Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T05:45:39.609Z Has data issue: false hasContentIssue false
  • English
  • Français

Estrous behavior in dairy cows: identification of underlying mechanisms and gene functions

Published online by Cambridge University Press:  26 October 2009

H. M. T. Boer ,
R. F. Veerkamp ,
B. Beerda  and
H. Woelders
H. M. T. Boer*
Affiliation:
Animal Breeding and Genomics Centre, Wageningen UR Livestock Research, 8200 AB Lelystad, The Netherlands Adaptation Physiology Group, Department of Animal Sciences, Wageningen University, 6700 AH Wageningen, The Netherlands
R. F. Veerkamp
Affiliation:
Animal Breeding and Genomics Centre, Wageningen UR Livestock Research, 8200 AB Lelystad, The Netherlands
B. Beerda
Affiliation:
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University, 6700 AH Wageningen, The Netherlands
H. Woelders
Affiliation:
Animal Breeding and Genomics Centre, Wageningen UR Livestock Research, 8200 AB Lelystad, The Netherlands
*
†E-mail: [email protected]
Get access

Abstract

Selection in dairy cattle for a higher milk yield has coincided with declined fertility. One of the factors is reduced expression of estrous behavior. Changes in systems that regulate the estrous behavior could be manifested by altered gene expression. This literature review describes the current knowledge on mechanisms and genes involved in the regulation of estrous behavior. The endocrinological regulation of the estrous cycle in dairy cows is well described. Estradiol (E2) is assumed to be the key regulator that synchronizes endocrine and behavioral events. Other pivotal hormones are, for example, progesterone, gonadotropin releasing hormone and insulin-like growth factor-1. Interactions between the latter and E2 may play a role in the unfavorable effects of milk yield-related metabolic stress on fertility in high milk-producing dairy cows. However, a clear understanding of how endocrine mechanisms are tied to estrous behavior in cows is only starting to emerge. Recent studies on gene expression and signaling pathways in rodents and other animals contribute to our understanding of genes and mechanisms involved in estrous behavior. Studies in rodents, for example, show that estrogen-induced gene expression in specific brain areas such as the hypothalamus play an important role. Through these estrogen-induced gene expressions, E2 alters the functioning of neuronal networks that underlie estrous behavior, by affecting dendritic connections between cells, receptor populations and neurotransmitter releases. To improve the understanding of complex biological networks, like estrus regulation, and to deal with the increasing amount of genomic information that becomes available, mathematical models can be helpful. Systems biology combines physiological and genomic data with mathematical modeling. Possible applications of systems biology approaches in the field of female fertility and estrous behavior are discussed.

Keywords

dairy cow, estrous behavior, physiology, genomics
Type
Full Paper
Information
animal , Volume 4 , Issue 3 , March 2010 , pp. 446 - 453
Copyright
Copyright © The Animal Consortium 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allrich, RD 1994. Endocrine and neural control of estrus in dairy cows. Journal of Dairy Science 77, 2738–2744.CrossRefGoogle ScholarPubMed
Arreguin-Arevalo, JA, Nett, TM 2006. A nongenomic action of estradiol as the mechanism underlying the acute suppression of secretion of luteinizing hormone in ovariectomized ewes. Biology of Reproduction 74, 202–208.Google Scholar
