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Chapter 3 - Neuroendocrinology of Female Reproduction

Published online by Cambridge University Press:  24 December 2018

Michael Wilkinson
Affiliation:
Dalhousie University, Nova Scotia
S. Ali Imran
Affiliation:
Dalhousie University, Nova Scotia
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Clinical Neuroendocrinology
An Introduction
, pp. 29 - 52
Publisher: Cambridge University Press
Print publication year: 2019

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References

Further Reading

Besser, G M & Thorner, M O. (2002). Comprehensive Clinical Endocrinology, 3rd Edition (St. Louis, MO: Mosby).Google Scholar
Boehm, U, Bouloux, P-M, Dattani, M T et al. (2015). European Consensus Statement on congenital hypogonadotropic hypogonadism – pathogenesis, diagnosis and treatment. Nat Revs Endocr 11, 547564.Google Scholar
Caronia, L M, Martin, C, Welt, C K et al. (2011). A genetic basis for functional hypothalamic amenorrhea. N Engl J Med 364, 215–25.CrossRefGoogle ScholarPubMed
Christian, C A & Moenter, S M. (2010). The neurobiology of preovulatory and estradiol-induced gonadotropin-releasing hormone surges. Endocr Revs 31, 544577.Google Scholar
Gordon, C M, Ackerman, K E, Berga, S L et al. (2017). Functional hypothalamic amenorrhea: An endocrine society clinical practice guideline. J Clin Endocr Metab 102, 14131439.CrossRefGoogle ScholarPubMed
Grumbach, M M. (2002). The neuroendocrinology of human puberty revisited. Horm Res 57 (Suppl 2), 214.Google Scholar
Hall, J E. (2014). Neuroendocrine control of the menstrual cycle. Yen and Jaffe’s Reproductive Endocrinology, 7th Edition; Strauss, J F & Barbieri, R L, Eds. (Philadelphia, PA: Elsevier), 141156CrossRefGoogle Scholar
Herbison, A E. (2015). Physiology of the adult gonadotropin-releasing hormone neuronal network. Knobil and Neill’s Physiology of Reproduction, 4th Edition; Plant, T M & Zeleznik, A J, Eds. (New York: Elsevier), 399467.Google Scholar
Pinilla, L, Aguilar, E, Dieguez, C, Millar, R P & Tena-Sempere, M. (2012). Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Revs 92, 12351316.CrossRefGoogle ScholarPubMed
Stamou, M I, Cox, K H & Crowley, W F Jr. (2015). Discovering genes essential to the hypothalamic regulation of human reproduction using a human disease model: Adjusting to life in the “-omics” era. Endocr Revs 36, 603621.Google Scholar
Vuong, C, Van Uum, S H M, O’Dell, L E, Lutfy, K & Friedman, T C. (2010). The effects of opioids and opioid analogs on animal and human endocrine systems. Endocr Revs 31, 98132.Google Scholar
Wierman, M E, Kiseljak-Vassiliades, K & Tobet, S. (2011). Gonadotropin-releasing hormone (GnRH) neuron migration: initiation, maintenance and cessation as critical steps to ensure normal reproductive function. Fronts Neuroendocr 32, 4352.CrossRefGoogle ScholarPubMed
Wilkinson, M & Brown, R E. (2015). An Introduction to Neuroendocrinology, 2nd Edition (Cambridge: Cambridge University Press).Google Scholar

References

Abbara, A, Jayasena, C N, Christopoulos, G et al. (2015). Efficacy of kisspeptin-54 to trigger oocyte maturation in women at high risk of ovarian hyperstimulation syndrome (OHSS) during in vitro fertilization (IVF) therapy. J Clin Endocr Metab 100, 33223331.Google Scholar
Abbara, A, Clarke, S, Islam, R et al. (2017). A second dose of kisspeptin-54 improves oocyte maturation in women at high risk of ovarian hyperstimulation syndrome: a phase 2 randomized controlled trial. Hum Reprod 32, 19151924Google Scholar
