Pituitary Network Connectivity as a Mechanism for the Luteinising Hormone Surge

Journal of Neuroendocrinology

Volumn 22, Issue 12, 2010, Pages 1267-1278

  Lyles, D ^a   Tien, J H ^b   McCobb, D P ^c   Zeeman, M L ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d BOWDOIN COLLEGE   (United States)

Author keywords

Folliculostellate network connectivity; Mathematical model; Oestradiol

Indexed keywords

ESTRADIOL; GONADORELIN; LUTEINIZING HORMONE;

ARTICLE; BRAIN NERVE CELL; CIRCADIAN RHYTHM; CONTROLLED STUDY; GONADOTROPIN SECRETING CELL; HORMONE SUBSTITUTION; HYPOPHYSIS CELL; KALLMANN SYNDROME; LUTEINIZING HORMONE RELEASE; MENSTRUAL CYCLE; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ESTRADIOL; FEMALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; KALLMANN SYNDROME; LUTEINIZING HORMONE; MODELS, BIOLOGICAL; OVARY; PITUITARY GLAND;

EID: 78649501007     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02084.x     Document Type: Article

References (84)

1. Ördög T, Goldsmith JR, Chen M-D, Connaughton MA, Hotchkiss J, Knobil E. On the mechanism of the positive feedback action of estradiol on luteinizing hormone secretion in the rhesus monkey. J Clin Endocrinol Metab 1998; 83: 4047-4053.
2. Strauss JF, Barbieri RL. Jaffe's Reproductive Endocrinology: Physiology, Pathophysiology, and Clinical Management. Philadelphia: Saunders, 2009.
3. Hotchkiss J, Knobil E. The menstrual cycle and its neuroendocrine control. In: Knobil E, Neill JDD, eds. The Physiology of Reproduction, Chapter 48. New York: Raven Press, 1994: 711-749.
4. Gueorguiev M, Prendergast K, Heras-Herzig A, Dalkin A. GnRH gonadotropin physiology and pathology. Chapter 8, Version 20, in, the free online Endocrine textbook, Leslie J De Groot, MD, President. Online at, 2010.
5. Ch'avez-Ross A, Franks S, Mason HD, Hardy K, Stark J. Modelling the control of ovulation and polycystic ovary syndrome. J Math Biol 1997; 36: 95-118.
6. Lacker HM, Akin E. How do the ovaries count? Math Biosci 1996; 90: 305-332.
7. Selgrade JF. A model of gonadotropin modeling hormonal control of the menstrual cycle. Comments Theor Biol 2001; 6: 79-101.
8. Scullion S, Brown D, Leng G. Modelling the pituitary response to luteinizing hormonereleasing hormone. J Neuroendocrinol 2004; 16: 265-271.
9. Bertram R, Li Y-X. A mathematical model for the actions of activin, inhibin, and follistatin on pituitary gonadotrophs. Bull Math Biol 2008; 70: 2211-2228.
10. Nakai Y, Plant TM, Hess DL, Keogh EJ, Knobil E. On the sites of the negative and positive feedback actions of estradiol in the control of gonadotropin secretion in the rhesus monkey. Endocrinology 1978; 102: 1008-1014.
11. Karsch FJ, Weick RF, Butler WR, Dierschke DJ, Krey LC, Weiss G, Hotchkiss J, Yamaji T, Knobil E. Induced LH surges in the rhesus monkey: Strength-duration characteristics of the estrogen stimulus. Endocrinology 1973; 92: 1740-1747.
12. Liu JH, Yen SSC. Induction of midcycle gonadotropin surge by ovarian steroids in women: a critical evaluation. J Clin Endocrinol Metab 1983; 57: 797-802.
13. Haighton J. An experimental study concerning animal impregnation. Philos Trans R Soc Lond A 1797; 87: 157-196.
14. Hyland JH, Wright PJ, Clarke IJ, Carson RS, Langsford DA, Jeffcott LB. Infusion of gonadotrophin-releasing hormone (gnrh) induces ovulation and fertile oestrus in mares during seasonal anoestrus. J Reprod Fertil Suppl 1987; 35: 211-220.
15. Everett JW, Sawyer CH, Markee JE. A neurogenic timing factor in control of the ovulatory discharge of luteinizing hormone in the cyclic rat. Endocrinology 1949; 44: 234-250.