Attardi, B, Scott, R, Pfaff, D, Fink, G 2007. Facilitation or inhibition of the oestradiol-induced gonadotrophin surge in the immature female rat by progesterone: effects on pituitary responsiveness to gonadotropin-releasing hormone (GnRH), GnRH self-priming and pituitary mRNAs for the progesterone receptor A and B isoforms. Journal of Neuroendocrinology 19, 988–1000.Google Scholar
Beerda, B, Wyszynska-Koko, J, te Pas, MFW, de Wit, AAC, Veerkamp, RF 2008. Expression profiles of genes regulating dairy cow fertility: recent findings, ongoing activities and future possibilities. Animal 2, 1158–1167.CrossRefGoogle ScholarPubMed
Bertani, GR, Gladney, CD, Johnson, RK, Pomp, D 2004. Evaluation of gene expression in pigs selected for enhanced reproduction using differential display PCR: II. Anterior pituitary. Journal of Animal Science 82, 32–40.CrossRefGoogle ScholarPubMed
Blum, JJ, Reed, MC, Janovick, JA, Conn, PM 2000. A mathematical model quantifying GnRH-induced LH secretion from gonadotropes. American Journal of Physiology, Endocrinology and Metabolism 278, E263–E272.Google Scholar
Blutstein, T, Choleris, E, Jasnow, AM, Pfaff, D, Mong, J 2006. Oestradiol up-regulates glutamine synthetase mRNA and protein expression in the hypothalamus and hippocampus: implications for a role of hormonally responsive glia in amino acid neurotransmission. Journal of Neuroendocrinology 18, 692–702.Google Scholar
Burbeck, S, Jordan, KE 2006. An assessment of the role of computing in systems biology. IBM Journal of Research and Development 50, 529–543.CrossRefGoogle Scholar
Chagas, LM, Bass, JJ, Blache, D, Burke, CR, Kay, JK, Lindsay, DR, Lucy, MC, Martin, GB, Meler, S, Rhodes, FM, Roche, JR, Thatcher, WW, Webb, R 2007. New perspectives on the roles of nutrition and metabolic priorities in the subfertility of high-producing dairy cows. Journal of Dairy Science 90, 4022–4032.CrossRefGoogle ScholarPubMed
Clément, F, Monniaux, D, Stark, J, Hardy, K, Thalabard, J-C, Franks, S, Claude, D 2001. Mathematical model of FSH-induced cAMP production in ovarian follicles. American Journal of Physiology, Endocrinology and Metabolism 281, E35–E53.Google Scholar
Coe, BL, Allrich, RD 1989. Relationship between endogenous estradiol-17 beta and estrous behavior in heifers. Journal of Animal Science 67, 1546–1551.CrossRefGoogle ScholarPubMed
Cook, DL, Winters, TA, Horstman, LA, Allrich, RD 1986. Induction of estrus in ovariectomized cows and heifers: effects of estradiol benzoate and gonadotropin releasing hormone. Journal of Animal Science 63, 546–550.CrossRefGoogle ScholarPubMed
Diskin, MG, Mackey, DR, Roche, JF, Sreenan, JM 2003. Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle. Animal Reproduction Science 78, 345–370.CrossRefGoogle ScholarPubMed
Dobson, H, Walker, SL, Morris, MJ, Routly, JE, Smith, RF 2008. Why is it getting more difficult to successfully artificially inseminate dairy cows? Animal 2, 1104–1111.CrossRefGoogle ScholarPubMed
Dransfield, MBG, Nebel, RL, Pearson, RE, Warnick, LD 1998. Timing of insemination for dairy cows identified in estrus by a radiotelemetric estrus detection system. Journal of Dairy Science 81, 1874–1882.CrossRefGoogle ScholarPubMed
Esslemont, RJ, Bryant, MJ 1976. Oestrous behaviour in a herd of dairy cows. Veterinary Record 99, 472–475.CrossRefGoogle Scholar
Etgen, AM, Acosta-Martinez, M 2003. Participation of growth factor signal transduction pathways in estradiol facilitation of female reproductive behavior. Endocrinology 144, 3828–3835.Google Scholar
Etgen, AM, González-Flores, O, Todd, BJ 2006. The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors. Frontiers in Neuroendocrinology 27, 363–375.CrossRefGoogle ScholarPubMed
