Endogenous hydrogen peroxide in the hypothalamic paraventricular nucleus regulates sympathetic nerve activity responses to L-glutamate

Journal of Applied Physiology

Volumn 113, Issue 9, 2012, Pages 1323-1331

  Cardoso, Leonardo M ^a,b   Colombari, Eduardo ^c   Toney, Glenn M ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Arterial blood pressure; Catalase; Glutamatergic transmission; Reactive oxygen species; Superoxide dismutase

Indexed keywords

AMITROLE; CATALASE; ENZYME INHIBITOR; GLUTAMIC ACID; HYDROGEN PEROXIDE;

ADRENERGIC SYSTEM; ANIMAL; ARTICLE; BLOOD PRESSURE; DRUG ANTAGONISM; DRUG EFFECT; HEART RATE; HISTOLOGY; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; INNERVATION; KIDNEY; MALE; METABOLISM; MICROINJECTION; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

AMITROLE; ANIMALS; BLOOD PRESSURE; CATALASE; ENZYME INHIBITORS; GLUTAMIC ACID; HEART RATE; HYDROGEN PEROXIDE; KIDNEY; MALE; MICROINJECTIONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; SYMPATHETIC NERVOUS SYSTEM;

EID: 84868331239     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00912.2012     Document Type: Article

References (61)

