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Response of Substances Co-Expressed in Hypothalamic Magnocellular Neurons to Osmotic Challenges in Normal and Brattleboro Rats

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Abstract

The intention of this review is to emphasize the current knowledge about the extent and importance of the substances co-localized with magnocellular arginine vasopressin (AVP) and oxytocin (OXY) as potential candidates for the gradual clarification of their actual role in the regulation of hydromineral homeostasis. Maintenance of the body hydromineral balance depends on the coordinated action of principal biologically active compounds, AVP and OXY, synthesized in the hypothalamic supraoptic and paraventricular nuclei. However, on the regulation of water–salt balance, other substances, co-localized with the principal neuropetides, participate. These can be classified as (1) peptides co-localized with AVP or OXY with unambiguous osmotic function, including angiotensin II, apelin, corticotropin releasing hormone, and galanin and (2) peptides co-localized with AVP or OXY with an unknown role in osmotic regulation, including cholecystokinin, chromogranin/secretogranin, dynorphin, endothelin-1, enkephalin, ferritin protein, interleukin 6, kininogen, neurokinin B, neuropeptide Y, vasoactive intestinal peptide, pituitary adenylate cyclase-activating polypeptide, TAFA5 protein, thyrotropin releasing hormone, tyrosine hydroxylase, and urocortin. In this brief review, also the responses of these substances to different hyperosmotic and hypoosmotic challenges are pointed out. Based on the literature data published recently, the functional implication of the majority of co-localized substances is still better understood in non-osmotic than osmotic functional circuits. Brattleboro strain of rats that does not express functional vasopressin was also included in this review. These animals suffer from chronic hypernatremia and hyperosmolality, accompanied by sustained increase in OXY mRNA in PVN and SON and OXY levels in plasma. They represent an important model of animals with constantly sustained osmolality, which in the future, will be utilizable for revealing the physiological importance of biologically active substances co-expressed with AVP and OXY, involved in the regulation of plasma osmolality.

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References

  • Abramova M, Calas A, Thibault J, Ugrumov M (2000) Tyrosine hydroxylase in vasopressinergic axons of the pituitary posterior lobe of rats under salt loading as a manifestation of neurochemical plasticity. Neural Plast 7:179–191. doi:10.1155/NP.2000.179

    PubMed  CAS  Google Scholar 

  • Aguilera G (1998) Corticotropin releasing hormone, receptor regulation and the stress response. Trends Endocrinol Metab 9:329–336. doi:10.1016/S1043-2760(98)00079-4

    PubMed  CAS  Google Scholar 

  • Almeida TA, Rojo J, Nieto PM, Pinto FM, Hernandez M, Martin JD et al (2004) Tachykinins and tachykinin receptors: structure and activity relationships. Curr Med Chem 11:2045–2081

    PubMed  CAS  Google Scholar 

  • Ang CW, Dotman CH, Winkler H, Fischer-Colbrie R, Sonnesmans MA, Van Leeuwen FW (1997) Specific expression of secretogranin II in magnocellular vasopressin neurons of the rat supraoptic and paraventricular nucleus in response to osmotic stimulation. Brain Res 765:13–20. doi:10.1016/S0006-8993(97)00462-9

    PubMed  CAS  Google Scholar 

  • Anita I, Yaira M, María del Rosario G (2006) Endothelin signaling pathways in rat adrenal medulla. Cell Mol Neurobiol 26:703–718. doi:10.1007/s10571-006-9111-3

    PubMed  Google Scholar 

  • Arima H, Aguilera G (2000) Vasopressinergic and oxytocinergic neurons of supraoptic and paraventricular nuclei co-express mRNA for type-1 and type-2 corticotropin releasing hormone receptors. J Neuroendocrinol 12:833–842. doi:10.1046/j.1365-2826.2000.00528.x

    PubMed  CAS  Google Scholar 

  • Arimura A (1998) Perspectives on pituitary adenylate cyclase activating polypeptide (PACAP) in the neuroendocrine, endocrine, and nervous systems. Jpn J Physiol 48:301–331. doi:10.2170/jjphysiol.48.301

    PubMed  CAS  Google Scholar 

  • Armstrong WE (1995) Morphological and electrophysiological classification of hypothalamic supraoptic neurons. Prog Neurobiol 47:291–339. doi:10.1016/0301-0082(95)00025-9

    PubMed  CAS  Google Scholar 

  • Armstrong WE (2004) Hypothalamic supraoptic and paraventricular nuclei. In: The rat nervous system, 3rd edn. (Paxinos G. ed.) Elsevier, USA, pp 369–388

  • Bacova Z, Kiss A, Jamal B, Payer J Jr, Strbak V (2006) Effect of swelling on TRH and oxytocin secretion from hypothalamic structures. Cell Mol Neurobiol 26:1045–1053. doi:10.1007/s10571-006-9013-4

    Google Scholar 

  • Baigent SM (2001) Peripheral corticotropin-releasing hormone and urocortin in the control of the immune response. Peptides 22:809–820. doi:10.1016/S0196-9781(01)00395-3

    PubMed  CAS  Google Scholar 

  • Baile CA, Della-Fera MA, McLaughlin CL (1983) Hormones and feed intake. Proc Nutr Soc 42:113–127. doi:10.1079/PNS19830018

    PubMed  CAS  Google Scholar 

  • Balment RJ, Brimble MJ, Forsling ML (1980) Release of oxytocin induced by salt loading and its influence on renal excretion in the male rat. J Physiol 308:439–449

    PubMed  CAS  Google Scholar 

  • Bardrum B, Ottesen B, Fahrenkrug J, Fuchs A-R (1988) Release of oxytocin and vasopressin by intracerebroventricular vasoactive intestinal polypeptide. Endocrinology 123:2249–2254

    PubMed  CAS  Google Scholar 

  • Beck B, Max JP (2007) Hypothalamic galanin and plasma leptin and ghrelin in the maintenance of energy intake in the Brattleboro rat. Biochem Biophys Res Commun 364:60–65. doi:10.1016/j.bbrc.2007.09.092