Fabre-Nys, C, Gelez, H 2007. Sexual behavior in ewes and other domestic ruminants. Hormones and Behavior 52, 18–25.CrossRefGoogle ScholarPubMed
Fabre-Nys, C, Martin, GB, Venier, G 1993. Analysis of the hormonal control of female sexual behavior and the preovulatory LH surge in the ewe: roles of quantity of estradiol and duration of its presence. Hormones and Behavior 27, 108–121.Google Scholar
Frohlich, J, Morgan, M, Ogawa, S, Burton, L, Pfaff, D 2002. Statistical analysis of hormonal influences on arousal measures in ovariectomized female mice. Hormones and Behavior 42, 414–423.CrossRefGoogle Scholar
Frohlich, J, Ogawa, S, Morgan, M, Burton, L, Pfaff, D 1999. Hormones, genes and the structure of sexual arousal. Behavioural Brain Research 105, 5–27.Google Scholar
Frye, CA, Rhodes, ME 2008. Infusions of 3α,5α-THP to the VTA enhance exploratory, anti-anxiety, social, and sexual behavior and increase levels of 3α,5α-THP in midbrain, hippocampus, diencephalon, and cortex of female rats. Behavioural Brain Research 187, 88–99.Google Scholar
Garey, J, Goodwillie, A, Frohlich, J, Morgan, M, Gustafsson, J-A, Smithies, O, Korach, KS, Ogawa, S, Pfaff, D 2003. Genetic contributions to generalized arousal of brain and behavior. Proceedings of the National Academy of Sciences of the United States of America 100, 11019–11022.CrossRefGoogle ScholarPubMed
Ginther, OJ, Wiltbank, MC, Fricke, PM, Gibbons, JR, Kot, K 1996. Selection of the dominant follicle in cattle. Biology of Reproduction 55, 1187–1194.CrossRefGoogle ScholarPubMed
Glidewell-Kenney, C, Hurley, LA, Pfaff, L, Weiss, J, Levine, JE, Jameson, JL 2007. Nonclassical estrogen receptor α signaling mediates negative feedback in the female mouse reproductive axis. Proceedings of the National Academy of Sciences of the United States of America 104, 8173–8177.Google Scholar
Hapgood, JP, Sadie, H, van Biljon, B, Ronacher, K 2005. Regulation of expression of mammalian gonadotrophin-releasing hormone receptor genes. Journal of Neuroendocrinology 17, 619–638.CrossRefGoogle ScholarPubMed
Heinze, K, Keener, RW, Midgley, AR 1998. A mathematical model of luteinizing hormone release from ovine pituitary cells in perifusion. American Journal of Physiology, Endocrinology and Metabolism 275, 1061–1071.CrossRefGoogle ScholarPubMed
Kelly, MJ, Rønnekleiv, OK 2009. Control of CNS neuronal excitability by estrogens via membrane-initiated signaling. Molecular and Cellular Endocrinology 308, 17–25.Google Scholar
Kow, L-M, Pfaff, D 1998. Mapping of neural and signal transduction pathways for lordosis in the search for estrogen actions on the central nervous system. Behavioural Brain Research 92, 169–180.Google Scholar
Kyle, SD, Callahan, CJ, Allrich, RD 1992. Effect of progesterone on the expression of estrus at the first postpartum ovulation in dairy cattle. Journal of Dairy Science 75, 1456–1460.Google Scholar
Laissue, P, L’Hôte, D, Serres, C, Vaiman, D 2009. Mouse models for identifying genes modulating fertility parameters. Animal 3, 55–71.Google Scholar
Lee, AW, Kyrozis, A, Chevaleyre, V, Kow, LM, Devidze, N, Zhang, Q, Etgen, AM, Pfaff, DW 2008. Estradiol modulation of phenylephrine-induced excitatory responses in ventromedial hypothalamic neurons of female rats. Proceedings of the National Academy of Sciences of the United States of America 105, 7333–7338.Google Scholar
Lee, AW, Pfaff, DW 2008. Hormone effects on specific and global brain functions. Journal of Physiological Sciences 58, 213–220.CrossRefGoogle ScholarPubMed
