Seasonal changes in RFamide-related peptide-3 neurons in the hypothalamus of a seasonally breeding marsupial species, the brushtail possum (Trichosurus vulpecula)

Journal of Comparative Neurology

Volumn 521, Issue 13, 2013, Pages 3030-3041

  Harbid, Anan A ^a   Mcleod, Bernie J ^b   Caraty, Alain ^c   Anderson, Greg M ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b INVERMAY AGRICULTURAL CENTRE   (New Zealand)

^c UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

GnRH; Neuroendocrinology; Possums; RFamide related peptide 3; Tract tracing; Tyrosine hydroxylase

Indexed keywords

HORMONE INHIBITOR; RFAMIDE RELATED PEPTIDE 3; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; HYPOTHALAMUS; IMMUNOREACTIVITY; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEASONAL VARIATION; SUMMER; THALAMUS; TRICHOSURUS; TRICHOSURUS VULPECULA; WINTER;

GNRH; NEUROENDOCRINOLOGY; POSSUMS; RFAMIDE RELATED PEPTIDE-3; TRACT TRACING; TYROSINE HYDROXYLASE;

ANIMALS; BREEDING; FEMALE; GENE EXPRESSION REGULATION; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; NERVE FIBERS; NEURAL PATHWAYS; NEURONS; NEUROPEPTIDES; SEASONS; STILBAMIDINES; TRICHOSURUS; TYROSINE 3-MONOOXYGENASE;

EID: 84880631453     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23328     Document Type: Article

