Visualizing oxidative stress-induced depression of cardiac vagal baroreflex by MRI/DTI in a mouse neurogenic hypertension model

NeuroImage

Volumn 82, Issue , 2013, Pages 190-199

  Tsai, Ching Yi ^a   Su, Chia Hao ^a   Baudrie, Véronique ^b   Laude, Dominique ^c   Weng, Jun Cheng ^d   Chang, Alice Y W ^a   Chan, Julie Y H ^a   Elghozi, Jean Luc ^e   Chan, Samuel H H ^a  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^c CENTRE DE RECHERCHE DES CORDELIERS   (France)

^d CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

Cardiac vagal baroreflex; Diffusion tensor imaging; Magnetic resonance imaging; Neurogenic hypertension; Nucleus ambiguus; Nucleus tractus solitarii; Oxidative stress

Indexed keywords

ANGIOTENSIN II; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

AMBIGUUS NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; BRAIN LEVEL; BRAIN STEM; CARDIAC VAGAL BAROREFLEX; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; DISEASE MODEL; HEART RATE; INTRACRANIAL HYPERTENSION; MALE; MEDULLA OBLONGATA; MOUSE; NEGATIVE FEEDBACK; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PRESSORECEPTOR; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; SOLITARY TRACT NUCLEUS; TELEMETRY; VAGUS NERVE;

CARDIAC VAGAL BAROREFLEX; DIFFUSION TENSOR IMAGING; MAGNETIC RESONANCE IMAGING; NEUROGENIC HYPERTENSION; NUCLEUS AMBIGUUS; NUCLEUS TRACTUS SOLITARII; OXIDATIVE STRESS;

ANIMALS; BAROREFLEX; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; HYPERTENSION; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOPRECIPITATION; MAGNETIC RESONANCE IMAGING; MALE; MEDULLA OBLONGATA; MICE; MICE, INBRED C57BL; NEURAL PATHWAYS; OXIDATIVE STRESS; SOLITARY NUCLEUS; VAGUS NERVE;

EID: 84879727532     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.05.124     Document Type: Article

References (50)

