Examination of the influence of leptin and acute metabolic challenge on RFRP-3 neurons of mice in development and adulthood

Neuroendocrinology

Volumn 100, Issue 4, 2014, Pages 317-333

  Poling, Matthew C ^a   Shieh, Morris P ^a   Munaganuru, Nagambika ^a   Luo, Elena ^a   Kauffman, Alexander S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; GnIH; Leptin; Reproduction; RFRP 3

Indexed keywords

LEPTIN; LEPTIN RECEPTOR; LUTEINIZING HORMONE; MELANOCORTIN 4 RECEPTOR; MESSENGER RNA; NEUROPEPTIDE; NEUROPEPTIDE Y; PROTIRELIN; RFAMIDE RELATED PEPTIDE 3; UNCLASSIFIED DRUG; RFAMIDE PEPTIDE;

ADULT; ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIET RESTRICTION; FEEDING; FEMALE; GENE EXPRESSION; HYPOTHALAMUS; IN SITU HYBRIDIZATION; JUVENILE; LUTEINIZING HORMONE RELEASE; MALE; METABOLIC REGULATION; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NONHUMAN; OBESITY; PRIORITY JOURNAL; AGE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FOOD DEPRIVATION; METABOLISM; SECRETION (PROCESS);

AGE FACTORS; ANIMALS; FEMALE; FOOD DEPRIVATION; LEPTIN; LUTEINIZING HORMONE; MALE; MICE; MICE, INBRED C57BL; NEURONS; NEUROPEPTIDES; RECEPTORS, LEPTIN;

EID: 84923060590     PISSN: 00283835     EISSN: 14230194     Source Type: Journal    
DOI: 10.1159/000369276     Document Type: Article

References (63)

1. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ: A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 2000; 275: 661-667
2. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R: Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A 2006; 103: 2410-2415
3. Anderson GM, Relf HL, Rizwan MZ, Evans JJ: Central and peripheral effects of RFamiderelated peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinology 2009; 150: 1834-1840
4. Ducret E, Anderson GM, Herbison AE: RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. Endocrinology 2009; 150: 2799-2804
5. Wu M, Dumalska I, Morozova E, van den Pol AN, Alreja M: Gonadotropin inhibitory hormone inhibits basal forebrain vGluT2-gonadotropin-releasing hormone neurons via a direct postsynaptic mechanism. J Physiol 2009; 587: 1401-1411
6. Khan AR, Kauffman AS: The role of kisspeptin and RFRP-3 neurons in the circadiantimed preovulatory luteinizing hormone surge. J Neuroendocrinology 2012;24:131-143
7. Johnson MA, Tsutsui K, Fraley GS: Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm Behav 2007; 51: 171-180
8. Rizwan MZ, Poling MC, Corr M, Cornes PA, Augustine RA, Quennell JH, Kauffman AS, Anderson GM: RFamide-related peptide-3 receptor gene expression in GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology 2012; 153: 3770-3779
9. Poling MC, Kim J, Dhamija S, Kauffman AS: Development, sex steroid regulation, and phenotypic characterization of RFamide-related peptide (Rfrp) gene expression and RFamide receptors in the mouse hypothalamus. Endocrinology 2012; 153: 1827-1840
10. Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, Fujii R, Watanabe T, Kikuchi K, Terao Y, Yano T, Yamamoto T, Kawamata Y, Habata Y, Asada M, Kitada C, Kurokawa T, Onda H, Nishimura O, Tanaka M, Ibata Y, Fujino M: New neuropeptides containing carboxy-Terminal RFamide and their receptor in mammals. Nat Cell Biol 2000; 2: 703-708
11. Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK, Jiang Q, Zeng Z, Jacobson M, Williams DL Jr, Yu H, Bomford D, Figueroa D, Mallee J, Wang R, Evans J, Gould R, Austin CP: Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem 2001; 276: 36961-36969
12. Yano T, Iijima N, Kakihara K, Hinuma S, Tanaka M, Ibata Y: Localization and neuronal response of RFamide related peptides in the rat central nervous system. Brain Res 2003; 982: 156-167
13. Bellinger LL, Bernardis LL: The dorsomedial hypothalamic nucleus and its role in ingestive behavior and body weight regulation: lessons learned from lesioning studies. Physiol Behav 2002; 76: 431-442
14. Mieda M, Williams SC, Richardson JA, Tanaka K, Yanagisawa M: The dorsomedial hypothalamic nucleus as a putative food-entrainable circadian pacemaker. Proc Natl Acad Sci U S A 2006; 103: 12150-12155
15. Bi S: Role of dorsomedial hypothalamic neuropeptide Y in energy homeostasis. Peptides 2007; 28: 352-356
16. Ingalls AM, Dickie MM, Snell GD: Obese, a new mutation in the house mouse. J Hered 1950; 41: 317-318
17. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM: Positional cloning of the mouse obese gene and its human homologue. Nature 1994; 372: 425-432
18. Quennell JH, Mulligan AC, Tups A, Liu X, Phipps SJ, Kemp CJ, Herbison AE, Grattan DR, Anderson GM: Leptin indirectly regulates gonadotropin-releasing hormone neuronal function. Endocrinology 2009; 150: 2805-2812
19. Louis GW, Greenwald-Yarnell M, Phillips R, Coolen LM, Lehman MN, Myers MG Jr: Molecular mapping of the neural pathways linking leptin to the neuroendocrine reproductive axis. Endocrinology 2011; 152: 2302-2310
20. Elmquist JK, Ahima RS, Maratos-Flier E, Flier JS, Saper CB: Leptin activates neurons in ventrobasal hypothalamus and brainstem. Endocrinology 1997; 138: 839-842
21. Oliveira VX Jr, Fazio MA, Miranda MT, da Silva JM, Bittencourt JC, Elias CF, Miranda A: Leptin fragments induce Fos immunoreactivity in rat hypothalamus. Regul Pept 2005; 127: 123-132
22. Myers MG Jr, Munzberg H, Leinninger GM, Leshan RL: The geometry of leptin action in the brain: more complicated than a simple ARC. Cell Metab 2009; 9: 117-123
23. Johnson MA, Fraley GS: Rat RFRP-3 alters hypothalamic GHRH expression and growth hormone secretion but does not affect KiSS-1 gene expression or the onset of puberty in male rats. Neuroendocrinology 2008; 88: 305-315
24. Clarke IJ, Smith JT, Henry BA, Oldfield BJ, Stefanidis A, Millar RP, Sari IP, Chng K, Fabre-Nys C, Caraty A, Ang BT, Chan L, Fraley GS: Gonadotropin-inhibitory hormone is a hypothalamic peptide that provides a molecular switch between reproduction and feeding. Neuroendocrinology 2012; 95: 305-316
25. Klingerman CM, Williams WP 3rd, Simberlund J, Brahme N, Prasad A, Schneider JE, Kriegsfeld LJ: Food restriction-induced changes in gonadotropin-inhibiting hormone cells are associated with changes in sexual motivation and food hoarding, but not sexual performance and food intake. Front Endocrinol (Lausanne) 2012; 2: 101
26. Leon S, Garcia-Galiano D, Ruiz-Pino F, Barroso A, Manfredi-Lozano M, Romero-Ruiz A, Roa J, Vazquez MJ, Gaytan F, Blomenrohr M, van Duin M, Pinilla L, Tena-Sempere M: Physiological roles of gonadotropin-inhibitory hormone signaling in the control of mammalian reproductive axis: studies in the NPFF1 receptor null mouse. Endocrinology 2014; 155: 2953-2965
27. Swerdloff RS, Batt RA, Bray GA: Reproductive hormonal function in the genetically obese (ob/ob) mouse. Endocrinology 1976; 98: 1359-1364
28. Ahima RS, Prabakaran D, Flier JS: Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest 1998; 101: 1020-1027
29. Bouret SG, Draper SJ, Simerly RB: Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 2004; 304: 108-110
30. Bouret SG, Draper SJ, Simerly RB: Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci 2004; 24: 2797-2805
31. Molnar CS, Kallo I, Liposits Z, Hrabovszky E: Estradiol down-regulates RF-Amide-related peptide (RFRP) expression in the mouse hypothalamus. Endocrinology 2011; 152: 1684-1690
32. Mercer JG, Hoggard N, Williams LM, Lawrence CB, Hannah LT, Trayhurn P: Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization. FEBS Lett 1996; 387: 113-116
