Immunohistochemical evidence for the presence of various kisspeptin isoforms in the mammalian brain

Journal of Neuroendocrinology

Volumn 25, Issue 9, 2013, Pages 839-851

  Franceschini, I ^a,b,c,d   Yeo, S H ^e,g   Beltramo, M ^a,b,c,d   Desroziers, E ^a,b,c,d   Okamura, H ^f   Herbison, A E ^e   Caraty, A ^a,b,c,d  

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

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d IFCE   (France)

^e UNIVERSITY OF OTAGO   (New Zealand)

^f NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Antibodies; Brain; Immunohistochemistry; Kisspeptin

Indexed keywords

GONADORELIN; KISSPEPTIN; METASTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN LEVEL; CARBOXY TERMINAL SEQUENCE; CLINICAL RESEARCH; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; FOREBRAIN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MAMMAL; MOUSE; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PUBERTY; RAT; SEQUENCE ANALYSIS; TISSUE DISTRIBUTION;

ANTIBODIES; BRAIN; IMMUNOHISTOCHEMISTRY; KISSPEPTIN;

ANIMALS; BRAIN; CELL COUNT; ESTROUS CYCLE; FEMALE; IMMUNOHISTOCHEMISTRY; KISSPEPTINS; MALE; MICE; MICE, KNOCKOUT; NEURONS; PROTEIN ISOFORMS; RATS;

EID: 84882700289     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12069     Document Type: Article

References (47)