    PubMed  CAS  Google Scholar 

  • Bodnar RJ, Klein GE (2005) Endogenous opiates and behavior. Peptides 26:2629–2711. doi:10.1016/j.peptides.2005.06.010

    PubMed  CAS  Google Scholar 

  • Brailoiu GC, Dun SL, Yang J, Ohsawa M, Chang JK, Dun NJ (2002) Apelin immunoreactivity in the rat hypothalamus and pituitary. Neurosci Lett 327:193–197. doi:10.1016/S0304-3940(02)00411-1

    PubMed  CAS  Google Scholar 

  • Brimble MJ, Balment RJ, Smith CP, Windle RJ, Forsling ML (1991) Influence of oxytocin on sodium excretion in the anaesthetized Brattleboro rat. J Endocrinol 129:49–54

    PubMed  CAS  Google Scholar 

  • Bruhn TO, Sutton SW, Plotsky PM, Vale WW (1986) Central administration of corticotropin-releasing factor modulates oxytocin secretion in the rat. Endocrinology 119:1558–1563

    PubMed  CAS  Google Scholar 

  • Burazin TCD, Larm JA, Gundlach AL (2001) Regulation by osmotic stimuli of galanin-R1 receptor expression in magnocelular neurones of the paraventricular and supraoptic nuclei of the rat. J Neuroendocrinol 13:358–370. doi:10.1046/j.1365-2826.2001.00640.x

    PubMed  CAS  Google Scholar 

  • Carter DA, Vallejo M, Lightman SL (1985) Cardiovascular effects of neuropeptide Y in the nucleus tractus solitarius of rats: relationship with noradrenaline and vasopressin. Peptides 6:421–425. doi:10.1016/0196-9781(85)90107-X

    PubMed  CAS  Google Scholar 

  • Ceccatelli S, Fahrenkrug J, Villar MJ, Hökfelt T (1991) Vasoactive intestinal polypeptide/peptide histidine isoleucine immunoreactive neuron systems in the basal hypothalamus of the rat with special reference to the portal vasculature: an immunohistochemical and in situ hybridization study. Neuroscience 43:483–502. doi:10.1016/0306-4522(91)90310-K

    PubMed  CAS  Google Scholar 

  • Chahl LA (2006) Tachykinins and neuropsychiatric disorders. Curr Drug Targets 7:993–1003. doi:10.2174/138945006778019309

    PubMed  CAS  Google Scholar 

  • Chandra R, Liddle RA (2007) Cholecystokinin. Curr Opin Endocrinol Diabetes Obes 14:63–67

    PubMed  CAS  Google Scholar 

  • Chen D, Assad-Kottner C, Orrego C, Torre-Amione G (2008a) Cytokines and acute heart failure. Crit Care Med 36:S9–S16

    PubMed  CAS  Google Scholar 

  • Chen JX, Tang YT, Yang JX (2008b) Changes of glucocorticoid receptor and levels of CRF mRNA, POMC mRNA in brain of chronic immobilization stress rats. Cell Mol Neurobiol 28:237–244. doi:10.1007/s10571-007-9170-0

    PubMed  CAS  Google Scholar 

  • Ciosek J, Stempniak B (1995) Thyrotropin-releasing hormone (TRH) modifies oxytocin release from the hypothalamo-neurohypophysial system in salt loaded rats. J Physiol Pharmacol 46:169–177

    PubMed  CAS  Google Scholar 

  • Cisowska-Maciejewska A, Ciosek J (2005) Galanin influences vasopressin and oxytocin release from the hypothalamo-neurohypophysial system of salt loaded rats. J Physiol Pharmacol 56:673–688

    PubMed  CAS  Google Scholar 

  • Cox BM, Ghazarossian VE, Goldstein A (1980) Levels of immunoreactive dynorphin in brain and pituitary of Brattleboro rats. Neurosci Lett 20:85–88. doi:10.1016/0304-3940(80)90238-4

    PubMed  CAS  Google Scholar 

  • Crawley JN (1999) The role of galanin in feeding behavior. Neuropeptides 33:369–375. doi:10.1054/npep.1999.0049

    PubMed  CAS  Google Scholar 

  • Cummings S, Elde R, Ells J, Lindall A (1983) Corticotropin-releasing factor immunoreactivity is widely distributed within the central nervous system of the rat: an immunohistochemical study. J Neurosci 3:1355–1368

    PubMed  CAS  Google Scholar 

  • da Silveira LT, Junta CM, Monesi N, De Oliveira-Pelegrin GR, Passos GA, Rocha MJ (2007) Time course of c-fos, vasopressin and oxytocin mRNA expression in the hypothalamus following long-term dehydration. Cell Mol Neurobiol 27:284–575. doi:10.1007/s10571-007-9144-2

    Google Scholar 

  • Day NC, Hall MD, Hughes J (1989) Modulation of hypothalamic cholecystokinin receptor density with changes in magnocellular activity: a quantitative autoradiographic study. Neuroscience 29:371–383. doi:10.1016/0306-4522(89)90064-X

    PubMed  CAS  Google Scholar 

  • de Stahl TD, Hartmann C, De Bustos C, Piotrowski A, Benetkiewicz M, Mantripragada KK et al (2005) Chromosome 22 tiling-path array-CGH analysis identifies germ-line- and tumor-specific aberrations in patients with glioblastoma multiforme. Genes Chromosomes Cancer 44:161–169. doi:10.1002/gcc.20226

    PubMed  Google Scholar 

  • Dohanics J, Kovacs KJ, Makara GB (1990) Oxytocinergic neurons in rat hypothalamus. Dexamethasone-reversible increase in their corticotropin-releasing factor-41-like immunoreactivity in the response to osmotic stimulation. Neuroendocrinology 51:515–522. doi:10.1159/000125385

