Disparate changes in kisspeptin and neurokinin B expression in the arcuate nucleus after sex steroid manipulation reveal differential regulation of the two KNDy peptides in rats

Endocrinology (United States)

Volumn 155, Issue 10, 2014, Pages 3945-3955

  Overgaard, Agnete ^a   Ruiz Pino, Francisco ^b,c,d   Castellano, Juan M ^b,e   Tena Sempere, Manuel ^b,c,d   Mikkelsen, Jens D ^a  

^a University of Copenhagen   (Denmark)

^b UNIVERSITY OF CÓRDOBA   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNORPHIN A; ESTRADIOL; KISSPEPTIN; NEUROKININ B; SEX HORMONE; DYNORPHIN; KISS1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CELLULAR PARAMETERS; CONTROLLED STUDY; FEMALE; FIBER DENSITY; GONADECTOMY; HORMONE SUBSTITUTION; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; MALE; NERVE CELL; NONHUMAN; OVARIECTOMY; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SEX DIFFERENCE; ANIMAL; CASTRATION; CELL COUNT; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT; WISTAR RAT;

ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; CASTRATION; CELL COUNT; DYNORPHINS; FEMALE; GONADAL STEROID HORMONES; KISSPEPTINS; MALE; NEUROKININ B; NEURONS; RATS; RATS, WISTAR; SEX CHARACTERISTICS;

EID: 84907212740     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1200     Document Type: Article

References (54)

