Hypothalamic insulin-like growth factor-i receptors are necessary for hormone-dependent luteinizing hormone surges: Implications for female reproductive aging

Endocrinology

Volumn 151, Issue 3, 2010, Pages 1356-1366

  Todd, Brigitte J ^a   Merhi, Zaher O ^a   Shu, Jun ^a   Etgen, Anne M ^a   Neal Perry, Genevieve S ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; GONADORELIN; PROGESTERONE; SOMATOMEDIN C RECEPTOR;

AGED; AGING; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME REGULATION; FEMALE; FEMALE GENITAL SYSTEM; LUTEINIZING HORMONE RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

AGING; ANIMALS; BODY WEIGHT; ESTRADIOL; FEMALE; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INSULIN-LIKE GROWTH FACTOR I; LUTEINIZING HORMONE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, IGF TYPE 1; RECEPTORS, LHRH; REPRODUCTION;

EID: 77149173162     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-1009     Document Type: Article

References (64)

1. Cardona-Gómez GP, DonCarlos L, Garcia-Segura LM 2000 Insulin-like growth factor I receptors and estrogen receptors colocalize in female rat brain. Neuroscience 99:751-760
2. Garcia-Segura LM, Rodriguez JR, Torres-Aleman I 1997 Localization of the insulin-like growth factor I receptor in the cerebellum and hypothalamus of adult rats: an electron microscopic study. J Neurocytol 26:479-490
3. Daftary SS, Gore AC 2003 Developmental changes in hypothalamic insulin-like growth factor-1: relationship to gonadotropin-releasing hormone neurons. Endocrinology 144:2034-2045
4. Daftary SS, Gore AC 2004 The hypothalamic insulin-like growth factor-1 receptor and its relationship to gonadotropin-releasing hormones neurones during postnatal development. J Neuroendocrinol 16:160-169
5. Todd BJ, Fraley GS, Peck AC, Schwartz GJ, Etgen AM 2007 Central insulin-like growth factor 1 receptors play distinct roles in the control of reproduction, food intake, and body weight in female rats. Biol Reprod 77:492-503
6. Quesada A, Etgen AM 2002 Functional interactions between estrogen and insulin-like growth factor-I in the regulation of α1B-adrenoceptors and female reproductive function. J Neurosci 22:2401-2408
7. Etgen AM, Acosta-Martinez M 2003 Participation of growth factor signal transduction pathways in estradiol facilitation of female reproductive behavior. Endocrinology 144:3828-3835
8. Fernandez-Galaz MC, Naftolin F, Garcia-Segura LM 1999 Phasic synaptic remodeling of the rat arcuate nucleus during the estrous cycle depends on insulin-like growth factor-I receptor activation. J Neurosci Res 55:286-292
9. Cardona-Gómez GP, Trejo JL, Fernandez AM, Garcia-Segura LM 2000 Estrogen receptors and insulin-like growth factor-I receptors mediate estrogen-dependent synaptic plasticity. Neuroreport 11: 1735-1738
10. Wu Y, Sun H, Yakar S, LeRoith D 2009 Elevated levels of insulinlike growth factor (IGF)-I in serum rescue the severe growth retardation of IGF-I null mice. Endocrinology 150:4395-4403
11. Downs JL, Wise PM 2009 The role of the brain in female reproductive aging. Mol Cell Endocrinol 299:32-38
12. Miller BH, Gore AC 2001 Alterations in hypothalamic insulin-like growth factor-I and its associations with gonadotropin releasing hormone neurones during reproductive development and ageing. J Neuroendocrinol 13:728-736
13. Bartke A, Chandrashekar V, Dominici F, Turyn D, Kinney B, Steger R, Kopchick JJ 2003 Insulin-like growth factor 1 (IGF-1) and aging: controversies and new insights. Biogerontology 4:1-8
