Gonadotropin-releasing hormone II stimulates female sexual behavior in marmoset monkeys

Endocrinology

Volumn 147, Issue 1, 2006, Pages 615-623

  Barnett, Deborah K ^a   Bunnell, Tina M ^a   Millar, Robert P ^d   Abbott, David H ^a,b,c  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; GONADORELIN; GONADORELIN AGONIST; GONADORELIN ANTAGONIST; INOSITOL PHOSPHATE; PEPTIDE;

ANIMAL BEHAVIOR; ARTICLE; CANNULA; FEMALE; HORMONE ACTION; HORMONE DETERMINATION; HORMONE SUBSTITUTION; MALE; MARMOSET; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; SEX ROLE; SEXUAL BEHAVIOR; TONGUE;

AMINO ACID SEQUENCE; AMPHIBIA; ANIMALS; BIRDS; CALLITHRIX; CONSERVED SEQUENCE; ESTRADIOL; FEMALE; GOLDFISH; GONADOTROPIN-RELEASING HORMONE; HUMANS; INJECTIONS, INTRAVENTRICULAR; REPTILES; SEXUAL BEHAVIOR, ANIMAL; SPECIES SPECIFICITY;

EID: 29344448884     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2005-0662     Document Type: Article

References (85)

1. Kendrick KM, Dixson AF 1983 The effect of the ovarian cycle on the sexual behavior of the common marmoset (Callithrix jacchus). Physiol Behav 30:735-742
2. Keverne EB 1987 Processing of environmental stimuli and primate reproduction. J Zool (Lond) 213:395-408
3. Kendrick KM, Dixson AF 1984 Ovariectomy does not abolish proceptive behavior cyclicity in the common marmoset (Callithrix jacchus). J Endocrinol 101:155-162
4. Wallen K 2001 Sex and context: hormones and primate sexual motivation. Horm Behav 40:339-357
5. Wallen K, Zehr JL 2004 Hormones and history: the evolution and development of primate female sexuality. J Sex Res 41:101-112
6. Baum MJ, Everitt BJ, Herbert J, Keverne EB 1977 Hormonal basis of proceptivity and receptivity in female primates. Arch Sex Behav 6:173-192
7. Zehr JL, Maestripieri D, Wallen K 1998 Estradiol increases female sexual initiation independent of male responsiveness in rhesus monkeys. Horm Behav 33:95-103
8. Pawson AJ, Morgan K, Maudsley SR, Millar RP 2003 Type II gonadotrophin-releasing hormone (GnRH-II) in reproductive biology. Reproduction 126:271-278
9. Millar RP, Lu ZL, Pawson AJ, Flanagan CA, Morgan K, Maudsley SR 2004 Gonadotropin-releasing hormone receptors. Endocr Rev 25:235-275
10. Vickers ED, Laberge F, Adams BA, Hara TJ, SherwoodNM2004 Cloning and localization of three forms of gonadotropin-releasing hormone, including the novel whitefish form, in a salmonid, Coregonus clupeaformis. Biol Reprod 70:1136-1146
11. Millar RP 2003 GnRH II and type II GnRH receptors. Trends Endocrinol Metab 14:35-43
12. Schally AV, Arimura A, Baba Y, Nair RM, Matsuo H Redding TW, Debeljuk L 1971 Isolation and properties of FSH and LH-releasing hormone. Biochem Biophys Res Commun 43:393-399
13. Matsuo H, Baba Y, Nair RM, Arimura A, Schally AV 1971 Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem Biophys Res Commun 43:1334-1339
14. Baba Y, Matsuo H, Schally AV 1971 Structure of the porcine LH- and FSH-releasing hormone. II. Confirmation of structure by conventional sequential analyses. Biochem Biophys Res Commun 44:459-463
15. King JA, Millar RP 1990 Genealogy of the GnRH family. Prog Clin Biol Res 342:54-59
16. Morgan K, Millar RP 2004 Evolution of GnRH ligand precursors and GnRH receptors in protochordate and vertebrate species. Gen Comp Endocrinol 139:191-197
17. Kauffman AS 2004 Emerging functions of gonadotropin-releasing hormone II in mammalian physiology and behavior. J Neuroendocrinol 16:794-806
18. Kauffman AS, Rissman EF 2004 A critical role for the evolutionarily conserved gonadotropin-releasing hormone II: mediation of energy status and female sexual behavior. Endocrinology 145:3639-3646
19. Terasawa E 2003 Gonadotropin-releasing hormone II: is this neuropeptide important for mammalian reproduction? Endocrinology 144:3-4
