Contribution of central nervous system endothelial nitric oxide synthase to neurohumoral activation in heart failure rats

Hypertension

Volumn 58, Issue 3, 2011, Pages 454-463

  Biancardi, Vinicia C ^a   Son, Sook J ^a   Sonner, Patrick M ^b   Zheng, Hong ^c   Patel, Kaushik P ^c   Stern, Javier E ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b WRIGHT STATE UNIVERSITY   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

astrocyte; Heart failure; hypothalamus; NO; sympathetic

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; NEUROHORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; HEART FAILURE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SHAM PROCEDURE; SYMPATHOEXCITATORY OUTFLOW;

ANIMALS; ASTROCYTES; CENTRAL NERVOUS SYSTEM; ECHOCARDIOGRAPHY; GENE KNOCKDOWN TECHNIQUES; HEART; HEART FAILURE; HEMODYNAMICS; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; NEURONS; NEUROTRANSMITTER AGENTS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OLIGONUCLEOTIDES, ANTISENSE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, WISTAR;

EID: 80051940610     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.111.175810     Document Type: Article

References (48)

1. Krukoff TL. Central actions of nitric oxide in regulation of autonomic functions. Brain Res Brain Res Rev. 1999;30:52-65. (Pubitemid 29331515)
2. Paton JF, Kasparov S, Paterson DJ. Nitric oxide and autonomic control of heart rate: a question of specificity. Trends Neurosci. 2002;25:626-631. (Pubitemid 35356510)
3. Stern JE. Nitric oxide and homeostatic control: an intercellular signalling molecule contributing to autonomic and neuroendocrine integration? Prog Biophys Mol Biol. 2004;84:197-215. (Pubitemid 38215212)
4. Swanson LW, Sawchenko PE. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci. 1983;6: 269-324. (Pubitemid 13101466)
5. Li Y, Zhang W, Stern JE. Nitric oxide inhibits the firing activity of hypothalamic paraventricular neurons that innervate the medulla oblongata: role of GABA. Neuroscience. 2003;118:585-601. (Pubitemid 36506949)
6. Stern JE, Ludwig M. No inhibits supraoptic oxytocin and vasopressin neurons via activation of gabaergic synaptic inputs. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1815-R1822.
7. Zhang K, Mayhan WG, Patel KP. Nitric oxide within the paraventricular nucleus mediates changes in renal sympathetic nerve activity. Am J Physiol. 1997;273:R864-R872. (Pubitemid 27425632)
8. Zheng H, Li YF, Cornish KG, Zucker IH, Patel KP. Exercise training improves endogenous nitric oxide mechanisms within the paraventricular nucleus in rats with heart failure. Am J Physiol Heart Circ Physiol. 2005;288:H2332-H2341. (Pubitemid 40604122)
9. Zhang K, Li YF, Patel KP. Blunted nitric oxide-mediated inhibition of renal nerve discharge within pvn of rats with heart failure. Am J Physiol Heart Circ Physiol. 2001;281:H995-H1004.
10. Stern JE, Zhang W. Cellular sources, targets and actions of constitutive nitric oxide in the magnocellular neurosecretory system of the rat. J Physiol. 2005;562:725-744. (Pubitemid 40246789)
11. Nylen A, Skagerberg G, Alm P, Larsson B, Holmqvist BI, Andersson KE. Detailed organization of nitric oxide synthase, vasopressin and oxytocin immunoreactive cell bodies in the supraoptic nucleus of the female rat. Anat Embryol (Berl). 2001;203:309-321. (Pubitemid 32391435)
12. Zhang K, Zucker IH, Patel KP. Altered number of diaphorase (nos) positive neurons in the hypothalamus of rats with heart failure. Brain Res. 1998;786:219-225. (Pubitemid 28191733)
