Activation of the (Pro)renin receptor in the paraventricular nucleus increases sympathetic outflow in anesthetized rats

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 5, 2015, Pages H880-H887

  Huber, Michael J ^a   Basu, Rupsa ^a   Cecchettini, Cassie ^a   Cuadra, Adolfo E ^b   Chen, Qing Hui ^a   Shan, Zhiying ^a  

^a MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

(Pro)renin receptor; Paraventricular nucleus; Reactive oxygen species; Sympathetic nerve activity

Indexed keywords

ANGIOTENSIN II; BIOLOGICAL MARKER; FOS LIKE ANTIGEN 1; INDUCIBLE NITRIC OXIDE SYNTHASE; LOSARTAN; MESSENGER RNA; PRORENIN; PRORENIN RECEPTOR; PROTEIN FOS; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TIRON; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; CYBB PROTEIN, RAT; MEMBRANE PROTEIN; PROTEIN C FOS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RENIN; TRANSCRIPTION FACTOR FRA 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SPLANCHNIC NERVE; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE; ACTION POTENTIAL; ADRENERGIC SYSTEM; ANESTHESIA; ANIMAL; BLOOD PRESSURE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; HUMAN; HYPOTHALAMUS; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANESTHESIA; ANIMALS; BLOOD PRESSURE; CELLS, CULTURED; HUMANS; HYPOTHALAMUS; MALE; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; NEURONS; NITRIC OXIDE SYNTHASE TYPE II; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, CELL SURFACE; RENIN; RNA, MESSENGER; SYMPATHETIC NERVOUS SYSTEM; TRANSCRIPTION FACTOR AP-1;

EID: 84940733285     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00095.2015     Document Type: Article

References (47)