    PubMed  CAS  Google Scholar 

  • Dores RM, Lecaudé S, Bauer D, Danielson PB (2002) Analyzing the evolution of the opioid/orphanin gene family. Mass Spectrom Rev 21:220–243. doi:10.1002/mas.10029

    PubMed  CAS  Google Scholar 

  • Drolet G, Dumont EC, Gosselin I, Kinkead R, Laforest S, Trottier JF (2001) Role of endogenous opioid system in the regulation of the stress response. Prog Neuropsychopharmacol Biol Psychiatry 25:729–741. doi:10.1016/S0278-5846(01)00161-0

    PubMed  CAS  Google Scholar 

  • Edwards BR, LaRochelle FT Jr (1984) Antidiuretic effect of endogenous oxytocin in dehydrated Brattleboro homozygous rats. Am J Physiol 247:F453–F465

    PubMed  CAS  Google Scholar 

  • Falcao-Pires I, Leite-Moreira AF (2005) Apelin: a novel neurohumoral modulator of the cardiovascular system. Pathophysiologic importance and potential use as a therapeutic target. Rev Port Cardiol 24:1263–1276

    PubMed  Google Scholar 

  • Gaymann W, Martin R (1989) Immunoreactive galanin-like material in magnocellular hypothalamo-neurohypophysial neurones of the rat. Cell Tissue Res 255:139–147. doi:10.1007/BF00229075

    PubMed  CAS  Google Scholar 

  • Gerdes HH, Phillips E, Huttner WB (1988) The primary structure of rat secretogranin II deduced from a cDNA sequence. Nucleic Acids Res 16:11811. doi:10.1093/nar/16.24.11811

    PubMed  CAS  Google Scholar 

  • Ghorbel MT, Sharman G, Leroux M, Barrett T, Donovan DM, Becker KG et al (2003) Microarray analysis reveals interleukin-6 as a novel secretory product of the hypothalamo-neurohyphyseal system. J Biol Chem 278:19280–19285. doi:10.1074/jbc.M209902200

    PubMed  CAS  Google Scholar 

  • Gillard ER, León-Olea M, Mucio-Ramírez S, Coburn CG, Sánchez-Islas E, De Leon A et al (2006) A novel role for endogenous pituitary adenylate cyclase activating polypeptide in the magnocellular neuroendocrine system. Endocrinology 147:791–803. doi:10.1210/en.2005-1103

    PubMed  CAS  Google Scholar 

  • Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629–683

    PubMed  CAS  Google Scholar 

  • Giovannelli L, Shiromani PJ, Jirikowski GF, Bloom FE (1990) Oxytocin neurons in the rat hypothalamus exhibit c-fos immunoreactivity upon osmotic stress. Brain Res 531:299–303. doi:10.1016/0006-8993(90)90789-E

    PubMed  CAS  Google Scholar 

  • Glazova MV, Krasnovskaia IA (1996) The effect of thyroliberin on the nonapeptidergic hypothalamo-hypophyseal neurosecretory system in rats (in-vivo and in-vitro research). Fiziol Zh Im I M Sechenova 82:65–69

    PubMed  CAS  Google Scholar 

  • Gottlieb HB, Ji LL, Jones H, Penny ML, Fleming T, Cunningham JT (2006) Differential effects of water and saline intake on water deprivation-induced c-fos staining in the rat. Am J Physiol Regul Integr Comp Physiol 290:1251–1261. doi:10.1152/ajpregu.00727.2005

    Google Scholar 

  • Guldenaar SE, Noctor SC, McCabe JT (1992) Fos-like immunoreactivity in the brain of homozygous diabetes insipidus Brattleboro and normal Long-Evans rats. J Comp Neurol 322:439–448. doi:10.1002/cne.903220310

    PubMed  CAS  Google Scholar 

  • Haanwinckel MA, Elias LK, Favaretto AL, Gutkowska J, McCann SM, Antunes RJ (1995) Oxytocin mediates atrial natiuretic peptide release and natriuresis after volume expansion in the rat. Proc Natl Acad Sci USA 92:7096–7902. doi:10.1073/pnas.92.17.7902

    Google Scholar 

  • Hara Y, Ueta Y, Isse T, Kabashima N, Shibuya I, Hattori Y et al (1997a) Increase of urocortin-like immunoreactivity in the rat hypothalamo-neurohypophysial system after salt loading and hypophysectomy. Neurosci Lett 227:127–130. doi:10.1016/S0304-3940(97)00327-3

    PubMed  CAS  Google Scholar 

  • Hara Y, Ueta Y, Isse T, Kabashima N, Shibuya I, Hattori Y et al (1997b) Increase of urocortin-like immunoreactivity in the rat supraoptic nucleus after dehydration but not food deprivation. Neurosci Lett 229:65–68. doi:10.1016/S0304-3940(97)00419-9

    PubMed  CAS  Google Scholar 

  • Harding JW, Jensen LL, Hanesworth JM, Roberts KA, Page TA, Wright JW (1992) Release of angiotensins in paraventricular nucleus of rat in response to physiological and chemical stimuli. Am J Physiol 262:F17–F23

    PubMed  CAS  Google Scholar 

  • Hatae T, Kawano H, Karpitskiy V, Krause JE, Masuko S (2001a) 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 64:37–44. doi:10.1679/aohc.64.37

    PubMed  CAS  Google Scholar 

  • Hatae T, Nakayama Y, Kawano H, Masuko S (2001b) Effects of water deprivation on neurokinin B production by the arginine-vasopressin neurons of hypothalamic paraventricular and supraoptic nuclei. Fukuoka Igaku Zasshi 92:89–98

    PubMed  CAS  Google Scholar 

  • Hatakeyama S, Kawai Y, Ueyama T, Senba E (1996) Nitric oxide synthase-containing magnocellular neurons of the rat hypothalamus synthesize oxytocin and vasopressin and express fos following stress stimuli. J Chem Neuroanat 11:243–256. doi:10.1016/S0891-0618(96)00166-4