References (60)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Ancel C, Bentsen AH, Sebert ME, Tena-Sempere M, Mikkelsen JD, Simonneaux V. 2012. Stimulatory effect of RFRP-3 on the gonadotrophic axis in the male Syrian hamster: the exception proves the rule. Endocrinology 153:1352-1363.
3. Anderson GM. 2011. Pituitary actions of RFamide peptides: a critique of the evidence. Open Neuroendocrinol J 4:51-63.
4. Anderson GM, Relf HL, Rizwan MZ, Evans JJ. 2009. Central and peripheral effects of RFamide-related peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinology 150:1834-1840.
5. Bentley GE, Perfito N, Ukena K, Tsutsui K, Wingfield JC. 2003. Gonadotropin-inhibitory peptide in song sparrows (Melospiza melodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadotropin-releasing hormone. J Neuroendocrinol 15:794-802.
6. Bjorklund A, Lindvall O, Nobin A. 1975. Evidence of an incerto-hypothalamic dopamine neurone system in the rat. Brain Res 89:29-42.
7. Cheng CK, Leung PC. 2005. Molecular biology of gonadotropin-releasing hormone (GnRH)-I, GnRH-II, and their receptors in humans. Endocr Rev 26:283-306.
8. 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. 2008. Potent action of RFRP-3 on pituitary gonadotropes indicative of an hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 149:5811-5821.
9. 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. 2012. Gonadotropin-inhibitory hormone is a hypothalamic peptide that provides a molecular switch between reproduction and feeding. Neuroendocrinology 95:305-316.
10. 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.
11. 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.
12. Dardente H, Birnie M, Lincoln GA, Hazlerigg DG. 2008. RFamide-related peptide and its cognate receptor in the sheep: cDNA cloning, mRNA distribution in the hypothalamus and the effect of photoperiod. J Neuroendocrinol 20:1252-1259.
13. Ducret E, Anderson GM, Herbison AE. 2009. RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. Endocrinology 150:2799-2804.
14. Franklin BJ, Paxinos G. 2008. The mouse brain atlas in stereotaxic coordinates. New York: Elsevier.
15. Gibson EM, Humber SA, Jain S, Williams WP 3rd, Zhao S, Bentley GE, Tsutsui K, Kriegsfeld LJ. 2008. Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology 149:4958-4969.
16. Goldsmith PC, Thind KK, Song T, Kim EJ, Boggant JE. 1990. Location of the neuroendocrine dopamine neurons in the monkey hypothalamus by retrograde tracing and immunostaining. J Neuroendocrinol 2:169-179.
17. Goubillon M, Delaleu B, Tillet Y, Caraty A, Herbison AE. 1999. Localization of estrogen-receptive neurons projecting to the GnRH neuron-containing rostral preoptic area of the ewe. Neuroendocrinology 70:228-236.
18. 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.
19. Herbison AE. 1998. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr Rev 19:302-330.
20. Herbison AE. 2006. Physiology of the GnRH neuronal networks. Physiol Reprod :1415-1482.
21. 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. 2000. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2:703-708.
22. Johnson MA, Tsutsui K, Fraley GS. 2007. 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 51:171-180.
23. Kadokawa H, Shibata M, Tanaka Y, Kojima T, Matsumoto K, Oshima K, Yamamoto N. 2009. Bovine C-terminal octapeptide of RFamide-related peptide-3 suppresses luteinizing hormone (LH) secretion from the pituitary as well as pulsatile LH secretion in bovines. Domest Anim Endocrinol 36:219-224.
24. King JC, Anthony EL, Gustafson AW, Damassa DA. 1984. Luteinizing hormone-releasing hormone (LH-RH) cells and their projections in the forebrain of the bat Myotis lucifugus lucifugus. Brain Res 298:289-301.
25. King JA, Hinds LA, Mehl AE, Saunders NR, Millar RP. 1990. Chicken GnRH II occurs together with mammalian GnRH in a South American species of marsupial (Monodelphis domestica). Peptides 11:521-525.
26. 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.
27. Kirby ED, Geraghty AC, Ubuka T, Bentley GE, Kaufer D. 2009. Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc Natl Acad Sci U S A 106:11324-11329.
28. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R. 2006. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A 103:2410-2415.
29. Mason AO, Duffy S, Zhao S, Ubuka T, Bentley GE, Tsutsui K, Silver R, Kriegsfeld LJ. 2010. Photoperiod and reproductive condition are associated with changes in RFamide-related peptide (RFRP) expression in Syrian hamsters (Mesocricetus auratus). J Biol Rhythms 25:176-185.
30. McLeod BJ, Thompson EG, Crawford JL, Shackell GH. 1997. Successful group housing of wild-caught brushtail possums (Trichosurus vulpecula). Anim Welfare 6:67-76.
31. Merchenthaler I. 1991. Neurons with access to the general circulation in the central nervous system of the rat: a retrograde tracing study with fluoro-gold. Neuroscience 44:655-662.
