Neuronal nitric oxide synthase gene inactivation reduces the expression of vasopressin in the hypothalamic paraventricular nucleus and of catecholamine biosynthetic enzymes in the adrenal gland of the mouse

References

• Akasaka S, Nomura M, Nishii H, Fujimoto N, Ueta Y, Tsutsui M, Shimokawa H, Yanagihara N, Matsumoto T. The hypothalamo-pituitary axis responses to lipopolysaccharide-induced endotoxemia in mice lacking inducible nitric oxide synthase. Brain Res 2006; 1089: 1–9
   PubMed Web of Science ®Google Scholar
• Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: Structure, function and inhibition. Biochem J 2001; 357: 593–615
   PubMed Web of Science ®Google Scholar
• Antoni FA. Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age. Front Neuroendocrinol 1993; 14: 76–122
   PubMed Web of Science ®Google Scholar
• Appel NM, Kiritsy-Roy JA, Van Loon GR. Hypothalamic opioid peptide regulation of catecholamine secretion. Neuropeptides 1984; 5: 287–290
   PubMed Web of Science ®Google Scholar
• Aubry JM, Bartanusz V, Jezova D, Belin D, Kiss JZ. Single stress induces long-lasting elevations in vasopressin mRNA levels in CRF hypophysiotrophic neurones, but repeated stress is required to modify AVP immunoreactivity. J Neuroendocrinol 1999; 11: 377–384
   PubMed Web of Science ®Google Scholar
• Barnes RD, Ward LE, Frank KP, Tyce GM, Hunter LW, Rorie DK. Nitric oxide modulates evoked catecholamine release from canine adrenal medulla. Neuroscience 2001; 104: 1165–1173
   PubMed Web of Science ®Google Scholar
• Bernstein HG, Keilhoff G, Seidel B, Stanarius A, Huang PL, Fishman MC, Reiser M, Bogerts B, Wolf G. Expression of hypothalamic peptides in mice lacking neuronal nitric oxide synthase: Reduced beta-END immunoreactivity in the arcuate nucleus. Neuroendocrinology 1998; 68: 403–411
   PubMed Web of Science ®Google Scholar
• Bornstein SR, Tian H, Haidan A, Bottner A, Hiroi N, Eisenhofer G, McCann SM, Chrousos GP, Roffler-Tarlov S. Deletion of tyrosine hydroxylase gene reveals functional interdependence of adrenocortical and chromaffin cell system in vivo. Proc Natl Acad Sci USA 2000; 97: 14742–14747
   PubMed Web of Science ®Google Scholar
• Brunetti L, Preziosi P, Ragazzoni E, Vacca M. Involvement of nitric oxide in basal and interleukin-1 beta-induced CRH and ACTH release in vitro. Life Sci 1993; 53: PL219–PL222
   PubMed Web of Science ®Google Scholar
• Burbach JP, De Hoop MJ, Schmale H, Richter D, De Kloet ER, Ten Haaf JA, De Wied D. Differential responses to osmotic stress of vasopressin-neurophysin mRNA in hypothalamic nuclei. Neuroendocrinology 1984; 39: 582–584
   PubMed Web of Science ®Google Scholar
• Chiavegatto S, Nelson RJ. Interaction of nitric oxide and serotonin in aggressive behavior. Horm Behav 2003; 44: 233–241
   PubMed Web of Science ®Google Scholar
• Chiavegatto S, Dawson VL, Mamounas LA, Koliatsos VE, Dawson TM, Nelson RJ. Brain serotonin dysfunction accounts for aggression in male mice lacking neuronal nitric oxide synthase. Proc Natl Acad Sci USA 2001; 98: 1277–1281
   PubMed Web of Science ®Google Scholar
• Chrousos GP, Gold PW. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 1992; 267: 1244–1252
   PubMed Web of Science ®Google Scholar
• Costa A, Trainer P, Besser M, Grossman A. Nitric oxide modulates the release of corticotropin-releasing hormone from the rat hypothalamus in vitro. Brain Res 1993; 605: 187–192
