Photoperiodic co-regulation of kisseptin, neurokinin B and dynorphin in the hypothalamus of a seasonal rodent

Journal of Neuroendocrinology

Volumn 26, Issue 8, 2014, Pages 510-520

  Bartzen Sprauer, J ^a   Klosen, P ^a   Ciofi, P ^b,c   Mikkelsen, J D ^d   Simonneaux, V ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT FRANÇOIS MAGENDIE   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d Rigshospitalet   (Denmark)

Author keywords

Dynorphin; Kisspeptin; Neurokinin B; RFRP 3; Seasonal reproduction

Indexed keywords

DYNORPHIN; G PROTEIN COUPLED RECEPTOR 54; KISSPEPTIN; NEUROKININ B; NEUROPEPTIDE; RFAMIDE PEPTIDE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN CORTEX; BRAIN THIRD VENTRICLE; CONTROLLED STUDY; FOOD INTAKE; HYPOTHALAMUS; LATERAL HYPOTHALAMUS; MALE; MAMMILLARY BODY; MEDIAN EMINENCE; MEDIOBASAL HYPOTHALAMUS; NONHUMAN; PHOTOPERIODICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEASONAL VARIATION; SEXUAL BEHAVIOR; STRIA TERMINALIS; SUBSTANTIA NIGRA; SUPRACHIASMATIC NUCLEUS; SUPRAOPTIC NUCLEUS; SYRIAN HAMSTER; ANIMAL; BIOSYNTHESIS; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; GENE EXPRESSION REGULATION; HAMSTER; MESOCRICETUS; METABOLISM; NERVE CELL; SEASON;

ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; CRICETINAE; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; DYNORPHINS; GENE EXPRESSION REGULATION; KISSPEPTINS; MALE; MESOCRICETUS; NEUROKININ B; NEURONS; NEUROPEPTIDES; PHOTOPERIOD; SEASONS;

EID: 84904577193     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12171     Document Type: Article

References (68)