14. Chung YH, Shin CM, Joo KM, Kim MJ, Cha CI 2002 Regionspecific alterations in insulin-like growth factor receptor type I in the cerebral cortex and hippocampus of aged rats. Brain Res 946:307-313
15. Pietrzkowski Z, Wernicke D, Porcu P, Jameson BA, Baserga R 1992 Inhibition of cellular proliferation by peptide analogues of insulinlike growth factor 1. Cancer Res 52:6447-6451
16. Neal-Perry GS, Zeevalk GD, Santoro NF, Etgen AM 2005 Attenuation of preoptic area glutamate release correlates with reduced luteinizing hormone secretion in middle-aged female rats. Endocrinology 146:4331-4339
17. Foecking EM, Szabo M, Schwartz NB, Levine JE 2005 Neuroendocrine consequences of prenatal androgen exposure in the female rat: absence of luteinizing hormone surges, suppression of progesterone receptor gene expression, and acceleration of the gonadotropin-releasing hormone pulse generator. Biol Reprod 72:1475-1483
18. Neal-Perry G, Lebesgue D, Lederman M, Shu J, Zeevalk GD, Etgen AM 2009 The excitatory peptide kisspeptin restores the luteinizing hormone surge and modulates amino acid neurotransmission in the medial preoptic area of middle-aged rats. Endocrinology 150:3699-3708
19. Rubin BS 2000 Hypothalamic alterations and reproductive aging in female rats: evidence of altered luteinizing hormone-releasing hormone neuronal function. Biol Reprod 63:968-976
20. Wise PM, Smith MJ, Dubal DB, Wilson ME, Rau SW, Cashion AB, Böttner M, Rosewell KL 2002 Neuroendocrine modulation and repercussions of female reproductive aging. Recent Prog Horm Res 57:235-256
21. Arias P, Carbone S, Szwarcfarb B, Feleder C, Rodríguez M, Scacchi P, Moguilevsky JA 1996 Effects of aging on N-methyl-D- aspartate (NMDA)-induced GnRH and LH release in female rats. Brain Res 740:234-238
22. Krajnak K, Rosewell KL, Wise PM 2001 Fos-induction in gonadotropin-releasing hormone neurons receiving vasoactive intestinal polypeptide innervation is reduced in middle-aged female rats. Biol Reprod 64:1160-1164
23. Le WW, Wise PM, Murphy AZ, Coolen LM, Hoffman GE 2001 Parallel declines in Fos activation of the medial anteroventral periventricular nucleus and LHRH neurons in middle-aged rats. Endocrinology 142:4976-4982
24. Neal-Perry GS, Zeevalk GD, Shu J, Etgen AM 2008 Restoration of the luteinizing hormone surge in middle-aged female rats by altering the balance of GABA and glutamate transmission in the medial preoptic area. Biol Reprod 79:878-888
25. Cappola AR, Xue QL, Ferrucci L, Guralnik JM, Volpato S, Fried LP 2003 Insulin-like growth factor I and interleukin-6 contribute synergistically to disability and mortality in older women. J Clin Endocrinol Metab 88:2019-2025
26. Kovacs P, Parlow AF, Karkanias GB 2002 Effect of centrally administered insulin on gonadotropin-releasing hormone neuron activity and luteinizing hormone surge in the diabetic female rat. Neuroendocrinology 76:357-365
27. Christian CA, Moenter SM 2008 Vasoactive intestinal polypeptide can excite gonadotropin-releasing hormone neurons in a manner dependent on estradiol and gated by time of day. Endocrinology 149:3130-3136
28. Gerhold LM, Rosewell KL, Wise PM 2005 Suppression of vasoactive intestinal polypeptide in the suprachiasmatic nucleus leads to aging-like alterations in cAMP rhythms and activation of gonadotropin-releasing hormone neurons. J Neurosci 25:62-67
29. Gerhold LM, Sellix MT, Freeman ME 2002 Antagonism of vasoactive intestinal peptide mRNA in the suprachiasmatic nucleus disrupts the rhythm of FRAs expression in neuroendocrine dopaminergic neurons. J Comp Neurol 450:135-143