   PubMed Web of Science ®Google Scholar
• Csete K, Kovacs GL, Szekeres L. Disturbance of motoric function as behavioral measure of impaired cerebral circulation in mice. Physiol Behav 1986; 36: 409–412
   PubMed Web of Science ®Google Scholar
• Dash R, Kadambi V, Schmidt AG, Tepe NM, Biniakiewicz D, Gerst MJ, Canning AM, Abraham WT, Hoit BD, Liggett SB, Lorenz JN, Dorn GWn, Kranias EG. Interactions between phospholamban and beta-adrenergic drive may lead to cardiomyopathy and early mortality. Circulation 2001; 103: 889–896
   PubMed Web of Science ®Google Scholar
• Dun NJ, Dun SL, Wu SY, Forstermann U. Nitric oxide synthase immunoreactivity in rat superior cervical ganglia and adrenal glands. Neurosci Lett 1993; 158: 51–54
   PubMed Web of Science ®Google Scholar
• Eliasson MJ, Blackshaw S, Schell MJ, Snyder SH. Neuronal nitric oxide synthase alternatively spliced forms: Prominent functional localizations in the brain. Proc Natl Acad Sci USA 1997; 94: 3396–3401
   PubMed Web of Science ®Google Scholar
• Engelmann M, Landgraf R, Wotjak CT. The hypothalamic-neurohypophysial system regulates the hypothalamic–pituitary–adrenal axis under stress: An old concept revisited. Front Neuroendocrinol 2004; 25: 132–149
   PubMed Web of Science ®Google Scholar
• Giordano M, Vermeulen M, Trevani AS, Dran G, Andonegui G, Geffner JR. Nitric oxide synthase inhibitors enhance plasma levels of corticosterone and ACTH. Acta Physiol Scand 1996; 157: 259–264
   PubMedGoogle Scholar
• Givalois L, Li S, Pelletier G. Central nitric oxide regulation of the hypothalamic-pituitary-adrenocortical axis in adult male rats. Brain Res Mol Brain Res 2002; 102: 1–8
   PubMedGoogle Scholar
• Grouzmann E, Cavadas C, Grand D, Moratel M, Aubert JF, Brunner HR, Mazzolai L. Blood sampling methodology is crucial for precise measurement of plasma catecholamines concentrations in mice. Pflugers Arch 2003; 447: 254–258
   PubMed Web of Science ®Google Scholar
• Gulya K, Dave JR, Hoffman PL. Chronic ethanol ingestion decreases vasopressin mRNA in hypothalamic and extrahypothalamic nuclei of mouse brain. Brain Res 1991; 557: 129–135
   PubMed Web of Science ®Google Scholar
• Hashimoto K, Nishioka T, Tojo C, Takao T. Nitric oxide plays no role in ACTH release induced by interleukin-1 beta, corticotropin-releasing hormone, arginine vasopressin and phorbol myristate acetate in rat pituitary cell cultures. Endocr J 1995; 42: 435–439
   PubMed Web of Science ®Google Scholar
• Hatakeyama S, Kawai Y, Ueyama T, Senba E. Nitric oxide synthase-containing magnocellular neurons of the rat hypothalamus synthesize oxytocin and vasopressin and express Fos following stress stimuli. J Chem Neuroanat 1996; 11: 243–256
   PubMed Web of Science ®Google Scholar
• Heym C, Colombo-Benckmann M, Mayer B. Immunohistochemical demonstration of the synthesis enzyme for nitric oxide and of comediators in neurons and chromaffin cells of the human adrenal medulla. Ann Anat 1994; 176: 11–16
   PubMed Web of Science ®Google Scholar
• Horn T, Smith PM, McLaughlin BE, Bauce L, Marks GS, Pittman QJ, Ferguson AV. Nitric oxide actions in paraventricular nucleus: Cardiovascular and neurochemical implications. Am J Physiol 1994; 266: R306–R313
   PubMedGoogle Scholar
• Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 1993; 75: 1273–1286
   PubMed Web of Science ®Google Scholar
