Socially regulated reproductive development: Analysis of GnRH-1 and kisspeptin neuronal systems in cooperatively breeding naked mole-rats (Heterocephalus glaber)

Journal of Comparative Neurology

Volumn 521, Issue 13, 2013, Pages 3003-3029

  Zhou, Shuzhi ^a   Holmes, Melissa M ^b   Forger, Nancy G ^c   Goldman, Bruce D ^d   Lovern, Matthew B ^e   Caraty, Alain ^f   Kalló, Imre ^a,g   Faulkes, Christopher G ^h   Coen, Clive W ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TORONTO   (Canada)

^c GEORGIA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF CONNECTICUT   (United States)

^e OKLAHOMA STATE UNIVERSITY   (United States)

^f CEMAGREF   (France)

^g INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^h QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Anteroventral periventricular nucleus; Arcuate nucleus; Cooperation; Dorsomedial hypothalamic nucleus; Estradiol; Eusociality; GnRH 1; Heterocephalus glaber; Kisspeptin; Naked mole rat; Progesterone; Reproductive suppression; RP3V; Social behavior; Social status; Testosterone

Indexed keywords

ESTRADIOL; GNRH 1; GONADOTROPIN; KISSPEPTIN; PROGESTERONE; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; FEMALE; HORMONE ACTION; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; MALE; MOLE RAT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; ORGANOGENESIS; PHYLOGENY; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REPRODUCTIVE SYSTEM DEVELOPMENT; SEX DIFFERENCE; TESTOSTERONE BLOOD LEVEL; UPREGULATION;

ANTEROVENTRAL PERIVENTRICULAR NUCLEUS; ARCUATE NUCLEUS; COOPERATION; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; ESTRADIOL; EUSOCIALITY; GNRH-1; HETEROCEPHALUS GLABER; KISSPEPTIN; NAKED MOLE-RAT; PROGESTERONE; REPRODUCTIVE SUPPRESSION; RP3V; SOCIAL BEHAVIOR; SOCIAL STATUS; TESTOSTERONE;

ANIMALS; BODY WEIGHT; BRAIN; CASTRATION; CELL COUNT; COOPERATIVE BEHAVIOR; ESTRADIOL; FEMALE; KISSPEPTINS; MALE; MOLE RATS; NEURONS; PROGESTERONE; RADIOIMMUNOASSAY; RECEPTORS, LHRH; SEXUAL BEHAVIOR, ANIMAL; TESTOSTERONE;

EID: 84880592443     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23327     Document Type: Article

References (138)

