Kisspeptin as a link between metabolism and reproduction: Evidences from rodent and primate studies

Metabolism: Clinical and Experimental

Volumn 62, Issue 7, 2013, Pages 898-910

  Wahab, Fazal ^a,b   Atika, Bibi ^a   Shahab, Muhammad ^a  

^a QUAID I AZAM UNIVERSITY   (Pakistan)

^b KHYBER MEDICAL UNIVERSITY   (Pakistan)

Author keywords

GnRH; GPR54; Kiss1; Kisspeptin; Metabolism; Reproduction; Rodent

Indexed keywords

ADIPONECTIN; DYNORPHIN A; G PROTEIN COUPLED RECEPTOR 54; GHRELIN; GLUCAGON; GLUCOSE; GONADOTROPIN; GROWTH HORMONE; HYDROCORTISONE; INSULIN; KISSPEPTIN; LEPTIN; LIOTHYRONINE; LUTEINIZING HORMONE; NEUROKININ B; OXYTOCIN; PROLACTIN; RESISTIN; THYROTROPIN; THYROXINE;

ARCUATE NUCLEUS; DIABETES MELLITUS; DIET RESTRICTION; ENERGY BALANCE; ESTRUS CYCLE; FEEDING; GONADOTROPIN RELEASE; HORMONAL REGULATION; HYPOTHALAMUS; LACTATION; LUTEINIZING HORMONE RELEASE; METABOLISM; NERVE CELL NETWORK; NONHUMAN; NUTRITIONAL DEFICIENCY; OBESITY; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPRODUCTION; REVIEW; RODENT; SATIETY; SIGNAL TRANSDUCTION;

ANIMALS; ENERGY METABOLISM; FEMALE; FOOD DEPRIVATION; GONADOTROPIN-RELEASING HORMONE; HUMANS; HYPOTHALAMUS; INFERTILITY; KISSPEPTINS; LACTATION; MALE; NEURONS; RECEPTORS, G-PROTEIN-COUPLED; REPRODUCTION; SIGNAL TRANSDUCTION;

EID: 84879554065     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2013.01.015     Document Type: Review

References (155)

1. G.N. Wade, and J.E. Jones Neuroendocrinology of nutritional infertility Am J Physiol Regul Integr Comp Physiol 287 6 2004 R1277 R1296
2. G.N. Wade, J.E. Schneider, and H.Y. Li Control of fertility by metabolic cues Am J Physiol Endocrinol Metab 270 1 Pt 1 1996 E1 E19
3. G.C. Kennedy, and J. Mitra Body-weight and food intake as initiating factors for puberty in the rat J Physiol 166 1963 408 418
4. D.L. Foster, and D.H. Olster Effects of restricted nutrition on puberty in the lamb: pattern of tonic luteinizing hormone (LH) secretion and competency of the LH surge system Endocrinology 116 1 1985 375 381
5. K.K. Schillo Effects of dietary energy on control of luteinizing hormone secretion in cattle and sheep J Anim Sci 70 4 1992 1271 1282
6. C.J. Gill, and E.F. Rissmann Female sexual behavior is inhibited by short- and long-term food restriction Physiol Behav 61 3 1997 387 394
7. D.B. Parfitt, K.R. Church, and J.L. Cameron Restoration of pulsatile LH secretion after fasting in rhesus monkeys (Macaca mulatta): dependence on size of the refeed meal Endocrinology 129 2 1991 749 756
8. M. Bergendahl, A. Perheentupa, and I. Huhtaniemi Starvation-induced suppression of pituitary-testicular function in rats is reversed by pulsatile gonadotropin-releasing hormone substitution Biol Reprod 44 3 1991 413 419
9. G.A. Campbell, M. Kurcz, and S. Marshall Effects of starvation in rats on serum levels of follicle stimulating hormone, luteinizing hormone, thyrotropin, growth hormone and prolactin; response to LH-releasing hormone and thyrotropin-releasing hormone Endocrinology 100 2 1977 580 587
10. J.L. Cameron, T.E. Weltzin, and C. McConaha Slowing of pulsatile luteinizing hormone secretion in men after forty-eight hours of fasting J Clin Endocrinol Metab 73 1 1991 35 41
11. J.A. Aloi, M. Bergendahl, and A. Iranmanesh Pulsatile intravenous gonadotropin-releasing hormone administration averts fasting-induced hypogonadotropism and hypoandrogenemia in healthy, normal weight men J Clin Endocrinol Metab 82 5 1997 1543 1548
12. A. Crown, D.K. Clifton, and R.A. Steiner Neuropeptide signaling in the integration of metabolism and reproduction Neuroendocrinology 86 3 2007 175 182