1. Abele R, Lampinen M, Keinanen K, Madden DR. Disulfide bonding and cysteine accessibility in the alpha-amino-3-hydroxy-5-methylisoxazole-4- propionic acid receptor subunit GluRD. Implications for redox modulation of glutamate receptors. J Biol Chem 273: 25132-25138, 1998.
2. Aizenman E, Hartnett KA, Reynolds IJ. Oxygen free radicals regulate NMDA receptor function via a redox modulatory site. Neuron 5: 841-846, 1990.
3. Aizenman E, Lipton SA, Loring RH. Selective modulation of NMDA responses by reduction and oxidation. Neuron 2: 1257-1263, 1989.
4. Aragon CM, Rogan F, Amit Z. Dose-and time-dependent effect of an acute 3-amino-1, 2, 4-triazole injection on rat brain catalase activity. Biochem Pharmacol 42: 699-702, 1991.
5. Avshalumov MV, Chen BT, Rice ME. Mechanisms underlying H2O2-mediated inhibition of synaptic transmission in rat hippocampal slices. Brain Res 882: 86-94, 2000.
6. Badoer E, McKinley MJ, Oldfield BJ, McAllen RM. A comparison of hypotensive and non-hypotensive hemorrhage on Fos expression in spinally projecting neurons of the paraventricular nucleus and rostral ventrolateral medulla. Brain Res 610: 216-223, 1993.
7. Boudaba C, Schrader LA, Tasker JG. Physiological evidence for local excitatory synaptic circuits in the rat hypothalamus. J Neurophysiol 77: 3396-3400, 1997.
8. Brooks VL, Qi Y, O'Donaughy TL. Increased osmolality of conscious water-deprived rats supports arterial pressure and sympathetic activity via a brain action. Am J Physiol Regul Integr Comp Physiol 288: R1248-R1255, 2005.
9. Busnardo C, Tavares RF, Correa FM. Role of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptors in the cardiovascular effects of L-glutamate microinjection into the hypothalamic paraventricular nucleus of unanesthetized rats. J Neurosci Res 87: 2066-2077, 2009.
10. Cardoso LM, Colombari DS, Menani JV, Toney GM, Chianca DA Jr, Colombari E. Cardiovascular responses to hydrogen peroxide into the nucleus tractus solitarius. Am J Physiol Regul Integr Comp Physiol 297: R462-R469, 2009.
11. Cato MJ, Toney GM. Angiotensin II excites paraventricular nucleus neurons that innervate the rostral ventrolateral medulla: an in vitro patchclamp study in brain slices. J Neurophysiol 93: 403-413, 2005.
12. Chen F, Dworak M, Wang Y, Cham JL, Badoer E. Role of the hypothalamic PVN in the reflex reduction in mesenteric blood flow elicited by hyperthermia. Am J Physiol Regul Integr Comp Physiol 295: R1874-R1881, 2008.
13. Chen QH, Haywood JR, Toney GM. Sympathoexcitation by PVNinjected bicuculline requires activation of excitatory amino acid receptors. Hypertension 42: 725-731, 2003.
14. Chen QH, Toney GM. AT1-receptor blockade in the hypothalamic PVN reduces central hyperosmolality-induced renal sympathoexcitation. Am J Physiol Regul Integr Comp Physiol 281: R1844-R1853, 2001.
15. Chen QH, Toney GM. Identification and characterization of two functionally distinct groups of spinal cord-projecting paraventricular nucleus neurons with sympathetic-related activity. Neuroscience 118: 797-807, 2003.
16. Chen QH, Toney GM. In vivo discharge properties of hypothalamic paraventricular nucleus neurons with axonal projections to the rostral ventrolateral medulla. J Neurophysiol 103: 4-15, 2010.
17. Coote JH, Yang Z, Pyner S, Deering J. Control of sympathetic outflows by the hypothalamic paraventricular nucleus. Clin Exp Pharmacol Physiol 25: 461-463, 1998.
18. Dampney RA, Horiuchi J, Killinger S, Sheriff MJ, Tan PS, McDowall LM. Long-term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions. Clin Exp Pharmacol Physiol 32: 419-425, 2005.
19. Ferguson AV, Latchford KJ, Samson WK. The paraventricular nucleus of the hypothalamus-a potential target for integrative treatment of autonomic dysfunction. Expert Opin Ther Targets 12: 717-727, 2008.
20. Freeman KL, Brooks VL. AT1 and glutamatergic receptors in paraventricular nucleus support blood pressure during water deprivation. Am J Physiol Regul Integr Comp Physiol 292: R1675-R1682, 2007.
21. Gao H, Miyata K, Bhaskaran MD, Derbenev AV, Zsombok A. Transient receptor potential vanilloid type 1-dependent regulation of liverrelated neurons in the paraventricular nucleus of the hypothalamus diminished in the type 1 diabetic mouse. Diabetes 61: 1381-1390, 2012.
22. Giusti MF, Sato MA, Cardoso LM, Braga VA, Colombari E. Central antioxidant therapy inhibits parasympathetic baroreflex control in conscious rats. Neurosci Lett 489: 115-118, 2011.
23. Haywood JR, Mifflin SW, Craig T, Calderon A, Hensler JG, Hinojosa-Laborde C. γ-Aminobutyric acid (GABA)-a function and binding in the paraventricular nucleus of the hypothalamus in chronic renal-wrap hypertension. Hypertension 37: 614-618, 2001.
24. Heim WG, Appleman D, Pyfrom HT. Production of catalase changes in animals with 3-amino-1, 2, 4-triazole. Science 122: 693-694, 1955.
25. Herman JP, Eyigor O, Ziegler DR, Jennes L. Expression of ionotropic glutamate receptor subunit mRNAs in the hypothalamic paraventricular nucleus of the rat. J Comp Neurol 422: 352-362, 2000.
26. Kantzides A, Badoer E. Fos, RVLM-projecting neurons, and spinally projecting neurons in the PVN following hypertonic saline infusion. Am J Physiol Regul Integr Comp Physiol 284: R945-R953, 2003.
27. Kleiber AC, Zheng H, Schultz HD, Peuler JD, Patel KP. Exercise training normalizes enhanced glutamate-mediated sympathetic activation from the PVN in heart failure. Am J Physiol Regul Integr Comp Physiol 294: R1863-R1872, 2008.
28. Lauar MR, Colombari DS, De Paula PM, Colombari E, Cardoso LM, De Luca LA Jr, Menani JV. Inhibition of central angiotensin II-induced pressor responses by hydrogen peroxide. Neuroscience 171: 524-530, 2010.
29. Li DP, Byan HS, Pan HL. Switch to glutamate receptor 2-lacking AMPA receptors increases neuronal excitability in hypothalamus and sympathetic drive in hypertension. J Neurosci 32: 372-380, 2012.
