Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0048
Animal Reproduction (AR)
Thematic Section: 37th Annual Meeting of the Brazilian Embryo Technology Society (SBTE)

Puberty in beef heifers: effects of prenatal and postnatal nutrition on the development of the neuroendocrine axis

Sarah West; Viviana Garza; Rodolfo Cardoso

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Abstract

Reproductive maturation is a complex physiological process controlled by the neuroendocrine system and is characterized by an increase in gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) pulsatile secretion. Nutrition during early development is a key factor regulating puberty onset, which is defined as first ovulation in females. In heifers, nutrient restriction after weaning delays puberty, whereas elevated levels of nutrition and energy reserves advance reproductive maturation. Recent studies in cattle and other animal models have shown that the dam’s nutrition during gestation can also program the neuroendocrine system in the developing fetus and has the potential to alter timing of puberty in the offspring. Among the metabolic signals that modulate brain development and control timing of puberty is leptin, a hormone produced primarily by adipocytes that communicates energy status to the brain. Leptin acts within the arcuate nucleus of the hypothalamus to regulate GnRH secretion via an upstream network of neurons that includes neurons that express neuropeptide Y (NPY), an orexigenic peptide with inhibitory effects on GnRH secretion, and alpha melanocyte-stimulating hormone (αMSH), an anorexigenic peptide with excitatory effects on GnRH neurons. Another important population of neurons are KNDy neurons, neurons in the arcuate nucleus that co-express the neuropeptides kisspeptin, neurokinin B, and dynorphin and have strong stimulatory effects on GnRH secretion. Our studies in beef heifers indicate that increased nutrition between 4 to 8 months of age advances puberty by diminishing NPY inhibitory tone and by increasing excitatory inputs of αMSH and kisspeptin, which collectively lead to increased GnRH/LH pulsatility. Our ongoing studies indicate that different planes of nutrition during gestation can alter maternal leptin concentrations and promote changes in the fetal brain. Nonetheless, at least in Bos indicus-influenced heifers, deficits programmed prenatally can be overcome by adequate postnatal nutrition without negatively impacting age at puberty or subsequent fertility.

Keywords

heifers, hypothalamus, nutrition, puberty

References

Allen CC, Alves BR, Li X, Tedeschi LO, Zhou H, Paschal JC, Riggs PK, Braga-Neto UM, Keisler DH, Williams GL, Amstalden M. Gene expression in the arcuate nucleus of heifers is affected by controlled intake of high-and low-concentrate diets. J Anim Sci. 2012;90(7):2222-32. http://doi.org/10.2527/jas.2011-4684. PMid:22266992.

Allen CC, Tedeschi LO, Keisler DH, Cardoso RC, Alves BRC, Amstalden M, Williams GL. Interaction of dietary energy source and body weight gain during the juvenile period on metabolic endocrine status and age at puberty in beef heifers. J Anim Sci. 2017;95(5):2080-8. PMid:28727020.

Alves BR, Cardoso RC, Prezotto LD, Thorson JF, Bedenbaugh M, Sharpton SM, Caraty A, Keisler DH, Tedeschi LO, Williams GL, Amstalden M. Elevated body weight gain during the juvenile period alters neuropeptide Y-gonadotropin-releasing hormone circuitry in prepubertal heifers. Biol Reprod. 2015;92(2):46. http://doi.org/10.1095/biolreprod.114.124636. PMid:25505201.

Amstalden M, Alves BR, Liu S, Cardoso RC, Williams GL. Neuroendocrine pathways mediating nutritional acceleration of puberty: insights from ruminant models. Front Endocrinol (Lausanne). 2011;2:109. http://doi.org/10.3389/fendo.2011.00109. PMid:22654842.

Amstalden M, Garcia MR, Stanko RL, Nizielski SE, Morrison CD, Keisler DH, Williams GL. Central infusion of recombinant ovine leptin normalizes plasma insulin and stimulates a novel hypersecretion of luteinizing hormone after short-term fasting in mature beef cows. Biol Reprod. 2002;66(5):1555-61. http://doi.org/10.1095/biolreprod66.5.1555. PMid:11967223.

Amstalden M, Garcia MR, Williams SW, Stanko RL, Nizielski SE, Morrison CD, Keisler DH, Williams GL. Leptin gene expression, circulating leptin, and luteinizing hormone pulsatility are acutely responsive to short-term fasting in prepubertal heifers: relationships to circulating insulin and insulin-like growth factor I(1). Biol Reprod. 2000;63(1):127-33. http://doi.org/10.1095/biolreprod63.1.127. PMid:10859251.