13. Waki H, Kasparov S, Wong LF, Murphy D, Shimizu T, Paton JF. Chronic inhibition of endothelial nitric oxide synthase activity in nucleus tractus solitarii enhances baroreceptor reflex in conscious rats. J Physiol. 2003; 546:233-242. (Pubitemid 36104983)
14. Paton JF, Deuchars J, Ahmad Z, Wong LF, Murphy D, Kasparov S. Adenoviral vector demonstrates that angiotensin ii-induced depression of the cardiac baroreflex is mediated by endothelial nitric oxide synthase in the nucleus tractus solitarii of the rat. J Physiol. 2001;531:445-458. (Pubitemid 32232943)
15. Gingerich S, Krukoff TL. Estrogen in the paraventricular nucleus attenuates l-glutamate-induced increases in mean arterial pressure through estrogen receptor and no. Hypertension. 2006;48:1130-1136. (Pubitemid 44772718)
16. Topel I, Stanarius A, Wolf G. Distribution of the endothelial constitutive nitric oxide synthase in the developing rat brain: an immunohistochemical study. Brain Res. 1998;788:43-48. (Pubitemid 28202142)
17. Lin LH, Taktakishvili O, Talman WT. Identification and localization of cell types that express endothelial and neuronal nitric oxide synthase in the rat nucleus tractus solitarii. Brain Res. 2007;1171:42-51. (Pubitemid 47404537)
18. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by akt-dependent phosphorylation. Nature. 1999;399:601-605.
19. Garthwaite J. Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci. 2008;27:2783-2802. (Pubitemid 351832227)
20. Hopper RA, Garthwaite J. Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J Neurosci. 2006;26:11513-11521. (Pubitemid 44772122)
21. Francis J, Weiss RM, Wei SG, Johnson AK, Felder RB. Progression of heart failure after myocardial infarction in the rat. Am J Physiol Regul Integr Comp Physiol. 2001;281:R1734-R1745.
22. Biancardi VC, Campos RR, Stern JE. Altered balance ofa-aminobutyric acidergic and glutamatergic afferent inputs in rostral ventrolateral medulla-projecting neurons in the paraventricular nucleus of the hypothalamus of renovascular hypertensive rats. J Comp Neurol. 2010;518: 567-585.
23. Fabian RH, Perez-Polo JR, Kent TA. Perivascular nitric oxide and superoxide in neonatal cerebral hypoxia-ischemia. Am J Physiol Heart Circ Physiol. 2008;295:H1809-H1814.
24. Wang Y, Liu XF, Cornish KG, Zucker IH, Patel KP. Effects of NNOS antisense in the paraventricular nucleus on blood pressure and heart rate in rats with heart failure. Am J Physiol Heart Circ Physiol. 2005;288: H205-H213. (Pubitemid 40023848)
25. Theodosis DT, Poulain DA, Oliet SH. Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev. 2008; 88:983-1008.
26. Rees DD, Palmer RM, Schulz R, Hodson HF, Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol. 1990;101:746-752. (Pubitemid 20357206)
27. Bauser-Heaton HD, Song J, Bohlen HG. Cerebral microvascular nnos responds to lowered oxygen tension through a bumetanide-sensitive cotransporter and sodium-calcium exchanger. Am J Physiol Heart Circ Physiol. 2008;294:H2166-H2173.
28. Fleming I, Busse R. Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol. 2003;284:R1-R12. (Pubitemid 36008649)
29. Sporbert A, Mertsch K, Smolenski A, Haseloff RF, Schonfelder G, Paul M, Ruth P, Walter U, Blasig IE. Phosphorylation of vasodilatorstimulated phosphoprotein: a consequence of nitric oxide-and CGMPmediated signal transduction in brain capillary endothelial cells and astrocytes. Brain Res Mol Brain Res. 1999;67:258-266. (Pubitemid 29193182)
