RNA interference of gonadotropin-inhibitory hormone gene induces arousal in songbirds

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Ubuka, Takayoshi ^a,c   Mukai, Motoko ^b,d   Wolfe, Jordan ^a   Beverly, Ryan ^a   Clegg, Sarah ^a   Wang, Ariel ^a   Hsia, Serena ^a   Li, Molly ^a   Krause, Jesse S ^b   Mizuno, Takanobu ^c   Fukuda, Yujiro ^c   Tsutsui, Kazuyoshi ^c   Bentley, George E ^a   Wingfield, John C ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WASEDA UNIVERSITY   (Japan)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN; GONADOTROPIN INHIBITORY HORMONE; MESSENGER RNA; MESSENGER RNA PRECURSOR; NEUROPEPTIDE; UNCLASSIFIED DRUG; AVIAN PROTEIN; HYPOTHALAMUS HORMONE; RNA PRECURSOR; TESTOSTERONE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; BRAIN NERVE CELL; BRAIN THIRD VENTRICLE; BRAIN TISSUE; CELL DENSITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE PRODUCT; GENE SILENCING; GONADOTROPIN INHIBITORY HORMONE GENE; HORMONE RELEASE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; MALE; MOTIVATION; NERVE FIBER; NEUROMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; REPRODUCTION; REST; RNA INTERFERENCE; SEXUAL BEHAVIOR; SPARROW; TERRITORIALITY; VENTRAL TEGMENTUM; VOCALIZATION; WHITE CROWNED SPARROW; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; BRAIN; CYTOLOGY; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MOTOR ACTIVITY; NERVE CELL; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SONGBIRD;

AVES; PASSERI; PHASIANIDAE; ZONOTRICHIA LEUCOPHRYS;

ANALYSIS OF VARIANCE; ANIMALS; AROUSAL; AVIAN PROTEINS; BRAIN; FEMALE; GENE EXPRESSION; HYPOTHALAMIC HORMONES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOTOR ACTIVITY; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA PRECURSORS; SONGBIRDS; TESTOSTERONE; VOCALIZATION, ANIMAL;

EID: 84862487788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030202     Document Type: Article

References (56)

1. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, et al. (2000) A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275: 661-667.
2. Ubuka T, Ukena K, Sharp PJ, Bentley GE, Tsutsui K, (2006) Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology 147: 1187-1194.
3. Ubuka T, Ueno M, Ukena K, Tsutsui K, (2003) Developmental changes in gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica) hypothalamo-hypophysial system. J Endocrinol 178: 311-318.
4. Ubuka T, Kim S, Huang YC, Reid J, Jiang J, et al. (2008) Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and-II neurons in European starling brain. Endocrinology 149: 268-278. Erratum in: Endocrinology 149: 4229.
5. 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.
6. Tobari Y, Iijima N, Tsunekawa K, Osugi T, Okanoya K, et al. (2010) Identification of gonadotropin-inhibitory hormone in the zebra finch (Taeniopygia guttata): Peptide isolation, cDNA cloning and brain distribution. Peptides 31: 816-826.
7. Yin H, Ukena K, Ubuka T, Tsutsui K, (2005) A novel G protein-coupled receptor for gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica): identification, expression and binding activity. J Endocrinol 184: 257-266.
8. Bentley GE, Jensen JP, Kaur GJ, Wacker DW, Tsutsui K, et al. (2006) Rapid inhibition of female sexual behavior by gonadotropin-inhibitory hormone (GnIH). Horm Behav 49: 550-555.
9. Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, et al. (2000) New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2: 703-708.
10. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, et al. (2006) Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A 103: 2410-2415.
11. Ubuka T, Lai H, Kitani M, Suzuuchi A, Pham V, et al. (2009) Gonadotropin-inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol 517: 841-855.
12. Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, et al. (2009) 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.
13. 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.
14. Ubuka T, McGuire NL, Calisi RM, Perfito N, Bentley GE, (2008) The control of reproductive physiology and behavior by gonadotropin-inhibitory hormone. Integr Comp Biol 48: 560-569.
15. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
16. Pfaff D, Ribeiro A, Matthews J, Kow LM, (2008) Concepts and mechanisms of generalized central nervous system arousal. Ann N Y Acad Sci 1129: 11-25.
17. Pfaff DW, (2006) Brain arousal and information theory: neural and genetic mechanisms. Cambridge, MA Harvard University Press.
18. 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.
19. 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.
20. Osugi T, Ukena K, Bentley GE, O'Brien S, Moore IT, et al. (2004) Gonadotropin-inhibitory hormone in Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii): cDNA identification, transcript localization and functional effects in laboratory and field experiments. J Endocrinol 182: 33-42.
21. Chilton G, Baker MC, Barrentine CD, Cunningham MA, (1995) White-crowned Sparrow (Zonotrichia leucophrys). The Birds of North America Online (Poole, A. Ed.) Ithaca Cornell Lab of Ornithology http://bna.birds.cornell.edu/bna/species/183.
22. Spitler-Nabors KJ, Baker MC, (1983) Reproductive behavior by a female songbird: differential stimulation by natal and alien dialects. Condor 85: 491-494.
23. Hill BG, Lein MR, (1985) The non-song vocal repertoire of the white-crowned sparrow. Condor 87: 327-335.
24. Ubuka T, Bentley GE, Ukena K, Wingfield JC, Tsutsui K, (2005) Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc Natl Acad Sci U S A 102: 3052-3057.
25. Stokes TM, Leonard CM, Nottebohm F, (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J Comp Neurol 156: 337-374.
26. Wingfield JC, Farner DS, (1975) The determination of five steroids in avian plasma by radioimmunoassay and competitive protein-binding. Steroids 26: 311-321.
27. Wingfield JC, Hegner RE, Lewis D, (1991) Circulating levels of luteinizing hormone and steroid hormones in relation to social status in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. J Zool London 225: 43-58.
28. Nottebohm F, Kelley DB, Paton JA, (1982) Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol 207: 344-357.
29. Nottebohm F, Stokes TM, Leonard CM, (1976) Central control of song in the canary, Serinus canarius. J Comp Neurol 165: 457-486.
30. Lewis JW, Ryan SM, Arnold AP, Butcher LL, (1981) Evidence for a catecholaminergic projection to area×in the zebra finch. J Comp Neurol 196: 347-354.
31. Appeltants D, Absil P, Balthazart J, Ball GF, (2000) Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. J Chem Neuroanat 18: 117-133.
32. 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.
33. Burgus R, Butcher M, Amoss M, Ling N, Monahan M, et al. (1972) Primary structure of the ovine hypothalamic luteinizing hormone-releasing factor (LRF) (LH-hypothalamus-LRF-gas chromatography-mass spectrometry-decapeptide-Edman degradation). Proc Natl Acad Sci U S A 69: 278-282.
34. King JA, Millar RP, (1982) Structure of chicken hypothalamic luteinizing hormone-releasing hormone. I. Structural determination on partially purified material. J Biol Chem 257: 10722-10728.
35. Miyamoto K, Hasegawa Y, Minegishi T, Nomura M, Takahashi Y, et al. (1982) Isolation and characterization of chicken hypothalamic luteinizing hormone-releasing hormone. Biochem Biophys Res Commun 107: 820-827.
36. Ubuka T, Bentley GE, (2009) Identification, localization, and regulation of passerine GnRH-I messenger RNA. J Endocrinol 201: 81-87.
37. Ubuka T, Cadigan PA, Wang A, Liu J, Bentley GE, (2009) Identification of European starling GnRH-I precursor mRNA and its seasonal regulation. Gen Comp Endocrinol 162: 301-306.
38. Stevenson TJ, Lynch KS, Lamba P, Ball GF, Bernard DJ, (2009) Cloning of gonadotropin-releasing hormone I complementary DNAs in songbirds facilitates dissection of mechanisms mediating seasonal changes in reproduction. Endocrinology 150: 1826-1833.
39. Miyamoto K, Hasegawa Y, Nomura M, Igarashi M, Kangawa K, et al. (1984) Identification of the second gonadotropin-releasing hormone in chicken hypothalamus: evidence that gonadotropin secretion is probably controlled by two distinct gonadotropin-releasing hormones in avian species. Proc Natl Acad Sci U S A 81: 3874-3878.
40. Ubuka T, Bentley GE, (2010) Neuroendocrine control of reproduction in birds. In: Norris DO, Lopez KH, editors. Hormones and Reproduction of Vertebrates Vol 4. Birds Academic Press pp. 1-25.
41. Krebs MD, Alsberg E, (2011) Localized, targeted, and sustained siRNA delivery. Chemistry.doi:10.1002/chem.201003144.
42. Makimura H, Mizuno TM, Mastaitis JW, Agami R, Mobbs CV, (2002) Reducing hypothalamic AGRP by RNA interference increases metabolic rate and decreases body weight without influencing food intake. BMC Neurosci 3: 18.
43. Dorn G, Patel S, Wotherspoon G, Hemmings-Mieszczak M, Barclay J, et al. (2004) siRNA relieves chronic neuropathic pain. Nucleic Acids Res 32: e49.
44. Thakker DR, Natt F, Hüsken D, Maier R, Müller M, et al. (2004) Neurochemical and behavioral consequences of widespread gene knockdown in the adult mouse brain by using nonviral RNA interference. Proc Natl Acad Sci U S A 101: 17270-17275.
45. Thakker DR, Natt F, Hüsken D, van der Putten H, Maier R, et al. (2005) siRNA-mediated knockdown of the serotonin transporter in the adult mouse brain. Mol Psychiatry 10: 782-789.
46. Hoyer D, Thakker DR, Natt F, Maier R, Huesken D, et al. (2006) Global down-regulation of gene expression in the brain using RNA interference, with emphasis on monoamine transporters and GPCRs: implications for target characterization in psychiatric and neurological disorders. J Recept Signal Transduct Res 26: 527-547.
47. Weil ZM, Zhang Q, Hornung A, Blizard D, Pfaff DW, (2010) Impact of generalized brain arousal on sexual behavior. Proc Natl Acad Sci U S A 107: 2265-2270.
48. Nelson DA, Poesel A, (2010) Song length variation serves multiple functions in the white-crowned sparrow. Behav Ecol Sociobiol 65: 1103-1111.
49. Moss RL, McCann SM, (1973) Induction of mating behavior in rats by luteinizing hormone-releasing factor. Science 181: 177-179.
50. Pfaff DW, (1973) Luteinizing hormone-releasing factor potentiates lordosis behavior in hypophysectomized ovariectomized female rats. Science 182: 1148-1149.
51. Saper CB, Scammell TE, Lu J, (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437: 1257-1263.
52. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, et al. (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92: 573-585.
53. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, et al. (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95: 322-327.
54. Lin L, Faraco J, Li R, Kadotani H, Rogers W, et al. (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98: 365-376.
55. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, et al. (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98: 437-451.
56. Qi Y, Oldfield BJ, Clarke IJ, (2009) Projections of RFamide-related peptide-3 neurones in the ovine hypothalamus, with special reference to regions regulating energy balance and reproduction. J Neuroendocrinol 21: 690-697.