30. Li DP, Pan HL. Angiotensin II attenuates synaptic GABA release and excites paraventricular-rostral ventrolateral medulla output neurons. J Pharmacol Exp Ther 313: 1035-1045, 2005.
31. Li DP, Pan HL. Glutamatergic inputs in the hypothalamic paraventricular nucleus maintain sympathetic vasomotor tone in hypertension. Hypertension 49: 916-925, 2007.
32. Li DP, Pan HL. Increased group I metabotropic glutamate receptor activity in paraventricular nucleus supports elevated sympathetic vasomotor tone in hypertension. Am J Physiol Regul Integr Comp Physiol 299: R552-R561, 2010.
33. Li YF, Cornish KG, Patel KP. Alteration of NMDA NR1 receptors within the paraventricular nucleus of hypothalamus in rats with heart failure. Circ Res 93: 990-997, 2003.
34. Li YF, Jackson KL, Stern JE, Rabeler B, Patel KP. Interaction between glutamate and GABA systems in the integration of sympathetic outflow by the paraventricular nucleus of the hypothalamus. Am J Physiol Heart Circ Physiol 291: H2847-H2856, 2006.
35. Martin DS, Haywood Jr. Reduced GABA inhibition of sympathetic function in renal-wrapped hypertensive rats. Am J Physiol Regul Integr Comp Physiol 275: R1523-R1529, 1998.
36. Mifflin SW. What does the brain know about blood pressure? News Physiol Sci 16: 266-271, 2001.
37. Nicholls P. The reaction between aminotriazole and catalase. Biochim Biophys Acta 59: 414-420, 1962.
38. Pakhomov AG, Semenov I, Brenner R, Toney GM. Hydraulically coupled microejection technique for precise local solution delivery in tissues. J Neurosci Methods 155: 231-240, 2006.
39. Pandit R, de Jong JW, Vanderschuren LJ, Adan RA. Neurobiology of overeating and obesity: the role of melanocortins and beyond. Eur J Pharmacol 660: 28-42, 2011.
40. Potapenko ES, Biancardi VC, Florschutz RM, Ryu PD, Stern JE. Inhibitory-excitatory synaptic balance is shifted toward increased excitation in magnocellular neurosecretory cells of heart failure rats. J Neurophysiol 106: 1545-1557, 2011.
41. Rice ME. H2O2: a dynamic neuromodulator. Neuroscientist 17: 389-406, 2011.
42. Shi P, Stocker SD, Toney GM. Organum vasculosum laminae terminalis contributes to increased sympathetic nerve activity induced by central hyperosmolality. Am J Physiol Regul Integr Comp Physiol 293: R2279-R2289, 2007.
43. Stocker SD, Hunwick KJ, Toney GM. Hypothalamic paraventricular nucleus differentially supports lumbar and renal sympathetic outflow in water-deprived rats. J Physiol 563: 249-263, 2005.
44. Stocker SD, Simmons JR, Stornetta RL, Toney GM, Guyenet PG. Water deprivation activates a glutamatergic projection from the hypothalamic paraventricular nucleus to the rostral ventrolateral medulla. J Comp Neurol 494: 673-685, 2006.
45. Stocker SD, Toney GM. Median preoptic neurones projecting to the hypothalamic paraventricular nucleus respond to osmotic, circulating Ang II and baroreceptor input in the rat. J Physiol 568: 599-615, 2005.
46. Tasker JG, Boudaba C, Schrader LA. Local glutamatergic and GABAergic synaptic circuits and metabotropic glutamate receptors in the hypothalamic paraventricular and supraoptic nuclei. Adv Exp Med Biol 449: 117-121, 1998.
47. van den Pol AN. Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons. J Neurosci 11: 2087-2101, 1991.
48. Volterra A, Trotti D, Tromba C, Floridi S, Racagni G. Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. J Neurosci 14: 2924-2932, 1994.
49. Ward KR, Bardgett JF, Wolfgang L, Stocker SD. Sympathetic response to insulin is mediated by melanocortin 3/4 receptors in the hypothalamic paraventricular nucleus. Hypertension 57: 435-441, 2011.
50. Xu B, Zheng H, Patel KP. Enhanced activation of RVLM-projecting PVN neurons in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 302: H1700-H1711, 2012.
51. Xu Y, Gao Q, Gan XB, Chen L, Zhang L, Zhu GQ, Gao XY. Endogenous hydrogen peroxide in paraventricular nucleus mediates sympathetic activation and enhanced cardiac sympathetic afferent reflex in renovascular hypertensive rats. Exp Physiol 96: 1282-1292, 2011.
52. Xu Y, Gao Q, Gan XB, Chen L, Zhang L, Zhu GQ, Gao XY. Endogenous hydrogen peroxide in paraventricular nucleus mediates sympathetic activation and enhanced cardiac sympathetic afferent reflex in renovascular hypertensive rats. Exp Physiol 96: 1282-1292, 2011.
53. Yu Y, Zhong MK, Li J, Sun XL, Xie GQ, Wang W, Zhu GQ. Endogenous hydrogen peroxide in paraventricular nucleus mediating cardiac sympathetic afferent reflex and regulating sympathetic activity. Pflügers Arch 454: 551-557, 2007.
54. Yusa T, Beckman JS, Crapo JD, Freeman BA. Hyperoxia increases H2O2 production by brain in vivo. J Appl Physiol 63: 353-358, 1987.
55. Zhang K, Li YF, Patel KP. Reduced endogenous GABA-mediated inhibition in the PVN on renal nerve discharge in rats with heart failure. Am J Physiol Regul Integr Comp Physiol 282: R1006-R1015, 2002.
56. Zhang ZH, Francis J, Weiss RM, Felder RB. The renin- angiotensinaldosterone system excites hypothalamic paraventricular nucleus neurons in heart failure. Am J Physiol Heart Circ Physiol 283: H423-H433, 2002.
57. Zimmerman MC, Davisson RL. Redox signaling in central neural regulation of cardiovascular function. Prog Biophys Mol Biol 84: 125-149, 2004.
58. Zimmerman MC, Lazartigues E, Lang JA, Sinnayah P, Ahmad IM, Spitz DR, Davisson RL. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ Res 91: 1038-1045, 2002.
59. Zimmerman MC, Lazartigues E, Sharma RV, Davisson RL. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res 95: 210-216, 2004.
60. Zimmerman MC, Zucker IH. Mitochondrial dysfunction and mitochondrial-produced reactive oxygen species: new targets for neurogenic hypertension? Hypertension 53: 112-114, 2009.
61. Zoccarato F, Valente M, Alexandre A. Hydrogen peroxide induces a long-lasting inhibition of the Ca2-dependent glutamate release in cerebrocortical synaptosomes without interfering with cytosolic Ca2. J Neurochem 64: 2552-2558, 1995.