    PubMed  CAS  Google Scholar 

  • Hauser KF, Aldrich JV, Anderson KJ, Bakalkin G, Christie MJ, Hall ED et al (2005) Pathobiology of dynorphins in trauma and disease. Front Biosci 10:216–235. doi:10.2741/1522

    PubMed  CAS  Google Scholar 

  • Hawkins RL, Printz MP (1983) Distribution of angiotensinogen in Brattleboro rat brain. Brain Res Bull 10:163–166. doi:10.1016/0361-9230(83)90089-8

    PubMed  CAS  Google Scholar 

  • Hinks GL, Poat JA, Hughes J (1995) Changes in hypothalamic cholecystokininA and cholecystokininB receptor subtypes and associated neuropeptide expression in response to salt stress in the rat and mouse. Neuroscience 68:765–781. doi:10.1016/0306-4522(95)00148-C

    PubMed  CAS  Google Scholar 

  • Hoene M, Weigert C (2008) The role of interleukin-6 in insulin resistance, body fat distribution and energy balance. Obes Rev 9:20–29

    PubMed  CAS  Google Scholar 

  • Hooi SC, Richardson GS, McDonald JK, Allen JM, Martin JB, Koening JI (1989) Neuropeptide Y (NPY) and vasopressin (AVP) in the hypothalamo-neurohypophysial axis of salt loaded or Brattleboro rats. Brain Res 486:214–220. doi:10.1016/0006-8993(89)90507-6

    PubMed  CAS  Google Scholar 

  • Hou Yu A, Lamme AT, Zimmerman EA, Silverman AJ (1986) Comparative distribution of vasopressin and oxytocin neurons in the rat brain using a double-label procedure. Neuroendocrinology 44:235–246. doi:10.1159/000124651

    PubMed  CAS  Google Scholar 

  • Hoysoya Y, Matsushita M (1979) Identification and distribution of the spinal and hypophysial projection neurons in the apraventricular nucleus of the rat: a light and electron microscopic study with the horseradish peroxidase method. Exp Brain Res 35:315–332

    Google Scholar 

  • Huttner WB, Gerdes HH, Rosa P (1991) The granin (chromogranin/secretogranin) family. Trends Biochem Sci 16:27–30. doi:10.1016/0968-0004(91)90012-K

    PubMed  CAS  Google Scholar 

  • Imaki T, Katsumata H, Miyata M, Naruse M, Imaki J, Minami S (2001) Expression of corticotropin releasing factor (CRF), urocortine and CRF type 1 receptors in hypotalamic-hypophyseal systems under osmotic stimulation. J Neuroendocrinol 13:328–338. doi:10.1046/j.1365-2826.2001.00629.x

    PubMed  CAS  Google Scholar 

  • Imboden H, Felix D (1991) An immunocytochemical comparison of the angiotensin and vasopressin hypothalamo-neurohypophysial systems in normotensive rats. Regul Pept 36:197–218. doi:10.1016/0167-0115(91)90057-N

    PubMed  CAS  Google Scholar 

  • Israel A, Plunkett L, Saavedra JM (1986) Increased number of angiotensin II binding sites determined by autoradiography in anterior pituitary of water-deprived and Brattleboro rats. Neuroendocrinology 42:57–63. doi:10.1159/000124249

    PubMed  CAS  Google Scholar 

  • Jankovic BD, Radulovic J (1992) Enkephalins, brain and immunity: modulation of immune responses by methionine-enkephalin injected into the cerebral cavity. Int J Neurosci 67:241–270

    Article  PubMed  CAS  Google Scholar 

  • Jessop D, Sidhu R, Lightman SL (1990) Osmotic regulation of methionine enkephalin in the posterior pituitary of the rat. Brain Res 516:41–45. doi:10.1016/0006-8993(90)90895-I

    PubMed  CAS  Google Scholar 

  • Johnson AK, Thunhorst RL (1997) The neuroendocrinology of thirst and salt appetite: visceral sensory signals and mechanisms of central integration. Front Neuroendocrinol 18:292–353. doi:10.1006/frne.1997.0153

    PubMed  CAS  Google Scholar 

  • Kagotani Y, Hisano S, Tsuruo Y, Daikoku S, Chihara K (1990) Vasopressin-deficient paraventricular magnocellular neurons of homozygous Brattleboro rats synthesize neuropeptide Y. Neurosci Lett 112:37–42. doi:10.1016/0304-3940(90)90318-4

    PubMed  CAS  Google Scholar 

  • Kakiya S, Yokoi H, Arima H, Iwasaki Y, Oki Y, Oiso Y (1998) Central administration of urocortin inhibits vasopressin release in conscious rats. Neurosci Lett 248:144–146. doi:10.1016/S0304-3940(98)00357-7

    PubMed  CAS  Google Scholar 

  • Katoh T, Chang H, Uchida S, Okuda T, Kurokawa K (1990) Direct effects of endothelin in the rat kidney. Am J Physiol 258:F397–F402

    PubMed  CAS  Google Scholar 

  • Kiss JZ, Mezey E (1986) Tyrosine hydroxylase in magnocellular neurosecretory neurons response to physiological manipulations. Neuroendocrinology 43:519–525. doi:10.1159/000124576

    PubMed  CAS  Google Scholar 

  • Kiss A, Mikkelsen JD (2005) Oxytocin—anatomy and functional assignments: a minireview. Endocr Regul 39:97–105

    PubMed  CAS  Google Scholar 

  • Kjaer A, Knigge U, Bach FW, Warberg J (1993) Impaired histamine- and stress-induced secretion of ACTH and beta-endorphin in vasopressin-deficient Brattleboro rats. Neuroendocrinology 57:1035–1041. doi:10.1159/000126468

    PubMed  CAS  Google Scholar 

  • Koenig JI, Hooi S, Gabriel SM, Martin JB (1989) Potential involvement of galanin in the regulation of fluid homeostasis in the rat. Regul Pept 24:81–86. doi:10.1016/0167-0115(89)90213-9

