Review Articles

Stress and Female Reproductive System: Disruption of Corticotropin-Releasing Hormone/Opiate Balance by Sympathetic Nerve Traffic

Abstract

Nowadays stress is an integral part of everyday living and the physiological and behavioral consequences of exposure to stressful situations have been extensively studied for decades. The stress response is a necessary mechanism but disrupts homeostatic process and it is sub served by a complex system located in both the central nervous system (CNS) and the periphery. Stressor-induced activation of the hypothalamus–pituitary–adrenal (HPA) axis and the sympathetic nervous system (SNS) results in a series of neural and endocrine adaptations known as the "stress response" or "stress cascade." The stress cascade is responsible for allowing the body to make the necessary physiological and metabolic changes required to cope with the demands of a homeostatic challenge. Normal activation of the HPA axis is essential for reproduction, growth, metabolic homeostasis, and responses to stress and they are critical for adapting to changes in the external environment. The regulation of gonadal function in men and women is under the control of the HPA. This regulation is complex and sex steroids are important regulators of GnRH and gonadotropin release through classical feedback mechanisms in the hypothalamus and the pituitary. The present overview focuses on the neuroendocrine infrastructure of the adaptive response to stress and its effects on the female reproductive system. 

Charmandari E, Tsigos C, Chrousos G. Endocrinology of stress response. Annual Review of Physiology 2005; 67: 259-84.

Makino S, Hashimoto K, Gold PW. Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress. Pharmacol Biochem Behav. 2002; 73: 147-58.

Benarroch EE. Basic Neurosciences with Clinical Applications. Mayo Foundation for Medical Education and research. United States of America, Chap: Central control of homeostasis and adaptation, 2006: 761-9.

Chrousos GP, Gold PW. The concepts of stress system disorders: overview of behavioral and physical homeostasis. J Am Med Assoc.1992; 267: 1244–52.

Miller DB, O'Callaghan JP. Neuroendocrine aspects of the response to stress. Metabolism 2002; 51: 5-10.

Tsigos C, Kyrou I, Chrousos GP. Stress, endocrine manifestations, and diseases. In: Cooper CL. (ed.) Handbook of Stress, Medicine, and Health. 2nd Edition. Boca Raton FL: CRC Press2005:101 – 31.

Charmandari E, Kino T, Souvatzoglou E, Chrousos GP. Pediatric stress: hormonal mediators and human development. Horm Res 2003; 59: 161-79.

Lehnert H, Schulz C, Dieterich K. Physiological and neurochemical aspects of corticotropin-releasing factor actions in the brain: the role of the locus coeruleus, Neurochem Res 1998; 23: 1039–52.

Swaab DF. The human hypothalamus. Basic and clinical aspects. Part I: Nuclei of the hypothalamus. In: Aminoff MJ, Boller F, Swaab DF, Editors, Handbook of Clinical Neurology. Elsevier, Amsterdam 2003; 79: 476.

Chrousos GP. Stressors, stress, and neuroendocrine integration of the adaptive response. The 1997 Hans Selye Memorial Lecture. Ann NY Acad Sc 1998;851: 311–35.

Shibasaki T, Imaki T, Hotta M, Ling N, Demura H. Psychological stress increases arousal through brain corticotropin-releasing hormone without significant increase in adrenocorticotropin and catecholamine secretion. Brain Res 1993;618: 71–5.

Habib KE, Weld KP, Rice KC, Pushkas J, Champoux M, Listwak S, et al. Oral administration of a corticotropin-releasing hormone receptor antagonist significantly attenuates behavioral, neuroendocrine, and autonomic responses to stress in primates. Proc Natl Acad Sci USA 2000; 97: 6079– 84.

Luque JM, de Blas MR, Segovia S, Guillamón A. Sexual dimorphism of the dopamine-beta-hydroxylase-immunoreactive neurons in the rat locus ceruleus. Brain Res Dev Brain Res 1992;67:211–5.

Pinos H, Collado P, Rodríguez-Zafra M, Rodríguez C, Segovia S, Guillamón A. The development of sex differences in the locus coeruleus of the rat. Brain Res Bull 2001;56:73–8.

Ter Horst JG, Wichmann R, Gerrits M, Westenbroek C, Lin Y. Sex differences in stress responses: Focus on ovarian hormones. Physiology & Behavior 2009; 97: 239-49.

Malyala A.,Kelly J.M. Rønnekleiv O.K. Estrogen modulation of hypothalamic neurons: Activation of multiple signaling pathways and gene expression changes. Steroids 2005; 70: 397-406.

Chen MD, O’Byrne KT, Chiappini SE, Hotchkiss J, Knobil E. Hypoglycemic 'stress' and gonadotropin-releasing hormone pulse generator activity in the rhesus monkey: role of the ovary. Neuroendocrinology 1992; 56: 666-73.

Rabine DS, Johnson EO, Liapi C, Chrousos GP. Glucocorticoids inhibit estradiol mediated uterine growth: possible role of the uterine estradiol receptor. Biol Reprod 1990; 42: 74-80.

Sakakura N, Takebe K, Nakagawa S. Inhibition of luteinizing hormone secretion induced by synthetic LRH by long-term treatment with glucocorticoids in human subgects. J Clin Endocrinol Metab 1975; 40: 774-9.

Mastorakos G, Scopa CD, Kao LC, Vryonidou A, Friedman TC, Kattis D, et al. Presence of immunoreactive corticotropin releasing hormone in human endometrium. J Clin Endocronol Metab 1996; 81: 1046-50.