1. Baudrie V., Laude D., Elghozi J.L. Optimal frequency ranges for extracting information on cardiovascular autonomic control from the blood pressure and pulse interval spectrograms in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R904-R912.
2. Chan J.Y.H., Chen W.S., Lee H.Y., Chan S.H.H. Elevated Fos expression in the NTS is associated with reduced baroreflex response in SHR. Hypertension 1998, 32:939-944.
3. Chan J.Y.H., Wang L.L., Lee H.Y., Chan S.H.H. Augmented up-regulation by c-fos of angiotensin subtype 1 receptors in nucleus tractus solitarii of spontaneously hypertensive rats. Hypertension 2002, 40:335-341.
4. Chan S.H.H., Chan J.Y.H. Brain stem oxidative stress and its associated signaling in the regulation of sympathetic vasomotor tone. J. Appl. Physiol. 2012, 113:1921-1928.
5. Chan S.H.H., Hsu K.S., Huang C.C., Wang L.L., Ou C.C., Chan J.Y.H. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla. Cir. Res. 2005, 97:772-780.
6. Chan S.H.H., Tai M.H., Li C.Y., Chan J.Y.H. Reduction in molecular synthesis or enzyme activity of superoxide dismutases and catalase contributes to oxidative stress and neurogenic hypertension in spontaneously hypertensive rats. Free Radic. Biol. Med. 2006, 40:2028-2039.
7. 1 receptor gene on activation of PKCβ-NADPH oxidase-ERK1/2-c-fos signaling cascade mediates long-term pressor effect of angiotensin II in rostral ventrolateral medulla. J. Hypertens. 2007, 25:1845-1861.
8. Chaves G.Z., Caligiorne S.M., Santos R.A., Khosla M.C. Modulation of the baroreflex control of heart rate by angiotensin-(1-7) at the nucleus tractus solitarii of normotensive and spontaneously hypertensive rats. J. Hypertens. 2000, 18:1841-1848.
9. 1a receptors in mouse brain. Hypertension 2006, 47:230-237.
10. Dampney R.A.L. Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev. 1994, 74:323-364.
11. phox. J. Biol. Chem. 1996, 271:17013-17020.
12. Elghozi J.L., Head G.A. Spinal noradrenergic pathways and pressor responses to central angiotensin II. Am. J. Physiol. 1990, 258:H240-H246.
13. Frangou S., Chitins X., Williams S.C. Mapping IQ and gray matter density in healthy young people. NeuroImage 2004, 23:800-805.
14. Gao L., Wang W., Li Y.L., Schultz H.D., Liu D., Cornish K.G., Zucker I.H. Superoxide mediates sympathoexcitation in heart failure: roles of angiotensin II and NAD(P)H oxidase. Circ. Res. 2004, 95:937-944.
15. phox in dendrites of rat dorsomedial nucleus tractus solitarius neurons in response to chronic administration of hypertensive agents. Exp. Neurol. 2007, 205:383-395.
16. Griendling K.K., Minieri C.A., Ollerenshaw J.D., Alexander R.W. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 1994, 74:1141-1148.
17. Griendling K.K., Sorescu D., Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 2000, 86:494-501.
18. Healy D.P., Rettig R., Printz M.P. Evidence of an endogenous Ang II system in the rat nucleus tractus solitarius. Clin. Exp. Hypertens. 1984, A6:1743-1747.
19. Horsfield M.A., Jones D.K. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases-a review. NMR Biomed. 2002, 15:570-577.
20. Huisman T.A. Diffusion-weighted imaging: basic concepts and application in cerebral stroke and head trauma. Eur. Radiol. 2003, 13:2283-2297.
21. http://www.who.int/gho/ncd/risk_factors/blood_pressure_prevalence_text/en/index.html.
22. http://www.who.int/gho/publications/world_health_statistics/2012/en/index.html.
23. Jiang H., van Zijl P.C., Kim J., Pearlson G.D., Mori S. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput. Methods Programs Biomed. 2006, 81:106-116.
24. Jarvis S. Angiotensin receptor blockers in clinical practice-implications of the ONTARGET study. J. Int. Med. Res. 2012, 40:10-17.
25. Katsunuma N., Tsukamoto K., Ito S., Kanmatsuse K. Enhanced angiotensin-mediated responses in the nucleus tractus solitarii of spontaneously hypertensive rats. Brain Res. Bull. 2003, 60:209-214.
26. Kim J.H., Wu T.H., Budde M.D., Lee J.M., Song S.K. Noninvasive detection of brainstem and spinal cord axonal degeneration in an amyotrophic lateral sclerosis mouse model. NMR Biomed. 2011, 24:163-169.
27. Kishi T., Hirooka Y., Kimura Y., Ito K., Shimokawa H., Takeshita A. Increased reactive oxygen species in rostral ventrolateral medulla contribute to neural mechanisms of hypertension in stroke-prone spontaneously hypertensive rats. Circulation 2004, 109:2357-2362.
28. Laude D., Baudrie V., Elghozi J.L. Applicability of recent methods used to estimate spontaneous baroreflex sensitivity to resting mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R142-R150.
29. - production, vascular tone, and mitogen-activated protein kinase activation. Circulation 2004, 109:1307-1313.
30. Lim K.O., Helpern J.A. Neuropsychiatric applications of DTI-a review. NMR Biomed. 2002, 15:587-593.
31. 2 receptor subtypes in the tonic inhibitory modulation of baroreceptor reflex response by endogenous angiotensins at the nucleus tractus solitarii in the rat. Brain Res. 1998, 782:73-82.
32. Michelini L.C., Bonagamba L.G.H. Angiotensin II as a modulator of baroreceptor reflexes in the brainstem of conscious rats. Hypertension 1990, 15(Suppl. I):145-150.
33. Mohazzab K.M., Kaminski P.M., Wolin M.S. NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am. J. Physiol. 1994, 266:H2568-H2572.
34. National Taiwan University DSI studio http://dsi-studio.labsolver.org.
35. Pierpaoli C. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. NeuroImage 2001, 13:1174-1185.
36. Polson J.W., Dampney R.A.L., Boscan P., Pickering A.E., Paton J.F.R. Differential baroreflex control of sympathetic drive by angiotensin II in the nucleus tractus solitarii. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R1954-R1960.
37. Sakai K. Local production of angiotensin II in the subfornical organ causes elevated drinking. J. Clin. Invest. 2007, 117:1088-1095.
38. Shih C.D., Chan S.H.H., Chan J.Y.H. Participation of Fos protein at the nucleus tractus solitarius in inhibitory modulation of baroreceptor reflex response in the rat. Brain Res. 1996, 738:39-47.
39. Spyer K.M. Central nervous mechanisms contributing to cardiovascular control. J. Physiol. 1994, 474:1-19.
40. Sun C., Zubcevic J., Polson J.W., Potts J.T., Diez-Freire C., Zhang Q., Paton J.F.R., Raizada M.K. Shift to an involvement of phosphatidylinositol 3-kinase in angiotensin II actions on nucleus tractus solitarii neurons of the spontaneously hypertensive rat. Circ. Res. 2009, 105:1248-1255.
41. Taber K.H. The future for diffusion tensor imaging in neuropsychiatry. J. Neuropsychiatry Clin. Neurosci. 2002, 14:1-5.
42. Tai M.H., Wang L.L., Wu K.L.H., Chan J.Y.H. Increased superoxide anion in rostral ventrolateral medulla contributes to hypertension in spontaneously hypertensive rats via interactions with nitric oxide. Free Radic. Biol. Med. 2005, 38:450-462.
43. Taylor W.D., Hsu E., Krishnan K.R., MacFall J.R. Diffusion tensor imaging: background, potential, and utility in psychiatric research. Biol. Psychiatry 2004, 55:201-207.
44. Touyz R.M., Chen X., Tabet F., Yao G., He G., Quinn M.T., Pagano P.J., Schiffrin E.L. Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ. Res. 2002, 90:1205-1213.
45. 2+, and protein kinase C play a role in angiotensin II-induced free radical production in nucleus tractus solitarius. Hypertension 2006, 48:482-489.
46. Wang G., Anrather J., Huang J., Speth R.C., Pickel V.M., Iadecola C. NADPH oxidase contributes to angiotensin II signaling in the nucleus tractus solitarius. J. Neurosci. 2004, 24:5516-5524.
47. Weyhenmeyer J.A., Phillips M.I. Angiotensin-like immunoreactivity in the brain of spontaneously hypertensive rat. Hypertension 1982, 4:514-523.
48. Wong L.F., Polson J.W., Murphy D., Paton J.F.R., Kasparov S. Genetic and pharmacological dissection of pathways involved in the angiotensin II-mediated depression of baroreflex function. FASEB J. 2002, 16:1595-1601.
49. Zimmerman M.C., Lazartigues E., Lang J.A., Sinnayah P., Ahmad I.M., Spitz D.R., Davission R.L. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ. Res. 2002, 91:1038-1045.
50. Zimmerman M.C., Lazartigues E., Sharma R.V., Davisson R.L. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ. Res. 2004, 95:210-216.