13. R. Fernandez-Fernandez, A.C. Martini, and V.M. Navarro Novel signals for the integration of energy balance and reproduction Mol Cell Endocrinol 254-255 2006 127 132
14. J. Hill, J.K. Elmquist, and C.F. Elias Hypothalamic pathways linking energy balance and reproduction Am J Physiol Endocrinol Metab 294 5 2008 E827 E832
15. H. Kageyama, F. Takenoya, and T. Kita Galanin-like peptide in the brain: effects on feeding, energy metabolism and reproduction Regul Pept 126 1-2 2005 21 26
16. K. Wynne, S. Stanley, and B. McGowan Appetite control J Endocrinol 184 2 2005 291 318
17. B.G. Stanley, and S.F. Leibowitz Neuropeptide Y injected in the paraventricular hypothalamus: a powerful stimulant of feeding behavior PNAS 82 11 1985 3940 3943
18. M. Rossi, S.J. Choi, and D. O'Shea Melanin-concentrating hormone acutely stimulates feeding, but chronic administration has no effect on body weight Endocrinology 138 1 1997 351 355
19. M.S. Kim, M. Rossi, and S. Abusnana Hypothalamic localization of the feeding effect of agouti-related peptide and alpha-melanocyte-stimulating hormone Diabetes 49 2 2000 177 182
20. V.S. Drescher, H.L. Chen, and D.R. Romsos Corticotropin-releasing hormone decreases feeding, oxygen consumption and activity of genetically obese (ob/ob) and lean mice J Nutr 124 4 1994 524 530
21. Y. Uehara, H. Shimizu, and K. Ohtani Hypothalamic corticotropin-releasing hormone is a mediator of the anorexigenic effect of leptin Diabetes 47 6 1998 890 893
22. C.M. Edwards, C.R. Abbott, and D. Sunter Cocaine- and amphetamine-regulated transcript, glucagon-like peptide-1 and corticotrophin releasing factor inhibit feeding via agouti-related protein independent pathways in the rat Brain Res 866 1-2 2000 128 134
23. B. Xu, P.S. Kalra, and W.G. Farmerie Daily changes in hypothalamic gene expression of neuropeptide Y, galanin, pro-opiomelanocortin, and adipocyte leptin gene expression and secretion: effects of food restriction Endocrinology 140 6 1999 2868 2875
24. C. Li, P. Chen, and M.S. Smith Corticotropin releasing hormone (CRH) neurons in the paraventricular nucleus (PVH) are direct targets for neuropeptide Y (NPY) neurons in the arcuate nucleus (ARH): an anterograde tracing study Brain Res 854 1-2 2000 122 129
25. T. Füzesi, G. Wittmann, and Z. Liposits Contribution of noradrenergic and adrenergic cell groups of the brainstem and agouti-related protein-synthesizing neurons of the arcuate nucleus to neuropeptide-y innervation of corticotropin-releasing hormone neurons in hypothalamic paraventricular nucleus of the rat Endocrinology 148 11 2007 5442 5450
26. M. Tena-Sempere Roles of ghrelin and leptin in the control of reproductive function Neuroendocrinology 86 3 2007 229 241
27. E. Valassi, M. Scacchi, and F. Cavagnini Neuroendocrine control of food intake Nutr Metab Cardiovasc Dis 18 2 2008 158 168
28. J. Jürimäe, J. Mäestu, and T. Jürimäe Peripheral signals of energy homeostasis as possible markers of training stress in athletes: a review Metabolism 60 3 2011 335 350
29. M.L. Gottsch, M.J. Cunningham, and J.T. Smith A role for kisspeptins in the regulation of gonadotropin secretion in the mouse Endocrinology 145 9 2004 4073 4077
30. M.S. Irwig, G.S. Fraley, and J.T. Smith Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat Neuroendocrinology 80 4 2004 264 272
31. A.M. Rometo, S.J. Krajewski, and M.L. Voytko Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys J Clin Endocrinol Metab 92 7 2007 2744 2750
32. M. Shahab, C. Mastronardi, and S.B. Seminara Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates PNAS 102 2 2005 2129 2134
