involvement of melatonin in psychiatric disease and importance of neuroimmunoendocrine interactions, Experientia, 1993, vol. 49, pp. 671–681.CrossRefPubMedGoogle Scholar
  98. Watanabe, K., Wakatsuki, A., Shinohara, K., et al., Maternally administered melatonin protects against ischemia and reperfusion-induced oxidative mitochondrial damage in premature fetal rat brain, J. Pineal Res., 2004, vol. 37, pp. 276–280.CrossRefPubMedGoogle Scholar

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© Pleiades Publishing, Inc. 2015

Authors and Affiliations

  1. 1.Council of International Society for DOHaDSanta Maria—RSBrazil

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