    PubMed  CAS  Google Scholar 

  • Koob GF, Bloom FE (1985) Corticotropin-releasing factor and behavior. Fed Proc 44:259–263

    PubMed  CAS  Google Scholar 

  • Kozuka M, Ito T, Hirose S, Takahashi K, Hagiwara H (1989) Endothelin induces two types of contractions of rat uterus: phasic contractions by way of voltage-dependent calcium channels and developing contractions through a second type of calcium channels. Biochem Biophys Res Commun 159:317–323. doi:10.1016/0006-291X(89)92440-6

    PubMed  CAS  Google Scholar 

  • Lang R, Gundlach AL, Kofler B (2007) The galanin peptide family: receptor pharmacology, pleiotropic biological actions, and implications in health and disease. Pharmacol Ther 115:177–207. doi:10.1016/j.pharmthera.2007.05.009

    PubMed  CAS  Google Scholar 

  • Larsen PJ, Jukes KE, Chowdrey HS, Lightman SL, Jessop DS (1994) Neuropeptide-Y potentiates the secretion of vasopressin from the neurointermediate lobe of the rat pituitary gland. Endocrinology 134:1635–1639. doi:10.1210/en.134.4.1635

    PubMed  CAS  Google Scholar 

  • Larsen PJ, Mikkelsen JD (1992) Vasoactive intestinal peptide (VIP) in magnocellular neurons of the hypothalamo-neurohypophysial system of the mink (Mustela vision) is co-localized with vasopressin or oxytocin. J Comp Neurol 326:180–192. doi:10.1002/cne.903260203

    PubMed  CAS  Google Scholar 

  • Larsen PJ, Sheikh SP, Mikkelsen JD (1992) Osmotic regulation of neuropeptide Y and its binding sites in the magnocellular hypothalamo-neurohypophysial pathway. Brain Res 573:181–189. doi:10.1016/0006-8993(92)90761-W

    PubMed  CAS  Google Scholar 

  • Laulin JP, Simonnet G, Brudieux R, Carayon A, Vincent JD (1988) A ldosterone secretion and adrenal angiotensin II receptors in Brattleboro rat. J Endocrinol 117:215–221

    PubMed  CAS  Google Scholar 

  • Leng G, Brown CH, Russell JA (1999) Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 57:625–655. doi:10.1016/S0301-0082(98)00072-0

    PubMed  CAS  Google Scholar 

  • Lind RW, Swanson LW, Bruhn TO, Ganten D (1985a) The distribution of angiotensin II-immunoreactive cells and fibers in the paraventriculo-hypophysial system of the rat. Brain Res 338:81–89. doi:10.1016/0006-8993(85)90250-1

    PubMed  CAS  Google Scholar 

  • Lind RW, Swanson LW, Ganten D (1985b) Organization of angiotensin II immunoreactive cells and fibers in the rat central nervous system. An immunohistochemical study. Neuroendocrinology 40:2–24. doi:10.1159/000124046

    PubMed  CAS  Google Scholar 

  • Liu H, Hökfelt T (2002) The participation of galanin in pain processing at the spinal level. Trends Pharmacol Sci 23:468–474. doi:10.1016/S0165-6147(02)02074-6

    PubMed  CAS  Google Scholar 

  • Liu S, Ju G (1994) Origin of CCK-like immunoreactive nerve fibers in the neurohypophysis of the rat. Brain Res 651:7–15. doi:10.1016/0006-8993(94)90675-0

    PubMed  CAS  Google Scholar 

  • Llorens-Cortés C, Beaudet A (2005) Apelin, a neuropeptide that counteracts vasopressin secretion. Med Sci (Paris) 21:741–746

    Google Scholar 

  • Llorens-Cortes C, Moos F (2008) Opposite potentiality of hypothalamic coexpressed neuropeptides, apelin, and vasopressin in maintaining body-fluid homeostasis. Prog Brain Res 170:559–570. doi:10.1016/S0079-6123(08)00443-3

    PubMed  CAS  Google Scholar 

  • Lukiw WJ (2006) Endogenous signaling complexity in neuropeptides-leucine and methionine-enkephalin. Cell Mol Neurobiol 26:1003–1010. doi:10.1007/s10571-006-9100-6

    PubMed  CAS  Google Scholar 

  • Ma D, Morris JF (2002) Protein synthetic machinery in the dendrites of the magnocellular neurosecretory neurons of wild-type Long-Evans and homozygous Brattleboro rats. J Chem Neuroanat 23:171–186. doi:10.1016/S0891-0618(01)00158-2

    PubMed  CAS  Google Scholar 

  • Mahata K, Mahata M, Hörtnagl H, Fischer-Colbrie R, Steiner HJ, Dietze O et al (1993) Concomitant changes of messenger ribonucleic acid levels of secretogranin II, VGF, vasopressin and oxytocin in the paraventricular nucleus of rats after adrenalectomy and during lactation. J Neuroendocrinol 5:323–330. doi:10.1111/j.1365-2826.1993.tb00489.x

    PubMed  CAS  Google Scholar 

  • Mahata SK, Mahata M, Steiner HJ, Fischer-Colbrie R, Winkler H (1992) In situ hybridization: mRNA levels of secretogranin II, neuropeptides and carboxypeptidase H in brains of salt loaded and Brattleboro rats. Neuroscience 48:669–680. doi:10.1016/0306-4522(92)90410-4

    PubMed  CAS  Google Scholar 

  • Marsais F, Parmentier C, Terao E, Taxi J, Calas A (2002) Expression of tyrosine hydroxylase and vasopressin in magnocellular neurons of salt loaded aged rats. Microsc Res Tech 56:81–91. doi:10.1002/jemt.10018

    PubMed  CAS  Google Scholar 

  • Martin R, Voigt KH (1981) Enkephalins co-exist with oxytocin and vasopressin in nerve terminals of rat neurohypophysis. Nature 289:502–504. doi:10.1038/289502a0