30. Caillol M, Devinoy E, Lacroix MC, Schirar A. Endothelial and neuronal nitric oxide synthases are present in the suprachiasmatic nuclei of Syrian hamsters and rats. Eur J Neurosci. 2000;12:649-661. (Pubitemid 30142767)
31. Gabbott PL, Bacon SJ. Localisation of NADPH diaphorase activity and NOS immunoreactivity in astroglia in normal adult rat brain. Brain Res. 1996;714:135-144. (Pubitemid 26120801)
32. Pekny M, Pekna M. Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol. 2004;204:428-437. (Pubitemid 39468154)
33. Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem. 1998;70: 2446-2453.
34. Pajolla GP, Accorsi-Mendonca D, Lunardi CN, Bendhack LM, Machado BH, Llewellyn-Smith IJ. Immunoreactivity for neuronal NOS and fluorescent indication of NO formation in the NTS of juvenile rats submitted to chronic intermittent hypoxia. Auton Neurosci. 2009;148:55-62.
35. Weiss ML, Chowdhury SI, Patel KP, Kenney MJ, Huang J. Neural circuitry of the kidney: NO-containing neurons. Brain Res. 2001;919: 269-282. (Pubitemid 33042573)
36. Pyner S, Coote JH. Identification of an efferent projection from the paraventricular nucleus of the hypothalamus terminating close to spinally projecting rostral ventrolateral medullary neurons. Neuroscience. 1999; 88:949-957. (Pubitemid 28518270)
37. Tagawa T, Dampney RA. At(1) receptors mediate excitatory inputs to rostral ventrolateral medulla pressor neurons from hypothalamus. Hypertension. 1999;34:1301-1307. (Pubitemid 30002398)
38. Allen AM. Inhibition of the hypothalamic paraventricular nucleus in spontaneously hypertensive rats dramatically reduces sympathetic vasomotor tone. Hypertension. 2002;39:275-280. (Pubitemid 34165228)
39. Stocker SD, Keith KJ, Toney GM. Acute inhibition of the hypothalamic paraventricular nucleus decreases renal sympathetic nerve activity and arterial blood pressure in water-deprived rats. Am J Physiol Regul Integr Comp Physiol. 2004;286:R719-R725. (Pubitemid 38375003)
40. Knowles RG, Moncada S. Nitric oxide synthases in mammals. Biochem J. 1994;298:249-258. (Pubitemid 24072462)
41. Hirooka Y, Sakai K, Kishi T, Takeshita A. Adenovirus-mediated gene transfer into the nts in conscious rats: a new approach to examining the central control of cardiovascular regulation. Ann N Y Acad Sci. 2001;940: 197-205. (Pubitemid 32623394)
42. Brenman JE, Bredt DS. Synaptic signaling by nitric oxide. Curr Opin Neurobiol. 1997;7:374-378. (Pubitemid 27321029)
43. Tsoukias NM, Popel AS. A model of nitric oxide capillary exchange. Microcirculation. 2003;10:479-495. (Pubitemid 39004274)
44. Felder RB, Francis J, Weiss RM, Zhang ZH, Wei SG, Johnson AK. Neurohumoral regulation in ischemia-induced heart failure: role of the forebrain. Ann N Y Acad Sci. 2001;940:444-453. (Pubitemid 32623414)
45. Kang KT, Sullivan JC, Spradley FT, d'Uscio LV, Katusic ZS, Pollock JS. Antihypertensive therapy increases tetrahydrobiopterin levels and NO/CGMP signaling in small arteries of angiotensin II-infused hypertensive rats. Am J Physiol Heart Circ Physiol. 2010;300:H718-H724.
46. Smith CJ, Sun D, Hoegler C, Roth BS, Zhang X, Zhao G, Xu XB, Kobari Y, Pritchard K Jr, Sessa WC, Hintze TH. Reduced gene expression of vascular endothelial NO synthase and cyclooxygenase-1 in heart failure. Circ Res. 1996;78:58-64. (Pubitemid 26004121)
47. Cohn JN. The sympathetic nervous system in heart failure. J Cardiovasc Pharmacol. 1989;14(suppl 5):S57-S61. (Pubitemid 19237362)
48. Zucker IH, Schultz HD, Li YF, Wang Y, Wang W, Patel KP. The origin of sympathetic outflow in heart failure: the roles of angiotensin II and nitric oxide. Prog Biophys Mol Biol. 2004;84:217-232. (Pubitemid 38215213)