Abbara, A, Islam, R, Clarke, S A et al. (2018). Clinical parameters of ovarian hyperstimulation syndrome (OHSS) following different hormonal triggers of oocyte maturation in IVF treatment. Clin Endocr 88, 920927.Google Scholar
Abs, R, Verhelst, J, Maeyaert, J et al. (2000). Endocrine consequences of long-term intrathecal administration of opioids. J Clin Endocr Metab 85, 22152222.Google Scholar
Ahmed, M I, Duleba, A J, El Shahat, O, Ibrahim, M E & Salem, A. (2008). Naltrexone treatment in clomiphene-resistant women with polycystic ovary syndrome. Human Reprod 23, 25642569.CrossRefGoogle ScholarPubMed
Antunes, J L, Carmel, P W, Housepian, E M & Ferin, M. (1978). Luteinizing hormone-releasing hormone in human pituitary blood. J Neurosurg 49, 382386.Google Scholar
Azziz, R, Marin, C, Hoq, L, Badamgarav, E & Song, P. (2005). Health care-related economic burden of the polycystic ovary syndrome during the reproductive life span. J Clin Endocr Metab 90, 46504658.Google Scholar
Balasubramanian, R, Dwyer, A, Seminara, S B, Pitteloud, N, Kaiser, U B & Crowley, W F Jr. (2010). Human GnRH deficiency: a unique disease model to unravel the ontogeny of GnRH neurons. Neuroendocr 92, 8199.Google Scholar
Barbieri, R L. (2014). The endocrinology of the menstrual cycle. Methods Mol Biol 1154, 145169.CrossRefGoogle ScholarPubMed
Belchetz, P E, Plant, T M, Nakai, Y, Keogh, E J & Knobil, E. (1978). Hypophysial responses to continuous and intermittent delivery of hypothalamic gonadotropin-releasing hormone. Science 202, 631633.Google Scholar
Besser, G M & Thorner, M O. (2002). Comprehensive Clinical Endocrinology, 3rd Edition (St. Louis, MO: Mosby).Google Scholar
Bianco, S D & Kaiser, U B. (2009). The genetic and molecular basis of idiopathic hypogonadotropic hypogonadism. Nat Rev Endocr 5, 569576.Google Scholar
Boehm, U, Bouloux, P-M, Dattani, M T et al. (2015). European Consensus Statement on congenital hypogonadotropic hypogonadism – pathogenesis, diagnosis and treatment. Nat Revs Endocr 11, 547564.CrossRefGoogle ScholarPubMed
Boron, W F & Boulpaep, E L. (2009). Medical Physiology, 2nd Edition (Philadelphia, PA: Elsevier Saunders).Google Scholar
Borsay, B A, Skrapits, K, Herczeg, L et al. (2014). Hypophysiotropic gonadotropin-releasing hormone projections are exposed to dense plexuses of kisspeptin, neurokinin B and substance P immunoreactive fibers in the human: a study on tissues from postmenopausal women. Neuroendocr 100, 141152.Google Scholar
Boyar, R, Katz, J, Finkelstein, J W et al. (1974). Immaturity of 24-hour luteinizing hormone secretory pattern. New Engl J Med 291, 861865.CrossRefGoogle ScholarPubMed
Brennan, M J. (2013). The effect of opioid therapy on endocrine function. Am J Med 126, S12S18.Google Scholar
Brown, R E, Imran, S A, Ur, E & Wilkinson, M. (2008). KiSS-1 mRNA in adipose tissue is regulated by sex hormones and food intake. Mol Cell Endocr 281, 6472.CrossRefGoogle ScholarPubMed
Cockwell, H, Wilkinson, DA, Bouzayen, R, Imran, S A, Brown, R & Wilkinson, M. (2013). KISS1 expression in human female adipose tissue. Arch Gynecol Obstet 287, 143147.Google Scholar
Compton, W M, Jones, C M & Baldwin, G T. (2016). Relationship between nonmedical prescription-opioid use and heroin use. New Engl J Med 374, 154163.Google Scholar