1. Simonneaux V, Ribelayga C. Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol Rev 2003; 55: 325-395.
2. Reiter RJ. Photoperiod: its importance as an impeller of pineal and seasonal reproductive rhythms. Int J Biometeorol 1980; 24: 57-63.
3. Revel FG, Saboureau M, Masson-Pévet M, Pévet P, Mikkelsen JD, Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol 2006; 16: 1730-1735.
4. Revel FG, Saboureau M, Pévet P, Simonneaux V, Mikkelsen JD. RFamide-related peptide gene is a melatonin-driven photoperiodic gene. Endocrinology 2008; 149: 902-912.
5. Bentley GE, Tsutsui K, Kriegsfeld LJ. Recent studies of gonadotropin-inhibitory hormone (GnIH) in the mammalian hypothalamus, pituitary and gonads. Brain Res 2010; 1364: 62-71.
6. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 2012; 92: 1235-1316.
7. Lee JH, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE, Welch DR. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst 1996; 88: 1731-1737.
8. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brézillon 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.
9. 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.
10. 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.
11. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145: 4073-4077.
12. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006; 147: 5817-5825.
13. Uenoyama Y, Inoue N, Pheng V, Homma T, Takase K, Yamada S, Ajiki K, Ichikawa M, Okamura H, Maeda KI, Tsukamura H. Ultrastructural evidence of kisspeptin-gonadotrophin-releasing hormone (GnRH) interaction in the median eminence of female rats: implication of axo-axonal regulation of GnRH release. J Neuroendocrinol 2011; 23: 863-870.
14. 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.
15. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005; 25: 11349-11356.
16. 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.
17. 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.
18. 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 USA 2006; 103: 2410-2415.
19. Gibson EM, Humber SA, Jain S, Williams WP 3rd, Zhao S, Bentley GE, Tsutsui K, Kriegsfeld LJ. Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology 2008; 149: 4958-4969.
20. 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.
21. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenröhr 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.
22. Ancel C, Bentsen AH, Sébert 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.
23. Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, Tsutsui K. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology 2012; 153: 373-385.
24. Burke MC, Letts PA, Krajewski SJ, Rance NE. Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: Morphologic evidence of interrelated function within the arcuate nucleus. J Comp Neurol 2006; 498: 712-726.
25. Ciofi P, Leroy D, Tramu G. Sexual dimorphism in the organization of the rat hypothalamic infundibular area. Neuroscience 2006; 141: 1731-1745.
26. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H. Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci 2010; 30: 3124-3132.
27. Lehman MN, Coolen LM, Goodman RL. Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology 2010; 151: 3479-3489.
28. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet 2009; 41: 354-358.
29. Yang JJ, Caligioni CS, Chan YM, Seminara SB. Uncovering novel reproductive defects in neurokinin B receptor null mice: closing the gap between mice and men. Endocrinology 2012; 153: 1498-1508.
30. Klosen P, Maessen X, van den Bosch de Aguilar P. PEG embedding for immunocytochemistry: application to the analysis of immunoreactivity loss during histological processing. J Histochem Cytochem 1993; 41: 455-463.
31. Mikkelsen JD, Simonneaux V. The neuroanatomy of the kisspeptin system in the mammalian brain. Peptides 2009; 30: 26-33.
32. 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.
33. Ciofi P, Krause JE, Prins GS, Mazzuca M. Presence of nuclear androgen receptor-like immunoreactivity in neurokinin B-containing neurons of the hypothalamic arcuate nucleus of the adult male rat. Neurosci Lett 1994; 182: 193-196.
34. Griffond B, Deray A, Fellmann D, Ciofi P, Croix D, Bugnon C. Colocalization of prolactin- and dynorphin-like substances in a neuronal population of the rat lateral hypothalamus. Neurosci Lett 1993; 156: 91-95.
35. Marin LP, Wood RI. Stereotaxic Atlas of the Golden Hamster Brain. San Diego, CA: Academic Press, 2001.
36. Simonneaux V, Ancel C, Poirel VJ, Gauer F. Kisspeptins and RFRP-3 act in concert to synchronize rodent reproduction with seasons. Front Neurosci 2013; 7: 22.
37. Ansel L, Bolborea M, Bentsen AH, Klosen P, Mikkelsen JD, Simonneaux V. Differential regulation of kiss1 expression by melatonin and gonadal hormones in male and female Syrian hamsters. J Biol Rhythms 2010; 25: 81-91.
38. Brailoiu GC, Dun SL, Ohsawa M, Yin D, Yang J, Chang JK, Brailoiu E, Dun NJ. KiSS-1 expression and metastin-like immunoreactivity in the rat brain. J Comp Neurol 2005; 481: 314-329.
39. 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. Eur J Neurosci 2010; 32: 2031-2041.
40. Mason AO, Duffy S, Zhao S, Ubuka T, Bentley GE, Tsutsui K, Silver R, Kriegsfeld LJ. Photoperiod and reproductive condition are associated with changes in RFamide-related peptide (RFRP) expression in Syrian hamsters (Mesocricetus auratus). J Biol Rhythms 2010; 25: 176-185.
41. 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. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 2008; 149: 5770-5782.