Amstalden M, Zieba DA, Edwards JF, Harms PG, Welsh TH Jr, Stanko RL, Williams GL. Jr., Stanko, R.L., Williams, G.L. Leptin acts at the bovine adenohypophysis to enhance basal and gonadotropin-releasing hormone-mediated release of luteinizing hormone: differential effects are dependent upon nutritional history. Biol Reprod. 2003;69(5):1539-44. http://doi.org/10.1095/biolreprod.103.018119. PMid:12826579.

Bell AW, Greenwood PL. Prenatal origins of postnatal variation in growth, development and productivity of ruminants. Anim Prod Sci. 2016;56(8):1217-32. http://doi.org/10.1071/AN15408.

Buskirk DD, Faulkner DB, Ireland FA. Subsequent productivity of beef heifers that received creep feed for 0, 28, 56, or 84 d before weaning. Prof Anim Sci. 1996;12(1):37-43. http://doi.org/10.15232/S1080-7446(15)32480-3.

Candler T, Kuhnen P, Prentice AM, Silver M. Epigenetic regulation of POMC; implications for nutritional programming, obesity and metabolic disease. Front Neuroendocrinol. 2019;54:100773. http://doi.org/10.1016/j.yfrne.2019.100773. PMid:31344387.

Cardoso R, Alves B, Prezotto L, Thorson J, Tedeschi L, Keisler D, Park C, Amstalden M, Williams G. Use of a stair-step compensatory gain nutritional regimen to program the onset of puberty in beef heifers. J Anim Sci. 2014a;92(7):2942-9. http://doi.org/10.2527/jas.2014-7713. PMid:24879767.

Cardoso RC, Alves BR, Prezotto LD, Thorson JF, Tedeschi LO, Keisler DH, Amstalden M, Williams GL. Reciprocal changes in leptin and NPY during nutritional acceleration of puberty in heifers. J Endocrinol. 2014b;223(3):289-98. http://doi.org/10.1530/JOE-14-0504. PMid:25326602.

Cardoso R, Alves B, Sharpton S, Williams G, Amstalden M. Nutritional Programming of Accelerated Puberty in Heifers: Involvement of Pro‐Opiomelanocortin Neurones in the Arcuate Nucleus. J Neuroendocrinol. 2015;27(8):647-57. http://doi.org/10.1111/jne.12291. PMid:25944025.

Cardoso RC, Alves BR, Williams GL. Neuroendocrine signaling pathways and the nutritional control of puberty in heifers. Anim Reprod. 2018;15(Suppl 1):868-78. http://doi.org/10.21451/1984-3143-AR2018-0013. PMid:36249846.

Cardoso RC, West SM, Maia TS, Alves BR, Williams GL. Nutritional control of puberty in the bovine female: prenatal and early postnatal regulation of the neuroendocrine system. Domest Anim Endocrinol. 2020;73:106434. http://doi.org/10.1016/j.domaniend.2020.106434. PMid:32115309.

Caron A, Lemko HMD, Castorena CM, Fujikawa T, Lee S, Lord CC, Ahmed N, Lee CE, Holland WL, Liu C, Elmquist JK. POMC neurons expressing leptin receptors coordinate metabolic responses to fasting via suppression of leptin levels. Elife. 2018;7:e33710. http://doi.org/10.7554/eLife.33710. PMid:29528284.

Cheng G, Coolen LM, Padmanabhan V, Goodman RL, Lehman MN. The kisspeptin/neurokinin B/dynorphin (KNDy) cell population of the arcuate nucleus: sex differences and effects of prenatal testosterone in sheep. Endocrinology. 2010;151(1):301-11. http://doi.org/10.1210/en.2009-0541. PMid:19880810.

Clarke IJ, Cummins JTJE. The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes. Endocrinology. 1982;111(5):1737-9. http://doi.org/10.1210/endo-111-5-1737. PMid:6751801.

Cone RD, Cowley MA, Butler AA, Fan W, Marks DL, Low MJ. The arcuate nucleus as a conduit for diverse signals relevant to energy homeostasis. Int J Obes. 2001;25(Suppl 5):S63-7. http://doi.org/10.1038/sj.ijo.0801913. PMid:11840218.

Cushman R, McNeel AK, Freetly HC. The impact of cow nutrient status during the second and third trimesters on age at puberty, antral follicle count, and fertility of daughters. Livest Sci. 2014;162:252-8. http://doi.org/10.1016/j.livsci.2014.01.033.