32. Merchenthaler I. 1994. Induction of enkephalin in tuberoinfundibular dopaminergic neurons of pregnant, pseudopregnant, lactating and aged female rats. Neuroendocrinology 60:185-193.
33. Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K. 2008. Hypophysiotropic role of RFamide-related peptide-3 (RFRP-3) in the inhibition of LH secretion in female rats. J Endocrinol 199:105-112.
34. Paul MJ, Pyter LM, Freeman DA, Galang J, Prendergast BJ. 2009. Photic and nonphotic seasonal cues differentially engage hypothalamic kisspeptin and RFamide-related peptide mRNA expression in Siberian hamsters. J Neuroendocrinol 21:1007-1014.
35. Paxinos G, Watson C. 2005. The rat brain atlas in stereotaxic coordinates. Sydney: Elsevier.
36. Pilton PE, Sharman GB. 1962. Reproduction in the marsupial Trichosurus vulpecula. J Endocrinol 25:119-136.
37. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenrohr M, Pinilla L, van Noort P, Tena-Sempere M. 2010. Characterization of 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 299:E39-46.
38. Poling MC, Kim J, Dhamija S, Kauffman AS. 2012. Development, sex steroid regulation, and phenotypic characterization of RFamide-related peptide (Rfrp) gene expression and RFamide receptors in the mouse hypothalamus. Endocrinology 153:1827-1840.
39. Revel FG, Saboureau M, Pevet P, Simonneaux V, Mikkelsen JD. 2008. RFamide-related peptide gene is a melatonin-driven photoperiodic gene. Endocrinology 149:902-912.
40. Rizwan MZ, Porteous R, Herbison AE, Anderson GM. 2009. Cells expressing RFamide-related peptide-1/3, the mammalian gonadotropin-inhibitory hormone orthologs, are not hypophysiotropic neuroendocrine neurons in the rat. Endocrinology 150:1413-1420.
41. Rizwan MZ, Poling MC, Corr M, Cornes PA, Augustine RA, Quennell J, Kauffman AS, Anderson GM. 2012. RFamide-related peptide-3 receptor gene expression on GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology 153:3770-3779.
42. Romero MI, Phelps CJ. 1997. Identification of growth hormone-releasing hormone and somatostatin neurons projecting to the median eminence in normal and growth hormone-deficient Ames dwarf mice. Neuroendocrinology 65:107-116.
43. Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ. 2009. Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology 150:5549-5556.
44. 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.
45. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN. 2008. Variation in kisspeptin and gonadotropin-inhibitory hormone expression and terminal connections to GnRH neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 149:5770-5782.
46. Smith JT, Shahab M, Pereira A, Pau KY, Clarke IJ. 2010. Hypothalamic expression of KISS1 and gonadotropin inhibitory hormone genes during the menstrual cycle of a non-human primate. Biol Reprod 83:568-577.
47. Smith JT, Ross Young I, Veldhuis JD, Clarke IJ. 2012. Gonadotropin-inhibitory hormone (GnIH) secretion into the ovine hypophyseal portal system. Endocrinology 153:3368-3375.
48. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ. 2000. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275(2 Suppl):661-667.
49. Tyndale-Biscoe H. 1973. Life of marsupials. New York: Elsevier.
50. Tyndale-Biscoe H, Renfree M. 1987. Reproductive physiology of marsupials. New York: Cambridge University Press.
51. Ubuka T, Lai H, Kitani M, Suzuuchi A, Pham V, Cadigan PA, Wang A, Chowdhury VS, Tsutsui K, Bentley GE. 2009a. Gonadotropin-inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol 517:841-855.
52. Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H, Tsutsui K, Millar RP, Bentley GE. 2009b. Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS One 4:e8400.
53. Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, Tsutsui K. 2012. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology 153:373-385.
54. Ukena K, Tsutsui K. 2001. Distribution of novel RFamide-related peptide-like immunoreactivity in the mouse central nervous system. Neurosci Lett 300:153-156.
55. Ukena K, Ubuka T, Tsutsui K. 2003. Distribution of a novel avian gonadotropin-inhibitory hormone in the quail brain. Cell Tissue Res 312:73-79.
56. Ukena K, Tsutsui K. 2005. A new member of the hypothalamic RF-amide peptide family, LPXRF-amide peptides: structure, localization, and function. Mass Spectrom Rev 24:469-486.
57. Urbanski HF. 1991. Monoclonal antibodies to luteinizing hormone-releasing hormone: production, characterization, and immunocytochemical application. Biol Reprod 44:681-686.
58. Vaughan TA, Ryan JM, Czaplewski NJ. 2011. Mammalogy. Sudbury, MA: Jones and Bartlett.
59. Wu M, Dumalska I, Morozova E, van den Pol AN, Alreja M. 2009. Gonadotropin inhibitory hormone inhibits basal forebrain vGluT2-gonadotropin-releasing hormone neurons via a direct postsynaptic mechanism. J Physiol 587(Pt 7):1401-1411.
60. Yano T, Iijima N, Kakihara K, Hinuma S, Tanaka M, Ibata Y. 2003. Localization and neuronal response of RFamide related peptides in the rat central nervous system. Brain Res 982:156-167.