1. Abbott DH, Hodges JK, George LM. 1988. Social status controls LH secretion and ovulation in female marmoset monkeys (Callithrix jacchus). J Endocrinol 117:329-339.
2. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y, Tsukamura H, Inoue K, Maeda K. 2007. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 53:367-378.
3. Anthony EL, King JC, Stopa EG. 1984. Immunocytochemical localization of LHRH in the median eminence, infundibular stalk, and neurohypophysis. Evidence for multiple sites of releasing hormone secretion in humans and other mammals. Cell Tissue Res 236:5-14.
4. Bennett NC, Jarvis JUM. 1988. The social structure and reproductive biology of colonies of the mole-rat, Cryptomys damarensis (Rodentia: Bathyergidae). J Mammal 69:293-302.
5. Bennett NC, Jarvis JUM, Faulkes CG, Millar RP. 1993. LH responses to single doses of exogenous GnRH by freshly captured Damaraland molerats, Cryptomys damarensis. J Reprod Fertil 99:81-86.
6. Bentsen AH, Ansel L, Simonneaux V, Tena-Sempere M, Juul A, Mikkelsen JD. 2010. Maturation of kisspeptinergic neurons coincides with puberty onset in male rats. Peptides 31:275-283.
7. Bosch MA, Xue C, Rønnekleiv OK. 2012. Kisspeptin expression in guinea pig hypothalamus: effects of 17β-estradiol. J Comp Neurol 520:2143-2162.
8. Brett RA. 1991. The population structure of naked mole-rat colonies. In: Sherman PW, Jarvis JUM, Alexander RD, editors. The biology of the naked mole-rat. Princeton, NJ: Princeton University Press. p 97-136.
9. Buffenstein R. 2008. Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Comp Physiol B 178:439-445.
10. Cao J, Patisaul HB. 2011. Sexually dimorphic expression of hypothalamic estrogen receptors α and β and Kiss1 in neonatal male and female rats. J Comp Neurol 519:2954-2977.
11. Clarke FM, Faulkes CG. 1997. Dominance and queen succession in eusocial colonies of the naked mole-rat (Heterocephalus glaber). Proc R Soc Lond B 264:993-1000.
12. Clarke FM, Faulkes CG. 1998. Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. Proc Biol Sci 265:1391-1399.
13. Clarkson J, Herbison AE. 2006. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 147:5817-5825.
14. Clarkson J, d'Anglemont de Tassigny X, Moreno AS, Colledge WH, Herbison AE. 2008. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 28:8691-8697.
15. Clarkson J, d'Anglemont de Tassigny X, Colledge WH, Caraty A, Herbison AE. 2009. Distribution of kisspeptin neurones in the adult female mouse brain. J Neuroendocrinol 21:673-682.
16. Clarkson J, Han SK, Liu X, Lee K, Herbison AE. 2010. Neurobiological mechanisms underlying kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty. Mol Cell Endocrinol 324:45-50.
17. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15.
18. D'Anglemont de Tassigny X, Colledge WH. 2010. The role of kisspeptin signaling in reproduction. Physiology 25:207-217.
19. D'Anglemont de Tassigny X, Fagg LA, Dixon JP, Day K, Leitch HG, Hendrick AG, Zahn D, Franceschini I, Caraty A, Carlton MB, Aparicio SA, Colledge WH. 2007. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc Natl Acad Sci U S A 104:10714-10719.
20. De Roux N, Genin E, Carel J, Matsuda F, Chaussain J, Milgrom E. 2003. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 100:10972-10976.
21. Decourt C, Tillet Y, Caraty A, Franceschini I, Briant C. 2008. Kisspeptin immunoreactive neurons in the equine hypothalamus Interactions with GnRH neuronal system. J Chem Neuroanat 36:131-137.
22. Desroziers E, Mikkelsen J, Simonneaux V, Keller M, Tillet Y, Caraty A, Franceschini I. 2010. Mapping of kisspeptin fibres in the brain of the pro-oestrous rat. J Neuroendocrinol 22:1101-1112.
23. Du Toit L, Bennett NC, Katz AA, Kalló I, Coen CW. 2006. Relations between social status and the gonadotrophin-releasing hormone system in females of two cooperatively breeding species of African mole-rats, Cryptomys hottentotus hottentotus and Cryptomys hottentotus pretoriae: neuroanatomical and neuroendocrinological studies. J Comp Neurol 494:303-313.
24. Ebling FJ. 2010. Photoperiodic regulation of puberty in seasonal species. Mol Cell Endocrinol 324:95-101.
25. El Ouezzani S, Tramu G, Magoul R. 2000. The gonadotropin-releasing hormone neurosecretory system of the jerboa (Jaculus orientalis) and its seasonal variations. J Neuroendocrinol 12:1205-1212.