Day ML, Imakawa K, Garcia-Winder M, Zalesky DD, Schanbacher BD, Kittok RJ, Kinder JE. Endocrine mechanisms of puberty in heifers: estradiol negative feedback regulation of luteinizing hormone secretion. Biol Reprod. 1984;31(2):332-41. http://doi.org/10.1095/biolreprod31.2.332. PMid:6478017.

Day ML, Imakawa K, Wolfe PL, Kittok RJ, Kinder JE. Endocrine mechanisms of puberty in heifers. Role of hypothalamo-pituitary estradiol receptors in the negative feedback of estradiol on luteinizing hormone secretion. Biol Reprod. 1987;37(5):1054-65. http://doi.org/10.1095/biolreprod37.5.1054. PMid:2832005.

Dorling AA, Todman MG, Korach KS, Herbison AE. Critical role for estrogen receptor alpha in negative feedback regulation of gonadotropin-releasing hormone mRNA expression in the female mouse. Neuroendocrinology. 2003;78(4):204-9. http://doi.org/10.1159/000073703. PMid:14583652.

Eley RM, Thatcher WW, Bazer FW, Wilcox CJ, Becker RB, Head HH, Adkinson RW. Development of the conceptus in the bovine. J Dairy Sci. 1978;61(4):467-73. http://doi.org/10.3168/jds.S0022-0302(78)83622-4. PMid:659690.

Evans MC, Anderson GM. Neuroendocrine integration of nutritional signals on reproduction. J Mol Endocrinol. 2017;58(2):R107-28. http://doi.org/10.1530/JME-16-0212. PMid:28057770.

Fernandez-Fernandez R, Navarro V, Barreiro M, Vigo E, Tovar S, Sirotkin A, Casanueva F, Aguilar E, Dieguez C, Pinilla LJ, Tena-Sempere M. Effects of chronic hyperghrelinemia on puberty onset and pregnancy outcome in the rat. Endocrinology. 2005;146(7):3018-25. http://doi.org/10.1210/en.2004-1622. PMid:15790726.

Foster DL, Ryan KD. Endocrine mechanisms governing transition into adulthood: a marked decrease in inhibitory feedback action of estradiol on tonic secretion of luteinizing hormone in the lamb during puberty. Endocrinology. 1979;105(4):896-904. http://doi.org/10.1210/endo-105-4-896. PMid:477603.

Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett. 2006;401(3):225-30. http://doi.org/10.1016/j.neulet.2006.03.039. PMid:16621281.

Frisch RE. Fatness, menarche, and female fertility. Perspect Biol Med. 1985;28(4):611-33. http://doi.org/10.1353/pbm.1985.0010. PMid:4034365.

Garcia MR, Amstalden M, Williams SW, Stanko RL, Morrison CD, Keisler DH, Nizielski SE, Williams GL. Serum leptin and its adipose gene expression during pubertal development, the estrous cycle, and different seasons in cattle. J Anim Sci. 2002;80(8):2158-67. http://doi.org/10.2527/2002.8082158x. PMid:12211386.

Garza V, West SM, Cardoso RC. Review: gestational and postnatal nutritional effects on the neuroendocrine control of puberty and subsequent reproductive performance in heifers. Animal. 2023;17(Suppl 1):100782. http://doi.org/10.1016/j.animal.2023.100782. PMid: 37567667.

Goodman RL, Coolen LM, Lehman MN. A role for neurokinin B in pulsatile GnRH secretion in the ewe. Neuroendocrinology. 2014;99(1):18-32. http://doi.org/10.1159/000355285. PMid:24008670.

Goodman RL, Hileman SM, Nestor CC, Porter KL, Connors JM, Hardy SL, Millar RP, Cernea M, Coolen LM, Lehman MN. Kisspeptin, neurokinin B, and dynorphin act in the arcuate nucleus to control activity of the GnRH pulse generator in ewes. Endocrinology. 2013;154(11):4259-69. http://doi.org/10.1210/en.2013-1331. PMid:23959940.

Goodman RL, Karsch FJ. The hypothalamic pulse generator: a key determinant of reproductive cycles in sheep. In: Follett BK, Follett DE, editors. Biological clocks in seasonal reproductive cycles. Vol. 32. Bristol: John Wright & Sons; 1981. p. 223-36.

Goodman, R.L., Ohkura, S., Okamura, H., Coolen, L.M., Lehman, M. KNDy hypothesis for generation of GnRH pulses: evidence from sheep and goats. In: Herbison AE, Plant TM, editors. The GnRH neuron and its control. Hoboken: Wiley; 2018. p. 289-324. http://doi.org/10.1002/9781119233275.ch12.