    PubMed  CAS  Google Scholar 

  • McDonald MP, Gleason TC, Robinson JK, Crawley JN (1998) Galanin inhibits performance on rodent memory tasks. Ann NY Acad Sci 863:305–322. doi:10.1111/j.1749-6632.1998.tb10704.x

    PubMed  CAS  Google Scholar 

  • Meister B, Cortés R, Villar MJ, Schalling M, Hökfelt T (1990a) Peptides and transmitter enzymes in hypothalamic magnocellular neurons after administration of hyperosmotic stimuli: comparison between messenger RNA and peptide/protein levels. Cell Tissue Res 260:279–297. doi:10.1007/BF00318631

    PubMed  CAS  Google Scholar 

  • Meister B, Villar MJ, Ceccatelli S, Hökfelt T (1990b) Localization of chemical messengers in magnocellular neurons of the hypothalamic supraoptic and paraventricular nuclei: an immunohistochemical study using experimental manipulations. Neuroscience 37:603–633. doi:10.1016/0306-4522(90)90094-K

    PubMed  CAS  Google Scholar 

  • Micevych PE, Park SS, Akesson TR, Elde R (1987) Distribution of cholecystokinin-immunoreactive cell bodies in the male and female rat: I. Hypothalamus. J Comp Neurol 255:124–136. doi:10.1002/cne.902550110

    PubMed  CAS  Google Scholar 

  • Mikkelsen JD (1989) Immunohistochemical localization of vasoactive intestinal peptide (VIP) in the circumventricular organs of the rat. Cell Tissue Res 255:307–3013. doi:10.1007/BF00224113

    PubMed  CAS  Google Scholar 

  • Mikkelsen JD, Møller M (1988) Vasoactive intestinal peptide in the hypothalamohypophysial system of the Mongolian gerbil. J Comp Neurol 273:87–98. doi:10.1002/cne.902730108

    PubMed  CAS  Google Scholar 

  • Mlynarik M, Zelena D, Bagdy G, Makara GB, Jezova D (2007) Signs of attenuated depression-like behavior in vasopressin deficient Brattleboro rats. Horm Behav 51:395–405. doi:10.1016/j.yhbeh.2006.12.007

    PubMed  CAS  Google Scholar 

  • Nakamura S, Naruse M, Naruse K, Shioda S, Nakai Y, Uemura H (1993) Colocalization of immunoreactive endothelin-1 and neurohypophysial hormones in the axons of the neural lobe of the rat pituitary. Endocrinology 132:530–533. doi:10.1210/en.132.2.530

    PubMed  CAS  Google Scholar 

  • Nakata M, Kohno D, Shintani N, Nemoto Y, Hashimoto H, Baba A et al (2004) PACAP deficient mice display reduced carbohydrate intake and PACAP activates NPY-containing neurons in the rat hypothalamic arcuate nucleus. Neurosci Lett 370:252–256. doi:10.1016/j.neulet.2004.08.034

    PubMed  CAS  Google Scholar 

  • Namer B, Hilliges M, Orstavik K, Schmidt R, Weidner C, Torebjörk E et al (2007) Endothelin1 activates and sensitizes human C-nociceptors. Pain 137(1):41–49

    PubMed  Google Scholar 

  • Nomura M, Ueta Y, Serino R, Kabashima N, Shibuya I, Yamashita H (1996) PACAP type I receptor gene expression in the paraventricular and supraoptic nuclei of rats. Neuroreport 8:67–70. doi:10.1097/00001756-199612200-00014

    PubMed  CAS  Google Scholar 

  • Nomura M, Ueta Y, Serino R, Yamamoto Y, Shibuya I, Yamashita H (1999) Effects of centrally administered pituitary adenylate cyclase-activating polypeptide on c-fos gene expression and heteronuclear RNA for vasopressin in rat paraventricular and supraoptic nuclei. Neuroendocrinology 69:167–180. doi:10.1159/000054416

    PubMed  CAS  Google Scholar 

  • O’Shea RD, Gundlach AL (1996) Food or water deprivation modulate nitric oxide synthase (NOS) activity and gene expression in rat hypothalamic neurones: correlation with neurosecretory activity? J Neuroendocrinol 8:417–425. doi:10.1046/j.1365-2826.1996.04682.x

    PubMed  CAS  Google Scholar 

  • Orino K, Lehman L, Tsuji Y, Ayaki H, Torti SV, Torti FM (2001) Ferritin and the response to oxidative stress. Biochem J 357:241–247. doi:10.1042/0264-6021:3570241

    PubMed  CAS  Google Scholar 

  • Panayotacopoulou MT, Raadsheer FC, Swaab DF (1994) Colocalization of tyrosine hydroxylase with oxytocin or vasopressin in neurons of the human paraventricular and supraoptic nucleus. Brain Res Dev Brain Res 83:59–66. doi:10.1016/0165-3806(94)90179-1

    PubMed  CAS  Google Scholar 

  • Paulsen SJ, Christensen MT, Vrang N, Larsen LK (2008) The putative neuropeptide TAFA5 is expressed in the hypothalamic paraventricular nucleus and is regulated by dehydration. Brain Res 1199:1–9. doi:10.1016/j.brainres.2007.12.074

    PubMed  CAS  Google Scholar 

  • Phillips MI (1987) Functions of angiotensin in the central nervous system. Annu Rev Physiol 49:413–435. doi:10.1146/annurev.ph.49.030187.002213

    PubMed  CAS  Google Scholar 

  • Reaux A, De Mota N, Skultetyova I, Lenkei Z, El Messari S, Gallatz K, Corvol P, Palkovits M, Llorens-Cortés C (2001) Physiological role of a novel neuropeptide, apelin, and its receptor in the rat brain. J Neurochem 77:1085–1096. doi:10.1046/j.1471-4159.2001.00320.x