Couzinet, B, Young, J, Brailly, S, Chanson, P & Schaison, G. (1995). Even after priming with ovarian steroids or pulsatile gonadotrophin releasing hormone administration, naltrexone is unable to induce ovulation in women with functional hypothalamic amenorrhea. J Clin Endocr Metab 80, 21022107.Google ScholarPubMed
Daniell, H W. (2008). Opioid endocrinopathy in women consuming prescribed sustained-action opioids for control of nonmalignant pain. J Pain 9, 2836.CrossRefGoogle ScholarPubMed
de Kretser, D M & O’Donnell, L. (2013). Endocrinology of the Male Reproductive System. www.endotext.orgGoogle Scholar
Delvigne, A & Rozenberg, S. (2002). Epidemiology and prevention of ovarian hyperstimulation syndrome (OHSS): a review. Hum Reprod Update 8, 559577.Google Scholar
Dhillo, W S, Chaudhri, O B, Thompson, E L et al. (2007). Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocr Metab 92, 39583966.Google Scholar
Dudas, B & Merchenthaler, I. (2001). Catecholaminergic axons innervate LH-releasing hormone immunoreactive neurons of the human diencephalon. J Clin Endocr Metab 86, 56205626.Google Scholar
Dudas, B & Merchenthaler, I. (2004). Close anatomical associations between β-endorphin and luteinizing hormone-releasing hormone neuronal systems in the human diencephalon. Neurosci 124, 221229.CrossRefGoogle ScholarPubMed
Dudas, B & Merchenthaler, I. (2006). Three-dimensional representation of the neurotransmitter systems of the human hypothalamus: inputs of the gonadotrophin hormone-releasing hormone neuronal system. J Neuroendocr 18, 7995.Google Scholar
Engel, J B & Schally, A V. (2007). Drug Insight: clinical use of agonists and antagonists of luteinizing-hormone-releasing hormone. Nat Clin Practice Endocr Metab 3, 157167.Google Scholar
Eyvazzadeh, A D, Pennington, K P, Pop-Busui, R, Sowers, M, Zubieta, J-K & Smith, Y R. (2009). The role of the endogenous opioid system in polycystic ovary syndrome. Fertil Steril 92, 112.Google Scholar
Ferin, M, Wehrenberg, W B, Lam, N Y, Alston, E J & Vande Wiele, R L. (1982). Effects and site of action of morphine on gonadotropin secretion in the female rhesus monkey. Endocr 111, 16521656.Google Scholar
Filicori, M, Santoro, N, Merriam, G R & Crowley, W F Jr. (1986). Characterization of the physiological pattern of episodic gonadotropin secretion throughout the human menstrual cycle. J Clin Endocr Metab 62, 11361144.Google Scholar
Fraser, H M. (1993). GnRH analogues for contraception. Brit Med Bull 49, 6272.Google Scholar
Fruzzetti, F, Bersi, C, Parrini, D, Ricci, C & Genazzani, AR. (2002). Effect of long-term naltrexone treatment on endocrine profile, clinical features, and insulin sensitivity in obese women with polycystic ovary syndrome. Fertil Steril 77, 936944.Google Scholar
Genazzani, AD, Gastaldi, M, Petraglia, F et al. (1995). Naltrexone administration modulates the neuroendocrine control of luteinizing hormone secretion in hypothalamic amenorrhoea. Human Reprod 10, 28682871.Google Scholar
Giusti, M, Delitala, G, Marini, G et al. (1992). The effect of a met-enkephalin analogue on growth hormone, prolactin, gonadotropins, cortisol and thyroid stimulating hormone in healthy elderly men. Acta Endocr 127, 205209.Google Scholar
Graves, G R, Kennedy, T G, Weick, R F & Casper, R F. (1993). The effect of nalmefene on pulsatile secretion of luteinizing hormone and prolactin in men. Hum Reprod 8, 15981603.Google Scholar
Grumbach, M M. (2002). The neuroendocrinology of human puberty revisited. Horm Res 57 (Suppl2), 214.Google Scholar
Hall, J E. (2014). Neuroendocrine control of the menstrual cycle. Yen and Jaffe’s Reproductive Endocrinology, 7th Edition. Strauss, J F & Barbieri, R L, Eds. (Philadelphia, PA: Elsevier), 141156.Google Scholar
