Murine arcuate nucleus kisspeptin neurons communicate with GnRH neurons in utero

Journal of Neuroscience

Volumn 34, Issue 10, 2014, Pages 3756-3766

  Kumar, Devesh ^a,b   Freese, Maria ^b   Drexler, Dagmar ^b   Hermans Borgmeyer, Irm ^b   Marquardt, Annette ^b   Boehm, Ulrich ^a,b  

^a SAARLAND UNIVERSITY   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Cre recombinase; Gene targeting; Genetic transneuronal tracing; GPR54; Kisspeptin; Puberty

Indexed keywords

ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; GREEN FLUORESCENT PROTEIN; KISSPEPTIN;

ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CELL COMMUNICATION; CONNECTOME; CONTROLLED STUDY; EMBRYO; FEMALE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; SIGNAL TRANSDUCTION; SYNAPSE;

CRE RECOMBINASE; GENE TARGETING; GENETIC TRANSNEURONAL TRACING; GPR54; KISSPEPTIN; PUBERTY;

ANIMALS; ARCUATE NUCLEUS; FEMALE; GONADOTROPIN-RELEASING HORMONE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; NERVE NET; NEURONS; PREGNANCY; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84895426401     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5123-13.2014     Document Type: Article

References (61)

1. Abreu A. P, Dauber A, Macedo DB, Noel SD, Brito VN, Gill JC, Cukier P, Thompson I. R, Navarro VM, Gagliardi PC, Rodrigues T, Kochi C, Longui CA, Beckers D, de Zegher F, Montenegro LR, Mendonca BB, Carroll RS, Hirschhorn J. N, Latronico AC, et al (2013) Central precocious puberty caused by mutations in the imprinted gene MKRN3. N Engl J Med 368: 2467-2475. CrossRef Medline
2. Agulnik A. I, Bishop CE, Lerner JL, Agulnik SI, Solovyev VV (1997) Analysis of mutation rates in the SMCY/SMCX genes shows that mammalian evolution is male driven. Mamm Genome 8:134-138. CrossRef Medline
3. Aubert M. L, Begeot M, Winiger BP, Morel G, Sizonenko PC, Dubois PM (1985) Ontogeny of hypothalamic luteinizing hormone-releasing hormone (GnRH) and pituitary GnRH receptors in fetal and neonatal rats. Endocrinology 116:1565-1576. CrossRef Medline
4. Bakker J, BaumMJ (2008) Role for estradiol in female-typical brain and behavioral sexual differentiation. Front Neuroendocrinol 29:1-16. CrossRef Medline
5. Boehm U., Zou Z, Buck LB (2005) Feedback loops link odor and pheromone signaling with reproduction. Cell 123:683-695. CrossRef Medline
6. Brock O., Bakker J (2013) The two kisspeptin neuronal populations are dif-ferentially organized and activated by estradiol in mice. Endocrinology 154:2739-2749. CrossRef Medline
7. Bronson F. H (1981) The regulation of luteinizing hormone secretion by estrogen: relationships among negative feedback, surge potential, and male stimulation in juvenile, peripubertal, and adult female mice. Endocrinology 108:506-516. CrossRef Medline
8. Buch T., Heppner FL, Tertilt C, Heinen TJ, Kremer M, Wunderlich FT, Jung S, Waisman A. (2005) A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods 2:419-426. CrossRef Medline
9. Callaway E. M (2008) Transneuronal circuit tracing with neurotropic viruses. Curr Opin Neurobiol 18:617-623. CrossRef Medline
10. Cao J., Patisaul HB (2011) Sexually dimorphic expression of hypothalamic estrogen receptors alpha and beta and Kiss1 in neonatal male and female rats. J Comp Neurol 519:2954-2977. CrossRef Medline
11. Castellano J. M, Gaytan M, Roa J, Vigo E, Navarro VM, Bellido C, Dieguez C, Aguilar E., Sánchez-Criado JE, Pellicer A, Pinilla L, Gaytan F, Tena-SempereM (2006) Expression of KiSS-1 in rat ovary: putative local regulator of ovulation? Endocrinology 147:4852-4862. CrossRef Medline
12. Clarkson J. (2013) Effects of estradiol on kisspeptin neurons during puberty. Front Neuroendocrinol 34:120-131. CrossRef Medline
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. CrossRef Medline
14. Clarkson J., Boon WC, Simpson ER, Herbison AE (2009a) Postnatal development of an estradiol-kisspeptin positive feedback mechanism implicated in puberty onset. Endocrinology 150:3214-3220. CrossRef Medline
15. Clarkson J., d'Anglemont de Tassigny X, Colledge WH, Caraty A, Herbison AE (2009b) Distribution of kisspeptin neurones in the adult female mouse brain. J Neuroendocrinol 21:673-682. CrossRef Medline