20. Millar R, Lowe S, Conklin D, Pawson A, Maudsley S, Troskie B, Ott T, Millar M, Lincoln G, Sellar R, Faurholm B, Scobie G, Kuestner R, Teresawa E, Katz A 2001 A novel mammalian receptor for the evolutionarily conserved type II GnRH. Proc Natl Acad Sci USA 98:9636-9641
21. Lescheid DW, Terasawa E, Abler LA, Urbanski HF, Warby CM, Millar RP, Sherwood NM 1997 A second form of gonadotropin-releasing hormone (GnRH) with characteristics of chicken GnRH-II is present in the primate brain. Endocrinology 138:5618-5629
22. Urbanski HF, White RB, Fernald RD, Kohama SG, Garyfallou VT, Densmore VS 1999 Regional expression of mRNA encoding a second form of gonadotropin- releasing hormone in the macaque brain. Endocrinology 140:1945-1948
23. Neill JD 2002 GnRH and GnRH receptor genes in the human genome. Endocrinology 143:737-743
24. i-coupling state of type I GnRH receptor. Cancer Res 64:7533-7544
25. Kastin AJ, Coy DH, Schally AV, Zandin JE 1980 Dissociation of effects of LHRH analogues on pituitary regulation and reproductive behavior. Pharmacol Biochem Behav 13:913-914
26. Sun YM, Flanagan CA, Illing N, Ott T, Sellar R, Fromme BJ, Hapgood J, Sharp P, Sealfon SC, Millar RP 2001 A chicken gonadotropin-releasing hormone receptor that confers agonist activity to mammalian antagonists. Identification of D-Lys(6) in the ligand and extracellular loop two of the receptor as determinants. J Biol Chem 276:7754-7761
27. Ott TR, Troskie BE, Roeske RW, Illing N, Flanagan CA, Millar RP 2002 Two mutations in extracellular loop 2 of the human GnRH receptor convert an antagonist to an agonist. Mol Endocrinol 16:1079-1088
28. Dixson AF, Hastings MH 1992 Effects of ibotenic acid-induced neuronal degeneration in the hypothalamus upon proceptivity and sexual receptivity in the female marmoset (Callithrix jacchus). J Neuroendocrinol 4:719-726
29. Kendrick KM, Dixson AF 1986 Anteromedial hypothalamic lesions block proceptivity but not receptivity in the female common marmoset (Callithrix jacchus). Brain Res 375:221-229
30. Dixson AF 1990 Medial hypothalamic lesions and sexual receptivity in the female common marmoset (Callithrix jacchus). Folia Primatol (Basel) 54:46-56
31. Dixson AF 1993 Callitrichid mating systems: Laboratory and field approaches to studies of monogamy and polyandry. In: Rylands AB, ed. Marmosets, tamarins: systematic, behavior and ecology. Oxford: Oxford University Press; 164-175
32. Dixson AF 1986 Proceptive displays of the female common marmoset (Callithrix jacchus): effects of ovariectomy and oestradiol 17β. Physiol Behav 36:971-973
33. Kendrick KM, Dixson AF 1984 Effects of oestradiol 17β, progesterone and testosterone upon proceptivity and receptivity in ovariectomized common marmosets (Callithrix jacchus). Physiol Behav 34:123-128
34. Kendrick KM, Dixson AF 1984 A quantitative description of copulatory and associated behaviors of captive marmosets (Callithrix jacchus). Int J Primatol 5:199-212
35. Dixson AF, Lunn SF 1987 Post-partum changes in hormones and sexual behaviour in captive groups of marmosets (Callithrix jacchus). Physiol Behav 41:577-583
36. Dixson AF 1987 Effects of adrenalectomy upon proceptivity, receptivity and sexual attractiveness in ovariectomized marmosets (Callithrix jacchus). Physiol Behav 39:495-499
37. Saltzman W, Schultz-Darken NJ, Wegner FH, Wittwer DJ, Abbott DH 1998 Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Horm Behav 33:58-74
38. Hearn JP 1977 Restraining device for small monkeys Lab Anim 11:261-262
39. Saltzman W, Schultz-Darken NJ, Scheffler G, Wegner FH, Abbott DH 1994 Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiol Behav 56:801-810
40. Baker JV, Abbott DH, Saltzman W 1999 Social determinants of reproductive failure in male common marmosets housed with their natal family. Anim Behav 58:501-513
41. Dudley CA, Moss RL 1991 Facilitation of sexual receptivity in the female rat by C-terminal fragments of LHRH. Physiol Behav 50:1205-1208