Lehman, MN, Ebling, FJP, Moenter, SM, Karsch, FJ 1993. Distribution of estrogen receptor-immunoreactive cells in the sheep brain. Endocrinology 133, 876–886.CrossRefGoogle ScholarPubMed
Lopez, H, Bunch, TD, Shipka, MP 2002. Estrogen concentrations in milk at estrus and ovulation in dairy cows. Animal Reproduction Science 72, 37–46.Google Scholar
Lopez, H, Satter, LD, Wiltbank, MC 2004. Relationship between level of milk production and estrous behavior of lactating dairy cows. Animal Reproduction Science 81, 209–223.CrossRefGoogle ScholarPubMed
Lovendahl, P, Chagunda, MGG 2009. Short communication: Genetic variation in estrus activity traits. Journal of Dairy Science 92, 4683–4688.Google Scholar
Lucy, MC 2001. Reproductive loss in high-producing dairy cattle: where will it end? Journal of Dairy Science 84, 1277–1293.CrossRefGoogle ScholarPubMed
Lyimo, ZC, Nielen, M, Ouweltjes, W, Kruip, TAM, van Eerdenburg, FJCM 2000. Relationship among estradiol, cortisol and intensity of estrous behavior in dairy cattle. Theriogenology 53, 1783–1795.CrossRefGoogle ScholarPubMed
Malyala, A, Pattee, P, Nagalla, SR, Kelly, MJ, Ronnekleiv, OK 2004. Suppression subtractive hybridization and microarray identification of estrogen-regulated hypothalamic genes. Neurochemical Research 29, 1189–1200.Google Scholar
Mani, SK, Allen, JMC, Rettori, V, McCann, SM, O’Malley, BW, Clark, JH 1994. Nitric oxide mediates sexual behavior in female rats. Proceedings of the National Academy of Sciences of the United States of America 91, 6468–6472.Google Scholar
Mendez, P, Wandosell, F, Garcia-Segura, LM 2006. Cross-talk between estrogen receptors and insulin-like growth factor-I receptor in the brain: cellular and molecular mechanisms. Frontiers in Neuroendocrinology 27, 391–403.CrossRefGoogle ScholarPubMed
Micevych, P, Dominguez, R 2009. Membrane estradiol signaling in the brain. Frontiers in Neuroendocrinology 30, 315–327.Google Scholar
Micevych, PE, Kuo, J, Christensen, A 2009. Physiology of membrane oestrogen receptor signalling in reproduction. Journal of Neuroendocrinology 21, 249–256.Google Scholar
Mihm, M, Baker, PJ, Ireland, JLH, Smith, GW, Coussens, PM, Evans, ACO, Ireland, JJ 2006. Molecular evidence that growth of dominant follicles involves a reduction in follicle-stimulating hormone dependence and an increase in luteinizing hormone dependence in cattle. Biology of Reproduction 74, 1051–1059.CrossRefGoogle Scholar
Molenda-Figueira, HA, Williams, CA, Griffin, AL, Rutledge, EM, Blaustein, JD, Tetel, MJ 2006. Nuclear receptors coactivators function in estrogen receptor- and progestin receptor-dependent aspects of sexual behavior in female rats. Hormones and Behavior 50, 383–392.Google Scholar
Mong, J, Easton, A, Kow, L-M, Pfaff, D 2003a. Neural, hormonal and genetic mechanisms for the activation of brain and behavior. European Journal of Pharmacology 480, 229–231.CrossRefGoogle ScholarPubMed
Mong, JA, Devidze, N, Goodwillie, A, Pfaff, DW 2003b. Reduction of lipocalin-type prostaglandin D synthase in the preoptic area of female mice mimics estradiol effects on arousal and sex behavior. Proceedings of the National Academy of Sciences of the United States of America 100, 15206–15211.CrossRefGoogle ScholarPubMed
Mong, JA, Pfaff, DW 2003c. Hormonal and genetic influences underlying arousal as it drives sex and aggression in animal and human brains. Neurobiology of Aging 24, S83–S88.CrossRefGoogle ScholarPubMed
Mong, JA, Devidze, N, Frail, DE, O’Connor, LT, Samuel, M, Choleris, E, Ogawa, S, Pfaff, DW 2003d. Estradiol differentially regulates lipocalin-type prostaglandin D synthase transcript levels in the rodent brain: Evidence from high-density oligonucleotide arrays and in situ hybridization. Proceedings of the National Academy of Sciences of the United States of America 100, 318–323.Google Scholar
