Prenatal Testosterone Excess Decreases Neurokinin 3 Receptor Immunoreactivity within the Arcuate Nucleus KNDy Cell Population

Journal of Neuroendocrinology

Volumn 27, Issue 2, 2015, Pages 100-110

  Ahn, T ^a,b   Fergani, C ^c   Coolen, L M ^c   Padmanabhan, V ^d,e   Lehman, Michael N ^c  

^a WESTERN UNIVERSITY   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Developmental programming; GnRH; Kisspeptin; Neuroendocrine; Neurokinin B; Reproduction

Indexed keywords

DYNORPHIN; ESTRADIOL; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; NEUROKININ 3 RECEPTOR; NEUROKININ B; PEPTIDE; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; AUTOREGULATION; BRAIN SYNAPTOSOME; CELL BODY; CELL POPULATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; FETUS; GONADORELIN RELEASE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LUTEINIZING HORMONE RELEASE; MALE; MEDIOBASAL HYPOTHALAMUS; NERVE CELL; NEUROFEEDBACK; NEUROTRANSMISSION; NONHUMAN; POSITIVE FEEDBACK; PRENATAL EXPOSURE; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REPRODUCTION; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; IMMUNOLOGY; METABOLISM; PREGNANCY; SHEEP;

ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; DYNORPHINS; FEMALE; FETUS; GONADOTROPIN-RELEASING HORMONE; KISSPEPTINS; NEUROKININ B; PREGNANCY; RECEPTORS, NEUROKININ-3; SHEEP; TESTOSTERONE;

EID: 84921535232     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12244     Document Type: Article

References (59)