33. J.T. Smith, B.V. Acohido, and D.K. Clifton KiSS-1 neurones are direct targets for leptin in the ob/ob mouse J Neuroendocrinol 18 4 2006 298 303
34. J.T. Smith, M.J. Cunningham, and E.F. Rissman Regulation of KiSS-1 gene expression in the brain of the female mouse Endocrinology 146 9 2005 3686 3692
35. F. Wahab, F. Ullah, and Y.M. Chan Decrease in hypothalamic Kiss1 and Kiss1r expression: a potential mechanism for fasting-induced suppression of the HPG axis in the adult male rhesus monkey (Macaca mulatta) Horm Metab Res 43 2 2011 81 85
36. E.L. Thompson, M. Patterson, and K.G. Murphy Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis J Neuroendocrinol 16 10 2004 850 858
37. J.M. Castellano, V.M. Navarro, and R. Fernandez-Fernandez Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition Endocrinology 146 9 2005 3917 3925
38. J.M. Castellano, V.M. Navarro, and R. Fernandez-Fernandez Expression of hypothalamic KiSS-1 system and rescue of defective gonadotropic responses by kisspeptin in streptozotocin-induced diabetic male rats Diabetes 55 9 2006 2602 2610
39. R.E. Brown, S.A. Imran, and E. Ur KiSS-1 mRNA in adipose tissue is regulated by sex hormones and food intake Mol Cell Endocrinol 281 1-2 2008 64 72
40. R.M. Luque, R.D. Kineman, and M. Tena-Sempere Regulation of hypothalamic expression of KiSS-1 and GPR54 genes by metabolic factors: Analyses using mouse models and a cell line Endocrinology 148 10 2007 4601 4611
41. J.L. Cameron, and C. Nosbisch Slowing of pulsatile LH and testosterone secretion during short-term fasting in adult male rhesus monkeys (Macaca mulatta) Endocrinology 128 3 1991 1532 1540
42. J.L. Cameron Regulation of reproductive hormone secretion in primates by short-term changes in nutrition Rev Reprod 1 2 1996 117 126
43. F. Wahab, F. Aziz, and S. Irfan Short-term fasting attenuates the response of the HPG axis to kisspeptin challenge in the adult male rhesus monkey (Macaca mulatta) Life Sci 83 19-20 2008 633 637
44. M. Kotani, M. Detheux, and A. Vandenbogaerde The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54 J Biol Chem 276 37 2001 34631 34636
45. J.H. Lee, M.E. Miele, and D.J. Hicks KiSS-1, a novel malignant melanoma metastasis-suppressor gene J Natl Cancer Inst 88 23 1996 1731 1737
46. A.I. Muir, L. Chamberlain, and N.A. Elshourbagy AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1 J Biol Chem 276 31 2001 28969 28975
47. T. Ohtaki, Y. Shintani, and S. Honda Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor Nature 411 6837 2001 613 617
48. E. Gutiérrez-Pascual, A.J. Martínez-Fuentes, and L. Pinilla Direct pituitary effects of kisspeptin: activation of gonadotrophs and somatotrophs and stimulation of luteinising hormone and growth hormone secretion J Neuroendocrinol 19 7 2007 521 530
49. A.C. Hauge-Evans, C.C. Richardson, and H.M. Milne A role for kisspeptin in islet function Diabetologia 49 9 2006 2131 2135
50. H. Kadokawa, M. Matsui, and K. Hayashi Peripheral administration of kisspeptin-10 increases plasma concentrations of GH as well as LH in prepubertal Holstein heifers J Endocrinol 196 2 2008 331 334
51. H. Kadokawa, S. Suzuki, and T. Hashizume Kisspeptin-10 stimulates the secretion of growth hormone and prolactin directly from cultured bovine anterior pituitary cells Anim Reprod Sci 105 3-4 2008 404 408
52. Y. Nakamura, S. Aoki, and Y. Xing Metastin stimulates aldosterone synthesis in human adrenal cells Reprod Sci 14 8 2007 836 845
53. R.A. Silvestre, E.M. Egido, and R. Hernández Kisspeptin-13 inhibits insulin secretion without affecting glucagon or somatostatin release: study in the perfused rat pancreas J Endocrinol 196 2 2008 283 290