16. McElhinny TL, Sisk CL, Holekamp KE, Smale L. A morning surge in plasma luteinizing hormone coincides with elevated Fos expression in gonadotropin-releasing hormoneimmunoreactive neurons in the diurnal rodent, Arvicanthis niloticus. Biol Reprod 1999; 61: 1115-1122.
17. Karsch FJ, Bowen JM, Caraty A, Evans NP, Moenter SM. Gonadotropin-releasing hormone requirements for ovulation. Biol Reprod 1997; 56: 303-309.
18. Moenter SM, Caraty A, Locatelli A, Karsch FJ. Pattern of gonadotropin-releasing hormone (GnRH) secretion leading up to ovulation in the ewe: Existence of a preovulatory gnrh surge. Endocrinology 1991; 129: 1175-1182.
19. Pau KY, Berria M, Hess DL, Spies HG. Preovulatory gonadotropin-releasing hormone surge in ovarian-intact rhesus macaques. Endocrinology 1993; 133: 1650-1656.
20. Edwards RG. Current status of human conception in vitro. Proc R Soc Lond B Biol Sci 1985; 223: 417-448.
21. Crowley Jr WF, McArthur JW. Stimulation of the normal menstrual cycle in Kallman's syndrome by pulsatile administration of luteinizing hormone-releasing hormone (LHRH). J Clin Endocrinol Metab 1980; 51: 173-175.
22. Leyendecker G, Struve T, Plotz EJ. Induction of ovulation with chronic intermittent (pulsatile) administration of LH-RH in women with hypothalamic and hyperprolactinemic amenorrhea. Arch Gynecol 1980; 229: 177-190.
23. Knobil E, Plant TM, Wildt L, Belchetz PE, Marshall G. Control of the rhesus monkey menstrual cycle: permissive role of hypothalamic gonadotropin-releasing hormone. Science 1980; 207: 1371-1373.
24. Becker SE, Johnson AL. Effects of gonadotropin-releasing hormone infused in a pulsatile or continuous fashion on serum gonadotropin concentrations and ovulation in the mare. J Anim Sci 1992; 70: 1208-1215.
25. Knobil E. On the control of gonadotropin secretion in the rhesus monkey. Recent Prog Horm Res 1974; 30: 1-36.
26. McCormack JT, Plant TM, Hess DL, Knobil E. The effect of luteinizing hormone releasing hormone (LHRH) antiserum administration on gonadotropin secretion in the rhesus monkey. Endocrinology 1977; 100: 663.
27. Wildt L, Häusler JS, Hutchison A, Marshall G, Knobil E. Estradiol as a gonadotropin releasing hormone in the rhesus monkey. Endocrinology 1981; 108: 2011-2012.
28. Wilks JW, Folkers K, Humphries J, Bowers CY. Effect of [D-Phe2, Pro3, D-Phe6 ]-luteinizing hormone releasing hormone, an antagonist, on pre-ovulatory gonadotropin secretion in the rhesus monkey. Biol Reprod 1980; 23: 1.
29. Khadra A, Li YX. A model for the pulsatile secretion of gonadotropin-releasing hormone from synchronized hypothalamic neurons. Biophys J 2006; 91: 74-83.
30. Khadra A. Synchrony due to parametric averaging in neurons coupled by a shared signal. Physica D 2009; 238: 771-781.
31. LeBeau AP, Van Goor F, Stojilkovic SS, Sherman A. Modeling of membrane excitability in gonadotropin-releasing hormone-secreting hypothalamic neurons regulated by Ca2+-mobilizing and adenylyl cyclase-coupled receptors. J Neurosci 2000; 20: 9290-9297.
32. Levine JE. Pulsatility in primatesa perspective from the placode. Endocrinology 1999; 140: 1033-1035.
33. Li YX, Khadra A. Robust synchrony and rhythmogenesis in endocrine neurons via autocrine regulations in vitro and in vivo. Bull Math Biol 2008; 70: 2103-2125.
34. Moenter SM, DeFazio AR, Pitts GR, Nunemaker CS. Mechanisms underlying episodic gonadotropin-releasing hormone secretion. Front Neuroendocrinol 2003; 24: 79-93.