    PubMed  CAS  Google Scholar 

  • Reaux-Le Goazigo A, Morinville A, Burlet A, Llorens-Cortés C, Beaudet A (2004) Dehydration-induced cross-regulation of apelin and vasopressin immunoreactivity levels in magnocellular hypothalamic neurons. Endocrinology 145:4392–4400. doi:10.1210/en.2004-0384

    PubMed  CAS  Google Scholar 

  • Recalcati S, Invernizzi P, Arosio P, Cairo G (2008) New functions for an iron storage protein: the role of ferritin in immunity and autoimmunity. J Autoimmun 30:84–89. doi:10.1016/j.jaut.2007.11.003

    PubMed  CAS  Google Scholar 

  • Richoux JP, Gelly JL, Bouhnik J, Baussant T, Alhene-Gelas F, Grignon G et al (1991) The kallikrein–kinin system in the rat hypothalamus. Immunohistochemical localization of high molecular weight kininogen and T-kininogen in different neuronal systems. Histochemistry 96:229–243. doi:10.1007/BF00271541

    PubMed  CAS  Google Scholar 

  • Rökaeus Å, Young WSIII, Mezey E (1988) Galanin coexists with vasopressin in the normal rat hypothalamus and galanin’s synthesis is increased in the Brattleboro (diabetes insipidus) rat. Neurosci Lett 90:45–50. doi:10.1016/0304-3940(88)90784-7

    PubMed  Google Scholar 

  • Rossmanith WG, Clifton DK, Steiner RA (1996) Galanin gene expression in hypothalamic GnRH-containing neurons of the rat: a model for autocrine regulation. Horm Metab Res 28:257–266

    Article  PubMed  CAS  Google Scholar 

  • Saul GBII, Garrity EB, Benirschke K, Valtin H (1968) Inherited hypothalamic diabetes insipidus in the Brattleboro strain of rats. J Hered 59:113–117

    PubMed  Google Scholar 

  • Schlosser SF, Almeida OF, Patchev VK, Yassoiridis A, Elands J (1994) Oxytocin-stimulated release of adrenocorticotropin from the rat pituitary is mediated by arginine vasopressin receptors of the V1b type. Endocrinology 135:2058–2063. doi:10.1210/en.135.5.2058

    PubMed  CAS  Google Scholar 

  • Shen PJ, Gundlach AL (1996) Chromogranin mRNA levels in the brain as a marker for acute and chronic changes in neuronal activity: effect of treatments including seizures, osmotic stimulation and axotomy in the rat. Eur J Neurosci 8:988–1000. doi:10.1111/j.1460-9568.1996.tb01586.x

    PubMed  CAS  Google Scholar 

  • Sherin JE, Elmquist JK, Torrealba F, Saper CB (1998) Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18:4705–4721

    PubMed  CAS  Google Scholar 

  • Sherman TG, Day R, Civelli O, Douglass J, Herbert E, Akil H et al (1988) Regulation of hypothalamic magnocellular neuropeptides and their mRNAs in the Brattleboro rat: coordinate responses to further osmotic challenge. J Neurosci 8:3785–3796

    PubMed  CAS  Google Scholar 

  • Skofitsch G, Jacobowitz DM (1986) Quantitative distribution of galanin-like immunoreactivity in the rat central nervous system. Peptides 7:609–613. doi:10.1016/0196-9781(86)90035-5

    PubMed  CAS  Google Scholar 

  • Smith BN, Armstrong WE (1990) Tuberal supraoptic neurons. I. Morphological and electrophysiological characteristics observed with intracellular recording and biocytin filling in vitro. Neuroscience 38:469–483. doi:10.1016/0306-4522(90)90043-4

    PubMed  CAS  Google Scholar 

  • Smith AP, Lee NM (1988) Pharmacology of dynorphin. Annu Rev Pharmacol Toxicol 28:123–140. doi:10.1146/annurev.pa.28.040188.001011

    PubMed  CAS  Google Scholar 

  • Snyder SH (2004) Opiate receptors and beyond: 30 years of neural signaling research. Neuropharmacology 47:274–285. doi:10.1016/j.neuropharm.2004.06.006

    PubMed  CAS  Google Scholar 

  • Swanson LW, Kuypers HGJM (1980) The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and the organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling method. J Comp Neurol 194:555–570. doi:10.1002/cne.901940306

    PubMed  CAS  Google Scholar 

  • Telleria-Diaz A, Grinevich VV, Jirikowski GF (2001) Colocalization of vasopressin and oxytocin in hypothalamic magnocellular neurons in water-deprived rats. Neuropeptides 35:162–167. doi:10.1054/npep.2001.0859

    PubMed  CAS  Google Scholar 

  • Tokunaga A, Ono K, Ono T, Ogawa M (1992) Magnocellular neurosecretory neurons with ferritin-like immunoreactivity in the hypothalamic supraoptic and paraventricular nuclei of the rat. Brain Res 597:170–175. doi:10.1016/0006-8993(92)91522-G

    PubMed  CAS  Google Scholar 

  • Treschan TA, Peters J (2006) The vasopressin system: physiology and clinical strategies. Anesthesiology 105:444–445. doi:10.1097/00000542-200609000-00026

    Google Scholar 

  • Turnbull AV, Rivier C (1997) Corticotropin-releasing factor (CRF) and endocrine responses to stress: CRF receptors, binding protein and related peptides. Proc Soc Exp Biol Med 215:1–10

    PubMed  CAS  Google Scholar 

  • Uemura H, Naruse M, Nakamura S, Naruse K, Yamamoto T, Demura H et al (1994) Immunoreactive endothelin-1 in the neural lobe of the rat pituitary following hemorrhage and dehydration. Endocr J 41:685–691

    PubMed  CAS  Google Scholar 

  • Urban JH, Leitermann RJ, Dejoseph MR, Somponpun SJ, Wolak ML, Sladek CD (2006) Influence of dehydration on the expression of neuropeptide Y Y1 receptors in hypothalamic magnocellular neurons. Endocrinology 147:4122–4131. doi:10.1210/en.2006-0377