26. Faulkes CG, Abbott DH. 1991. Social control of reproduction in breeding and non-breeding male naked mole-rats (Heterocephalus glaber). J Reprod Fertil 93:427-435.
27. Faulkes CG, Abbott DH. 1993. Evidence that primer pheromones do not cause social suppression of reproduction in male and female naked mole-rats (Heterocephalus glaber). J Reprod Fertil 9:225-230.
28. Faulkes CG, Abbott DH, Jarvis JU. 1990a. Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber. J Reprod Fertil 88:559-568.
29. Faulkes CG, Abbott DH, Jarvis JU, Sherriff FE. 1990b. LH responses of female naked mole-rats, Heterocephalus glaber, to single and multiple doses of exogenous GnRH. J Reprod Fertil 89:317-323.
30. Faulkes CG, Abbott DH, Jarvis JU. 1991. Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber. J Reprod Fertil 91:593-604.
31. Faulkes CG, Trowell SN, Jarvis JU, Bennett NC. 1994. Investigation of numbers and motility of spermatozoa in reproductively active and socially suppressed males of two eusocial African mole-rats, the naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Cryptomys damarensis). J Reprod Fertil 100:411-416.
32. Faulkes CG, Bennett NC, Bruford MW, O'Brien HP, Aguilar GH, Jarvis JUM. 1997. Ecological constraints drive social evolution in the African mole-rats. Proc R Soc Lond B 264:1619-1627.
33. Feder HH, Resko JA, Goy RW. 1968. Progesterone concentrations in the arterial plasma of guinea-pigs during the oestrous cycle. J Endocrinol 40:505-513.
34. Fernandez AM, Muniz E, Gragera RR, Martinez-Rodriguez R. 1992. Immunocytochemical localization of GnRH in the hypothalamus of the bat Miniopterus schreibersii schreibersii. J Hirnforsch 33:195-202.
35. 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 alpha. Neurosci Lett 401:225-230.
36. Funes S, Hedrick J, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma F, Gustafson E. 2003. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 312:1357-1363.
37. Glass JD. 1986. Short photoperiod-induced gonadal regression: effects on the gonadotropin-releasing hormone (GnRH) neuronal system of the white-footed mouse, Peromyscus leucopus. Biol Reprod 35:733-743.
38. Goldman SL, Forger NG, Goldman BD. 2006. Influence of gonadal sex hormones on behavioral components of the reproductive hierarchy in naked mole-rats. Horm Behav 50:77-84.
39. Goodman RL, Lehman MN. 2012. Kisspeptin neurons from mice to men: similarities and differences. Endocrinology 153:5105-5118.
40. Gottsch M, Cunningham M, Smith J, Popa S, Acohido B, Crowley W, Seminara S, Clifton D, Steiner R. 2004. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073-4077.
41. Greives TJ, Mason AO, Scotti MA, Levine J, Ketterson ED, Kriegsfeld LJ, Demas GE. 2007. Environmental control of kisspeptin: implications for seasonal reproduction. Endocrinology 148:1158-1166.
42. Greives TJ, Humber SA, Goldstein AN, Scotti MA, Demas GE, Kriegsfeld LJ. 2008. Photoperiod and testosterone interact to drive seasonal changes in kisspeptin expression in Siberian hamsters (Phodopus sungorus). J Neuroendocrinol 20:1339-1347.
43. Gross DS. 1984. The mammalian hypophysial pars tuberalis: a comparative immunocytochemical study. Gen Comp Endocrinol 56:283-298.
44. Guillery RW, Herrup K. 1997. Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2-7.
45. Hahn JD, Coen CW. 2006. A comparative study of the sources of neuronal projections to the site of gonadotrophin-releasing hormone perikarya and to the anteroventral periventricular nucleus in female rats. J Comp Neurol 494:190-214.
46. Hahn JD, Kalamatianos T, Coen CW. 2003. Studies on the neuroanatomical basis for stress-induced oestrogen-potentiated suppression of reproductive function: evidence against direct corticotropin-releasing hormone projections to the vicinity of luteinizing hormone-releasing hormone cell bodies in female rats. J Neuroendocrinol 15:732-742.
47. Halasz B, Gorski RA. 1967. Gonadotrophic hormone secretion in female rats after partial or total interruption of neural afferents to the medial basal hypothalamus. Endocrinology 80:608-622.
48. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. 2005. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25:11349-11356.