1. Burmeister MA, Young CN, Braga VA, Butler SD, Sharma RV, Davisson RL. Vivo bioluminescence imaging reveals redox-regulated activator protein-1 activation in paraventricular nucleus of mice with renovascular hypertension. Hypertension 57: 289-297, 2011
2. Campese VM, Ye S, Zhong H, Yanamadala V, Ye Z, Chiu J. Reactive oxygen species stimulate central and peripheral sympathetic nervous system activity. Am J Physiol Heart Circ Physiol 287: H695-H703, 2004
3. Campos RR. Oxidative stress in the brain and arterial hypertension. Hypertens Res 32: 1047-1048, 2009
4. Chan SH, Chan JY. Brain stem NOS and ROS in neural mechanisms of hypertension. Antioxid Redox Signal 20: 146-163, 2014
5. 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
6. Chen QH, Toney GM. Vivo discharge properties of hypothalamic paraventricular nucleus neurons with axonal projections to the rostral ventrolateral medulla. J Neurophysiol 103: 4-15, 2010
7. Contrepas A, Walker J, Koulakoff A, Franek KJ, Qadri F, Giaume C, Corvol P, Schwartz CE, Nguyen G. A role of the (pro)renin receptor in neuronal cell differentiation. Am J Physiol Regul Integr Comp Physiol 297: R250-R257, 2009
8. Cruciat CM, Ohkawara B, Acebron SP, Karaulanov E, Reinhard C, Ingelfinger D, Boutros M, Niehrs C. Requirement of prorenin receptor and vacuolar H-ATPase-mediated acidification for Wnt signaling. Science 327: 459-463, 2010
9. Cuadra AE, Shan Z, Sumners C, Raizada MK. A current view of brain renin-angiotensin system: is the (pro)renin receptor the missing link? Pharmacol Ther 125: 27-38, 2010
10. Forstermann U, Closs EI, Pollock JS, Nakane M, Schwarz P, Gath I, Kleinert H. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 23: 1121-1131, 1994
11. Fujita M, Ando K, Kawarazaki H, Kawarasaki C, Muraoka K, Ohtsu H, Shimizu H, Fujita T. Sympathoexcitation by brain oxidative stress mediates arterial pressure elevation in salt-induced chronic kidney disease. Hypertension 59: 105-112, 2012
12. Fujita M, Ando K, Nagae A, Fujita T. Sympathoexcitation by oxidative stress in the brain mediates arterial pressure elevation in salt-sensitive hypertension. Hypertension 50: 360-367, 2007
13. Gui L, LaGrange LP, Larson RA, Gu M, Zhu J, Chen QH. Role of small conductance calcium-activated potassium channels expressed in PVN in regulating sympathetic nerve activity and arterial blood pressure in rats. Am J Physiol Regul Integr Comp Physiol 303: R301-R310, 2012
14. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci 7: 335-346, 2006
15. Hirooka Y. Oxidative stress in the cardiovascular center has a pivotal role in the sympathetic activation in hypertension. Hypertens Res 34: 407-412, 2011
16. Kannan H, Hayashida Y, Yamashita H. Increase in sympathetic outflow by paraventricular nucleus stimulation in awake rats. Am J Physiol Regul Integr Comp Physiol 256: R1325-R1330, 1989
17. Kannan H, Niijima A, Yamashita H. Inhibition of renal sympathetic nerve activity by electrical stimulation of the hypothalamic paraventricular nucleus in anesthetized rats. J Auton Nerv Syst 21: 83-86, 1987
18. Kimura Y, Hirooka Y, Kishi T, Ito K, Sagara Y, Sunagawa K. Role of inducible nitric oxide synthase in rostral ventrolateral medulla in blood pressure regulation in spontaneously hypertensive rats. Clin Exp Hypertens 31: 281-286, 2009
19. Kimura Y, Hirooka Y, Sagara Y, Ito K, Kishi T, Shimokawa H, Takeshita A, Sunagawa K. Overexpression of inducible nitric oxide synthase in rostral ventrolateral medulla causes hypertension and sympathoexcitation via an increase in oxidative stress. Circ Res 96: 252-260, 2005
20. 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
21. Li W, Peng H, Cao T, Sato R, McDaniels SJ, Kobori H, Navar LG, Feng Y. Brain-targeted (pro)renin receptor knockdown attenuates angiotensin II-dependent hypertension. Hypertension 59: 1188-1194, 2012
22. Li W, Peng H, Mehaffey EP, Kimball CD, Grobe JL, van Gool JM, Sullivan MN, Earley S, Danser AH, Ichihara A, Feng Y. Neuronspecific (pro)renin receptor knockout prevents the development of saltsensitive hypertension. Hypertension 63: 316-323, 2014
23. Li W, Peng H, Seth DM, Feng Y. The prorenin and (pro)renin receptor: new players in the brain renin-angiotensin system? Int J Hypertens 2012: 290635, 2012
24. McAllen RM, Dampney RA. Vasomotor neurons in the rostral ventrolateral medulla are organized topographically with respect to type of vascular bed but not body region. Neurosci Lett 110: 91-96, 1990