    PubMed  CAS  Google Scholar 

  • Valtin H, Schroeder HA, Bernischke K, Sokol HW (1962) Familial hypothalamic diabetes insipidus in rats. Nature 196:1109–1110. doi:10.1038/1961109a0

    PubMed  CAS  Google Scholar 

  • Vanderhaeghen JJ, Lotstra F, Vandesande F, Dierickx K (1981) Coexistence of cholecystokinin and oxytocin-neurophysin in some magnocellular hypothalamo-hypophyseal neurons. Cell Tissue Res 221:227–231. doi:10.1007/BF00216585

    PubMed  CAS  Google Scholar 

  • Vandesande F, Dierickx K (1976) Immuno-cytochemical demonstration of the inability of the homozygous Brattleboro rat to synthesize vasopressin and vasopressin-associated neurophysin. Cell Tissue Res 165:307–316. doi:10.1007/BF00222435

    PubMed  CAS  Google Scholar 

  • Vaughan J, Donaldson C, Bittencourt J, Perrin M, Lewis K, Sutton S et al (1995) Urocortin, a mammalian neuropeptide related to fish urotensin I and corticotrophin-releasing factor. Nature 378:287–292. doi:10.1038/378287a0

    PubMed  CAS  Google Scholar 

  • Verbalis JG, Dohanics J (1991) Vasopressin and oxytocin secretion in chronically hyposmolar rats. Am J Physiol Regul Integr Comp Physiol 261:R1028–R1038

    CAS  Google Scholar 

  • Wall KM, Ferguson AV (1992) Endothelin acts at the subfornical organ to influence the activity of putative vasopressin and oxytocin-secreting neurons. Brain Res 586:111–116. doi:10.1016/0006-8993(92)91378-R

    PubMed  CAS  Google Scholar 

  • Walsh DA, Mc F, Williams D (2006) Tachykinins and the cardiovascular system. Curr Drug Targets 7:1031–1042. doi:10.2174/138945006778019291

    PubMed  CAS  Google Scholar 

  • Watson SJ, Akil H, Fischli W, Goldstein A, Zimmerman E, Nilaver G et al (1982) Dynorphin and vasopressin: common localization in magnocellular neurons. Science 216:85–87. doi:10.1126/science.6121376

    PubMed  CAS  Google Scholar 

  • Weihe E, Depboylu C, Schütz B, Schäfer MK, Eiden LE (2006) Three types of tyrosine hydroxylase-positive CNS neurons distinguished by dopa decarboxylase and VMAT2 co-expression. Cell Mol Neurobiol 26:659–678. doi:10.1007/s10571-006-9053-9

    PubMed  CAS  Google Scholar 

  • Wiegand SJ, Price JL (1980) Cells of origin of the afferent fibers to the median eminence in the rat. J Comp Neurol 192:1–19. doi:10.1002/cne.901920102

    PubMed  CAS  Google Scholar 

  • Xapelli S, Agasse F, Ferreira R, Silva AP, Malva JO (2006) Neuropeptide Y as an endogenous antiepileptic, neuroprotective and pro-neurogenic peptide. Recent Patents CNS Drug Discov 1:315–324

    PubMed  CAS  Google Scholar 

  • Yamamoto Y, Ueta Y, Nomura M, Serino R, Kabashima N, Shibuya I et al (1997) Upregulation of neuronal NOS mRNA in the PVN and SON of inherited diabetes insipidus rats. Neuroreport 8:3907–3911

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi A, Dohgu S, Nishioku T, Shuto H, Naito M, Tsuruo T et al (2007) An inhibitory role of nitric oxide in the dynamic regulation of the blood–brain barrier function. Cell Mol Neurobiol 27:263–270. doi:10.1007/s10571-007-9139-z

    PubMed  CAS  Google Scholar 

  • You SA, Wang Q (2005) Ferritin in atherosclerosis. Clin Chim Acta 357:1–16. doi:10.1016/j.cccn.2005.02.001

    PubMed  CAS  Google Scholar 

  • Young SF, Griffante C, Aguilera G (2007) Dimerization between vasopressin V1b and corticotropin releasing hormone type 1 receptors. Cell Mol Neurobiol 27:439–461. doi:10.1007/s10571-006-9135-8

    PubMed  CAS  Google Scholar 

  • Young WSIII, Warden M, Mezey E (1987) Tyrosine hydroxylase mRNA is increased by hyperosmotic stimuli in the paraventricular and supraoptic nuclei. Neuroendocrinology 46:439–444. doi:10.1159/000124858

    PubMed  Google Scholar 

  • Yue C, Mutsuga N, Verbalis J, Gainer H (2006) Microarray analysis of gene expression in the supraoptic nucleus of normoosmotic and hypoosmotic rats. Cell Mol Neurobiol 26:959–978. doi:10.1007/s10571-006-9017-0

    PubMed  CAS  Google Scholar 

  • Zhang B, Glasgow E, Murase T, Verbalis JG, Gainer H (2001) Chronic hypoosmolality induces a selective decrease in magnocellular neurone soma and nuclear size in the rat hypothalamic supraoptic nucleus. J Neuroendocrinol 13:29–36. doi:10.1046/j.1365-2826.2001.00593.x

    PubMed  Google Scholar 

  • Zudenigo D, Lackovic Z (1989) Vasoactive intestinal polypeptide: a potential neurotransmitter. Lijec Vjesn 111:349–354

    Google Scholar 

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Acknowledgments

This work was supported by Vega 2/7003/27, CE SAS CENDO, and APVV-0148-06 grants.

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Bundzikova, J., Pirnik, Z., Zelena, D. et al. Response of Substances Co-Expressed in Hypothalamic Magnocellular Neurons to Osmotic Challenges in Normal and Brattleboro Rats. Cell Mol Neurobiol 28, 1033–1047 (2008). https://doi.org/10.1007/s10571-008-9306-x

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