Pfaff, D 2005. Hormone-driven mechanisms in the central nervous system facilitate the analysis of mammalian behaviours. Journal of Endocrinology 184, 447–453.Google Scholar
Pfaff, D, Kow, L-M, Loose, MD, Flanagan-Cato, LM 2008. Reverse engineering the lordosis behavior circuit. Hormones and Behavior 54, 347–354.CrossRefGoogle ScholarPubMed
Potter, LK, Tobin, FL 2007. Perspectives on mathematical modeling for receptor-mediated processes. Journal of Receptors and Signal Transduction 27, 1–25.CrossRefGoogle ScholarPubMed
Pryce, JE, Royal, M, Garnsworthy, PC, Mao, IL 2004. Fertility in the high-producing dairy cow. Livestock Production Science 86, 125–135.Google Scholar
Pryce, JE, Veerkamp, RF 2001. The incorporation of fertility indices in genetic improvement programmes. BSAS occasional publication 26, 237–249.Google Scholar
Reinecke, I, Deuflhard, P 2007. A complex mathematical model of the human menstrual cycle. Journal of Theoretical Biology 247, 303–330.CrossRefGoogle ScholarPubMed
Richter, TA, Robinson, JE, Lozano, JM, Evans, NP 2005. Progesterone can block the preovulatory gonadotropin-releasing hormone/luteinizing hormone surge in the ewe by a direct inhibitory action on oestradiol-responsive cells within the hypothalamus. Journal of Endocrinology 17, 161–169.Google ScholarPubMed
Roche, JF 2006. The effect of nutritional management of the dairy cow on reproductive efficiency. Animal Reproduction Science 96, 282–296.Google Scholar
Roelofs, JB, Bouwman, EG, Dieleman, SJ, Van Eerdenburg, FJCM, Kaal-Lansbergen, LMTE, Soede, NM, Kemp, B 2004. Influence of repeated rectal ultrasound examinations on hormone profiles and behaviour around oestrus and ovulation in dairy cattle. Theriogenology 62, 1337–1352.CrossRefGoogle ScholarPubMed
Roelofs, JB, van Eerdenburg, FJCM, Soede, NM, Kemp, B 2005a. Pedometer readings for estrous detection and as predictor for time of ovulation in dairy cattle. Theriogenology 64, 1690–1703.Google Scholar
Roelofs, JB, van Eerdenburg, FJCM, Soede, NM, Kemp, B 2005b. Various behavioral signs of oestrus and their relationship with time of ovulation in dairy cattle. Theriogenology 63, 1366–1377.CrossRefGoogle ScholarPubMed
Royal, M, Mann, GE, Flint, APF 2000. Strategies for reversing the trend towards subfertility in dairy cattle. The Veterinary Journal 160, 53–60.CrossRefGoogle ScholarPubMed
Saïd, SB, Lomet, D, Chesneau, D, Lardic, L, Canepa, S, Guillaume, D, Briant, C, Fabre-Nys, C, Caraty, A 2007. Differential estradiol requirement for the induction of estrus behavior and the luteinizing hormone surge in two breeds of sheep. Biology of Reproduction 76, 673–680.Google Scholar
Schutz, MM, Pajor, EA 2001. Genetic control of dairy cattle behavior. Journal of Dairy Science 84, E31–E38.CrossRefGoogle Scholar
Sica, M, Martini, M, Viglietti-Panzica, C, Panzica, GC 2009. Estrous cycle influences the expression of neuronal nitric oxide synthase in the hypothalamus and limbic system of female mice. BMC Neuroscience 10, 78.Google Scholar
Skinner, DC, Harris, TG, Evans, NP 2000. Duration and amplitude of the luteal phase progesterone increment times the estradiol-induced luteinizing hormone surge in ewes. Biology of Reproduction 63, 1135–1142.CrossRefGoogle ScholarPubMed
Smith, MJ, Jennes, L 2001. Neural signals that regulate GnRH neurones directly during the oestrous cycle. Reproduction 122, 1–10.CrossRefGoogle ScholarPubMed