Harihar, S, Pounds, K M, Iwakuma, T, Seidah, N G & Welch, D R. (2015). Furin is the major proprotein convertase required for KISS1-to-kisspeptin processing. PLoS One 9, e84958.CrossRefGoogle Scholar
Herbison, A E. (2015). Physiology of the adult gonadotropin-releasing hormone neuronal network. Knobil and Neill’s Physiology of Reproduction, 4th Edition. Plant, T M & Zeleznik, A J, Eds. (New York: Elsevier), 399467.Google Scholar
Herbison, A E. (2016). Control of puberty onset and fertility by gonadotropin-releasing hormone neurons. Nat Rev Endocr 12, 452466.Google Scholar
Hrabovszky, E, Ciofi, P, Vida, B et al. (2010). The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin-releasing hormone and neurokinin B neurons. Europ J Neurosci 31, 19841998.Google Scholar
Hrabovszky, E, Molnár, C S, Nagy, R et al. (2012). Glutamatergic and GABAergic innervation of human gonadotropin-releasing hormone-I neurons. Endocr 153, 27662776.Google Scholar
Hrabovszky, E & Liposits, Z. (2013). Afferent neuronal control of type-1 gonadotropin releasing hormone neurons in the human. Fronts Endocr 4, 119.Google Scholar
Hrabovszky, E. (2014). Neuroanatomy of the human hypothalamic kisspeptin system. Neuroendocr 99, 3348.Google Scholar
Jayasena, C N, Nijher, G M K, Chaudhri, O B et al. (2009). Subcutaneous injection of kisspeptin-54 acutely stimulates gonadotropin secretion in women with hypothalamic amenorrhea, but chronic administration causes tachyphylaxis. J Clin Endocr Metab 94, 43154323.Google Scholar
Jayasena, C N, Comninos, A N, Veldhuis, J D et al. (2013). A single injection of kisspeptin-54 temporarily increases luteinizing hormone pulsatility in healthy women. Clin Endocr 79, 558563.Google Scholar
Jayasena, C N, Abbara, A, Veldhuis, J D et al. (2014). Increasing LH pulsatility in women with hypothalamic amenorrhoea using intravenous infusion of kisspeptin-54. J Clin Endocr Metab 99, E953E961.Google Scholar
Jayasena, C N, Abbara, A, Comninos, A N et al. (2014a). Kisspeptin-54 triggers egg maturation in women undergoing in vitro fertilization. J Clin Invest 124, 36673677.Google Scholar
Jayasena, C N, Abbara, A, Narayanaswamy, S et al. (2015). Direct comparison of the effects of intravenous kisspeptin-10, kisspeptin-54 and GnRH on gonadotrophin secretion in healthy men. Hum Reprod 30, 19341941.Google Scholar
Kapen, S, Boyar, R M, Finkelstein, J W, Hellman, L & Weitzman, E D. (1974). Effect of sleep-wake cycle reversal on luteinizing hormone secretory pattern in puberty. J Clin Endocr Metab 39, 293299.Google Scholar
Katz, N & Mazer, N A. (2009). The impact of opioids on the endocrine system. Clin J Pain 25, 170175.CrossRefGoogle ScholarPubMed
Khoury, S A, Reame, N E, Kelch, R P & Marshall, J C. (1987). Diurnal patterns of pulsatile luteinizing hormone secretion in hypothalamic amenorrhea: reproducibility and responses to opiate blockade and an α2-adrenergic agonist. J Clin Endocr Metab 64, 755762.Google Scholar
Knight, P J, Satchell, L & Glister, C. (2012). Intra-ovarian roles of activins and inhibins. Mol Cell Endocr 359,5365.Google Scholar
Koons, A L, Rayl Greenberg, M, Cannon, R D & Beauchamp, G A. (2018). Women and the experience of pain and opioid use disorder: a literature-based commentary. Clin Therap 40, 190196.Google Scholar
Krsmanovic, L Z, Hu, L, Leung, P-K, Feng, H & Catt, K J. (2009). The hypothalamic GnRH pulse generator: multiple regulatory mechanisms. Trends Endocr Metab 20, 402408.Google Scholar