49. Hart L, Bennett NC, Kalamatianos T, Oosthuizen MK, Jarvis JU, O'Riain MJ, Coen CW. 2008. Neuroanatomical investigation of the gonadotrophin-releasing hormone 1 system in the seasonally breeding Cape dune mole-rat, Bathyergus suillus. Brain Res Bull 77:185-188.
50. Herbison AE. 2006. Physiology of the gonadotropin-releasing hormone neuronal network. In: Neill JD, editor. Physiology of reproduction, 3rd ed. Amsterdam: Elsevier Academic Press p. 1415-1482.
51. Herbison AE. 2008. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 57:277-287.
52. Herbison AE, Porteous R, Pape JR, Mora JM, Hurst PR. 2008. Gonadotropin-releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 149:597-604.
53. Hoffman GE, Gibbs FP. 1982. 1982. LHRH pathways in rat brain: 'deafferentation' spares a sub-chiasmatic LHRH projection to the median eminence. Neuroscience 7:1979-1993.
54. Holmes MM, Rosen GJ, Jordan CL, de Vries GJ, Goldman BD, Forger NG. 2007. Social control of brain morphology in a eusocial mammal. Proc Natl Acad Sci U S A 104:10548-10552.
55. Holmes MM, Goldman BD, Forger NG. 2008. Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain. Horm Behav 54:278-285.
56. Holmes MM, Goldman BD, Goldman SL, Seney ML, Forger NG. 2009. Neuroendocrinology and sexual differentiation in eusocial mammals. Front Neuroendocrinol 30:519-533.
57. Holmes MM, Seney ML, Goldman BD, Forger NG. 2011. Social and hormonal triggers of neural plasticity in naked mole-rats. Behav Brain Res 17:234-239.
58. Homma T, Sakakibara M, Yamada S, Kinoshita M, Iwata K, Tomikawa J, Kanazawa T, Matsui H, Takatsu Y, Ohtaki T, Matsumoto H, Uenoyama Y, Maeda K, Tsukamura H. 2009. Significance of neonatal testicular sex steroids to defeminize anteroventral periventricular kisspeptin neurons and the GnRH/LH surge system in male rats. Biol Reprod 81:1216-1225.
59. Huchon D, Douzery EJ. 2001. From the Old World to the New World: a molecular chronicle of the phylogeny and biogeography of hystricognath rodents. Mol Phylogenet Evol 20:238-251.
60. Inoue N, Sasagawa K, Ikai K, Sasaki Y, Tomikawa J, Oishi S, Fujii N, Uenoyama Y, Ohmori Y, Yamamoto N, Hondo E, Maeda K, Tsukamura H. 2011. Kisspeptin neurons mediate reflex ovulation in the musk shrew (Suncus murinus). Proc Natl Acad Sci U S A 108:17527-17532.
61. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. 2004. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 80:264-272.
62. Jarvis JUM. 1981. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571-573.
63. Jarvis JUM. 1991. Reproduction of naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD, editors. The biology of the naked mole-rat. Princeton, NJ: Princeton University Press. p 384-425.
64. Jarvis JUM, Bennett NC. 1993. Eusociality has evolved independently in two genera of bathyergid mole-rats - but occurs in no other subterranean mammal. Behav Ecol Sociobiol 33:353-360.
65. Jennes L, Stumpf WE. 1980. LHRH-system in the brain of the golden hamster. Cell Tissue Res 209:239-256.
66. Jimenez-Linan M, Rubin BS, King JC. 1997. Examination of guinea pig luteinizing hormone-releasing hormone gene reveals a unique decapeptide and existence of two transcripts in the brain. Endocrinology 138:4123-4130.
67. Kalamatianos T, Kalló I, Piggins HD, Coen CW. 2004. Expression of VIP and PACAP receptor mRNA in peptide synthesising cells within the suprachiasmatic nucleus of the rat and in its efferent target sites. J Comp Neurol 475:19-35.
68. Kalamatianos T, du Toit L, Hrabovszky E, Kalló I, Marsh PJ, Bennett NC, Coen CW. 2005. Characterization of gonadotrophin-releasing hormone precursor cDNA in the Old World mole-rat Cryptomys hottentotus pretoriae: high degree of identity with the New World guinea pig sequence. J Neuroendocrinol 17:265-268.
69. Kalamatianos T, Grimshaw SE, Poorun R, Hahn JD, Coen CW. 2008. Fasting reduces KiSS-1 expression in the anteroventral periventricular nucleus (AVPV): effects of fasting on the expression of KiSS-1 and neuropeptide Y in the AVPV or arcuate nucleus of female rats. J Neuroendocrinol 20:1089-1097.
70. Kalamatianos T, Faulkes CG, Oosthuizen MK, Poorun R, Bennett NC, Coen CW. 2010. Telencephalic binding sites for oxytocin and social organization: a comparative study of eusocial naked mole-rats and solitary cape mole-rats. J Comp Neurol 518:1792-1813.