42. Dardente H, Birnie M, Lincoln GA, Hazlerigg DG. RFamide-related peptide and its cognate receptor in the sheep: cDNA cloning, mRNA distribution in the hypothalamus and the effect of photoperiod. J Neuroendocrinol 2008; 20: 1252-1259.
43. Janati A, Talbi R, Klosen P, Mikkelsen JD, Magoul R, Simonneaux V, El Ouezzani S. Distribution and seasonal variation in hypothalamic RF-amide peptides in a semi-desert rodent, the jerboa. J Neuroendocrinol 2013; 25: 402-411.
44. Greives TJ, Humber SA, Goldstein AN, Scotti MA, Demas GE, Kriegsfeld LJ. Photoperiod and testosterone interact to drive seasonal changes in kisspeptin expression in Siberian hamsters (Phodopus sungorus). J Neuroendocrinol 2008; 20: 1339-1347.
45. Wagner GC, Johnston JD, Clarke IJ, Lincoln GA, Hazlerigg DG. Redefining the limits of day length responsiveness in a seasonal mammal. Endocrinology 2008; 149: 32-39.
46. Quennell JH, Howell CS, Roa J, Augustine RA, Grattan DR, Anderson GM. Leptin deficiency and diet-induced obesity reduce hypothalamic kisspeptin expression in mice. Endocrinology 2011; 152: 1541-1550.
47. Marksteiner J, Saria A, Krause JE. Comparative distribution of neurokinin B-, substance P- and enkephalin-like immunoreactivities and neurokinin B messenger RNA in the basal forebrain of the rat: evidence for neurochemical compartmentation. Neuroscience 1992; 51: 107-120.
48. Amstalden M, Coolen LM, Hemmerle AM, Billings HJ, Connors JM, Goodman RL, Lehman MN. Neurokinin 3 receptor immunoreactivity in the septal region, preoptic area and hypothalamus of the female sheep: colocalisation in neurokinin B cells of the arcuate nucleus but not in gonadotrophin-releasing hormone neurones. J Neuroendocrinol 2010; 22: 1-12.
49. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 2009; 29: 11859-11866.
50. Zamir N, Palkovits M, Brownstein MJ. Distribution of immunoreactive dynorphin in the central nervous system of the rat. Brain Res 1983; 280: 81-93.
51. Lin S, Boey D, Lee N, Schwarzer C, Sainsbury A, Herzog H. Distribution of prodynorphin mRNA and its interaction with the NPY system in the mouse brain. Neuropeptides 2006; 40: 115-123.
52. Foradori CD, Goodman RL, Lehman MN. Distribution of preprodynorphin mRNA and dynorphin-a immunoreactivity in the sheep preoptic area and hypothalamus. Neuroscience 2005; 130: 409-418.
53. Hurd YL. Differential messenger RNA expression of prodynorphin and proenkephalin in the human brain. Neuroscience 1996; 72: 767-783.
54. Goodman RL, Maltby MJ, Millar RP, Hileman SM, Nestor CC, Whited B, Tseng AS, Coolen LM, Lehman MN. Evidence that dopamine acts via kisspeptin to hold GnRH pulse frequency in check in anestrous ewes. Endocrinology 2012; 153: 5918-5927.
55. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CV, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 2007; 148: 5752-5760.
56. Rometo AM, Rance NE. Changes in prodynorphin gene expression and neuronal morphology in the hypothalamus of postmenopausal women. J Neuroendocrinol 2008; 20: 1376-1381.
57. Eghlidi DH, Haley GE, Noriega NC, Kohama SG, Urbanski HF. Influence of age and 17beta-estradiol on kisspeptin, neurokinin B, and prodynorphin gene expression in the arcuate-median eminence of female rhesus macaques. Endocrinology 2010; 151: 3783-3794.
58. Krajewski SJ, Burke MC, Anderson MJ, McMullen NT, Rance NE. Forebrain projections of arcuate neurokinin B neurons demonstrated by anterograde tract-tracing and monosodium glutamate lesions in the rat. Neuroscience 2010; 166: 680-697.
59. Todman MG, Han SK, Herbison AE. Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent protein-promoter transgenics and microarrays. Neuroscience 2005; 132: 703-712.
60. Krajewski SJ, Anderson MJ, Iles-Shih L, Chen KJ, Urbanski HF, Rance NE. Morphologic evidence that neurokinin B modulates gonadotropin-releasing hormone secretion via neurokinin 3 receptors in the rat median eminence. J Comp Neurol 2005; 489: 372-386.
61. Mijiddorj T, Kanasaki H, Purwana IN, Oride A, Sukhbaatar U, Miyazaki K. Role of neurokinin B and dynorphin A in pituitary gonadotroph and somatolactotroph cell lines. Endocr J 2012; 59: 631-640.
62. Clarke IJ, Qi Y, Puspita Sari I, Smith JT. Evidence that RF-amide related peptides are inhibitors of reproduction in mammals. Front Neuroendocrinol 2009; 30: 371-378.
63. Sandoval-Guzmán T, Rance NE. Central injection of senktide, an NK3 receptor agonist, or neuropeptide Y inhibits LH secretion and induces different patterns of Fos expression in the rat hypothalamus. Brain Res 2004; 1026: 307-312.
64. Billings HJ, Connors JM, Altman SN, Hileman SM, Holaskova I, Lehman MN, McManus CJ, Nestor CC, Jacobs BH, Goodman RL. Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology 2010; 151: 3836-3846.
65. Navarro VM, Castellano JM, McConkey SM, Pineda R, Ruiz-Pino F, Pinilla L, Clifton DK, Tena-Sempere M, Steiner RA. Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat. Am J Physiol Endocrinol Metab 2011; 300: E202-E210.
66. Ferin M, Vande Wiele R. Endogenous opioid peptides and the control of the menstrual cycle. Eur J Obstet Gynecol Reprod Biol 1984; 18: 365-373.
67. Goodman RL, Coolen LM, Anderson GM, Hardy SL, Valent M, Connors JM, Fitzgerald ME, Lehman MN. Evidence that dynorphin plays a major role in mediating progesterone negative feedback on gonadotropin-releasing hormone neurons in sheep. Endocrinology 2004; 145: 2959-2967.
68. Choe HK, Kim HD, Park SH, Lee HW, Park JY, Seong JY, Lightman SL, Son GH, Kim K. Synchronous activation of gonadotropin-releasing hormone gene transcription and secretion by pulsatile kisspeptin stimulation. Proc Natl Acad Sci USA 2013; 110: 5677-5682.