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. CrossRef Medline
17. Constantin S., Caligioni CS, Stojilkovic S, Wray S (2009a) Kisspeptin-10 facilitates a plasma membrane-driven calcium oscillator in gonadotropinreleasing hormone-1 neurons. Endocrinology 150:1400-1412. CrossRef Medline
18. Constantin S., Caraty A, Wray S, Duittoz AH (2009b) Development of gonadotropin-releasing hormone-1 secretion in mouse nasal explants. Endocrinology 150:3221-3227. CrossRef Medline
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. CrossRef Medline
20. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, 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. CrossRef Medline
21. Desroziers E., Droguerre M, Bentsen AH, Robert V, Mikkelsen JD, Caraty A, Tillet Y., Duittoz A, Franceschini I (2012) Embryonic development of kisspeptin neurones in rat. J Neuroendocrinol 24:1284-1295. CrossRef Medline
22. Dumalska I., Wu M, Morozova E, Liu R, van den Pol A, Alreja M (2008) Excitatory effects of the puberty-initiating peptide kisspeptin and group I metabotropic glutamate receptor agonists differentiate two distinct subpopulations of gonadotropin-releasing hormone neurons. J Neurosci 28: 8003-8013. CrossRef Medline
23. Fiorini Z., Jasoni CL (2010) A novel developmental role for kisspeptin in the growth of gonadotrophin-releasing hormone neurites to the median eminence in the mouse. J Neuroendocrinol 22:1113-1125. CrossRef Medline
24. Greco T. L, Payne AH (1994) Ontogeny of expression of the genes for steroidogenic enzymes P450 side-chain cleavage, 3 beta-hydroxysteroid dehydrogenase, P450 17 alpha-hydroxylase/C17-20 lyase, and P450 aromatase in fetal mouse gonads. Endocrinology 135:262-268. CrossRef Medline
25. Han S. K, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner R. A, 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. CrossRef Medline
26. Herbison A. E, de Tassigny Xd, Doran J, Colledge WH (2010) Distribution and postnatal development of Gpr54 gene expression in mouse brain and gonadotropin-releasing hormone neurons. Endocrinology 151:312-321. CrossRef Medline
27. Horowitz L. F, Montmayeur JP, Echelard Y, Buck LB (1999) A genetic approach to trace neural circuits. Proc Natl Acad Sci U S A 96:3194-3199. CrossRef Medline
28. Irwig M. S, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch M. L, 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. CrossRef Medline
29. Kaufmann M. H (2001) The atlas of mouse development, Ed 2. Amsterdam: Elsevier Academic.
30. Knoll J. G, Clay CM, Bouma GJ, Henion TR, Schwarting GA, Millar RP, Tobet SA (2013) Developmental profile and sexually dimorphic expression of kiss1 and kiss1r in the fetal mouse brain. Front Endocrinol (Lausanne) 4:140. CrossRef Medline
31. Lo L., Anderson DJ (2011) ACre-dependent, anterograde transsynaptic viral tracer for mapping output pathways of genetically marked neurons. Neuron 72:938-950. CrossRef Medline
32. Losa S. M, Todd KL, Sullivan AW, Cao J, Mickens JA, Patisaul HB (2011) Neonatal exposure to genistein adversely impacts the ontogeny of hypothalamic kisspeptin signaling pathways and ovarian development in the peripubertal female rat. Reprod Toxicol 31:280-289. CrossRef Medline
33. Low L. K, Cheng HJ (2006) Axon pruning: an essential step underlying the developmental plasticity of neuronal connections. Philos Trans R Soc Lond B Biol Sci 361:1531-1544. CrossRef Medline
34. Maskos U., Kissa K, St Cloment C, Brûlet P (2002) Retrograde trans-synaptic transfer of green fluorescent protein allows the genetic mapping of neuronal circuits in transgenic mice. Proc Natl Acad Sci U S A 99:10120-10125. CrossRef Medline
35. 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. CrossRef Medline
36. Mayer C., Boehm U (2011) Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat Neurosci 14:704-710. CrossRef Medline
37. Mayer C., Acosta-Martinez M, Dubois SL, Wolfe A, Radovick S, Boehm U, Levine J. E (2010) Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc Natl Acad Sci U S A 107:22693-22698. CrossRef Medline
38. Nakashiba T., Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188-201. CrossRef Medline