35. Stojilkovic SS, Krsmanovic LZ, Spergel DJ, Catt KJ. Gonadotropin-releasing hormone neurons: intrinsic pulsatility and receptor-mediated regulation. Endocrinol Metab 1994; 5: 201-209.
36. Bergendahl M, Evans WS, Veldhuis JD. Current concepts on ultradian rhythms of luteinizing hormone secretion in the human. Hum Reprod Update 1996; 2: 507-518.
37. Cardenas H, Ördög T, O'Byrne KT, Knobil E. Single unit components of the hypothalamic multiunit electrical activity associated with the central signal generator that directs the pulsatile secretion of gonadotropic hormones. Proc Natl Acad Sci USA 1993; 90: 9630-9634.
38. Moenter SM, Brand RM, Midgley AR, Karsch FJ. Dynamics of gonadotropin-releasing hormone release during a pulse. Endocrinology 1992; 130: 503-510.
39. Filicori M, Santoro N, Merriam GR, Crowley Jr WF. Characterization of the physiological pattern of episodic gonadotropin secretion throughout the human menstrual cycle. J Clin Endocrinol Metab 1986; 62: 1136-1144.
40. O'Byrne KT, Thalabard JC, Grosser PM, Wilson RC, Williams C, Chen MD, Ladendorf D, Hotchkiss J, Knobil E. Radiotelemetric monitoring of hypothalamic gonadotropinreleasing hormone pulse generator activity throughout the menstrual cycle of the rhesus monkey. Endocrinology 1991; 129: 1207-1214.
41. Belchetz PE, Plant TM, Nakai Y, Keogh EJ, Knobil E. Hypophysial responses to continuous and intermittent delivery of hypothalamic gonadotropin-releasing hormone. Science 1978; 202: 631-633.
42. Filicori M, Flamigni C, Campaniello E, Ferrari P, Meriggiola MC, Michelacci L, Pareschi A, Valdiserri A. Evidence for a specific role of GnRH pulse frequency in the control of the human menstrual cycle. Am J Physiol 1989; 257: E930-E936.
43. Pohl CR, Richardson DW, Hutchison JS, Germak JA, Knobil E. Hypophysiotropic signal frequency and the functioning of the pituitary-ovarian system in the rhesus monkey. Endocrinology 1983; 112: 2076-2080.
44. Wildt L, Häusler A, Marshall G, Hutchison JS, Plant TM, Belchetz PE, Knobil E. Frequency and amplitude of gonadotropin-releasing hormone stimulation and gonadotropin secretion in the rhesus monkey. Endocrinology 1981; 109: 376-385.
45. Knobil E. The wisdom of the body revisited. News Physiol Sci 1999; 14: 1-11.
46. Tien JH, Lyles D, Zeeman ML. A potential role of modulating inosotol 1, 4, 5- triphosphate receptor desensitization and recovery rates in regulating ovulation. J Theor Biol 2005; 232: 105-117.
47. Zeeman ML, Weckesser W, Gokhman D. Resonance in the menstrual cycle, a new model of the lh surge. Reprod Biomed Online 2003; 7: 295-300.
48. Bonnefont X, Lacampagne A, Sanchez-Hormigo A, Fino E, Creff A, Mathieu MN, Smallwood S, Carmignac D, Fontanaud P, Travo P, Alonso G, Courtois-Coutry N, Pincus SM, Robinson IC, Mollard P. Revealing the large-scale network organization of growth hormone-secreting cells. Proc Natl Acad Sci USA 2005; 102: 16880-16885.
49. Fauquier T, Gu'erineau NC, McKinney RA, Bauer K, Mollard P. Folliculostellate cell network: a route for long-distance communication in the anterior pituitary. Proc Natl Acad Sci USA 2001; 98: 8891-8896.
50. Fauquier T, Lacampagne A, Travo P, Bauer K, Mollard P. Hidden face of the anterior pituitary. Trends Endocrinol Metab 2002; 13: 304-309.
51. Stojilkovic SS. A novel view of the function of pituitary folliculo-stellate cell network. Trends Endocrinol Metab 2001; 12: 378-380.
52. Yamamoto T, Hossain MZ, Hertzberg EL, Uemura H, Murphy LJ, Nagy JI. Connexin43 in rat pituitary: localization at pituicyte and stellate cell gap junctions and within gonadotrophs. Histochemistry 1993; 100: 53-64.