42. Kendrick KM, Dixson AF 1985 Luteinizing hormone releasing hormone enhances proceptivity in a primate. Neurendocrinology 41:449-453
43. Sokal RR, Rohlf FJ 1995 Biometry: the principles and practice of statistics in biological research. 3rd ed. New York: W. H. Freeman; 413-422
44. Bland JM, Altman DG 1996 Statistics notes: transforming data. BMJ 312:770-771
45. Bland JM, Altman DG 1996 Statistics note: transforming means and confidence intervals. BMJ 312:1079
46. Schultz-Darken NJ, Pape RM, Tannenbaum PL, Saltzman W, Abbott DH 2004 Novel restraint system for neuroendocrine studies of socially living common marmoset monkeys. Lab Anim 38:393-405
47. Chen A, Yahalom D, Ben-Aroya N, Kaganovsky E, Okon E, Koch Y 1998 A second isoform of gonadotropin-releasing hormone is present in the brain of human and rodents. FEBS Lett 435:199-203
48. Gestrin ED, White RB, Fernald RD 1999 Second form of gonadotropin- releasing hormone in mouse: immunocytochemistry reveals hippocampal and periventricular distribution. FEBS Lett 448:289-291
49. King JA, Steneveld AA, Curlewis JD, Rissman EF, Millar RP 1994 Identification of chicken GnRH II in brains of metatherian and early-evolved eutherian species of mammals. Regul Pept 54:467-477
50. King JA, Steneveld AA, Millar RP 1994 Differential regional distribution of gonadotropin-releasing hormones in amphibian (clawed toad, Xenopus laevis) brain. Regul Pept 50:277-289
51. King JA, Millar RP 1997 Coordinated evolution of GnRHs and their receptors. In: Parhar IS, SakumaY, eds. GnRH neurons: gene to behavior. Tokyo: Brain Shuppan; 51-77
52. Sherwood NM, Lovejoy DA, Coe IR 1993 Origin of mammalian gonadotropin-releasing hormones. Endocr Rev 14:241-254
53. Sealfon SC, Weinstein H, Millar RP 1997 Molecular mechanisms of ligand interaction with the gonadotropin-releasing hormone receptor. Endocr Rev 18:180-205
54. White RB, Eisen JA, Kasten TL, Fernald RD 1998 Second gene for gonadotropin-releasing hormone in humans. Proc Natl Acad Sci USA 95:305-309
55. Millar RP, King JA 1988 Evolution of gonadotropin-releasing hormone: multiple usage of a peptide. News Physiol Sci 3:49-53
56. Volkoff H, Peter RE 1999 Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. Gen Comp Endocrinol 116:347-355
57. Maney DL, Richardson RD, Wingfield JC 1997 Central administration of chicken gonadotropin-releasing hormone-II enhances courtship behavior in a female sparrow. Horm Behav 32:11-18
58. Temple JL, Millar RP, Rissman EF 2003 An evolutionarily conserved form of gonadotropin-releasing hormone coordinates energy and reproductive behavior. Endocrinology 144:13-19
59. Illing N, Troskie BE, Nahorniak CS, Hapgood JP, Peter RE, Millar RP 1999 Two gonadotropin-releasing hormone receptor subtypes with distinct ligand selectivity and differential distribution in brain and pituitary in the goldfish (Carassius auratus). Proc Natl Acad Sci USA 96:2526-2531
60. Kauffman AS, Wills A, Millar RP, Rissman EF 2005 Evidence that the type-2 gonadotropin-releasing hormone (GnRH) receptor mediates the behavioral effects of GnRH-II on feeding and reproduction in musk shrews. J Neuroendocrinol 17:489-497
61. Rissman EF, Li X 1998 Sex differences in mammalian and chicken-II gonadotropin-releasing hormone immunoreactivity in musk shrew brain. Gen Comp Endocrinol 11293:346-355
62. Densmore VS, Urbanski HF 2004 Effect of 17β-estradiol on hypothalamic GnRH-II gene expression in the female rhesus macaque. J Mol Endocrinol 33:145-153
63. Chen A, Zi K, Laskar-Levy O, Koch Y 2002 The transcription of the hGnRH-I and hGnRH-II genes in human neuronal cells is differentially regulated by estrogen. J Mol Neurosci 18:67-76
64. Harlow CR, Hearn JP, Hodges JK 1984 Ovulation in the marmoset monkey: endocrinology, prediction and detection. J Endocrinol 103:17-24
65. Wallen K 2000 Risky business: social context and hormonal modulation of primate sexual desire. In: Wallen K, Schneider JE, eds. Reproduction in context: social and environmental influences on reproductive physiology and behavior. Cambridge, MA: MIT Press; 289-323
