A Direct Neurokinin B Projection from the Arcuate Nucleus Regulates Magnocellular Vasopressin Cells of the Supraoptic Nucleus

Journal of Neuroendocrinology

Volumn 28, Issue 4, 2016, Pages

  Pineda, R ^a   Sabatier, N ^a   Ludwig, M ^a   Millar, R P ^b,c   Leng, G ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Electrophysiology; Hypothalamus; Magnocellular neurones; Neuroanatomy; Oxytocin

Indexed keywords

KISSPEPTIN; NEUROKININ B; NEUROKININ RECEPTOR 3 RECEPTOR; OXYTOCIN; SENKTIDE; TACHYKININ RECEPTOR; UNCLASSIFIED DRUG; VASOPRESSIN; KISS1 PROTEIN, MOUSE; NEUROKININ 3 RECEPTOR; PEPTIDE FRAGMENT; SUBSTANCE P; VASOPRESSIN DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTRIC ACTIVITY; GENE EXPRESSION; GIANT CELL; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; IN VIVO STUDY; MAGNOCELLULAR NUCLEUS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SUPRAOPTIC NUCLEUS; ACTION POTENTIAL; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENETICS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; MOUSE; NERVE CELL; NEUROANATOMICAL TRACT TRACING; PHYSIOLOGY; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; INFUSIONS, INTRAVENTRICULAR; KISSPEPTINS; MALE; MICE; MICE, TRANSGENIC; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEUROKININ B; NEURONS; OXYTOCIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PEPTIDE FRAGMENTS; RATS; RECEPTORS, NEUROKININ-3; SUBSTANCE P; SUPRAOPTIC NUCLEUS; VASOPRESSINS;

EID: 84964974061     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12342     Document Type: Article

References (57)