1. Cheng G, Coolen LM, Padmanabhan V, Goodman RL, Lehman MN. The kisspeptin/neurokinin B/dynorphin (KNDy) cell population of the arcuate nucleus: sex differences and effects of prenatal testosterone in sheep. Endocrinology. 2010;151(1):301-311.
2. 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(38):11859-11866.
3. 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(8):3479-3489.
4. Keen KL, Wegner FH, Bloom SR, Ghatei MA, Terasawa E. An increase in kisspeptin-54 release occurs with the pubertal increase in luteinizing hormone-releasing hormone-1 release in the stalk-median eminence of female rhesus monkeys in vivo. Endocrinology. 2008;149(8):4151-4157.
5. Messager S, Chatzidaki EE, Ma D, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release viaGprotein-coupled receptor 1. Proc Natl Acad Sci USA. 2005;102(5):1761-1766
6. Wakabayashi Y, Nakada T, Murata K, et al. Neurokinin B and dynorphinAin 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(8):3124-3132.
7. 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(5):712-726.
8. Amstalden M, Coolen LM, Hemmerle AM, et al. 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):1-12.
9. Foradori CD, Amstalden M, Goodman RL, Lehman MN. Colocalisation of dynorphin a and neurokinin B immunoreactivity in the arcuate nucleus and median eminence of the sheep. J Neuroendocrinol. 2006;18(7):534-541.
10. Goodman RL, Lehman MN, Smith JT, et al. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology. 2007;148(12):5752-5760.
11. Navarro VM, Gottsch ML, Wu M, et al. Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse. Endocrinology. 2011;152(11):4265-4275.
12. Hrabovszky E, Molnar CS, Sipos MT, et al. Sexual dimorphism of kisspeptin and neurokinin B immunoreactive neurons in the infundibular nucleus of agedmenand women. Front Endocrinol (Lausanne). 2011;2:80.
13. Molnar CS, Vida B, Sipos MT, et al. Morphological evidence for enhanced kisspeptin and neurokinin B signaling in the infundibular nucleus of the aging man. Endocrinology. 2012;153(11):5428-5439.
14. Hrabovszky E, Sipos MT, Molnar CS, et al. Low degree of overlap between kisspeptin, neurokinin B, and dynorphin immunoreactivities in the infundibular nucleus of young male human subjects challenges the KNDy neuron concept. Endocrinology. 2012;153(10): 4978-4989.
15. Kauffman AS, Navarro VM, Kim J, Clifton DK, Steiner RA. Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. Am J Physiol Endocrinol Metab, 2009;297(5): E1212-E1221.
16. 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(9):3686-3692.
17. Smith JT, Dungan HM, Stoll EA, et al. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology. 2005;146(7):2976-2984.
18. Dellovade TL, Merchenthaler I. Estrogen regulation of neurokinin B gene expression in the mouse arcuate nucleus is mediated by estrogen receptor alpha. Endocrinology. 2004;145(2):736-742.
19. Danzer SC, Price RO, McMullen NT, Rance NE. Sex steroid modulation of neurokinin B gene expression in the arcuate nucleus of adult male rats. Brain Res Mol Brain Res. 1999;66(1-2):200-204.
20. Gill JC, NavarroVM,KwongC, et al. Increased neurokininB(Tac2) expression in the mouse arcuate nucleus is an early marker of pubertal onset with differential sensitivity to sex steroid-negative feedback than Kiss1. Endocrinology. 2012;153(10):4883-4893.
21. Overgaard A, Tena-Sempere M, Franceschini I, Desroziers E, Simonneaux V, Mikkelsen JD. Comparative analysis of kisspeptin-immunoreactivity reveals genuine differences in the hypothalamic Kiss1 systems between rats and mice. Peptides. 2013;45:85-90.
22. Desroziers E, Mikkelsen JD, Duittoz A, Franceschini I. Kisspeptinimmunoreactivity changes in a sex-and hypothalamic-region-specific manner across rat postnatal development. J Neuroendocrinol. 2012;24(8):1154-1165.
23. Takumi K, Iijima N, Ozawa H. Developmental changes in the expression of kisspeptin mRNA in rat hypothalamus. J Mol Neurosci. 2011;43(2):138-145.
24. Kauffman AS, Gottsch ML, Roa J, et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology. 2007; 148(4):1774-1783.
25. Sandoval-Guzman T, Stalcup ST, Krajewski SJ, Voytko ML, Rance NE. Effects of ovariectomy on the neuroendocrine axes regulating reproduction and energy balance in young cynomolgus macaques. J Neuroendocrinol. 2004;16(2):146-153.
26. Navarro VM, Ruiz-Pino F, Sanchez-Garrido MA, et al. Role of neurokinin B in the control of female puberty and its modulation by metabolic status. J Neurosci. 2012;32(7):2388-2397.
27. Billings HJ, Connors JM, Altman SN, et al. NeurokininBacts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology. 2010;151(8): 3836-3846.
28. Kinsey-Jones JS, Grachev P, Li XF, et al. The inhibitory effects of neurokinin B on GnRH pulse generator frequency in the female rat. Endocrinology. 2012;153(1):307-315.
29. Sakamoto K, Murata K, Wakabayashi Y, et al. Central administration of neurokininBactivates kisspeptin/NKB neurons in the arcuate nucleus and stimulates luteinizing hormone secretion in ewes during the non-breeding season. J Reprod Dev. 2012;58(6):700-706.