30. Harney JP, Scarbrough K, Rosewell KL, Wise PM 1996 In vivo antisense antagonism of vasoactive intestinal peptide in the suprachiasmatic nuclei causes aging-like changes in the estradiol-induced luteinizing hormone and prolactin surges. Endocrinology 137: 3696-3701
31. Horvath TL, Cela V, van der Beek EM 1998 Gender-specific apposition between vasoactive intestinal peptide-containing axons and gonadotrophin-releasing hormone-producing neurons in the rat. Brain Res 795:277-281
32. van der Beek EM, Swarts HJ, Wiegant VM 1999 Central administration of antiserum to vasoactive intestinal peptide delays and reduces luteinizing hormone and prolactin surges in ovariectomized, estrogen-treated rats. Neuroendocrinology 69:227-237
33. van der Beek EM, van Oudheusden HJ, Buijs RM, van der Donk HA, van den Hurk R, Wiegant VM 1994 Preferential induction of c-fos immunoreactivity in vasoactive intestinal polypeptide-innervated gonadotropin-releasing hormone neurons during a steroidinduced luteinizing hormone surge in the female rat. Endocrinology 134:2636-2644
34. van der Beek EM, Wiegant VM, van der Donk HA, van den Hurk R, Buijs RM 1993 Lesions of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotrophin-releasing hormone neurons in the female rat. J Neuroendocrinol 5:137-144
35. Servoss SJ, Lee SJ, Gibney G, Gozes I, Brenneman DE, Hill JM 2001 IGF-I as a mediator of VIP/activity-dependent neurotrophic factor-stimulated embryonic growth. Endocrinology 142:3348-3353
36. Hiney JK, Srivastava V, Nyberg CL, Ojeda SR, Dees WL 1996 Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 137:3717-3728
37. Rubin BS, Elkind-Hirsch K, Bridges RS 1985 HypothalamicLHRH in aging rats: effects of ovariectomy and steroid replacement. Neurobiol Aging 6:309-315
38. Mora OA, Cabrera MM, Sánchez-Criado JE 1994 Hormonal pattern of the pheromonal restoration of cyclic activity in aging irregularly cycling and persistent-estrus female rats. Biol Reprod 51: 920-925
39. Lloyd JM, Hoffman GE, Wise PM 1994 Decline in immediate early gene expression in gonadotropin-releasing hormone neurons during proestrus in regularly cycling, middle-aged rats. Endocrinology 134: 1800-1805
40. Goodyer CG, De Stéphano L, Lai WH, Guyda HJ, Posner BI 1984 Characterization of insulin-like growth factor receptors in rat anterior pituitary, hypothalamus, and brain. Endocrinology 114: 1187-1195
41. Werther GA, Hogg A, Oldfield BJ, McKinley MJ, Figdor R, Mendelsohn FA 1989 Localization and characterization of insulinlike growth factor-I receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry: a distinct distribution from insulin receptors. J Neuroendocrinol 1:369-377
42. AdamCL,GaddTS, Findlay PA, Wathes DC 2000 IGF-I stimulation of luteinizing hormone secretion, IGF-binding proteins (IGFBPs) and expression ofmRNAsfor IGFs, IGF receptors and IGFBPs in the ovine pituitary gland. J Endocrinol 166:247-254
43. Butcher RL, Collins WE, Fugo NW 1974 Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17β throughout the 4-day estrous cycle of the rat. Endocrinology 94:1704-1708
44. Neill JD, Freeman ME, Tillson SA 1971 Control of the proestrus surge of prolactin and luteinizing hormone secretion by estrogens in the rat. Endocrinology 89:1448-1453
45. Pan JT, Gala RR 1985 Central nervous system regions involved in the estrogen-induced afternoon prolactin surge. I. Lesion studies. Endocrinology 117:382-387
46. Wiersma J, Kastelijn J 1990 Electrophysiological evidence for a key control function of the medial preoptic area in the regulation of prolactin secretion in cycling, pregnant and lactating rats. Neuroendocrinology 51:162-167