53. Chauvet N, El-Yandouzi T, Mathieu MN, Schlernitzauer A, Galibert E, Lafont C, Le Tissier P, Robinson IC, Mollard P, Coutry N. Characterization of adherens junction protein expression and localization in pituitary cell networks. J Endocrinol 2009; 202: 375-387.
54. Hodson DJ, Townsend J, Gregory SJ, Walters C, Tortonese DJ. Role of prolactin in the gonadotroph responsiveness to gonadotrophin-releasing hormone during the equine annual reproductive cycle. J Neuroendocrinol 2010; 22: 509-517.
55. Kurono C. Intercellular communication within the rat anterior pituitary gland: IV. Development of gap junctions between folliculo-stellate cells under the influence of ovariectomy and sex steroids in the female rat. Anat Rec 1996; 244: 366-373.
56. Soji T, Nishizono H, Yashiro T, Herbert DC. Intercellular communication within the rat anterior pituitary gland III: postnatal development and periodic changes of cell-to-cell communications in female rats. Anat Rec 1991; 231: 351-357.
57. Vitale ML, Cardin J, Gilula NB, Carbajal ME, Pelletier RM. Dynamics of connexin 43 levels and distribution in the mink (mustela vison) anterior pituitary are associated with seasonal changes in anterior pituitary prolactin content. Biol Reprod 2001; 64: 625-633.
58. Waite E, Lafont C, Carmignac D, Chauvet N, Coutry N, Christian H, Robinson I, Mollard P, Le Tissier P. Different degrees of somatotroph ablation compromise pituitary growth hormone cell network structure and other pituitary endocrine cell types. Endocrinology 2010; 151: 234-243.
59. Allaerts W, Carmeliet P, Denef C. Review: new perspectives in the function of pituitary folliculo-stellate cells. Mol Cell Endocrinol 1990; 71: 73-81.
60. Baes M, Allaerts W, Denef C. Evidence for functional communication between folliculostellate cells and hormone-secreting cells in perifused anterior pituitary cell aggregates. Endocrinology 1987; 120: 685-691.
61. Denef C. Paracrinicity: the story of 30 years of cellular pituitary crosstalk. J Neuroendocrinol 2008; 20: 1-70.
62. Morand I, Fonlupt P, Guerrier A, Trouillas J, Calle A, Remy C, Rousset B, Munari-Silem Y. Cell-to-cell communication in the anterior pituitary: evidence for gap junctionmediated exchanges between endocrine cells and folliculostellate cells. Endocrinology 1996; 137: 3356-3367.
63. Ortmann O, Wassmann D, Stojilkovic SS, Catt KJ, Schulz KD, Emons G. Ovarian steroids modulate endothelin-induced luteinizing hormone secretion from cultured rat pituitary cells. Endocrinology 1993; 133: 2632-2638.
64. Renner U, Gloddek J, Pereda MP, Arzt E, Stalla GK. Regulation and role of intrapituitary IL-6 production by folliculostellate cells. Domest Anim Endocrinol 1998; 15: 353-362.
65. Stojilkovic SS, Tabak J, Bertram R. Ion channels and signaling in the pituitary gland. Endocr Rev page Epub July 21. 2010; 31: 1-71.
66. Yamada E, Yoshida M, Kimura H, Kurita J, Kurono C. Immunohistochemical and ultrastructural study of the rat anterior pituitary gland conduction of information of LH-RH by the folliculo-stellate cells. Nagoya Med J 2001; 44: 173-186.
67. Gambacciani M, Liu JH, Swartz WH, Tueros VS, Yen SSC, Rasmussen DD. Intrinsic pulsatility of luteinizing hormone release from the human pituitary in vitro. Neuroendocrinology 1987; 45: 402-406.
68. Rossmanith WG, Yen SSC, Rasmussen DD. Synchronous pulsatile release of luteinizing hormone and immunoreactive beta-endorphin from the human pituitary in vitro. J Endocrinol 1990; 2: 91-94.