30. Ruiz-Pino F, Navarro VM, Bentsen AH, et al. Neurokinin B and the control of the gonadotropic axis in the rat: developmental changes, sexual dimorphism, and regulation by gonadal steroids. Endocrinology. 2012;153(10):4818-4829.
31. Roa J, Vigo E, Castellano JM, et al. Opposite roles of estrogen receptor (ER)-and ER in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology. 2008;149(4): 1627-1637.
32. Navarro VM, Castellano JM, McConkey SM, et al. Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat.AmJ Physiol Endocrinol Metab. 2011;300(1): E202-E210.
33. Goodman RL. A quantitative analysis of the physiological role of estradiol and progesterone in the control of tonic and surge secretion of luteinizing hormone in the rat. Endocrinology. 1978;102(1):142-150.
34. Bentsen AH, Ansel L, Simonneaux V, Tena-Sempere M, Juul A, Mikkelsen JD. Maturation of kisspeptinergic neurons coincides with puberty onset in male rats. Peptides. 2010;31(2):275-283.
35. Desroziers E, Mikkelsen J, Simonneaux V, et al. Mapping of kisspeptin fibres in the brain of the pro-oestrous rat. J Neuroendocrinol. 2010;22(10):1101-1112.
36. Ciofi P, Lapirot OC, Tramu G. An androgen-dependent sexual dimorphism visible at puberty in the rat hypothalamus. Neuroscience. 2007;146(2):630-642.
37. Ciofi P, Leroy D, Tramu G. Sexual dimorphism in the organization of the rat hypothalamic infundibular area. Neuroscience. 2006; 141(4):1731-1745.
38. Marksteiner J, Sperk G, Krause JE. Distribution of neurons expressing neurokinin B in the rat brain: immunohistochemistry and in situ hybridization. J Comp Neurol. 1992;317(4):341-356.
39. Franceschini I, Yeo S, Beltramo M, et al. Immunohistochemical evidence for the presence of various kisspeptin isoforms in the mammalian brain. J Neuroendocrinol. 2013;25(9):839-851.
40. Van't Veer A, Carlezon WA Jr. Role of-opioid receptors in stress and anxiety-related behavior. Psychopharmacology (Berl). 2013; 229(3):435-452.
41. Merkley CM, Porter KL, Coolen LM, et al. KNDy (kisspeptin/neurokinin B/dynorphin) neurons are activated during both pulsatile and surge secretion ofLHin the ewe. Endocrinology. 2012;153(11): 5406-5414.
42. Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ. Elevated KiSS-1 expression in the arcuate nucleus prior to the cyclic preovulatory gonadotrophin-releasing hormone/lutenising hormone surge in the ewe suggests a stimulatory role for kisspeptin in oestrogenpositive feedback. J Neuroendocrinol. 2006;18(10):806-809.
43. Alcin E, Sahu A, Ramaswamy S, et al. Ovarian regulation of kisspeptin neurones in the arcuate nucleus of the rhesus monkey (Macaca mulatta). J Neuroendocrinol. 2013;25(5):488-496.
44. Smith JT, Li Q, Pereira A, Clarke IJ. Kisspeptin neurons in the ovine arcuate nucleus and preoptic area are involved in the preovulatory luteinizing hormone surge. Endocrinology. 2009;150(12):5530-5538.
45. Goubillon ML, Forsdike RA, Robinson JE, Ciofi P, Caraty A, Herbison AE. Identification of neurokinin B-expressing neurons as an highly estrogen-receptive, sexually dimorphic cell group in the ovine arcuate nucleus. Endocrinology. 2000;141(11):4218-4225.
46. Mittelman-Smith MA, Williams H, Krajewski-Hall SJ, McMullen NT, Rance NE. Role for kisspeptin/neurokinin B/dynorphin (KNDy) neurons in cutaneous vasodilatation and the estrogen modulation of body temperature. Proc Natl Acad Sci USA. 2012; 109(48):19846-19851.
47. True C, Kirigiti M, Ciofi P, Grove KL, Smith MS. Characterisation of arcuate nucleus kisspeptin/neurokininBneuronal projections and regulation during lactation in the rat. J Neuroendocrinol. 2011; 23(1):52-64.
48. Kallo I, Vida B, Deli L, et al. Co-localisation of kisspeptin with galanin or neurokinin B in afferents to mouse GnRH neurones. J Neuroendocrinol. 2012;24(3):464-476.
49. Nestor CC, Briscoe AM, Davis SM, Valent M, Goodman RL, Hileman SM. Evidence of a role for kisspeptin and neurokinin B in puberty of female sheep. Endocrinology. 2012;153(6):2756-2765.
50. 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(2):680-697.
51. Yeo SH, Herbison AE. Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology. 2011;152(6):2387-2399.
52. Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM. Neurokinin B stimulatesGnRHrelease in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology. 2010;151(9):4494-4503.
53. Rance NE, Dacks PA, Mittelman-SmithMA,Romanovsky AA, Krajewski-Hall SJ. Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: a novel hypothesis on the mechanism of hot flushes. Front Neuroendocrinol. 2013;34(3):211-227.
54. Mittelman-Smith MA, Williams H, Krajewski-Hall SJ, Lai J, Ciofi P, McMullen NT, Rance NE. Arcuate kisspeptin/neurokinin B/dynorphin (KNDy) neurons mediate the estrogen suppression of gonadotropin secretion and body weight. Endocrinology. 2012; 153(6):2800-2812.