47. Hou Y, Yang SP, Voogt JL 2003 Changes in estrogen receptor-α expression in hypothalamic dopaminergic neurons during proestrous prolactin surge. Endocrine 20:131-138
48. Lieberman ME, Maurer RA, Gorski J 1978 Estrogen control of prolactin synthesis in vitro. Proc Natl Acad Sci USA 75:5946-5949
49. Quesada A, Etgen AM 2001 Insulin-like growth factor-1 regulation of α(1)-adrenergic receptor signaling is estradiol dependent in the preoptic area and hypothalamus of female rats. Endocrinology 142: 599-607
50. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073-4077
51. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA 2005 Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146:3686-3692
52. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A 2006 Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor α. Neurosci Lett 401: 225-230
53. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA 2005 Kisspeptin directly stimulates gonadotropin-releasing hormone release viaGprotein-coupled receptor 54. Proc Natl Acad Sci USA 102:1761-1766
54. Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T 2004 Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 320:383-388
55. Navarro VM, Castellano JM, Fernández-Fernández R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M 2005 Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 146: 156-163
56. Hiney JK, Srivastava VK, Pine MD, Les Dees W 2009 Insulin-like growth factor-I activates KiSS-1 gene expression in the brain of the prepubertal female rat. Endocrinology 150:376-384
57. Lederman MA, Lebesgue D, Gonzalez VV, Shu J, Merhi ZO, Etgen AM, Neal-Perry G 2010 Age-related LH surge dysfunction correlates with reduced responsiveness of hypothalamic anteroventral periventricular nucleus kisspeptin neurons to estradiol positive feedback in middle-aged rats. Neuropharmacology 58:314-320
58. Cashion AB, Smith MJ, Wise PM 2004 Glutamic acid decarboxylase 67 (GAD67) gene expression in discrete regions of the rostral preoptic area change during the oestrous cycle and with age. J Neuroendocrinol 16:711-716
59. Miller BH, Gore AC 2002 N-Methyl-D-aspartate receptor subunit expression in GnRH neurons changes during reproductive senescence in the female rat. Endocrinology 143:3568-3574
60. Maffucci JA, Walker DM, Ikegami A, Woller MJ, Gore AC 2008 NMDA receptor subunit NR2b: effects on LH release and GnRH gene expression in young and middle-aged female rats, with modulation by estradiol. Neuroendocrinology 87:129-141
61. Maffucci JA, Noel ML, Gillette R, Wu D, Gore AC 24 March 2009 Age- and hormone-regulation of NMDA receptor subunit NR2b in the anteroventral periventricular nucleus (AVPV) of the female rat: implications for reproductive senescence. J Neuroendocrinol JNE 1860[pii] 10.1111/j.1365-2826.2009.01860.x
62. Rubin BS, Bridges RS 1989 Alterations in luteinizing hormone-releasing hormone release from the mediobasal hypothalamus of ovariectomized, steroid-primed middle-aged rats as measured by push-pull perfusion. Neuroendocrinology 49:225-232
63. Le Grevés M, Le Grevés P, Nyberg F 2005 Age-related effects of IGF-1 on the NMDA-, GH- and IGF-1-receptor mRNA transcripts in the rat hippocampus. Brain Res Bull 65:369-374
64. Sonntag WE, Bennett C, Ingram R, Donahue A, Ingraham J, Chen H, Moore T, Brunso-Bechtold JK, Riddle D 2006 Growth hormone and IGF-I modulate local cerebral glucose utilization and ATP levels in a model of adult-onset growth hormone deficiency. Am J Physiol Endocrinol Metab 291:E604-E610