1. 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. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001; 276: 34631-34636.
2. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 2003; 100: 10972-10976.
3. 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. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349: 1614-1627.
4. Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ, Gustafson EL. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003; 312: 1357-1363.
5. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005; 102: 1761-1766.
6. Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, Gaytan F, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 2004; 561: 379-386.
7. Caraty A, Smith JT, Lomet D, Ben Said S, Morrissey A, Cognie J, Doughton B, Baril G, Briant C, Clarke IJ. Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 2007; 148: 5258-5267.
8. Lehman MN, Merkley CM, Coolen LM, Goodman RL. Anatomy of the kisspeptin neural network in mammals. Brain Res 2010; 1364: 90-102.
9. Smith JT, Shahab M, Pereira A, Pau KY, Clarke IJ. Hypothalamic expression of KISS1 and gonadotropin inhibitory hormone genes during the menstrual cycle of a non-human primate. Biol Reprod 2010; 83: 568-577.
10. Hrabovszky E, Ciofi P, Vida B, Horvath MC, Keller E, Caraty A, Bloom SR, Ghatei MA, Dhillo WS, Liposits Z, Kallo I. The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin-releasing hormone and neurokinin B neurons. Eur J Neurosci 2010; 31: 1984-1998.
11. Bosch MA, Xue C, Ronnekleiv OK. Kisspeptin expression in guinea pig hypothalamus: effects of 17beta-estradiol. J Comp Neurol 2012; 520: 2143-2162.
12. Clarkson J, d'Anglemont de Tassigny X, Colledge WH, Caraty A, Herbison AE. Distribution of kisspeptin neurones in the adult female mouse brain. J Neuroendocrinol 2009; 21: 673-682.
13. Roa J, Navarro VM, Tena-Sempere M. Kisspeptins in reproductive biology: consensus knowledge and recent developments. Biol Reprod 2011; 85: 650-660.
14. Terasawa E, Kurian JR, Guerriero KA, Kenealy BP, Hutz ED, Keen KL. Recent discoveries on the control of gonadotrophin-releasing hormone neurones in nonhuman primates. J Neuroendocrinol 2010; 22: 630-638.
15. Clarkson J, Han SK, Liu X, Lee K, Herbison AE. Neurobiological mechanisms underlying kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty. Mol Cell Endocrinol 2010; 324: 45-50.
16. Bilban M, Ghaffari-Tabrizi N, Hintermann E, Bauer S, Molzer S, Zoratti C, Malli R, Sharabi A, Hiden U, Graier W, Knofler M, Andreae F, Wagner O, Quaranta V, Desoye G. Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci 2004; 117: 1319-1328.
17. 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. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol 2009; 21: 527-537.
18. Desroziers E, Mikkelsen J, Simonneaux V, Keller M, Tillet Y, Caraty A, Franceschini I. Mapping of kisspeptin fibres in the brain of the pro-oestrous rat. J Neuroendocrinol 2010; 22: 1101-1112.
19. Clarke IJ. Control of GnRH secretion: one step back. Front Neuroendocrinol 2011; 32: 367-375.
20. Mikkelsen JD, Simonneaux V. The neuroanatomy of the kisspeptin system in the mammalian brain. Peptides 2009; 30: 26-33.
21. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA, Bloom SR. Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 2005; 90: 6609-6615.
22. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 2005; 146: 4431-4438.
23. Iijima N, Takumi K, Sawai N, Ozawa H. An immunohistochemical study on the expressional dynamics of kisspeptin neurons relevant to GnRH neurons using a newly developed anti-kisspeptin antibody. J Mol Neurosci 2010; 43: 146-154.
24. Porteous R, Petersen SL, Yeo SH, Bhattarai JP, Ciofi P, de Tassigny XD, Colledge WH, Caraty A, Herbison AE. Kisspeptin neurons co-express met-enkephalin and galanin in the rostral periventricular region of the female mouse hypothalamus. J Comp Neurol 2011; 519: 3456-3469.
25. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006; 401: 225-230.
26. Greives TJ, Mason AO, Scotti MA, Levine J, Ketterson ED, Kriegsfeld LJ, Demas GE. Environmental control of kisspeptin: implications for seasonal reproduction. Endocrinology 2007; 148: 1158-1166.
27. Ramaswamy S, Guerriero KA, Gibbs RB, Plant TM. 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 2008; 149: 4387-4395.
28. Nakada T, Wakabayashi Y, Ohkura S, Maeda K, Okamura H. Distribution of kisspeptin neurons in the Shiba goat brain: an immunohistochemical srtudy using two polyclonal antibodies against different epitopes of goat kisspeptin. Proc First World Conference on Kisspeptin Signaling in the Brain, Cordoba, Spain, 2008; p 104.
29. Caraty A, de Reviers MM, Pelletier J, Dubois MP. Reassessment of LRF radioimmunoassay in the plasma and hypothalamic extracts of rats and rams. Reprod Nutr Dev 1980; 20: 1489-1501.
30. 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. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc Natl Acad Sci USA 2007; 104: 10714-10719.
31. 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. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 2007; 53: 367-378.
32. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. New York, NY: Academic Press, 2001.
33. d'Anglemont de Tassigny X, Fagg LA, Carlton MB, Colledge WH. Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 2008; 149: 3926-3932.
34. Thompson EL, Murphy KG, Patterson M, Bewick GA, Stamp GW, Curtis AE, Cooke JH, Jethwa PH, Todd JF, Ghatei MA, Bloom SR. Chronic subcutaneous administration of kisspeptin-54 causes testicular degeneration in adult male rats. Am J Physiol Endocrinol Metab 2006; 291: E1074-E1082.
35. Pheng V, Uenoyama Y, Homma T, Inamoto Y, Takase K, Yoshizawa-Kumagaye K, Isaka S, Watanabe TX, Ohkura S, Tomikawa J, Maeda K, Tsukamura H. Potencies of centrally- or peripherally-injected full-length kisspeptin or its C-terminal decapeptide on LH release in intact male rats. J Reprod Dev 2009; 55: 378-382.
36. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007; 148: 1774-1783.
37. Takumi K, Iijima N, Ozawa H. Developmental changes in the expression of kisspeptin mRNA in rat hypothalamus. J Mol Neurosci 2010; 43: 138-145.
38. Desroziers E, Droguerre M, Bentsen AH, Robert V, Mikkelsen JD, Caraty A, Tillet Y, Duittoz A, Franceschini I. Embryonic development of kisspeptin neurones in rat. J Neuroendocrinol 2012; 24: 1284-1295.
39. Hoffman GE, Le WW, Sita LV. The importance of titrating antibodies for immunocytochemical methods. Curr Protoc Neurosci 2008; Chapter 2: Unit 2.12.
40. de Croft S, Piet R, Mayer C, Mai O, Boehm U, Herbison AE. Spontaneous kisspeptin neuron firing in the adult mouse reveals marked sex and brain region differences but no support for a direct role in negative feedback. Endocrinology 2012; 153: 5384-5393.
41. Wilkinson CW. Roles of acetylation and other post-translational modifications in melanocortin function and interactions with endorphins. Peptides 2006; 27: 453-471.
42. Masui T, Doi R, Mori T, Toyoda E, Koizumi M, Kami K, Ito D, Peiper SC, Broach JR, Oishi S, Niida A, Fujii N, Imamura M. Metastin and its variant forms suppress migration of pancreatic cancer cells. Biochem Biophys Res Commun 2004; 315: 85-92.
43. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005; 146: 3686-3692.
44. Decourt C, Tillet Y, Caraty A, Franceschini I, Briant C. Kisspeptin immunoreactive neurons in the equine hypothalamus Interactions with GnRH neuronal system. J Chem Neuroanat 2008; 36: 131-137.
45. Kriegsfeld LJ. Driving reproduction: RFamide peptides behind the wheel. Horm Behav 2006; 50: 655-666.
46. Rizwan MZ, Porteous R, Herbison AE, Anderson GM. Cells expressing RFamide-related peptide-1/3, the mammalian gonadotropin-inhibitory hormone orthologs, are not hypophysiotropic neuroendocrine neurons in the rat. Endocrinology 2009; 150: 1413-1420.
47. 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.