Grammatopoulos D, Chrousos GP. Structural and signaling diversity of corticotropin-releasing hormone (CRH) and related peptides and their receptors: potential clinical applications of CRH receptor antagonists. Trends Endocrinol Metab 2002;13: 436-44.

Ghizzoni L, Mastorakos G, vottero A, Barreca A, Furlini M, Cesarone A,et al. Corticotropin- releasing- hormone CRH inhibits steroid biosynthesis by cultured human granulosa-lutein a CRH and inteleukin 1 receptor mediated fashion. Endocrinology 1997; 138: 4806-11.

Bromberger JT, Matthews KA, Kuller LH, Wing RR, Meilaln EN, Plantinga P. Prospective study of the determinants of age at menopause. Am J Epidemiol 1997; 145: 124-33.

Barraclougii CA, Sawyer CH. Inhibition of the release of pituitary ovulation hormone in the rat by morphine. Endocrinology 1955; 57: 329-337.

Morgan WP. Affective beneficence of vigorous physical activity. Med Sci Sports Exerc 1985;17: 94–100.

Diez- Guerra FJ, Augood S, Emson PC, Dyer R G. Morphine inhibits electrically stimulated noradrenaline release from slices of rat medial preoptic area. Neuroendocrinology 1986; 43: 89-91.

Chean EC, Brzyski RG. Exercise and reproductive dysfunction. Fertil-Stril 1999; 71:1-6.

Angelopoulos TS, Deny BS, Weikart C, Dasilvas SG, Mickael TJ, Robertson RJ. Endogenous opioids may modulate catecholamine secretion during high intensity exercise. Eur J Appl Physiol Occup Physiol 1995; 70: 195-9.

Naryzhnaia NV, Maslov LN, Revinskaia IuG, Lishmanov IuB. Interrelations between sympathetic adrenal and opioids systems regulatory mechanism determining cardiac resistance to stress damage. USP Fiziol Nauk 2001; 32 :73-81.

Chatterton RT. The role of stress in female reproduction:animal and human considerations.Int J Fertil 1990; 35: 8-13.

Sabban EL, Kvetnansky R. Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events. Trends Neurosci 2001; 24: 91–98.

Grossman A,Sutton JR. Endorphins: What are they?How are they measured? What is their role in exercise.Med-Sci-Sports-Exerc1985; 17: 74-81.

Magiaku MA, Mastorakos G, Webster E.,Chrousos GP. The hypothalamic-pituitary-adrenal axis and the female reprodctive system. Ann NY Acad Sci 1997; 816: 42-56.

Dobson H, Smith RF. What is stress, and how does it affect reproduction. Anim Reprod Sci 2000; 60-61: 743-52.

Nankova B, Kvetnansky R, Hiremagalur B, Sabban B, Rusnak M, Sabban EL. Immobilization stress elevates gene expression for catecholamine biosynthetic enzymes and some neuropeptides in rat sympathetic ganglia: effects of adrenocorticotropin and glucocorticoids, Endocrinology1997; 137: 5597–5604.

Valentino RJ, Van Bockstaele EJ. Opposing regulation of the locus coeruleus by corticotropin releasing factor and opioids: potential for reciprocal interactions between stress and opioid sensitivity. Psychopharmacology 2001; 158: 331-342.

Franci JA, Antunes-Rodrigues J. Effect of locus ceruleus lesion on luteinizing hormone secretion under different experimental conditions. Neuroendocrinology1985; 41(1): 44-51.

Helena CV , Franci CR, Anselmo-Franci JArain Res. Luteinizing hormone and luteinizing hormone-releasing hormone secretion is under locus coeruleus control in female rats. Brain Res 2002; 955: 245- 52.

Martins-Afférri MP, Ferreira-Silva IA, Franci CR, Anselmo-Franci JA. LHRH release depends on Locus Coeruleus noradrenergic inputs to the medial preoptic area and median eminence. Brain Res Bull 2003; 61:521-7.

Manni L, Lundeberg T, Holmäng A, Aloe L, Stener-Victorin E. Effect of electro-acupuncture on ovarian expression of alpha (1)- and beta (2)-adrenoceptors, and p75 neurotrophin receptors in rats with steroid-induced polycystic ovaries. Reprod Biol Endocrino 2005; 7, 3:21.

Stener-Victorin ES, Lundeberg T, Waldenström U, Manni L, Aloe L, Gunnarsson S, et al.Effects of electro-acupuncture on nerve growth factor and ovarian morphology in rats with experimentally induced polycystic ovaries. Biol Reprod 2000; 63:1497-503.

47. Ricu M, Paredes A, Greiner M, Ojeda SR, Lara HE. Functional development of the ovarian noradrenergic innervation 2008; 149: 50-6.

McMillen IC. Fetal growth restriction: adaptations and consequences. Reproductio 2001; 122 , 195–204.

Dorfman M, Arancibia S, Fiedler JL, Lara HE. Chronic intermittent cold stress activates ovarian sympathetic nerves and modifies ovarian follicular development in the rat. Biol Reprod 2003; 68: 2038-43.

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IssueVol 3, No 3 (September 2009) QRcode
SectionReview Articles
Keywords
Stress Hypothalamic-pituitary-adrenal (HPA) axis Corticotropin-releasing hormone (CRH) Norepinephrine (NE) Opioid system Luteinizing hormone-releasing hormone (LHRH)

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How to Cite
1.
Zafari Zangeneh F. Stress and Female Reproductive System: Disruption of Corticotropin-Releasing Hormone/Opiate Balance by Sympathetic Nerve Traffic. J Family Reprod Health. 2009;3(3):69-76.