54. F. Wahab, R. Bano, and S. Jabeen Effect of peripheral kisspeptin administration on adiponectin, leptin, and resistin secretion under fed and fasting condition in the adult male rhesus monkey (Macaca mulatta) Horm Metab Res 42 8 2010 570 574
55. F. Wahab, R. Tanzeela, and M. Shahab Study of the effect of peripheral kisspeptin administration on basal and glucose-induced insulin secretion under fed and fasting conditions in the adult male rhesus monkey (Macaca mulatta) Horm Metab Res 43 1 2011 37 42
56. T.M. Plant The role of KiSS-1 in the regulation of puberty in higher primates Eur J Endocrinol 155 Suppl 1 2006 S11 S16
57. J.H. Lee, and D.R. Welch Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-1 Cancer Res 57 12 1997 2384 2387
58. A. West, P.J. Vojta, and D.R. Welch Chromosome localization and genomic structure of the KiSS-1 metastasis suppressor gene (KISS1) Genomics 54 1 1998 145 148
59. M.L. Gottsch, D.K. Clifton, and R.A. Steiner From KISS1 to kisspeptins: An historical perspective and suggested nomenclature Peptides 30 1 2009 4 9
60. Y. Terao, S. Kumano, and Y. Takatsu Expression of KiSS-1, a metastasis suppressor gene, in trophoblast giant cells of the rat placenta Biochim Biophys Acta 1678 2-3 2004 102 110
61. D.K. Lee, T. Nguyen, and G.P. O'Neill Discovery of a receptor related to the galanin receptors FEBS Lett 446 1 1999 103 107
62. J.M. Castellano, V.M. Navarro, and R. Fernandez-Fernandez Ontogeny and mechanisms of action for the stimulatory effect of kisspeptin on gonadotropin-releasing hormone system of the rat Mol Cell Endocrinol 257-258 2006 75 83
63. S.L. Dun, G.C. Brailoiu, and A. Parsons Metastin-like immunoreactivity in the rat medulla oblongata and spinal cord Neurosci Lett 335 3 2003 197 201
64. G.C. Brailoiu, S.L. Dun, and M. Ohsawa KiSS-1 expression and metastin-like immunoreactivity in the rat brain J Comp Neurol 481 3 2005 314 329
65. S. Ramaswamy, K.A. Guerriero, and R.B. Gibbs Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy Endocrinology 149 9 2008 4387 4395
66. M. Shibata, R.B. Gibbs, and M. Shahab GnRH neurons in the peripubertal male rhesus monkey (Macaca mulatta) express GPR54: Implication for the control of primate puberty Program of the 87th Annual Meeting of the Endocrine Society, San Diego, CA, USA 2005 1 98 [abstract]
67. M. Shibata, R.L. Friedman, and S. Ramaswamy Evidence that down regulation of hypothalamic KiSS-1 expression is involved in the negative feedback action of testosterone to regulate luteinising hormone secretion in the adult male rhesus monkey (Macaca mulatta) J Neuroendocrinol 19 6 2007 432 438
68. J. Clarkson, and A.E. Herbison Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons Endocrinology 147 12 2006 5817 5825
69. I. Franceschini, D. Lomet, and M. Cateau Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor α Neurosci Lett 401 3 2006 225 230
70. S. Pompolo, A. Pereira, and K.M. Estrada Colocalization of kisspeptin and gonadotropin-releasing hormone in the ovine brain Endocrinology 147 2 2006 804 810
71. J.T. Smith, H.M. Dungan, and E.A. Stoll Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse Endocrinology 146 7 2005 2976 2984
72. C.F. Elias, C.B. Saper, and E. Maratos-Flier Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area Comp J Neurol 402 4 1998 442 459
73. J.K. Elmquist, E. Maratos-Flier, and C.B. Saper Unraveling the central nervous system pathways underlying responses to leptin Nat Neurosci 1 6 1998 445 450
74. W.-P. Chen, J.W. Witkin, and A.-J. Silverman β-Endorphin and gonadotropin releasing hormone synaptic input to gonadotropin-releasing hormone neurosecretory cells in the male rat J Comp Neurol 286 1 1989 85 95