71. Kalló I, Kalamatianos T, Wiltshire N, Shen S, Sheward WJ, Harmar AJ, Coen CW. 2004. Transgenic approach reveals expression of the VPAC2 receptor in phenotypically defined neurons in the mouse suprachiasmatic nucleus and in its efferent target sites. Eur J Neurosci 19, 2201-2211.
72. Kalló I, Vida B, Deli L, Molnár CS, Hrabovszky E, Caraty A, Ciofi P, Coen CW, Liposits Z. 2012. Co-localisation of kisspeptin with galanin or neurokinin B in afferents to mouse GnRH neurones. J Neuroendocrinol 24:464-476.
73. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M. 2007. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148:1774-1783.
74. Kauffman AS, Navarro VM, Kim J, Clifton D, Steiner RA. 2009. Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. Am J Physiol Endocrinol Metab 297:E1212-1221.
75. Kim EB, Fang X, Fushan AA, Huang Z, Lobanov AV, Han L, Marino SM, Sun X, Turanov AA, Yang P, Yim SH, Zhao X, Kasaikina MV, Stoletzki N, Peng C, Polak P, Xiong Z, Kiezun A, Zhu Y, Chen Y, Kryukov GV, Zhang Q, Peshkin L, Yang L, Bronson RT, Buffenstein R, Wang B, Han C, Li Q, Chen L, Zhao W, Sunyaev SR, Park TJ, Zhang G, Wang J, Gladyshev VN. 2011a. Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature 479:223-227.
76. Kim J, Semaan SJ, Clifton DK, Steiner RA, Dhamija S, Kauffman AS. 2011b. Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology 152:2020-2030.
77. King JC, Anthony EL. 1984. LHRH neurons and their projections in humans and other mammals: species comparisons. Peptides 5(Suppl 1):195-207.
78. King JC, Anthony EL, Fitzgerald DM, Stopa EG. 1985. Luteinizing hormone-releasing hormone neurons in human preoptic/hypothalamus: differential intraneuronal localization of immunoreactive forms. J Clin Endocrinol Metab 60:88-97.
79. King JC, Kugel G, Zahniser D, Wooledge K, Damassa DA, Alexsavich B. 1987. Changes in populations of LHRH-immunopositive cell bodies following gonadectomy. Peptides 8:721-735.
80. King JC, Liu E, Ronsheim PM, Slonimski M, Rubin BS. 1998a. Expression of Fos within luteinizing hormone-releasing hormone neurons, in relation to the steroid-induced luteinizing hormone surge in guinea pigs. Biol Reprod 58:316-322.
81. King JC, Ronsheim P, Liu E, Powers L, Slonimski M, Rubin BS. 1998b. Fos expression in luteinizing hormone-releasing hormone neurons of guinea pigs, with knife cuts separating the preoptic area and the hypothalamus, demonstrating luteinizing hormone surges. Biol Reprod 58:323-329.
82. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K. 2005. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 146:4431-4436.
83. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M. 2001. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 276:34631-34636.
84. Kriegsfeld LJ, Nelson RJ. 1999. Photoperiod affects the gonadotropin-releasing hormone neuronal system of male prairie voles (Microtus ochrogaster). Neuroendocrinology 69:238-244.
85. Lacey EA, Sherman PW. 1991. Social organization of naked mole-rat colonies: evidence for a division of labor. In: Sherman PW, Jarvis JUM, Alexander RD, editors. The biology of the naked mole-rat. Princeton, NJ: Princeton University Press. p 275-336.
86. Lapatto R, Pallais JC, Zhang D, Chan YM, Mahan A, Cerrato F, Le WW, Hoffman GE, Seminara SB. 2007. Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. Endocrinology 148:4927-4936.
87. Lehman MN, Robinson JE, Karsch FJ, Silverman AJ. 1986. Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) pathways in the sheep brain during anoestrus and mid-luteal phase of the estrous cycle. J Comp Neurol 244:19-35.
88. Magee C, Foradori CD, Bruemmer JE, Arreguin-Arevalo JA, McCue PM, Handa RJ, Squires EL, Clay CM. 2009. Biological and anatomical evidence for kisspeptin regulation of the hypothalamic-pituitary-gonadal axis of estrous horse mares. Endocrinology 150:2813-2821.
89. Mason AO, Greives TJ, Scotti MA, Levine J, Frommeyer S, Ketterson ED, Demas GE, Kriegsfeld LJ. 2007. Suppression of kisspeptin expression and gonadotropic axis sensitivity following exposure to inhibitory day lengths in female Siberian hamsters. Horm Behav 52:492-498.
90. 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.
91. Merchenthaler I, Görcs T, Setalo G, Petrusz P, Flerkó B. 1984. Gonadotropin-releasing hormone (GnRH) neurons and pathways in the rat brain. Cell Tissue Res 237:15-29.