• Jansen AS, Nguyen XV, Karpitskiy V, Mettenleiter TC, Loewy AD. Central command neurons of the sympathetic nervous system: Basis of the fight-or-flight response. Science 1995; 270: 644–646
   PubMed Web of Science ®Google Scholar
• Kadekaro M. Nitric oxide modulation of the hypothalamo-neurohypophyseal system. Braz J Med Biol Res 2004; 37: 441–450
   PubMed Web of Science ®Google Scholar
• Keilhoff G, Seidel B, Reiser M, Stanarius A, Huang PL, Bogerts B, Wolf G, Bernstein HG. Lack of neuronal NOS has consequences for the expression of POMC and POMC-derived peptides in the mouse pituitary. Acta Histochem 2001; 103: 397–412
   PubMed Web of Science ®Google Scholar
• Kim D, Choi HJ, Kim SW, Cho SW, Hwang O. Upregulation of catecholamine biosynthetic enzymes by nitric oxide. J Neurosci Res 2003; 72: 98–104
   PubMed Web of Science ®Google Scholar
• Korte SM. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 2001; 25: 117–142
   PubMed Web of Science ®Google Scholar
• Lang RE, Heil JW, Ganten D, Hermann K, Unger T, Rascher W. Oxytocin unlike vasopressin is a stress hormone in the rat. Neuroendocrinology 1983; 37: 314–316
   PubMed Web of Science ®Google Scholar
• Lee S, Kim CK, Rivier C. Nitric oxide stimulates ACTH secretion and the transcription of the genes encoding for NGFI-B, corticotropin-releasing factor, corticotropin-releasing factor receptor type 1, and vasopressin in the hypothalamus of the intact rat. J Neurosci 1999; 19: 7640–7647
   PubMed Web of Science ®Google Scholar
• Marley PD, McLeod J, Anderson C, Thomson KA. Nerves containing nitric oxide synthase and their possible function in the control of catecholamine secretion in the bovine adrenal medulla. J Auton Nerv Syst 1995; 54: 184–194
   PubMedGoogle Scholar
• Miyagawa A, Okamura H, Ibata Y. Coexistence of oxytocin and NADPH-diaphorase in magnocellular neurons of the paraventricular and the supraoptic nuclei of the rat hypothalamus. Neurosci Lett 1994; 171: 13–16
   PubMed Web of Science ®Google Scholar
• Nelson RJ, Demas GE, Huang PL, Fishman MC, Dawson VL, Dawson TM, Snyder SH. Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase. Nature 1995; 378: 383–386
   PubMed Web of Science ®Google Scholar
• Nomura M, Tsutsui M, Shimokawa H, Fujimoto N, Ueta Y, Morishita T, Yanagihara N, Matsumoto T. Effects of nitric oxide synthase isoform deletion on oxytocin and vasopressin messenger RNA in mouse hypothalamus. Neuroreport 2005; 16: 413–417
   PubMed Web of Science ®Google Scholar
• Orlando GF, Langnaese K, Landgraf R, Spina MG, Wolf G, Engelmann M. Neural nitric oxide gene inactivation affects the release profile of oxytocin into the blood in response to forced swimming. Nitric Oxide 2007; 16: 64–70
   PubMed Web of Science ®Google Scholar
• Oset-Gasque MJ, Parramon M, Hortelano S, Bosca L, Gonzalez MP. Nitric oxide implication in the control of neurosecretion by chromaffin cells. J Neurochem 1994; 63: 1693–1700
   PubMed Web of Science ®Google Scholar
• Oset-Gasque MJ, Vicente S, Gonzalez MP, Rosario LM, Castro E. Segregation of nitric oxide synthase expression and calcium response to nitric oxide in adrenergic and noradrenergic bovine chromaffin cells. Neuroscience 1998; 83: 271–280
   PubMed Web of Science ®Google Scholar
• Palacios M, Knowles RG, Palmer RM, Moncada S. Nitric oxide from l-arginine stimulates the soluble guanylate cyclase in adrenal glands. Biochem Biophys Res Commun 1989; 165: 802–809
   PubMed Web of Science ®Google Scholar