Lehman, M N, Coolen, L M & Goodman, R L. (2010). Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocr 151, 34793489.Google Scholar
Liu, J H, Patel, B & Collins, G. (2016). Central causes of amenorrhea. www.endotext.orgGoogle Scholar
McCarthy, M M. (2013). A piece in the puzzle of puberty. Nat Neurosci 16, 251253.CrossRefGoogle ScholarPubMed
Meczekalski, B, Podfigurna-Stopa, A, Warenik-szymankiewicz, A & Genazzani, A R. (2008). Functional hypothalamic amenorrhea: current view on neuroendocrine aberrations. Gynecol Endocr 24, 411.CrossRefGoogle ScholarPubMed
Messager, S, Chatzidaki, E E, Ma, D et al. (2005). Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Nat Acad Sci USA 102, 17611766.Google Scholar
Messinis, I E, Messini, C I, & Dafopoulos, K. (2014). Novel aspects of the endocrinology of the menstrual cycle. Reprod Biomed Online 28, 714722.Google Scholar
Millar, R P, Sonigo, C, Anderson, R A et al. (2017). Hypothalamic–pituitary–ovarian axis reactivation by kisspeptin-10 in hyperprolactinemic women with chronic amenorrhea. J Endocr Soc 1, 13621371.Google Scholar
Moenter, S M. (2015). Leap of faith: does serum luteinizing hormone always accurately reflect central reproductive neuroendocrine activity? Neuroendocr 102, 256266.Google Scholar
Narayanaswamy, S, Jayasena, C N, Ng, N et al. (2015). Subcutaneous infusion of kisspeptin-54 stimulates gonadotrophin release in women and the response correlates with basal oestradiol levels. Clin Endocr 84, 939945.Google Scholar
Oakley, A E, Clifton, D K & Steiner, R A. (2009). Kisspeptin signaling in the brain. Endocr Rev 30, 713743.Google Scholar
Padmanabhan, V. (2009). Polycystic ovary syndrome – “a riddle wrapped in a mystery inside an enigma”. J Clin Endocr Metab 94, 18831885.Google Scholar
Peckys, D & Landwehrmeyer, G B. (1999). Expression of mu, kappa, and delta opioid receptor messenger RNA in the human CNS: a 33P in situ hybridization study. Neurosci 88, 10931135.Google Scholar
Petraglia, F, Degli Uberti, E C, Trasforini, G et al. (1985). Dermorphin decreases plasma LH levels in human: evidence for a modulatory role of gonadal steroids. Peptides 6, 869–72.Google Scholar
Pinilla, L, Aguilar, E, Dieguez, C, Millar, R P & Tena-Sempere, M. (2012). Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Revs 92, 12351316.Google Scholar
Prague, J K & Dhillo, W S. (2015). Potential clinical use of kisspeptin. Neuroendocr 102, 238245.Google Scholar
Prague, J K, Roberts, R E, Comninos, A N et al. (2017). Neurokinin 3 receptor antagonism as a novel treatment for menopausal hot flushes: a phase 2, randomised, double-blind, placebo-controlled trial. Lancet 389, 18091820.Google Scholar
Rabin, D & McNeil, L W. (1980). Pituitary and gonadal desensitization after continuous luteinizing hormone-releasing hormone infusion in normal females. J Clin Endocr Metab 51, 873876.Google Scholar
Rance, N E. (2009). Menopause and the human hypothalamus: Evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback. Peptides 30, 111122.Google Scholar
Rasmussen, D D, Gambacciani, M, Swartz, W, Tueros, V S & Yen, S S. (1989). Pulsatile gonadotropin-releasing hormone release from the human mediobasal hypothalamus in vitro: opiate receptor-mediated suppression. Neuroendocr 49, 150156.Google Scholar
Reed, B J & Carr, B R. (2015). The normal menstrual cycle and the control of ovulation. www.endotext.orgGoogle Scholar