33. Finn PD, Steiner RA, Clifton DK: Temporal patterns of gonadotropin-releasing hormone (GnRH), c-fos, and galanin gene expression in GnRH neurons relative to the luteinizing hormone surge in the rat. J Neurosci 1998; 18: 713-719
34. Sugrue ML, Vella KR, Morales C, Lopez ME, Hollenberg AN: The thyrotropin-releasing hormone gene is regulated by thyroid hormone at the level of transcription in vivo. Endocrinology 2010; 151: 793-801
35. Dror T, Franks J, Kauffman AS: Analysis of multiple positive feedback paradigms demonstrates a complete absence of LH surges and GnRH activation in mice lacking kisspeptin signaling. Biol Reprod 2013; 88: 146
36. Poling MC, Quennell JH, Anderson GM, Kauffman AS: Kisspeptin neurones do not directly signal to RFRP-3 neurones but RFRP-3 may directly modulate a subset of hypothalamic kisspeptin cells in mice. J Neuroendocrinol 2013; 25: 876-886
37. Chowen JA, Clifton DK: Semiquantitative analysis of cellular somatostatin mRNA levels by in situ hybridization histochemistry. Method Neurosci 1991; 5: 137-158
38. Kauffman AS, Navarro VM, Kim J, Clifton D, Steiner RA: Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. Am J Physiol Endocrinol Metab 2009; 297:E1212-E1221
39. Semaan SJ, Murray EK, Poling MC, Dhamija S, Forger NG, Kauffman AS: BAX-dependent and BAX-independent regulation of Kiss1 neuron development in mice. Endocrinology 2010; 151: 5807-5817
40. Kim J, Semaan SJ, Clifton DK, Steiner RA, Dhamija S, Kauffman AS: Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology 2011; 152: 2020-2030
41. Kauffman A, Sun Y, Kim J, Khan AR, Shu J, Neal-Perry G: Vasoactive intestinal peptide modulation of the steroid-induced LH surge involves kisspeptin signaling in young but not in middle-Aged female rats. Endocrinology 2014; 155: 2222-2232
42. Di Giorgio NP, Semaan SJ, Kim J, Lopez PV, Bettler B, Libertun C, Lux-Lantos VA, Kauffman AS: Impaired GABAB receptor signaling dramatically up-regulates Kiss1 expression selectively in nonhypothalamic brain regions of adult but not prepubertal mice. Endocrinology 2014; 155: 1033-1044
43. Sahu A, Kalra PS, Kalra SP: Food deprivation and ingestion induce reciprocal changes in neuropeptide Y concentrations in the paraventricular nucleus. Peptides 1988; 9: 83-86
44. Chan YY, Steiner RA, Clifton DK: Regulation of hypothalamic neuropeptide-Y neurons by growth hormone in the rat. Endocrinology 1996; 137: 1319-1325
45. Li C, Chen P, Smith MS: The acute suckling stimulus induces expression of neuropeptide Y (NPY) in cells in the dorsomedial hypothalamus and increases NPY expression in the arcuate nucleus. Endocrinology 1998; 139: 1645-1652
46. Lechan RM, Jackson IM: Immunohistochemical localization of thyrotropin-releasing hormone in the rat hypothalamus and pituitary. Endocrinology 1982; 111: 55-65
47. Elmquist JK, Bjorbaek C, Ahima RS, Flier JS, Saper CB: Distributions of leptin receptor mRNA isoforms in the rat brain. J Comp Neurol 1998; 395: 535-547
48. Kishi T, Aschkenasi CJ, Lee CE, Mountjoy KG, Saper CB, Elmquist JK: Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J Comp Neurol 2003; 457: 213-235
49. Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K: Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol 2008; 199: 105-112
50. Soga T, Kitahashi T, Clarke IJ, Parhar IS: Gonadotropin-inhibitory hormone promoterdriven enhanced green fluorescent protein expression decreases during aging in female rats. Endocrinology 2014; 155: 1944-1955
51. Clarke IJ, Sari IP, Qi Y, Smith JT, Parkington HC, Ubuka T, Iqbal J, Li Q, Tilbrook A, Morgan K, Pawson AJ, Tsutsui K, Millar RP, Bentley GE: Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 2008; 149: 5811-5821
52. Rizwan MZ, Porteous R, Herbison AE, Anderson GM: Cells expressing RFamide-related peptide-1/3, the mammalian gonadotropininhibitory hormone orthologs, are not hypophysiotropic neuroendocrine neurons in the rat. Endocrinology 2009; 150: 1413-1420
53. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenrohr M, Pinilla L, van Noort PI, Tena-Sempere M: Characterization of the inhibitory roles of RFRP3, the mammalian ortholog of GnIH, in the control of gonadotropin secretion in the rat: in vivo and in vitro studies. Am J Physiol Endocrinol Metab 2010; 299:E39-E46
54. Ancel C, Bentsen AH, Sebert ME, Tena-Sempere M, Mikkelsen JD, Simonneaux V: Stimulatory effect of RFRP-3 on the gonadotrophic axis in the male Syrian hamster: the exception proves the rule. Endocrinology 2012; 153: 1352-1363
55. Son YL, Ubuka T, Millar RP, Kanasaki H, Tsutsui K: Gonadotropin-inhibitory hormone inhibits GnRH-induced gonadotropin subunit gene transcriptions by inhibiting AC/cAMP/PKA-dependent ERK pathway in LβT2 cells. Endocrinology 2012; 153: 2332-2343
56. Rizwan MZ, Harbid AA, Inglis MA, Quennell JH, Anderson GM: Evidence that hypothalamic RFamide related peptide-3 neurones are not leptin-responsive in mice and rats. J Neuroendocrinol 2014; 26: 247-257
57. Bouret SG: Organizational actions of metabolic hormones. Front Neuroendocrinol 2013; 34: 18-26
58. Hayashida T, Nakahara K, Mondal MS, Date Y, Nakazato M, Kojima M, Kangawa K, Murakami N: Ghrelin in neonatal rats: distribution in stomach and its possible role. J Endocrinol 2002; 173: 239-245
59. Steculorum SM, Bouret SG: Maternal diabetes compromises the organization of hypothalamic feeding circuits and impairs leptin sensitivity in offspring. Endocrinology 2011; 152: 4171-4179
60. Mannan MA, O'Shaughnessy PJ: Ovarian steroid metabolism during post-natal development in the normal mouse and in the adult hypogonadal (hpg) mouse. J Reprod Fertil 1988; 82: 727-734
61. Simerly RB: Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 2002; 25: 507-536
62. Scott HM, Mason JI, Sharpe RM: Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds. Endocr Rev 2009; 30: 883-925
63. Poling MC, Kauffman AS: Organizational and activational effects of sex steroids on kisspeptin neuron development. Front Neuroendocrinol 2013; 34: 3-17