• Paulmyer-Lacroix O, Anglade G, Grino M. Insulin-induced hypoglycaemia increases colocalization of corticotrophin-releasing factor and arginine vasopressin mRNAs in the rat hypothalamic paraventricular nucleus. J Mol Endocrinol 1994; 13: 313–320
   PubMed Web of Science ®Google Scholar
• Paxinos G, Franklin KBJ. The mouse brain in stereotaxic coordinates. San Diego, USA 1997
   Google Scholar
• Pyner S, Coote JH. Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 2000; 100: 549–556
   PubMed Web of Science ®Google Scholar
• Ranson RN, Motawei K, Pyner S, Coote JH. The paraventricular nucleus of the hypothalamus sends efferents to the spinal cord of the rat that closely appose sympathetic preganglionic neurones projecting to the stellate ganglion. Exp Brain Res 1998; 120: 164–172
   PubMed Web of Science ®Google Scholar
• Riedel W. Role of nitric oxide in the control of the hypothalamic–pituitary–adrenocortical axis. Z Rheumatol 2000; 59(Suppl 2)II/36–II/42
   Google Scholar
• Rivier C, Shen GH. In the rat, endogenous nitric oxide modulates the response of the hypothalamic–pituitary–adrenal axis to interleukin-1 beta, vasopressin, and oxytocin. J Neurosci 1994; 14: 1985–1993
   PubMed Web of Science ®Google Scholar
• Roberts MM, Robinson AG, Fitzsimmons MD, Grant F, Lee WS, Hoffman GE. c-Fos expression in vasopressin and oxytocin neurons reveals functional heterogeneity within magnocellular neurons. Neuroendocrinology 1993; 57: 388–400
   PubMed Web of Science ®Google Scholar
• Rodriguez-Pascual F, Miras-Portugal MT, Torres M. Effect of cyclic GMP-increasing agents nitric oxide and C-type natriuretic peptide on bovine chromaffin cell function: Inhibitory role mediated by cyclic GMP-dependent protein kinase. Mol Pharmacol 1996; 49: 1058–1070
   PubMed Web of Science ®Google Scholar
• Sabban EL, Kvetnansky R. Stress-triggered activation of gene expression in catecholaminergic systems: Dynamics of transcriptional events. Trends Neurosci 2001; 24: 91–98
   PubMed Web of Science ®Google Scholar
• Salchner P, Lubec G, Engelmann M, Orlando GF, Wolf G, Sartori SB, Hoeger H, Singewald N. Genetic functional inactivation of neuronal nitric oxide synthase affects stress-related Fos expression in specific brain regions. Cell Mol Life Sci 2004; 61: 1498–1506
   PubMed Web of Science ®Google Scholar
• Sanchez F, Alonso JR, Arevalo R, Blanco E, Aijon J, Vazquez R. Coexistence of NADPH-diaphorase with vasopressin and oxytocin in the hypothalamic magnocellular neurosecretory nuclei of the rat. Cell Tissue Res 1994; 276: 31–34
   PubMed Web of Science ®Google Scholar
• Schafer MK-H, Day R. In situ hybridization techniques to map processing enzymes. Methods Neurosci 1995; 23: 16–44
   Google Scholar
• Sgoifo A, de Boer SF, Haller J, Koolhaas JM. Individual differences in plasma catecholamine and corticosterone stress responses of wild-type rats: Relationship with aggression. Physiol Behav 1996; 60: 1403–1407
   PubMed Web of Science ®Google Scholar
• Sherman TG, McKelvy JF, Watson SJ. Vasopressin mRNA regulation in individual hypothalamic nuclei: A northern and in situ hybridization analysis. J Neurosci 1986; 6: 1685–1694
   PubMed Web of Science ®Google Scholar
• Siaud P, Mekaouche M, Ixart G, Balmefrezol M, Givalois L, Barbanel G, Assenmacher I. A subpopulation of corticotropin-releasing hormone neurosecretory cells in the paraventricular nucleus of the hypothalamus also contain NADPH-diaphorase. Neurosci Lett 1994; 170: 51–54