75. C. Li, P. Chen, and M.S. Smith Morphological evidence for direct interaction between arcuate nucleus neuropeptide Y (NPY) neurons and gonadotropin releasing hormone (GnRH) neurons and the possible involvement of NPY Y1 receptors Endocrinology 140 11 1999 5382 5390
76. S. Messager, E.E. Chatzidaki, and D. Ma Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54 PNAS 102 5 2005 1761 1766
77. M. Wu, I. Dumalska, and E. Morozova Melanin-concentrating hormone directly inhibits GnRH neurons and blocks kisspeptin activation, linking energy balance to reproduction PNAS 106 40 2009 17217 17222
78. K. Backholer, J.T. Smith, and A. Rao Kisspeptin cells in the ewe brain respond to leptin and communicate with neuropeptide Y and proopiomelanocortin cells Endocrinology 151 5 2010 2233 2243
79. M. Kinoshita, H. Tsukamura, and S. Adachi Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats Endocrinology 146 10 2005 4431 4436
80. M. Patterson, K.G. Murphy, and E.L. Thompson Administration of kisspeptin-54 into discrete regions of the hypothalamus potently increases plasma luteinising hormone and testosterone in male adult rats J Neuroendocrinol 18 5 2006 349 354
81. J. Pielecka-Fortuna, Z. Chu, and S.M. Moenter Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol Endocrinology 149 4 2008 1979 1986
82. L.Y. Fu, and A.N. van den Pol Kisspeptin directly excites anorexigenic proopiomelanocortin neurons but inhibits orexigenic neuropeptide Y cells by an indirect synaptic mechanism J Neurosci 30 30 2010 10205 10219
83. R.L. Goodman, M.N. Lehman, and J.T. Smith Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B Endocrinology 148 12 2007 5752 5760
84. G.P. Frenkel, Z.T. Homonnai, and N. Drasnin Fertility of the streptozotocin-diabetic male rat Andrologia 10 2 1978 127 136
85. B.E. Howland, and E.J. Zebrowski Some effects of experimentally-induced diabetes on pituitary-testicular relationships in rats Horm Metab Res 8 6 1976 465 469
86. B.E. Howland, and E.J. Zebrowski Pituitary response to gonadotropin-releasing hormone in diabetic male rats Experientia 36 5 1980 610 611
87. F. Wahab, U. Zaman, and M. Shahab Differential response of the primate HPG axis to N-methyl-D, L- aspartate but not to kisspeptin challenge under euglycemic and hypoglycemic condition Horm Metab Res 44 6 2012 451 457
88. J.S. Kinsey-Jones, X.F. Li, and A.M. Knox Down-regulation of hypothalamic kisspeptin and its receptor, Kiss1r, mRNA expression is associated with stress-induced suppression of luteinising hormone secretion in the female rat J Neuroendocrinol 21 1 2009 20 29
89. S. Yamada, Y. Uenoyama, and M. Kinoshita Inhibition of metastin (kisspeptin-54)-GPR54 signaling in the arcuate nucleus-median eminence region during lactation in rats Endocrinology 148 2007 2226 2232
90. J. Roa, E. Vigo, and J.M. Castellano Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat Endocrinology 147 6 2006 2864 2878
91. J.H. Quennell, C.S. Howell, and J. Roa Leptin deficiency and diet-induced obesity reduce hypothalamic kisspeptin expression in mice Endocrinology 152 4 2011 1541 1550
92. T. Matsuzaki, T. Iwasa, and R. Kinouchi Fasting reduces the kiss1 mRNA levels in the caudal hypothalamus of gonadally intact adult female rats Endocr J 58 11 2011 1003 1012
93. J. Lado-Abeal, J.R. Hickox, and T.L. Cheung Neuroendocrine consequences of fasting in adult male macaques: effects of recombinant rhesus macaque leptin infusion Neuroendocrinology 71 3 2000 196 208
94. J. Lado-Abeal, J.D. Veldhuis, and R.L. Norman Glucose relays information regarding nutritional status to the neural circuits that control the somatotropic, corticotropic, and gonadotropic axes in adult male rhesus macaques Endocrinology 143 2 2002 403 410