Gorski JN, Dunn-Meynell AA, Hartman TG, Levin BE. Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol Regul Integr Comp Physiol. 2006;291(3):R768-78. http://doi.org/10.1152/ajpregu.00138.2006. PMid:16614055.

Grachev P, Porter K, Coolen L, McCosh R, Connors J, Hileman S, Lehman M, Goodman R. Surge‐Like Luteinising Hormone Secretion Induced by Retrochiasmatic Area NK 3R Activation is Mediated Primarily by Arcuate Kisspeptin Neurones in the Ewe. J Neuroendocrinol. 2016;28(6):28. http://doi.org/10.1111/jne.12393. PMid:27059932.

Guggeri D, Meikle A, Carriquiry M, Montossi F, De Barbieri I, Vinoles C. Effect of different management systems on growth, endocrine parameters and puberty in Hereford female calves grazing Campos grassland. Livest Sci. 2014;167:455-62. http://doi.org/10.1016/j.livsci.2014.06.026.

Guzmán A, Hernandez-Coronado CG, Rosales-Torres AM, Hernandez-Medrano JH. Leptin regulates neuropeptides associated with food intake and GnRH secretion. Ann Endocrinol (Paris). 2019;80(1):38-46. http://doi.org/10.1016/j.ando.2018.07.012. PMid:30243474.

Herbison AE. The gonadotropin-releasing hormone pulse generator. Endocrinology. 2018;159(11):3723-36. http://doi.org/10.1210/en.2018-00653. PMid:30272161.

Hill JW, Elmquist JK, Elias CF. Hypothalamic pathways linking energy balance and reproduction. Am J Physiol Endocrinol Metab. 2008;294(5):E827-32. http://doi.org/10.1152/ajpendo.00670.2007. PMid:18285524.

Hughes H. Raised replacement heifers: some economic considerations. Vet Clin North Am Food Anim Pract. 2013;29(3):643-52. http://doi.org/10.1016/j.cvfa.2013.07.013. PMid:24182440.

Ireland JL, Scheetz D, Jimenez-Krassel F, Themmen AP, Ward F, Lonergan P, Smith GW, Perez GI, Evans AC, Ireland JJ. Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol Reprod. 2008;79(6):1219-25. http://doi.org/10.1095/biolreprod.108.071670. PMid:18768912.

Kinder J, Bergfeld E, Wehrman M, Peters K, Kojima FN. Endocrine basis for puberty in heifers and ewes. J Reprod Fertil. 1995;49:393-407. PMid:7623330.

Kinder JE, Day ML, Kittok RJ. Endocrine regulation of puberty in cows and ewes. J Reprod Fertil Suppl. 1987;34:167-86. PMid:3305916.

Knobil E. The neuroendocrine control of the menstrual cycle. In: Greep RO, editor. Proceedings of the 1979 Laurentian Hormone Conference; 1980; USA. USA: Elsevier; 1980. vol. 36, p. 53-88. http://doi.org/10.1016/B978-0-12-571136-4.50008-5.

Lehman MN, Coolen LM, Goodman RL. Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology. 2010a;151(8):3479-89. http://doi.org/10.1210/en.2010-0022. PMid:20501670.

Lehman MN, Merkley CM, Coolen LM, Goodman RL. Anatomy of the kisspeptin neural network in mammals. Brain Res. 2010b;1364:90-102. http://doi.org/10.1016/j.brainres.2010.09.020. PMid:20858464.

Lesmeister J, Burfening P, Blackwell R. Date of first calving in beef cows and subsequent calf production. J Anim Sci. 1973;36(1):1-6. http://doi.org/10.2527/jas1973.3611.

Maia TS, Guimaraes HR, Garza V, Pohler KG, Cardoso RC, Williams GL. Early juvenile but not mid to late prenatal nutrition controls puberty in heifers but neither impact adult reproductive function. Biol Reprod. 2022;107(4):1035-45. http://doi.org/10.1093/biolre/ioac123. PMid:35703941.

Mossa F, Carter F, Walsh SW, Kenny DA, Smith GW, Ireland JL, Hildebrandt TB, Lonergan P, Ireland JJ, Evans AC. Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biol Reprod. 2013;88(4):92. PMid:23426432.

Nepomuceno DD, Pires AV, Ferraz MVC, Biehl MV, Goncalves JRS, Moreira EM, Day ML. Effect of pre-partum dam supplementation, creep-feeding and post-weaning feedlot on age at puberty in Nellore heifers. Livest Sci. 2017;195:58-62. http://doi.org/10.1016/j.livsci.2016.11.008.