Reid, R L, Hoff, J D, Yen, S S & Li, C H. (1981). Effects of exogenous beta-endorphin on pituitary hormone secretion and its disappearance in normal human subjects. J Clin Endocr Metab 52, 11791184.Google Scholar
Rhodin, A, Stridsberg, M & Gord, T. (2010). Opioid endocrinopathy: a clinical problem in patients with chronic pain and long-term oral opioid treatment. Clin J Pain 26, 373380.CrossRefGoogle ScholarPubMed
Roa, J, Aguilar, E, Dieguez, C, Pinilla, L & Tena-Sempere, M. (2008). New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front Neuroendocr 29, 4869.Google Scholar
Robertson, D M. (2012). Inhibins and activins in blood: predictors of female reproductive health? Mol Cell Endocr 34, 7884.Google Scholar
Robertson, D M, Hale, G E, Jolley, D, Fraser, I S, Hughes, C L & Burger, H G. (2009). Interrelationships between ovarian and pituitary hormones in ovulatory menstrual cycles across reproductive age. J Clin Endocr Metab 94, 138144.Google Scholar
Roche, D J O & King, A C. (2015). Sex differences in acute hormonal and subjective response to naltrexone: the impact of menstrual cycle phase. Psychoneuroendocr 52, 5971.Google Scholar
Rometo, A M & Rance, N E. (2008). Changes in prodynorphin gene expression and neuronal morphology in the hypothalamus of postmenopausal women. J Neuroendocr 20, 13761381.Google Scholar
Roozenburg, B J, van Dessel, H J H M, Evers, J L H & Bots, R S M. (1997). Successful induction of ovulation in normogonadotrophic clomiphene resistant anovulatory women by combined naltrexone and clomiphene citrate treatment. Human Reprod 12, 17201722.Google Scholar
Rossmanith, W G, Wirth, U, Sterzik, K & Yen, S S. (1989). The effects of prolonged opioidergic blockade on LH pulsatile secretion during the menstrual cycle. J Endocr Invest 12, 245252.Google Scholar
Schmittner, J, Schroeder, J R, Epstein, D H & Preston, K L. (2005). Menstrual cycle length during methadone maintenance. Addiction 100, 829836.Google Scholar
Semple, R K & Topaloglu, A K. (2010). Neurokinin B and its receptor in hypogonadotropic hypogonadism. Front Horm Res 39, 133141.CrossRefGoogle ScholarPubMed
Shaw, N D, Butler, J P, McKinney, S M, Nelson, S A, Ellenbogen, J M & Hall, J E. (2012). Insights into puberty: the relationship between sleep stages and pulsatile LH secretion. J Clin Endocr Metab 97, E2055E2062.Google Scholar
Silveira, L F G & Latronico, A C. (2013). Approach to the patient with hypogonadotropic hypogonadism. J Clin Endocr Metab 98, 17811788.Google Scholar
Silveira, L G, Latronico, A C & Seminara, S B. (2013). Kisspeptin and clinical disorders. Adv Exp Med Biol 784, 187199.Google Scholar
Skinner, D C, Albertson, A J, Navratil, A et al. (2009). Effects of gonadotrophin-releasing hormone outside the hypothalamic-pituitary-reproductive axis. J Neuroendocr 21, 282292.Google Scholar
Skorupskaite, K, George, J T & Anderson, R A. (2014). The kisspeptin–GnRH pathway in human reproductive health and disease. Human Reprod Update 20, 485500.Google Scholar
Skorupskaite, K, George, J T, Veldhuis, J D & Anderson, R A. (2018a). Neurokinin B regulates gonadotropin secretion, ovarian follicle growth, and the timing of ovulation in healthy women. J Clin Endocr Metab 103, 95104.Google Scholar
Skorupskaite, K, George, J T, Veldhuis, J D, Millar, R P & Anderson, R A. (2018b). Neurokinin 3 receptor antagonism reveals roles for neurokinin B in the regulation of gonadotropin secretion and hot flashes in postmenopausal women. Neuroendocr 106, 148157.CrossRefGoogle ScholarPubMed