69. Li YX, Rinzel J. Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J Theor Biol 1994; 166: 461-473.
70. Horiguchi K, Fujiwara K, Kouki T, Kikuchi M, Yashiro T. Immunohistochemistry of connexin 43 throughout anterior pituitary gland in a transgenic rat with green fluorescent protein-expressing folliculo-stellate cells. Anat Sci Int 2008; 83: 256-260.
71. Mabuchi Y, Shirasawa N, Sakuma E, Hashimoto Y, Kuno M, Coombs RJ, Herbert DC, Soji T. Intercellular communication within the rat anterior pituitary: relationship between LH-RH neurons and folliculo-stellate cells in the pars tuberalis. Cell Tissue Res 2004; 317: 79-90.
72. Shirasawa N, Sakuma E, Wada I, Naito A, Horiuchi O, Mabuchi Y, Kanai M, Herbert DC, Soji T. Intercellular communication within the rat anterior pituitary XIV: electron microscopic and immunohistochemical study on the relationship between the agranular cells and GnRH neurons in the dorsal pars tuberalis of the pituitary gland. Anat Rec 2007; 290: 1388-1398.
73. Yanagisono T, Kurita J, Kimura H, Yoshida M, Sakuma E. An immunohistochemical study of LH-RH and S-100 protein in the hypothalamus and the pars tuberalis of the anterior pituitary gland. Nagoya Med J 2001; 44: 153-171.
74. Spangelo BL, Judd AM, Isakson PC, MacLeod RM. Interleukin-6 stimulates anterior pituitary hormone release in vitro. Endocrinology 1989; 125: 575-577.
75. Yamaguchi M, Matsuzaki N, Hirota K, Miyake A, Tanizawa O. Interleukin 6 possibly induced by interleukin 1 beta in the pituitary gland stimulates the release of gonadotropins and prolactin. Acta Endocrinol 1990; 122: 201-205.
76. Tabak J, Senn W, O'Donovan MJ, Rinzel J. Modeling of spontaneous activity in developing spinal cord using activity-dependent depression in an excitatory network. J Neurosci 2000; 20: 3041-3056.
77. Zeeman EC. Catastrophe Theory. Selected Papers 1972-1977. Reading, MA: Addison-Wesley, 1977.
78. Rossoni E, Feng J, Tirozzi B, Brown D, Leng G, Moos F. Emergent synchronous bursting of oxytocin neuronal network. PLoS Comput Biol 2008; 4: e1000123.
79. Hall JE, Taylor AE, Martin KA, Rivier J, Schoenfeld DA, Crowley Jr WF. Decreased release of gonadotropin-releasing hormone during the preovulatory midcycle luteinizing hormone surge in normal women. Proc Natl Acad Sci USA 1994; 91: 6894-6898.
80. Plant TM. Hypothalamic control of the pituitary-gonadal axis in higher primates: key advances over the last two decades. J Neuroendocrinol 2008; 20: 719-726.
81. De Seranno S, D'Anglemont De Tassigny X, Estrella C, Loyens A, Kasparov S, Leroy D, Ojeda SR, Beauvillain JC, Prevot V. Role of estradiol in the dynamic control of tanycyte plasticity mediated by vascular endothelial cells in the median eminence. Endocrinology 2010; 151: 1760-1772.
82. Prevot V, Croix D, Bouret S, Dutoit S, Tramu G, Stefano GB, Beauvillain JC. Definitive evidence for the existence of morphological plasticity in the external zone of the median eminence during the rat estrous cycle: Implication of neuro-glio-endothelial interactions in gonadotropin-releasing hormone release. Neuroscience 1999; 94: 809-819.
83. Inoue K, Couch EF, Takano K, Ogawa S. The structure and function of folliculo-stellate cells in the anterior pituitary gland. Arch Histol Cytol 1999; 62: 205-218.
84. Filicori M, Crowley Jr WF Hypothalamic regulation of gonadotropin secretion in women. In: Norman RL, ed. Neuroendocrine Aspects of Reproduction. New York: Academic Press, 1983: 285-294.