92. Messager S, Chatzidaki E, Ma D, Hendrick A, Zahn D, Dixon J, Thresher R, Malinge I, Lomet D, Carlton M, Colledge W, Caraty A, Aparicio S. 2005. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci U S A 102:1761-1766.
93. Molteno AJ, Kalló I, Bennett NC, King JA, Coen CW. 2004. A neuroanatomical and neuroendocrinological study into the relationship between social status and the GnRH system in cooperatively breeding female Damaraland mole-rats, Cryptomys damarensis. Reproduction 127:13-21.
94. Mouchaty SK, Catzeflis F, Janke A, Arnason U. 2001. Molecular evidence of an African Phiomorpha-South American Caviomorpha clade and support for Hystricognathi based on the complete mitochondrial genome of the cane rat (Thryonomys swinderianus). Mol Phylogenet Evol 18:127-135.
95. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, Szekeres PG, Sarau HM, Chambers JK, Murdock P, Steplewski K, Shabon U, Miller JE, Middleton SE, Darker JG, Larminie CG, Wilson S, Bergsma DJ, Emson P, Faull R, Philpott KL, Harrison DC. 2001. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 276:28969-28975.
96. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Barreiro ML, Casanueva FF, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. 2005a. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 146:1689-1697.
97. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. 2005b. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 146:156-163.
98. Oakley AE, Clifton DK, Steiner RA. 2009. Kisspeptin signaling in the brain. Endocr Rev 30:713-743.
99. Ohkura S, Takase K, Matsuyama S, Mogi K, Ichimaru T, Wakabayashi Y, Uenoyama Y, Mori Y, Steiner RA, Tsukamura H, Maeda KI, Okamura H. 2009. Gonadotrophin-releasing hormone pulse generator activity in the hypothalamus of the goat. J Neuroendocrinol 21:813-821.
100. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M. 2001. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411:613-617.
101. Oosthuizen MK, Bennett NC, Coen CW. 2008. An immunohistochemical study of the gonadotrophin-releasing hormone 1 system in solitary Cape mole-rats, Georychus capensis, and social Natal mole-rats, Cryptomys hottentotus natalensis. Neuroscience 157:164-173.
102. O'Riain MJ, Jarvis JUM, Buffenstein R, Alexander R, Peeters C. 2000. Morphological castes in a vertebrate. Proc Natl Acad Sci U S A 97:13194-13197.
103. Peroulakis ME, Goldman B, Forger NG. 2002. Perineal muscles and motoneurons are sexually monomorphic in the naked mole-rat (Heterocephalus glaber). J Neurobiol 51:33-42.
104. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M. 2012. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 92:1235-1316.
105. Poling MC, Kauffman AS. 2013. Organizational and activational effects of sex steroids on kisspeptin neuron development. Front Neuroendocrinol 34:3-17.
106. Ramaswamy S, Guerriero KA, Gibbs RB, Plant TM. 2008. 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 149:4387-4395.
107. Revel FG, Ansel L, Klosen P, Saboureau M, Pevet P, Mikkelsen JD, Simonneaux V. 2007. Kisspeptin: a key link to seasonal breeding. Rev Endocr Metab Disord 8:57-65.
108. Richardson HN, Romeo RD, Sisk CL. 1999. Regional changes in GnRH immunoreactivity with puberty in the male Syrian hamster. Brain Res 817:232-235.
109. Robinson JE, Skinner DC, Skinner JD, Haupt MA. 1997. Distribution and morphology of luteinising hormone-releasing hormone neurones in a species of wild antelope, the springbok (Antidorcas marsupialis). J Comp Neurol 389:444-452.
110. Saper CB. 1996. Any way you cut it: a new journal policy for the use of unbiased counting methods. J Comp Neurol 364:5.
111. Schwanzel-Fukuda M, Pfaff DW. 1989. Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161-164.
112. Schwanzel-Fukuda M, Fadem BH, Garcia MS, Pfaff DW. 1988. Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) in the brain and nervus terminalis of the adult and early neonatal gray short-tailed opossum (Monodelphis domestica). J Comp Neurol 276:44-60.
113. Semaan SJ, Kauffman AS. 2010. Sexual differentiation and development of forebrain reproductive circuits. Curr Opin Neurobiol 20:424-431.
114. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley WF Jr, Aparicio SA, Colledge WH. 2003. The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614-1627.
115. Seney M, Goldman BD, Forger NG. 2006. Breeding status affects motoneuron number and muscle size in naked mole-rats: recruitment of perineal motoneurons? J Neurobiol 66:1354-1364.