Skrapits, K, Kanti, V, Savanyú, Z et al. (2015). Lateral hypothalamic orexin and melanin-concentrating hormone neurons provide direct input to gonadotropin-releasing hormone neurons in the human. Fronts Cellular Neurosci 9, 113.Google Scholar
Southworth, M B, Matsumoto, A M, Gross, K M, Soules, M R & Bremner, W J. (1991). The importance of signal pattern in the transmission of endocrine information: pituitary gonadotropin responses to continuous and pulsatile gonadotropin-releasing hormone. J Clin Endocr Metab 72, 12861289.Google Scholar
Stamou, M I, Cox, K H & Crowley, W F Jr. (2015). Discovering genes essential to the hypothalamic regulation of human reproduction using a human disease model: adjusting to life in the “-omics” era. Endocr Revs 36, 603621.Google Scholar
Stamou, M I & Georgopoulos, N A. (2017). Kallmann syndrome: phenotype and genotype of hypogonadotropic hypogonadism. Metab 86, 124–134.Google Scholar
Taziaux, M, Staphorsius, A S, Ghatei, M A, Bloom, S R, Swaab, D F & Bakker, J. (2016). Kisspeptin expression in the human infundibular nucleus in relation to sex, gender identity, and sexual orientation. J Clin Endocr Metab 101, 23802389.Google Scholar
Teles, M, Bianco, S D, Brito, V N et al. (2008). A GPR54-activating mutation in a patient with central precocious puberty. N Engl J Med 358, 709715.Google Scholar
Tenhola, H, Sinclair, D, Alho, H & Lahti, T. (2012). Effect of opioid antagonists on sex hormone secretion. J Endocr Invest 35, 227230.Google Scholar
Teoh, S K, Mendelson, J H, Mello, N K & Skupny, A. (1988). Alcohol effects on naltrexone-induced stimulation of pituitary, adrenal, and gonadal hormones during the early follicular phase of the menstrual cycle. J Clin Endocr Metab 66, 11811186.CrossRefGoogle ScholarPubMed
Thomsen, L & Humaidan, P. (2015). Ovarian hyperstimulation syndrome in the 21st century: the role of gonadotropin-releasing hormone agonist trigger and kisspeptin. Curr Opin Obst Gynecol 27, 210214.Google Scholar
Valdes-Socin, H, Almanza, M R, Fernández-Ladreda, M T, Debray, F G, Bours, V & Beckers, A. (2014). Reproduction, smell, and neurodevelopmental disorders: genetic defects in different hypogonadotropic hypogonadal syndromes. Fronts Endocr 5, 18.Google Scholar
Vuong, C, Van Uum, S H M, O’Dell, L E, Lutfy, K & Friedman, T C. (2010). The effects of opioids and opioid analogs on animal and human endocrine systems. Endocr Revs 31, 98132.Google Scholar
Wahab, F, Atika, B, Shahab, M & Behr, R. (2016). Kisspeptin signalling in the physiology and pathophysiology of the urogenital system. Nat Revs Urol 13, 2132.CrossRefGoogle ScholarPubMed
Wildt, L, Leyendecker, G, Sir-Petermann, T & Waibel-Treber, S. (1993). Treatment with naltrexone in hypothalamic ovarian failure: induction of ovulation and pregnancy. Human Reprod 8, 350358.Google Scholar
Wilkinson, M & Brown, R E. (2015). An Introduction to Neuroendocrinology, 2nd Edition (Cambridge: Cambridge University Press).Google Scholar
Williams, C L, Nishihara, M, Thalabard, J C et al. (1990). Duration and frequency of multiunit electrical activity associated with the hypothalamic gonadotropin releasing hormone pulse generator in the rhesus monkey: differential effects of morphine. Neuroendocr 52, 225228.Google Scholar
Zatelli, M C, Ambrosio, M R, Bondanelli, M & degli Uberti, E. (2014). Pituitary side effects of old and new drugs. J Endocr Invest 37, 917923.Google Scholar

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