95. J. Lado-Abeal, J.J. Robert-McComb, and X.-P. Qian Sex differences in the neuroendocrine response to Short-term fasting in rhesus macaques J Neuroendocrinol 17 7 2005 435 444
96. M. Kinoshita, R. Moriyama, and H. Tsukamura A rat model for the energetic regulation of gonadotropin secretion: role of the glucose-sensing mechanism in the brain Domest Anim Endocrinol 25 1 2003 109 120
97. M. Shahab, W. Zaman, and K. Bashir Fasting-induced suppression of hypothalamic-pituitary-gonadal axis in the adult rhesus monkey: evidence for involvement of excitatory amino acid neurotransmitters Life Sci 61 13 1997 1293 1300
98. S. Forbes, X.F. Li, and J. Kinsey-Jones Effects of ghrelin on Kisspeptin mRNA expression in the hypothalamic medial preoptic area and pulsatile luteinising hormone secretion in the female rat Neurosci Lett 460 2 2009 143 147
99. M.S. Smith, and K.L. Grove Integration of the regulation of reproductive function and energy balance: lactation as a model Front Neuroendocrinol 23 3 2002 225 256
100. J.A. Russell, A.J. Douglas, and C.D. Ingram Brain preparations for maternity adaptive changes in behavioral and neuroendocrine systems during pregnancy and lactation. An overview Prog Brain Res 133 2001 1 38
101. A.S. McNeilly, C.C. Tay, and A. Glasier Physiological mechanisms underlying lactational amenorrhea (Review) Ann N Y Acad Sci 709 1994 145 155
102. R.L. Lee, S.J. Paul, and M.S. Smith Dose response effects of pulsatile GnRH administration on restoration of pituitary GnRH receptors and pulsatile LH secretion during lactation Neuroendocrinology 49 6 1989 664 668
103. T.M. Plant, E. Schallenberger, and D.L. Hess Influence of suckling on gonadotropin secretion in the female rhesus monkey (Macaca mulatta) Biol Reprod 23 4 1980 760 766
104. K. Taya, and S. Sasamoto Mechanisms responsible for suppression of FSH and LH during lactation in the rat J Endocrinol 129 1 1991 119 130
105. S.R. Fox, and M.S. Smith The suppression of pulsatile LH secretion during lactation in the rat Endocrinology 115 6 1984 2045 2051
106. E. Knobil Patterns of hypophysiotropic signals and gonadotropin secretion in the rhesus monkey Biol Reprod 24 1 1981 44 49
107. E. Knobil, T.M. Plant, and L. Wildt Control of the rhesus monkey menstrual cycle: permissive role of hypothalamic gonadotropin-releasing hormone Science 207 4437 1980 1371 1373
108. T. Ordog, M.D. Chen, and K.T. O'Byrne On the mechanism of lactational anovulation in the rhesus monkey Am J Physiol Endocrinol Metab 274 4 Pt 1 1998 E665 E676
109. A.S. McNeilly Suckling and the control of gonadotropin secretion E. Knobil, J.D. Neill, 2nd ed. The physiology of Reproduction Vol. 2 1994 Raven press New York 179 182
110. R.G. Denis, G. Williams, and R.G. Vernon Regulation of serum leptin and its role in the hyperphagia of lactation in the rat J Endocrinol 176 2 2003 193 203
111. D.L. Marks, M.S. Smith, and D.K. Clifton Regulation of GnRH and galanin gene expression in GnRH neurons during lactation in the rat Endocrinology 133 3 1993 1450 1455
112. M.S. Smith A comparison of pituitary responsiveness to luteinizing hormone-releasing hormone during lactation and the estrous cycle of the rat Endocrinology 102 1 1978 121 127
113. M.S. Smith Hypthalamic responsiveness during lactation in the rat: luteinizing hormone release after electrochemical stimulation Biol Reprod 27 1 1982 125 131
114. C.R. Pohl, L.R. Lee, and M.S. Smith Qualitative changes in luteinizing hormone and prolactin responses to N-methyl-d-aspartic acid during lactation in the rat Endocrinology 124 4 1989 1905 1910