1. Anderson RJ, Chung HM, Kluge R, Schrier RW. Hyponatremia: a prospective analysis of its epidemiology and the pathogenetic role of vasopressin. Ann Intern Med 1985; 102: 164-168.
2. Fliers E, Swaab DF, Pool CW, Verwer RW. The vasopressin and oxytocin neurons in the human supraoptic and paraventricular nucleus; changes with aging and in senile dementia. Brain Res 1985; 342: 45-53.
3. Tamma G, Goswami N, Reichmuth J, De Santo NG, Valenti G. Aquaporins, vasopressin, and aging: current perspectives. Endocrinology 2015; 156: 777-788.
4. Swaab DF. Ageing of the human hypothalamus. Horm Res 1995; 43: 8-11.
5. Stachenfeld NS. Hormonal changes during menopause and the impact on fluid regulation. Reprod Sci 2014; 21: 555-561.
6. 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.
7. 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.
8. Molnar CS, Vida B, Sipos MT, Ciofi P, Borsay BA, Racz K, Herczeg L, Bloom SR, Ghatei MA, Dhillo WS, Liposits Z, Hrabovszky E. Morphological evidence for enhanced kisspeptin and neurokinin B signaling in the infundibular nucleus of the aging man. Endocrinology 2012; 153: 5428-5439.
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. 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: 146-153.
11. Cholanian M, Krajewski-Hall SJ, McMullen NT, Rance NE. Chronic oestradiol reduces the dendritic spine density of KNDy (kisspeptin/neurokinin B/dynorphin) neurones in the arcuate nucleus of ovariectomised Tac2-enhanced green fluorescent protein transgenic mice. J Neuroendocrinol 2015; 27: 253-263.
12. Saigo A, Takano Y, Matsumoto T, Tran M, Nakayama Y, Saito R, Yamada K, Kamiya H. Central administration of senktide, a tachykinin NK-3 agonist, has an antidiuretic action by stimulating AVP release in water-loaded rats. Neurosci Lett 1993; 159: 187-190.
13. Eguchi T, Takano Y, Hatae T, Saito R, Nakayama Y, Shigeyoshi Y, Okamura H, Krause JE, Kamiya H. Antidiuretic action of tachykinin NK-3 receptor in the rat paraventricular nucleus. Brain Res 1996; 743: 49-55.
14. Howe HE, Somponpun SJ, Sladek CD. Role of neurokinin 3 receptors in supraoptic vasopressin and oxytocin neurons. J Neurosci 2004; 24: 10103-10110.
15. Haley GE, Flynn FW. Tachykinin NK3 receptor contribution to systemic release of vasopressin and oxytocin in response to osmotic and hypotensive challenge. Am J Physiol Regul Integr Comp Physiol 2007; 293: R931-R937.
16. Vercelli A, Repici M, Garbossa D, Grimaldi A. Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 2000; 51: 11-28.
17. Cetin A, Komai S, Eliava M, Seeburg PH, Osten P. Stereotaxic gene delivery in the rodent brain. Nat Protoc 2006; 1: 3166-3173.
18. Paxinos G, Watson C. The Rat Brain Stereotaxic Coordinates. 6th edn. San Diego, CA: Academic Press, 2006.
19. Kuhlman SJ, Huang ZJ. High-resolution labeling and functional manipulation of specific neuron types in mouse brain by Cre-activated viral gene expression. PLoS ONE 2008; 3: e2005.
20. Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD, de Lecea L, Deisseroth K. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc 2010; 5: 439-456.
21. 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.
22. 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.
23. 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.
24. 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.
25. Gottsch ML, Popa SM, Lawhorn JK, Qiu J, Tonsfeldt KJ, Bosch MA, Kelly MJ, Rønnekleiv OK, Sanz E, McKnight GS, Clifton DK, Palmiter RD, Steiner RA. Molecular properties of Kiss1 neurons in the arcuate nucleus of the mouse. Endocrinology 2011; 152: 4298-4309.
26. Tsai HC, Zhang F, Adamantidis A, Stuber GD, Bonci A, de Lecea L, Deisseroth K. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 2009; 324: 1080-1084.
27. Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai HC, Finkelstein J, Kim SY, Adhikari A, Thompson KR, Andalman AS, Gunaydin LA, Witten IB, Deisseroth K. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 2013; 493: 537-541.
28. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. New York, NY: Elsevier Academic Press, 2004.
29. Leng G, Sabatier N. Electrophysiology of magnocellular neurons in vivo. In: Armstrong WE, Tasker JG, eds. Neurophysiology of Neuroendocrine Neurons. Chichester: John Wiley & Sons, Ltd, 2015: 3-28.
30. Sabatier N, Brown CH, Ludwig M, Leng G. Phasic spike patterning in rat supraoptic neurones in vivo and in vitro. J Physiol 2004; 558: 161-180.
31. Ding YQ, Shigemoto R, Takada M, Ohishi H, Nakanishi S, Mizuno N. Localization of the neuromedin K receptor (NK3) in the central nervous system of the rat. J Comp Neurol 1996; 364: 290-310.
32. Miklos Z, Flynn FW, Lessard A. Stress-induced dendritic internalization and nuclear translocation of the neurokinin-3 (NK3) receptor in vasopressinergic profiles of the rat paraventricular nucleus of the hypothalamus. Brain Res 2014; 1590: 31-44.