25. McAllen RM, May CN. Differential drives from rostral ventrolateral medullary neurons to three identified sympathetic outflows. Am J Physiol Regul Integr Comp Physiol 267: R935-R944, 1994
26. Montezano AC, Touyz RM. Oxidative stress, Noxs, and hypertension: experimental evidence and clinical controversies. Ann Med 44, Suppl 1: S2-16, 2012
27. Morimoto S, Sigmund CD. Angiotensin mutant mice: a focus on the brain renin-angiotensin system. Neuropeptides 36: 194-200, 2002
28. Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD. Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109: 1417-1427, 2002
29. Oliveira-Paula GH, Lacchini R, Tanus-Santos JE. Inducible nitric oxide synthase as a possible target in hypertension. Curr Drug Targets 15: 164-174, 2014
30. Osborn JW, Fink GD. Region-specific changes in sympathetic nerve activity in angiotensin II-salt hypertension in the rat. Exp Physiol 95: 61-68, 2010
31. Paravicini TM, Touyz RM. NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities. Diabetes Care 31, Suppl 2: S170-180, 2008
32. Peng H, Li W, Seth DM, Nair AR, Francis J, Feng Y. (Pro)renin receptor mediates both angiotensin II-dependent and -independent oxidative stress in neuronal cells. PLoS One 8: e58339, 2013
33. Peterson JR, Sharma RV, Davisson RL. Reactive oxygen species in the neuropathogenesis of hypertension. Curr Hypertens Rep 8: 232-241, 2006
34. Prast H, Philippu A. Nitric oxide as modulator of neuronal function. Prog Neurobiol 64: 51-68, 2001
35. Sakuma I, Togashi H, Yoshioka M, Saito H, Yanagida M, Tamura M, Kobayashi T, Yasuda H, Gross SS, Levi R. NG-methyl-L-arginine, an inhibitor of L-arginine-derived nitric oxide synthesis, stimulates renal sympathetic nerve activity in vivo. A role for nitric oxide in the central regulation of sympathetic tone? Circ Res 70: 607-611, 1992
36. Sawchenko PE, Swanson LW. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res 257: 275-325, 1982
37. Shan Z, Cuadra AE, Sumners C, Raizada MK. Characterization of a functional (pro)renin receptor in rat brain neurons. Exp Physiol 93: 701-708, 2008
38. Shan Z, Shi P, Cuadra AE, Dong Y, Lamont GJ, Li Q, Seth DM, Navar LG, Katovich MJ, Sumners C, Raizada MK. Involvement of the brain (pro)renin receptor in cardiovascular homeostasis. Circ Res 107: 934-938, 2010
39. Shi P, Grobe JL, Desland FA, Zhou G, Shen XZ, Shan Z, Liu M, Raizada MK, Sumners C. Direct pro-inflammatory effects of prorenin on microglia. PLoS One 9: e92937, 2014
40. Shi P, Raizada MK, Sumners C. Brain cytokines as neuromodulators in cardiovascular control. Clin Exp Pharmacol Physiol 37: e52-57, 2010
41. Shi Z, Gan XB, Fan ZD, Zhang F, Zhou YB, Gao XY, De W, Zhu GQ. Inflammatory cytokines in paraventricular nucleus modulate sympathetic activity and cardiac sympathetic afferent reflex in rats. Acta Physiol (Oxf) 203: 289-297, 2011
42. Stocker SD, Muntzel MS. Recording sympathetic nerve activity chronically in rats: surgery techniques, assessment of nerve activity, and quantification. Am J Physiol Heart Circ Physiol 305: H1407-H1416, 2013
43. Su Q, Qin DN, Wang FX, Ren J, Li HB, Zhang M, Yang Q, Miao YW, Yu XJ, Qi J, Zhu Z, Zhu GQ, Kang YM. Inhibition of reactive oxygen species in hypothalamic paraventricular nucleus attenuates the reninangiotensin system and proinflammatory cytokines in hypertension. Toxicol Appl Pharmacol 276: 115-120, 2014
44. Yamashita H, Kannan H, Kasai M, Osaka T. Decrease in blood pressure by stimulation of the rat hypothalamic paraventricular nucleus with L-glutamate or weak current. J Auton Nerv Syst 19: 229-234, 1987
45. Ye ZY, Li DP, Pan HL. Regulation of hypothalamic presympathetic neurons and sympathetic outflow by group ii metabotropic glutamate receptors in spontaneously hypertensive rats. Hypertension 62: 255-262, 2013
46. Zubcevic J, Jun JY, Lamont G, Murca TM, Shi P, Yuan W, Lin F, Carvajal JM, Li Q, Sumners C, Raizada MK, Shan Z. Nucleus of the solitary tract (pro)renin receptor-mediated antihypertensive effect involves nuclear factor-kappaB-cytokine signaling in the spontaneously hypertensive rat. Hypertension 61: 622-627, 2013
47. Zucker IH, Gao L. The regulation of sympathetic nerve activity by angiotensin II involves reactive oxygen species and MAPK. Circ Res 97: 737-739, 2005.