115. M.P. Cleary, H.M. Bergstrom, and T.L. Dodge Restoration of fertility in young obese (Lep(ob) Lep(ob)) male mice with low dose recombinant mouse leptin treatment Int J Obes Relat Metab Disord 25 1 2001 95 97
116. K. Mounzih, R. Lu, and F.F. Chehab Leptin treatment rescues the sterility of genetically obese ob/ob males Endocrinology 138 3 1997 1190 1193
117. F.F. Chehab, M.E. Lim, and R. Lu Correction of the sterility defect in homozygous obese female mice by treatment with human recombinant leptin Nat Genet 12 3 1996 318 320
118. R.N. Arison, E.I. Ciaccio, and M.S. Glitzer Light and electron microscopy of lesions in rats rendered diabetic with streptozotocin Diabetes 16 1 1967 51 56
119. W.J. Sexton, and J.P. Jarow Effect of diabetes mellitus upon male reproductive function Urology 49 1997 508 513
120. M. Spindler-Vomachka, and D.C. Johnson Altered hypothalamic-pituitary function in the adult female rat with streptozotocin-induced diabetes Diabetologia 28 1 1985 38 44
121. R.W. Clough, S.G. Kienast, and R.W. Steger Reproductive endocrinopathy in acute streptozotocin-induced diabetic male rats: studies on LHRH Endocrine 8 1 1998 37 43
122. L. Seethalakshmi, M. Menon, and D. Diamond The effect of streptozotocin-induced diabetes on the neuroendocrine male reproductive tract axis of the adult rat J Urol 138 1 1987 190 194
123. G. Bestetti, V. Locatelli, and F. Tirone One month of streptozotocin-diabetes induces different neuroendocrine and morphological alterations in the hypothalamo-pituitary axis of male and female rats Endocrinology 117 1 1985 208 216
124. J.T. George, J.D. Veldhuis, and M. Tena-Sempere Exploring the pathophysiology of hypogonadism in men with type 2 diabetes: Kisspeptin-10 stimulates serum testosterone and LH secretion in men with type 2 diabetes and mild biochemical hypogonadism Clin Endocrinol (Oxf) 2012 10.1111/cen.12103
125. T.A. Dardeno, S.H. Chou, and H.S. Moon Leptin in human physiology and therapeutics Front Neuroendocrinol 31 3 2010 377 393
126. G. Boden, X. Chen, and M. Mozzoli Effect of fasting on serum leptin in normal human subjects J Clin Endocrinol Metab 81 9 1996 3419 3423
127. J.W. Kolaczynski, R.V. Considine, and J. Ohannesian Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketones themselves Diabetes 45 11 1996 1511 1515
128. J.L. Chan, K. Heist, and A.M. DePaoli The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men J Clin Invest 111 9 2003 1409 1421
129. J.L. Chan, and C.S. Mantzoros Role of leptin in energy-deprivation states: normal human physiology and clinical implications for hypothalamic amenorrhoea and anorexia nervosa Lancet 366 9479 2005 74 85
130. S. Moschos, J.L. Chan, and C.S. Mantzoros Leptin and reproduction: a review Fertil Steril 77 3 2002 433 444
131. P.D. Finn, M.J. Cunningham, and K.Y. Pau The stimulatory effect of leptin on the neuroendocrine reproductive axis of the monkey Endocrinology 139 11 1998 4652 4662
132. F. Magkos, A. Brennan, and L. Sweeney Leptin replacement improves postprandial glycemia and insulin sensitivity in human immunodeficiency virus-infected lipoatrophic men treated with pioglitazone: a pilot study Metabolism 60 7 2011 1045 1049
133. M.L. Barker-Gibb, A. Sahu, and C.R. Pohl Elevating circulating leptin in prepubertal male rhesus monkeys (Macaca mulatta) does not elicit precocious gonadotropin-releasing hormone release, assessed indirectly J Clin Endocrinol Metab 87 11 2002 4976 4983
134. A. Strobel, T. Issad, and L. Camoin A leptin missense mutation associated with hypogonadism and morbid obesity Nat Genet 18 3 1998 213 215