66. Laumann EO, Paik A, Rosen RC 1999 Sexual dysfunction in the United States: prevalence and predictors. JAMA 281:537-544
67. Basson R 2005 Women's sexual dysfunction: revised and expanded definitions. CMAJ 172:1327-1333
68. Writing Group for the Women's Health Initiative Investigators 2002 Risk and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288:321-333
69. Morgan K, Conklin D, Pawson AJ, Sellar R, Ott TR, Millar RP 2003 A transcriptionally active human type II gonadotropin-releasing hormone receptor gene homolog overlaps two genes in the antisense orientation on chromosome 1q. 12. Endocrinology 144:423-436
70. Neill JD 2004 Newly recognized GnRH receptors: function and relative role 2004. Trends Endocrinol Metab 15:383-392
71. Gault PM, Morgan K, Pawson AJ, Millar RP, Lincoln GA 2004 Sheep exhibit novel variations in the organization of the mammalian type II gonadotropin-releasing hormone receptor gene. Endocrinology 145:2362-2374
72. Grundker C, Schlotawa L, Viereck V, Eicke N, Horst A, Kairies B, Emons G 2004 Antiproliferative effects of GnRH antagonist cetrorelix and of GnRH-II on human endometrial and ovarian cancer cells are not mediated through the GnRH type I receptor. Eur J Endocrinol 151:141-149
73. Emons G, Gunthert AR, Grundker C 2005 Gonadotropin releasing hormone, gynecological cancers. Proceedings of the 86th Annual Meeting of the Endocrine Society, San Diego, 2005, pp 31-32 (Abstract S173)
74. Millar RP, Pawson AJ 2004 Outside-in and inside-out signaling: the new concept that selectivity of ligand binding at the gonadotropin-releasing hormone receptor is modulated by the intracellular environment. Endocrinology 145:3590-3593
75. Kelley DB 1982 Female sex behaviors in the South African clawed frog, Xenopus laevis: gonadotropin-releasing, gonadotropic and steroid hormones. Horm Behav 16:158-174
76. Troskie B, King JA, Millar RP, Peng YY, Kim J, Figueras H, Illing N 1997 Chicken GnRH II-like peptides and a GnRH receptor selective for chicken GnRH II in amphibian sympathetic ganglia. Neuroendocrinology 65:396-402
77. Troskie B, Illing N, Rumbak E, Sun YM, Hapgood J, Sealfon SC, Conklin D, Millar RP 1998 Identification of three putative GnRH receptor subtypes in vertebrates. Gen Comp Endocrinol 112:296-302
78. Proper CR, Moore FL 1991 Effects of courtship on brain gonadotropin hormone-releasing hormone and plasma steroid concentrations in a female amphibian (Taricha granulosa). Gen Comp Endocrinol 81:304-312
79. Alderete MR, Tokarz RR, Crews D 1980 Luteinizing hormone-releasing hormone and thyrotropin-releasing hormone induction of female sexual receptivity in the lizard, Anolis carolinensis. Neuroendocrinology 30:200-205
80. Cheng MF 1977 Role of gonadotropin releasing hormones in the reproductive behavior of female ring doves (Streptopelia risoria). J Endocrinol 74:37-45
81. Dudley CA, Vale W, Rivier J, Moss RL 1983 The effect of LHRH antagonist analogs and an antibody to LHRH on mating behavior in female rats. Peptides 2:393-396
82. Luttge WG, Sheets CS 1977 Further studies on the restoration of estrogen-induced sexual receptivity in ovariectomized mice treated with dihydrotestoterone: effects of progesterone, dihydroprogesterone and LH-RH. Pharmocol Biochem Behav 7:563-566
83. Schiml PA, Rissman EF 2000 Effects of gonadotropin-releasing hormones, corticotropin-releasing hormone, and vasopressin on female sexual behavior. Horm Behav 37:212-220
84. Caraty A, Delaleu B, Chesneau D, Fabre-Nys C 2002 Sequential role of E2 and GnRH for the expression of estrous behavior in ewes. Endocrinology 143:139-145
85. Neill JD, Duck LW, Sellers JC, Musgrove LC 2001 A gonadotropin-releasing hormone (GnRH) receptor specific for GnRH II in primates. Biochem Biophys Res Commun 282:1012-1018