   PubMed Web of Science ®Google Scholar
• Thomas SA, Palmiter RD. Impaired maternal behavior in mice lacking norepinephrine and epinephrine. Cell 1997; 91: 583–592
   PubMed Web of Science ®Google Scholar
• Torres G, Lee S, Rivier C. Ontogeny of the rat hypothalamic nitric oxide synthase and colocalizatio with neuropeptides. Mol Cell Neurosci 1993; 4: 155–163
   PubMed Web of Science ®Google Scholar
• Uchiyama Y, Morita K, Kitayama S, Suemitsu T, Minami N, Miyasako T, Dohi T. Possible involvement of nitric oxide in acetylcholine-induced increase of intracellular Ca2+ concentration and catecholamine release in bovine adrenal chromaffin cells. Jpn J Pharmacol 1994; 65: 73–77
   PubMedGoogle Scholar
• Vale W, Spiess J, Rivier C, Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981; 213: 1394–1397
   PubMed Web of Science ®Google Scholar
• Van Loon GR, Appel NM, Ho D. Beta-endorphin-induced increases in plasma epinephrine, norepinephrine and dopamine in rats: Inhibition of adrenomedullary response by intracerebral somatostatin. Brain Res 1981a; 212: 207–214
   PubMed Web of Science ®Google Scholar
• Van Loon GR, Appel NM, Ho D. Beta-endorphin-induced stimulation of central sympathetic outflow: Beta-endorphin increases plasma concentrations of epinephrine, norepinephrine, and dopamine in rats. Endocrinology 1981b; 109: 46–53
   PubMed Web of Science ®Google Scholar
• Vicente S, Gonzalez MP, Oset-Gasque MJ. Neuronal nitric oxide synthase modulates basal catecholamine secretion in bovine chromaffin cells. J Neurosci Res 2002; 69: 327–340
   PubMed Web of Science ®Google Scholar
• Ward LE, Hunter LW, Grabau CE, Tyce GM, Rorie DK. Nitric oxide reduces basal efflux of catecholamines from perfused dog adrenal glands. J Auton Nerv Syst 1996; 61: 235–242
   PubMedGoogle Scholar
• Weitzdoerfer R, Hoeger H, Engidawork E, Engelmann M, Singewald N, Lubec G, Lubec B. Neuronal nitric oxide synthase knock-out mice show impaired cognitive performance. Nitric Oxide 2004; 10: 130–140
   PubMed Web of Science ®Google Scholar
• Wotjak CT, Kubota M, Liebsch G, Montkowski A, Holsboer F, Neumann I, Landgraf R. Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: A novel mechanism of regulating adrenocorticotropic hormone secretion?. J Neurosci 1996; 16: 7725–7732
   PubMed Web of Science ®Google Scholar
• Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M. Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: New insights into the secretory capacities of peptidergic neurons. Neuroscience 1998; 85: 1209–1222
   PubMed Web of Science ®Google Scholar
• Wotjak CT, Naruo T, Muraoka S, Simchen R, Landgraf R, Engelmann M. Forced swimming stimulates the expression of vasopressin and oxytocin in magnocellular neurons of the rat hypothalamic paraventricular nucleus. Eur J Neurosci 2001; 13: 2273–2281
   PubMed Web of Science ®Google Scholar
• Yamashita H, Inenaga K, Koizumi K. Possible projections from regions of paraventricular and supraoptic nuclei to the spinal cord: Electrophysiological studies. Brain Res 1984; 296: 373–378
   PubMed Web of Science ®Google Scholar
• Zigmond RE, Schwarzschild MA, Rittenhouse AR. Acute regulation of tyrosine hydroxylase by nerve activity and by neurotransmitters via phosphorylation. Annu Rev Neurosci 1989; 12: 415–461
   PubMed Web of Science ®Google Scholar