1. Mussap CJ, Geraghty DP, Burcher E. Tachykinin receptors: a radioligand binding perspective. J Neurochem 1993; 60: 1987-2009.
2. Almeida TA, Rojo J, Nieto PM, Pinto FM, Hernandez M, Martin JD, Candenas ML. Tachykinins and tachykinin receptors: structure and activity relationships. Curr Med Chem 2004; 11: 2045-2081.
3. Chawla MK, Gutierrez GM, Young WS III, McMullen NT, Rance NE. Localization of neurons expressing substance P and neurokinin B gene transcripts in the human hypothalamus and basal forebrain. J Comp Neurol 1997; 384: 429-442.
4. 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.
5. Young J, Bouligand J, Francou B, Raffin-Sanson ML, Gaillez S, Jeanpierre M, Grynberg M, Kamenicky P, Chanson P, Brailly-Tabard S, Guiochon-Mantel A. TAC3 and TACR3 defects cause hypothalamic congenital hypogonadotropic hypogonadism in humans. J Clin Endocrinol Metab 2010; 95: 2287-2295.
6. 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.
7. 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 2011; 30: 3124-3132.
8. Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM. Neurokinin B stimulates GnRH release in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology 2010; 151: 4494-4503.
9. 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.
10. 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.
11. 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 2009; 22: 1-12.
12. Navarro VM, Gottsch ML, Wu M, Garcia-Galiano D, Hobbs SJ, Bosch MA, Pinilla L, Clifton DK, Dearth A, Ronnekleiv OK, Braun RE, Palmiter RD, Tena-Sempere M, Alreja M, Steiner RA. Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse. Endocrinology 2011; 152: 4265-4275.
13. 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.
14. Goodman RL, Lehman MN. Kisspeptin neurons from mice to men: similarities and differences. Endocrinology 2012; 153: 5105-5118.
15. Hrabovszky E, Sipos MT, Molnar CS, Ciofi P, Borsay BA, Gergely P, Herczeg L, Bloom SR, Ghatei MA, Dhillo WS, Liposits Z. 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: 4978-4989.
16. Goodman RL, Hileman SM, Nestor CC, Porter KL, Connors JM, Hardy SL, Millar RP, Cernea M, Coolen LM, Lehman MN. Kisspeptin, neurokinin B, and dynorphin act in the arcuate nucleus to control activity of the GnRH pulse generator in ewes. Endocrinology 2013; 154: 4259-4269.
17. Caraty A, Fabre-Nys C, Delaleu B, Locatelli A, Bruneau G, Karsch FJ, Herbison A. Evidence that the mediobasal hypothalamus is the primary site of action of estradiol in inducing the preovulatory gonadotropin releasing hormone surge in the ewe. Endocrinology 1998; 139: 1752-1760.
18. Merkley CM, Porter KL, Coolen LM, Hileman SM, Billings HJ, Drews S, Goodman RL, Lehman MN. KNDy (kisspeptin/neurokinin B/dynorphin) neurons are activated during both pulsatile and surge secretion of LH in the ewe. Endocrinology 2012; 153: 5406-5414.
19. Fergani C, Routly JE, Jones DN, Pickavance LC, Smith RF, Dobson H. Kisspeptin, c-Fos and CRFR type 2 expression in the preoptic area and mediobasal hypothalamus during the follicular phase of intact ewes, and alteration after LPS. Physiol Behav 2013; 110-111: 158-168.
20. Porter KL, Hileman SM, Hardy SL, Goodman RL. Neurokinin B Signaling in the Retrochiasmatic Area is Essential for the Full Preovulatory LH Surge in Ewes. San Diego, CA: Society for Neuroscience, 2013.
21. 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 oestrogen-positive feedback. J Neuroendocrinol 2006; 18: 806-809.
22. 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: 5530-5538.
23. Pineda R, Garcia-Galiano D, Roseweir A, Romero M, Sanchez-Garrido MA, Ruiz-Pino F, Morgan K, Pinilla L, Millar RP, Tena-Sempere M. Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology 2010; 151: 722-730.
24. Smith JT, Li Q, Sing Yap K, Shahab M, Roseweir AK, Millar RP, Clarke IJ. Kisspeptin is essential for the full preovulatory LH surge and stimulates GnRH release from the isolated ovine median eminence. Endocrinology 2011; 152: 1001-1012.
25. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev 2009; 30: 713-743.
26. Gorski RA. Sexual dimorphisms of the brain. J Anim Sci 1985; 61(Suppl. 3): 38-61.
27. Simerly RB. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 2002; 25: 507-536.
28. Padmanabhan V, Veiga-Lopez A. Sheep models of polycystic ovary syndrome phenotype. Mol Cell Endocrinol 2013; 373: 8-20.
29. Padmanabhan V, Sarma HN, Savabieasfahani M, Steckler TL, Veiga-Lopez A. Developmental reprogramming of reproductive and metabolic dysfunction in sheep: native steroids vs. environmental steroid receptor modulators. Int J Androl 2010; 33: 394-404.
30. Sharma TP, Herkimer C, West C, Ye W, Birch R, Robinson JE, Foster DL, Padmanabhan V. Fetal programming: prenatal androgen disrupts positive feedback actions of estradiol but does not affect timing of puberty in female sheep. Biol Reprod 2002; 66: 924-933.
31. Veiga-Lopez A, Astapova OI, Aizenberg EF, Lee JS, Padmanabhan V. Developmental programming: contribution of prenatal androgen and estrogen to estradiol feedback systems and periovulatory hormonal dynamics in sheep. Biol Reprod 2009; 80: 718-725.