135. I.S. Farooqi, S.A. Jebb, and G. Langmack Effects of recombinant leptin therapy in a child with congenital leptin deficiency N Engl J Med 341 12 1999 879 884
136. I.S. Farooqi, G. Matarese, and G.M. Lord Beneficial effects of leptin on obesity, T cell hyporesponsiveness, and neuroendocrine/metabolic dysfunction of human congenital leptin deficiency J Clin Invest 110 8 2002 1093 1103
137. J. Licinio, S. Caglayan, and M. Ozata Phenotypic effects of leptin replacement on morbid obesity, diabetes mellitus, hypogonadism, and behavior in leptin-deficient adults PNAS 101 13 2004 4531 4536
138. M.L. Hâkansson, H. Brown, and N. Ghilardi Leptin receptor immunoreactivity in chemically defined target neurons of the hypothalamus J Neurosci 18 1 1998 559 572
139. J.H. Quennell, A.C. Mulligan, and A. Tups Leptin indirectly regulates gonadotropin-releasing hormone neuronal function Endocrinology 150 6 2009 2805 2812
140. R.M. Luque, J. Córdoba-Chacón, and M.D. Gahete Kisspeptin regulates gonadotroph and somatotroph function in nonhuman primate pituitary via common and distinct signaling mechanisms Endocrinology 152 3 2011 957 966
141. R.L. Goodman, and M.N. Lehman Kisspeptin neurons from mice to men: similarities and differences Endocrinology 153 11 2012 5105 5118
142. J.T. George, and S.B. Seminara Kisspeptin and the hypothalamic control of reproduction: lessons from the human Endocrinology 153 11 2012 5130 5136
143. H.M. Dungan Lemko, and C.F. Elias Kiss of the mutant mouse: how genetically altered mice advanced our understanding of kisspeptin's role in reproductive physiology Endocrinology 153 11 2012 5119 5129
144. F. Wahab, R. Quinton, and S.B. Seminara The kisspeptin signaling pathway and its role in human isolated GnRH deficiency Mol Cell Endocrinol 346 1-2 2011 29 36
145. Y.M. Chan, S. Broder-Fingert, and S. Paraschos GnRH-deficient phenotypes in humans and mice with heterozygous variants in KISS1/Kiss1 J Clin Endocrinol Metab 96 11 2011 E1771 E1781
146. S. Irfan, M. Anees, and F. Wahab Evidence for a direct intratesticular action of kisspeptin in the adult rhesus monkey (Macaca mulatta) Program of the 90th annual meeting of the Endocrine Society, San Francisco, CA, USA 2008 OR52 OR56 [abstract]
147. F.M. Pinto, A. Cejudo-Román, and C.G. Ravina Characterization of the kisspeptin system in human spermatozoa Int J Androl 35 1 2012 63 73
148. A. Cejudo Roman, F.M. Pinto, and I. Dorta Analysis of the expression of neurokinin B, kisspeptin, and their cognate receptors NK(3)R and KISS1R in the human female genital tract Fertil Steril 97 5 2012 1213 1219
149. S. Ramaswamy, R.B. Gibbs, and T.M. Plant Studies of the localisation of kisspeptin within the pituitary of the rhesus monkey (Macaca mulatta) and the effect of kisspeptin on the release of non-gonadotropic pituitary hormones J Neuroendocrinol 21 10 2009 795 804
150. Y.S. Rao, N.N. Mott, and T.R. Pak Effects of kisspeptin on parameters of the HPA axis Endocrine 39 3 2011 220 228
151. G. Neal-Perry, D. Lebesgue, and M. Lederman 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 8 2009 3699 3708
152. C. True, M.A. Kirigiti, and P. Kievit Leptin is not the critical signal for kisspeptin or luteinising hormone restoration during exit from negative energy balance J Neuroendocrinol 23 11 2011 1099 1112
153. M.A. Boyle, and S.L. Roth Personal nutrition 7th ed. 2008 Wadsworth Cengage Learning Belmont, CA, USA
154. M. Tena-Sempere Endocrinology and adolescence: deciphering puberty: novel partners, novel mechanisms Eur J Endocrinol 167 6 2012 733 747
155. R.M. Reynolds, J.J. Logie, and A.K. Roseweir A role for kisspeptins in pregnancy: facts and speculations Reproduction 138 1 2009 1 7