116. Seney ML, Kelly DA, Goldman BD, Sumbera R, Forger NG. 2009. Social structure predicts genital morphology in African mole-rats. PLoS One 4:e7477.
117. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. 2005. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 102:2129-2134.
118. Shivers BD, Harlan RE, Morrell JI, Pfaff DW. 1983. Immunocytochemical localization of luteinizing hormone-releasing hormone in male and female rat brains. Quantitative studies on the effect of gonadal steroids. Neuroendocrinology 36:1-12.
119. Silverman AJ. 1976. Distribution of luteinizing hormone-releasing hormone (LHRH) in the guinea pig brain. Endocrinology 99:30-41.
120. Silverman AJ, Antunes JL, Abrams GM, Nilaver G, Thau R, Robinson JA, Ferin M, Krey LC. 1982. The luteinising hormone releasing hormone pathways in rhesus (Macaca mulatta) and pigtailed monkeys: new observations on thick unembedded sections. J Comp Neurol 211:309-317.
121. Silverman AJ, Livne I, Witkin JW. 1994. The gonadotropin-releasing hormone (GnRH), neuronal systems: immunocytochemistry and in situ hybridisation. In: Knobil E, Neill JD, editors. Physiology of reproduction, 2nd ed. New York: Raven Press. p 1683-1709.
122. Smith TE, Faulkes CG, Abbott DH. 1997. Combined olfactory contact with the parent colony and direct contact with nonbreeding animals does not maintain suppression of ovulation in female naked mole-rats (Heterocephalus glaber). Horm Behav 31:277-288.
123. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. 2005a. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146:3686-3692.
124. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA. 2005b. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 146:2976-2984.
125. Smith JT, Clifton DK, Steiner RA. 2006a. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 131:623-630.
126. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA. 2006b. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 26:6687-6694.
127. Smith JT, Clay CM, Caraty A, Clarke IJ. 2007. KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 148:1150-1157.
128. Takase K, Uenoyama Y, Inoue N, Matsui H, Yamada S, Shimizu M, Homma T, Tomikawa J, Kanda S, Matsumoto H, Oka Y, Tsukamura H, Maeda KI. 2009. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol 21:527-537.
129. Thompson RH, Swanson LW. 2003. Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Rev 41:153-202.
130. Toumi FN, Martinet L, Peytevin J. 1992. Gonadotropin-releasing hormone neurons and pathways in the brain of the female mink (Mustela vison). Cell Tissue Res 270:383-393.
131. Urbanski HF. 1991. Monoclonal antibodies to luteinizing hormone-releasing hormone: production, characterization, and immunocytochemical application. Biol Reprod 44:681-686.
132. Urbanski HF, Doan A, Pierce M. 1991. Immunocytochemical investigation of luteinizing hormone-releasing hormone neurons in Syrian hamsters maintained under long or short days. Biol Reprod 44:687-692.
133. Vida B, Deli L, Hrabovszky E, Kalamatianos T, Caraty A, Coen CW, Liposits Z, Kalló I. 2010. Evidence for suprachiasmatic vasopressin neurones innervating kisspeptin neurones in the rostral periventricular area of the mouse brain: regulation by oestrogen. J Neuroendocrinol 22:1032-1039.
134. Witkin JW, Paden CM, Silverman JA. 1982. The luteinizing hormone-releasing hormone (LHRH) systems in the rat brain. Neuroendocrinology 35:429-438.
135. Wray S, Hoffman GE. 1986. A developmental study of the quantitative distribution of LHRH neurons within the central nervous system of postnatal male and female rats. J Comp Neurol 252:522-531.
136. Yellon SM, Lehman MN, Newman SW. 1990. The gonadotropin-releasing hormone neuronal system of the male Djungarian hamster: distribution from the olfactory tubercle to the medial basal hypothalamus. Neuroendocrinology 51:219-225.
137. Yeo SH, Herbison AE. 2011. Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology 152:2387-2399.
138. Yu C, Li Y, Holmes A, Szafranski K, Faulkes G, Coen CW, Buffenstein R, Platzer M, de Magalhães JP, Church GM. 2011. RNA sequencing reveals differential expression of mitochondrial and oxidation reduction genes in the long-lived naked mole-rat when compared to mice. PLoS One 6:e26729.