33. Warden MK, Young WS III. Distribution of cells containing mRNAs encoding substance P and neurokinin B in the rat central nervous system. J Comp Neurol 1988; 272: 90-113.
34. Lucas LR, Hurley DL, Krause JE, Harlan RE. Localization of the tachykinin neurokinin B precursor peptide in rat brain by immunocytochemistry and in situ hybridization. Neuroscience 1992; 51: 317-345.
35. 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: 341-356.
36. Hatae T, Kawano H, Karpitskiy V, Krause JE, Masuko S. Arginine-vasopressin neurons in the rat hypothalamus produce neurokinin B and co-express the tachykinin NK-3 receptor and angiotensin II type 1 receptor. Arch Histol Cytol 2001; 64: 37-44.
37. Polidori C, Saija A, Perfumi M, Costa G, de Caro G, Massi M. Vasopressin release induced by intracranial injection of tachykinins is due to activation of central neurokinin-3 receptors. Neurosci Lett 1989; 103: 320-325.
38. Ding YD, Shi J, Su LY, Xu JQ, Su CJ, Guo XE, Ju G. Intracerebroventricular injection of senktide-induced Fos expression in vasopressin-containing hypothalamic neurons in the rat. Brain Res 2000; 882: 95-102.
39. Bealer SL, Flynn FW. Central neurokinin 3 receptors increase systemic oxytocin release: interaction with norepinephrine. Exp Neurol 2003; 184: 1027-1033.
40. Haley GE, Flynn FW. Agonist and hypertonic saline-induced trafficking of the NK3-receptors on vasopressin neurons within the paraventricular nucleus of the hypothalamus. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1242-R1250.
41. Jensen D, Zhang Z, Flynn FW. Trafficking of tachykinin neurokinin 3 receptor to nuclei of neurons in the paraventricular nucleus of the hypothalamus following osmotic challenge. Neuroscience 2008; 155: 308-316.
42. Flynn FW, Jensen DD, Thakar A, Xu X, Flynn SW, Zhang Z. Neurokinin 3 receptor forms a complex with acetylated histone H3 and H4 in hypothalamic neurons following hyperosmotic challenge. Am J Physiol Regul Integr Comp Physiol 2011; 301: R822-R831.
43. Douglas AJ, Bicknell RJ, Leng G, Russell JA, Meddle SL. Beta-endorphin cells in the arcuate nucleus: projections to the supraoptic nucleus and changes in expression during pregnancy and parturition. J Neuroendocrinol 2002; 14: 768-777.
44. Sawchenko PE, Swanson LW, Joseph SA. The distribution and cells of origin of ACTH(1-39)-stained varicosities in the paraventricular and supraoptic nuclei. Brain Res 1982; 232: 365-374.
45. Leng G, Yamashita H, Dyball RE, Bunting R. Electrophysiological evidence for a projection from the arcuate nucleus to the supraoptic nucleus. Neurosci Lett 1988; 89: 146-151.
46. Ludwig M, Leng G. GABAergic projection from the arcuate nucleus to the supraoptic nucleus in the rat. Neurosci Lett 2000; 281: 195-197.
47. Ludwig M, Brown CH, Russell JA, Leng G. Local opioid inhibition and morphine dependence of supraoptic nucleus oxytocin neurones in the rat in vivo. J Physiol 1997; 505: 145-152.
48. Scott V, Brown CH. Kisspeptin activation of supraoptic nucleus neurons in vivo. Endocrinology 2011; 152: 3862-3870.
49. Scott V, Brown CH. Beyond the GnRH axis: kisspeptin regulation of the oxytocin system in pregnancy and lactation. Adv Exp Med Biol 2013; 784: 201-218.
50. True C, Kirigiti M, Ciofi P, Grove KL, Smith MS. Characterisation of arcuate nucleus kisspeptin/neurokinin B neuronal projections and regulation during lactation in the rat. J Neuroendocrinol 2011; 23: 52-64.
51. Brown CH, Bains JS, Ludwig M, Stern JE. Physiological regulation of magnocellular neurosecretory cell activity: integration of intrinsic, local and afferent mechanisms. J Neuroendocrinol 2013; 25: 678-710.
52. Sladek CD, Swenson KL, Kapoor R, Sidorowicz HE. The role of steroid hormones in the regulation of vasopressin and oxytocin release and mRNA expression in hypothalamo-neurohypophysial explants from the rat. Exp Physiol 2000; 85: 171S-177S.
53. Skowsky WR, Swan L, Smith P. Effects of sex steroid hormones on arginine vasopressin in intact and castrated male and female rats. Endocrinology 1979; 104: 105-108.
54. Sauvant J, Delpech JC, Palin K, De Mota N, Dudit J, Aubert A, Orcel H, Roux P, Layé S, Moos F, Llorens-Cortes C, Nadjar A. Mechanisms involved in dual vasopressin/apelin neuron dysfunction during aging. PLoS ONE 2014; 9: e87421.
55. Rachner TD, Khosla S, Hofbauer LC. Osteoporosis: now and the future. Lancet 2011; 377: 1276-1287.
56. Verbalis JG, Barsony J, Sugimura Y, Tian Y, Adams DJ, Carter EA, Resnick HE. Hyponatremia-induced osteoporosis. J Bone Miner Res 2010; 25: 554-563.
57. Gross PA, Pehrisch H, Rascher W, Schomig A, Hackenthal E, Ritz E. Pathogenesis of clinical hyponatremia: observations of vasopressin and fluid intake in 100 hyponatremic medical patients. Eur J Clin Invest 1987; 17: 123-129.