Soboleva, TK, Pleasants, AB, van Rens, BTTM, Van der Lende, T, Peterson, AJ 2004. A dynamic model for ovulation rate reveals an effect of the estrogen receptor genotype on ovarian follicular development in the pig. Journal of Animal Science 82, 2329–2332.Google Scholar
Stormshak, F, Bishop, CV 2008. Estrogen and progesterone signaling: genomic and nongenomic actions in domestic ruminants. Journal of Animal Science 86, 299–315.CrossRefGoogle ScholarPubMed
Uphouse, L 2000. Female gonadal hormones, serotonin, and sexual receptivity. Brain Research Reviews 33, 242–257.Google Scholar
Uphouse, L, Hiegel, C, Perez, E, Guptarak, J 2007. Serotonin receptor involvement in effects of restraint on female rat lordosis behavior. Pharmacology Biochemistry and Behavior 86, 631–636.CrossRefGoogle ScholarPubMed
Van Eerdenburg, FJCM, Karthaus, D, Taverne, MAM, Merics, I, Szenci, O 2002. The relationship between estrous behavioral score and time of ovulation in dairy cattle. Journal of Dairy Science 85, 1150–1156.CrossRefGoogle ScholarPubMed
Van Eerdenburg, FJCM, Loeffler, HSH, Van Vliet, JH 1996. Detection of oestrus in dairy cows: A new approach to an old problem. Veterinary Quarterly 18, 52–54.CrossRefGoogle Scholar
Vasudevan, N, Pfaff, D 2008. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Frontiers in Neuroendocrinology 29, 238–257.CrossRefGoogle ScholarPubMed
Veerkamp, RF, Beerda, B, van der Lende, T 2003. Effects of genetic selection for milk yield on energy balance, levels of hormones, and metabolites in lactating cattle, and possible links to reduced fertility. Livestock Production Science 83, 257–275.Google Scholar
Velazquez, MA, Spicer, LJ, Wathes, DC 2008. The role of endocrine insulin-like growth factor-I (IGF-I) in female bovine reproduction. Domestic Animal Endocrinology 35, 325–342.Google Scholar
Walf, AA, Frye, CA 2006. A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology 31, 1097–1111.Google Scholar
Walf, AA, Frye, CA 2008. Rapid and estrogen receptor beta mediated actions in the hippocampus mediate some functional effects of estrogen. Steroids 73, 997–1007.Google Scholar
Walker, SL, Smith, RF, Jones, DN, Routly, JE, Dobson, H 2008. Chronic stress, hormone profiles and estrus intensity in dairy cattle. Hormones and Behavior 53, 493–501.CrossRefGoogle ScholarPubMed
Washington, TM, Blum, JJ, Reed, MC, Conn, PM 2004. A mathematical model for LH release in response to continuous and pulsatile exposure of gonadotrophs to GnRH. Theoretical Biology and Medical Modelling 1, 9–25.Google Scholar
Weiss, JM, Polack, S, Treeck, O, Diedrich, K, Ortmann, O 2006. Regulation of GnRH1 receptor gene expression by the GnRH agonist triptorelin, estradiol, and progesterone in the gonadotroph-derived cell line αT3-1. Endocrine 30, 139–144.Google Scholar
Wiltbank, M, Lopez, H, Sartori, R, Sangsritavong, S, Gümen, A 2006. Changes in reproductive physiology of lactating dairy cows due to elevated steroid metabolism. Theriogenology 65, 17–29.CrossRefGoogle ScholarPubMed
Zalányi, S 2001. Progesterone and ovulation. European Journal of Obstetrics & Gynecology and Reproductive Biology 98, 152–159.Google Scholar
Zhou, J, Zhang, H, Cohen, RS, Pandey, SC 2005. Effects of estrogen treatment on expression of brain-derived neurotrophic factor and cAMP response element-binding protein expression and phosphorylation in rat amigdaloid and hippocampal structures. Neuroendocrinology 81, 294–310.Google Scholar
Zielak, AE, Forde, N, Park, SDE, Doohan, F, Coussens, PM, Smith, GW, Ireland, JJ, Lonergan, P, Evans, ACO 2007. Identification of novel genes associated with dominant follicle development in cattle. Reproduction, Fertility and Development 19, 967–975.Google Scholar