39. Navarro V. M, Fernández-Fernández R, Castellano JM, Roa J, Mayen A, Barreiro ML, Gaytan F, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M (2004) Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 561:379-386. CrossRef Medline
40. Norgren R. B Jr, LehmanMN (1998) Herpes simplex virus as a transneuronal tracer. Neurosci Biobehav Rev 22:695-708. CrossRef Medline
41. Oakley A. E, Clifton DK, Steiner RA (2009) Kisspeptin signaling in the brain. Endocr Rev 30:713-743. CrossRef Medline
42. Pineda R., Garcia-Galiano D, Roseweir A, Romero M, Sanchez-Garrido MA, Ruiz-Pino F, Morgan K, Pinilla L, Millar RP, Tena-Sempere M (2010) Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology 151:722-730. CrossRef Medline
43. Poling M. C, Kauffman AS (2012) Sexually dimorphic testosterone secretion in prenatal and neonatal mice is independent of kisspeptin-Kiss1r and GnRH signaling. Endocrinology 153:782-793. CrossRef Medline
44. Poling M. C, Kauffman AS (2013) Organizational and activational effects of sex steroids on kisspeptin neuron development. Front Neuroendocrinol 34:3-17. CrossRef Medline
45. Rodriguez I., Feinstein P, Mombaerts P (1999) Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199-208. CrossRef Medline
46. Schambra U. (2008) Prenatal mouse brain atlas. New York: Springer.
47. Schwanzel-Fukuda M, Pfaff DW (1989) Origin of luteinizing hormonereleasing hormone neurons. Nature 338:161-164. CrossRef Medline
48. Semaan S. J, Murray EK, Poling MC, Dhamija S, Forger NG, Kauffman AS (2010) BAX-dependent and BAX-independent regulation of Kiss1 neuron development in mice. Endocrinology 151:5807-5817. CrossRef Medline
49. Seminara S. B, Crowley WF Jr (2008) Kisspeptin and GPR54: discovery of a novel pathway in reproduction. J Neuroendocrinol 20:727-731. CrossRef Medline
50. Seminara S. B, 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, CrowleyWFJr, Aparicio SA, ColledgeWH (2003) The GPR54 gene as a regulator of puberty. NEngl J Med 349:1614-1627. CrossRef Medline
51. Sisk C. L, Foster DL (2004) The neural basis of puberty and adolescence. Nat Neurosci 7:1040-1047. CrossRef Medline
52. Smith J. T, Popa SM, Clifton DK, Hoffman GE, Steiner RA (2006) Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 26:6687-6694. CrossRef Medline
53. Styne D. M, Grumbach MM (2008) Puberty: ontogeny, neuroendocrinology, physiology, and disorders. In: Williams textbook of endocrinology, Ed 10 (Larsen PR, Kronenberg HM, Melmed S, Larsen PR, eds), pp 969-1166. Philadelphia: Saunders.
54. Tabuchi K., Sawamoto K, Suzuki E, Ozaki K, Sone M, Hama C, Tanifuji-Morimoto T., Yuasa Y, Yoshihara Y, Nose A, Okano H (2000) GAL4/ UAS-WGA system as a powerful tool for tracing Drosophila transsynaptic neural pathways. J Neurosci Res 59:94-99. CrossRef Medline
55. Teles M. G, Bianco SD, Brito VN, Trarbach EB, Kuohung W, Xu S, Seminara SB, Mendonca BB, Kaiser UB, Latronico AC (2008) A GPR54-activating mutation in a patient with central precocious puberty. N Engl J Med 358:709-715. CrossRef Medline
56. Terasawa E., FernandezDL (2001) Neurobiological mechanisms of the onset of puberty in primates. Endocr Rev 22:111-151. CrossRef Medline
57. Topaloglu A. K, Tello JA, Kotan LD, Ozbek MN, Yilmaz MB, Erdogan S, Gurbuz F, Temiz F, Millar RP, Yuksel B (2012) Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N Engl J Med 366:629-635. CrossRef Medline
58. Wen S., Ai W, Alim Z, Boehm U (2010) Embryonic gonadotropin-releasing hormone signaling is necessary for maturation of the male reproductive axis. Proc Natl Acad Sci U S A 107:16372-16377. CrossRef Medline
59. Wen S., Götze IN, Mai O, Schauer C, Leinders-Zufall T, Boehm U (2011) Genetic identification of GnRH receptor neurons: a new model for studying neural circuits underlying reproductive physiology in the mouse brain. Endocrinology 152:1515-1526. CrossRef Medline
60. Wray S., Grant P, Gainer H (1989) Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc Natl Acad Sci U S A 86:8132-8136. CrossRef Medline
61. Yeo S. H, Herbison AE (2011) Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology 152:2387-2399. CrossRef Medline