32. Herbosa CG, Dahl GE, Evans NP, Pelt J, Wood RI, Foster DL. Sexual differentiation of the surge mode of gonadotropin secretion: prenatal androgens abolish the gonadotropin-releasing hormone surge in the sheep. J Neuroendocrinol 1996; 8: 627-633.
33. 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: 301-311.
34. Jackson LM, Timmer KM, Foster DL. Organizational actions of postnatal estradiol in female sheep treated prenatally with testosterone: programming of prepubertal neuroendocrine function and the onset of puberty. Endocrinology 2009; 150: 2317-2324.
35. Jackson LM, Timmer KM, Foster DL. Sexual differentiation of the external genitalia and the timing of puberty in the presence of an antiandrogen in sheep. Endocrinology 2008; 149: 4200-4208.
36. Veiga-Lopez A, Steckler TL, Abbott DH, Welch KB, MohanKumar PS, Phillips DJ, Refsal K, Padmanabhan V. Developmental programming: impact of excess prenatal testosterone on intrauterine fetal endocrine milieu and growth in sheep. Biol Reprod 2011; 84: 87-96.
37. Veiga-Lopez A, Wurst AK, Steckler TL, Ye W, Padmanabhan V. Developmental programming: postnatal estradiol amplifies ovarian follicular defects induced by fetal exposure to excess testosterone and dihydrotestosterone in sheep. Reprod Sci 2014; 21: 444-455.
38. Jackson LM, Mytinger A, Roberts EK, Lee TM, Foster DL, Padmanabhan V, Jansen HT. Developmental programming: postnatal steroids complete prenatal steroid actions to differentially organize the GnRH surge mechanism and reproductive behavior in female sheep. Endocrinology 2013; 154: 1612-1623.
39. Veiga-Lopez A, Ye W, Phillips DJ, Herkimer C, Knight PG, Padmanabhan V. Developmental programming: deficits in reproductive hormone dynamics and ovulatory outcomes in prenatal, testosterone-treated sheep. Biol Reprod 2008; 78: 636-647.
40. Robinson JE, Birch RA, Foster DL, Padmanabhan V. Prenatal exposure of the ovine fetus to androgens sexually differentiates the steroid feedback mechanisms that control gonadotropin releasing hormone secretion and disrupts ovarian cycles. Arch Sex Behav 2002; 31: 35-41.
41. Karsch FJ, Foster DL, Legan SJ, Ryan KD, Peter GK. Control of the preovulatory endocrine events in the ewe: interrelationship of estradiol, progesterone, and luteinizing hormone. Endocrinology 1979; 105: 421-426.
42. Watson RE Jr, Wiegand SJ, Clough RW, Hoffman GE. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 1986; 7: 155-159.
43. Hunyady B, Krempels K, Harta G, Mezey E. Immunohistochemical signal amplification by catalyzed reporter deposition and its application in double immunostaining. J Histochem Cytochem 1996; 44: 1353-1362.
44. 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.
45. 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 2009; 151: 301-311.
46. 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: 4218-4225.
47. Goodman RL, Coolen LM, Lehman MN. A role for neurokinin B in pulsatile GnRH secretion in the ewe. Neuroendocrinology 2014; 99: 18-32.
48. 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: 2800-2812.
49. Yan X, Yuan C, Zhao N, Cui Y, Liu J. Prenatal androgen excess enhances stimulation of the GNRH pulse in pubertal female rats. J Endocrinol 2014; 222: 73-85.
50. Coolen LM, Smith TG, Lehman MN, Hileman SM, Connors JM, Goodman RL. Arcuate KNDy Neurons Receive Afferent Projections from the Retrochiasmatic Area in the Ewe. San Diego, CA: Society for Neuroscience, 2013.
51. 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.
52. Grachev P, Li XF, Lin YS, Hu MH, Elsamani L, Paterson SJ, Millar RP, Lightman SL, O'Byrne KT. GPR54-dependent stimulation of luteinizing hormone secretion by neurokinin B in prepubertal rats. PLoS ONE 2012; 7: e44344.
53. Ramaswamy S, Seminara SB, Plant TM. Evidence from the agonadal juvenile male rhesus monkey (Macaca mulatta) for the view that the action of neurokinin B to trigger gonadotropin-releasing hormone release is upstream from the kisspeptin receptor. Neuroendocrinology 2011; 94: 237-245.
54. Garcia-Galiano D, van Ingen Schenau D, Leon S, Krajnc-Franken MA, Manfredi-Lozano M, Romero-Ruiz A, Navarro VM, Gaytan F, van Noort PI, Pinilla L, Blomenrohr M, Tena-Sempere M. Kisspeptin signaling is indispensable for neurokinin B, but not glutamate, stimulation of gonadotropin secretion in mice. Endocrinology 2012; 153: 316-328.
55. Gaskins GT, Glanowska KM, Moenter SM. Activation of neurokinin 3 receptors stimulates GnRH release in a location-dependent but kisspeptin-independent manner in adult mice. Endocrinology 2013; 154: 3984-3989.
56. Glowinski J, Kemel ML, Desban M, Gauchy C, Lavielle S, Chassaing G, Beaujouan JC, Tremblay L. Distinct presynaptic control of dopamine release in striosomal- and matrix-enriched areas of the rat striatum by selective agonists of NK1, NK2 and NK3 tachykinin receptors. Regul Pept 1993; 46: 124-128.
57. Rance NE. Menopause and the human hypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback. Peptides 2009; 30: 111-122.
58. Rance NE, Young WS III. Hypertrophy and increased gene expression of neurons containing neurokinin-B and substance-P messenger ribonucleic acids in the hypothalami of postmenopausal women. Endocrinology 1991; 128: 2239-2247.
59. Rance NE, Krajewski SJ, Smith MA, Cholanian M, Dacks PA. Neurokinin B and the hypothalamic regulation of reproduction. Brain Res 2010; 1364: 116-128.