Noya A, Casasús I, Ferrer J, Sanz A. Effects of developmental programming caused by maternal nutrient intake on postnatal performance of beef heifers and their calves. Animals (Basel). 2019;9(12):1072. http://doi.org/10.3390/ani9121072. PMid:31816876.

Quennell JH, Mulligan AC, Tups A, Liu X, Phipps SJ, Kemp CJ, Herbison AE, Grattan DR, Anderson GM. Leptin indirectly regulates gonadotropin-releasing hormone neuronal function. Endocrinology. 2009;150(6):2805-12. http://doi.org/10.1210/en.2008-1693. PMid:19179437.

Redmond JS, Macedo GG, Velez IC, Caraty A, Williams G, Amstalden M. Kisspeptin activates the hypothalamic–adenohypophyseal–gonadal axis in prepubertal ewe lambs. Reproduction. 2011;141(4):541-8. http://doi.org/10.1530/REP-10-0467. PMid:21273366.

Reis MM, Cooke RF, Cappellozza BI, Marques RS, Guarnieri TA Fo, Rodrigues MC, Bradley JS, Mueller CJ, Keisler DH, Johnson SE, Bohnert DW. Creep-feeding to stimulate metabolic imprinting in nursing beef heifers: impacts on heifer growth, reproductive and physiological variables. Animal. 2015;9(9):1500-8. http://doi.org/10.1017/S1751731115000828. PMid:25990965.

Ryan KD, Foster DL. Neuroendocrine mechanisms involved in onset of puberty in the female: concepts derived from the lamb. Fed Proc. 1980;39(7):2372-7. PMid:7189478.

Schillo KK, Dierschke DJ, Hauser ER. Regulation of luteinizing hormone secretion in prepubertal heifers: increased threshold to negative feedback action of estradiol. J Anim Sci. 1982;54(2):325-36. http://doi.org/10.2527/jas1982.542325x. PMid:7076594.

Seeley RJ, Drazen DL, Clegg DJ. The critical role of the melanocortin system in the control of energy balance. Annu Rev Nutr. 2004;24(1):133-49. http://doi.org/10.1146/annurev.nutr.24.012003.132428. PMid:15189116.

Sisk CL, Foster DL. The neural basis of puberty and adolescence. Nat Neurosci. 2004;7(10):1040-7. http://doi.org/10.1038/nn1326. PMid:15452575.

Wang J, Wu Z, Li D, Li N, Dindot SV, Satterfield MC, Bazer FW, Wu G. Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal. 2012;17(2):282-301. http://doi.org/10.1089/ars.2011.4381. PMid:22044276.

Weller MMDCA, Fortes MRS, Marcondes MI, Rotta PP, Gionbeli TRS, Valadares SC Fo, Campos MM, Silva FF, Silva W, Moore S, Guimarães SEF. Effect of maternal nutrition and days of gestation on pituitary gland and gonadal gene expression in cattle. J Dairy Sci. 2016;99(4):3056-71. http://doi.org/10.3168/jds.2015-9673. PMid:26874426.

Williams G, Amstalden M, Garcia M, Stanko R, Nizielski S, Morrison C, Keisler D. Leptin and its role in the central regulation of reproduction in cattle. Domest Anim Endocrinol. 2002;23(1-2):339-49. http://doi.org/10.1016/S0739-7240(02)00169-8. PMid:12142250.

Williams, G.L., Alves, B.R., Cardoso, R.C. Female puberty: nutrition and endocrinology. In: Skinner M, editor. Encyclopedia of reproduction. Vol. 2. New York: Encyclopedia of Reproduction; 2018. p. 238-44.

Zhang F, Chen Y, Heiman M, DiMarchi R. Leptin: structure, function and biology. Vitam Horm. 2005;71:345-72. http://doi.org/10.1016/S0083-6729(05)71012-8. PMid:16112274.

Zieba DA, Amstalden M, Morton S, Maciel MN, Keisler DH, Williams GL. Regulatory roles of leptin at the hypothalamic-hypophyseal axis before and after sexual maturation in cattle. Biol Reprod. 2004;71(3):804-12. http://doi.org/10.1095/biolreprod.104.028548. PMid:15128593.

Zieba DA, Biernat W, Barc J. Roles of leptin and resistin in metabolism, reproduction, and leptin resistance. Domest Anim Endocrinol. 2020;73:106472. http://doi.org/10.1016/j.domaniend.2020.106472. PMid:32265081.
 


Submitted date:
04/12/2024

Accepted date:
05/29/2024

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