Contributions of vascular inflammation in the brainstem for neurogenic hypertension

Respiratory Physiology and Neurobiology

Volumn 178, Issue 3, 2011, Pages 422-428

  Waki, Hidefumi ^a   Gouraud, Sabine S ^a   Maeda, Masanobu ^a   Raizada, Mohan K ^b   Paton, Julian F R ^c  

^a WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Angiotensin II; Ccl5; ENOS; Heme oxygenase; JAM 1; Neurogenic hypertension; NTS; SHR; Vascular inflammation

Indexed keywords

ANGIOTENSIN III; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR3; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; JUNCTIONAL ADHESION MOLECULE A; MESSENGER RNA; RANTES; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PRESSURE; BRAIN STEM; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; ENDOTHELIUM CELL; FEEDBACK SYSTEM; GLIA CELL; HYPERTENSION; IMMUNOCOMPETENT CELL; LEUKOCYTE ADHERENCE; MICROVASCULATURE; NONHUMAN; PARACRINE SIGNALING; PERFUSION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; REVIEW; SOLITARY TRACT NUCLEUS; SPONTANEOUSLY HYPERTENSIVE HEART FAILURE RAT; SYMPATHETIC NERVE; VASCULAR RESISTANCE; VASCULITIS;

ANIMALS; BLOOD PRESSURE; BRAIN STEM; HUMANS; HYPERTENSION; INFLAMMATION; NEUROGENIC INFLAMMATION; SOLITARY NUCLEUS; VASCULAR DISEASES;

EID: 80052462112     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2011.05.004     Document Type: Review

References (107)

1. Allan S.M., Rothwell N.J. Inflammation in central nervous system injury. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2003, 358:1669-1677.
2. Allen A.M., McKinley M.J., Oldfield B.J., Dampney R.A., Mendelsohn F.A. Angiotensin II receptor binding and the baroreflex pathway. Clin. Exp. Hypertens. A 1988, 10(Suppl. 1):63-78.
3. Amoureux, S., Lorgis, L., Sicard, P., Girard, C., Rochette, L., Vergely, C. Vascular BDNF expression and oxidative stress during aging and the development of chronic hypertension. Fundam. Clin. Pharmacol., in press.
4. Bakhiet M., Tjernlund A., Mousa A., Gad A., Strömblad S., Kuziel W.A., Seiger A., Andersson J. RANTES promotes growth and survival of human first-trimester forebrain astrocytes. Nat. Cell Biol. 2001, 3:150-157.
5. Banisadr G., Rostène W., Kitabgi P., Parsadaniantz S.M. Chemokines and brain functions. Curr. Drug Targets Inflamm. Allergy 2005, 4:387-399.
6. Bendall J.K., Alp N.J., Warrick N., Cai S., Adlam D., Rockett K., Yokoyama M., Kawashima S., Channon K.M. Stoichiometric relationships between endothelial tetrahydrobiopterin, endothelial NO synthase (eNOS) activity, and eNOS coupling in vivo: insights from transgenic mice with endothelial-targeted GTP cyclohydrolase 1 and eNOS overexpression. Circ. Res. 2005, 97:864-871.
7. Benrick A., Schéle E., Pinnock S.B., Wernstedt-Asterholm I., Dickson S.L., Karlsson-Lindahl L., Jansson J.O. Interleukin-6 gene knockout influences energy balance regulating peptides in the hypothalamic paraventricular and supraoptic nuclei. J. Neuroendocrinol. 2009, 21:620-628.
8. Besong G., Battaglia G., D'Onofrio M., Di Marco R., Ngomba R.T., Storto M., Castiglione M., Mangano K., Busceti C.L., Nicoletti F.R., Bacon K., Tusche M., Valenti O., Conn P.J., Bruno V., Nicoletti F. Activation of group III metabotropic glutamate receptors inhibits the production of RANTES in glial cell cultures. J. Neurosci. 2002, 22:5403-5411.
9. Blackshaw S., Eliasson M.J., Sawa A., Watkins C.C., Krug D., Gupta A., Arai T., Ferrante R.J., Snyder S.H. Species, strain and developmental variations in hippocampal neuronal and endothelial nitric oxide synthase clarify discrepancies in nitric oxide-dependent synaptic plasticity. Neuroscience 2003, 119:979-990.
10. Boehning D., Snyder S.H. Novel neural modulators. Annu. Rev. Neurosci. 2003, 7:105-131.
11. Bolin L.M., Murray R., Lukacs N.W., Strieter R.M., Kunkel S.L., Schall T.J., Bacon K.B. Primary sensory neurons migrate in response to the chemokine RANTES. J. Neuroimmunol. 1998, 81:49-57.
12. Boos C.J., Lip G.Y. Is hypertension an inflammatory process?. Curr. Pharm. Des. 2006, 12:1623-1635.
13. Boscan P., Allen A.M., Paton J.F.R. Baroreflex inhibition of cardiac sympathetic outflow is attenuated by angiotensin II in the solitary tract nucleus. Neuroscience 2001, 103:153-160.
14. Briones A.M., Touyz R.M. Oxidative stress and hypertension: current concepts. Curr. Hypertens. Rep. 2010, 12:135-142.
15. Bucci M., Roviezzo F., Posadas I., Yu J., Parente L., Sessa W.C., Ignarro L.J., Cirino G. Endothelial nitric oxide synthase activation is critical for vascular leakage during acute inflammation in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:904-908.
16. Caillol M., Devinoy E., Lacroix M.C., 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.
17. Cartier L., Hartley O., Dubois-Dauphin M., Krause K.H. Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res. Brain Res. Rev. 2005, 48:16-42.
18. Cates, M.J., Steed, P.W., Abdala, A.P., Langton, P.D., Paton, J.F., Elevated vertebrobasilar artery resistance in neonatal spontaneously hypertensive rats. J Appl Physiol., in press.
19. Claesson H.E., Odlander B., Jakobsson P.J. Leukotriene B4 in the immune system. Int. J. Immunopharmacol. 1992, 14:441-449.
20. Coles B., Fielding C.A., Rose-John S., Scheller J., Jones S.A., O'Donnell V.B. Classic interleukin-6 receptor signaling and interleukin-6 trans-signaling differentially control angiotensin II-dependent hypertension, cardiac signal transducer and activator of transcription-3 activation, and vascular hypertrophy in vivo. Am. J. Pathol. 2007, 171:315-325.
21. Crockett-Torabi E., Ward P.A. The role of leukocytes in tissue injury. Eur. J. Anaesthesiol. 1996, 13:235-246.
22. Cuadra A.E., Shan Z., Sumners C., Raizada M.K. A current view of brain renin-angiotensin system: is the (pro)renin receptor the missing link?. Pharmacol. Ther. 2010, 125:27-38.
23. Cushing H. Concerning a definitive regulatory mechanism of the vaso-motor centre which controls blood pressure during cerebral compression. Bull. Johns Hopkins Hosp. 1901, 12:290-292.
24. de Haas A.H., van Weering H.R., de Jong E.K., Boddeke H.W., Biber K.P. Neuronal chemokines: versatile messengers in central nervous system cell interaction. Mol. Neurobiol. 2007, 36:137-151.
25. D'Arcangelo G., Tancredi V., Onofri F., D'Antuono M., Giovedi S., Benfenati F. Interleukin-6 inhibits neurotransmitter release and the spread of excitation in the rat cerebral cortex. Eur. J. Neurosci. 2000, 12:1241-1252.
26. Dinerman J.L., Dawson T.M., Schell M.J., Snowman A., Snyder S.H. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:4214-4218.
27. Dickinson C.J. Cerebral oxidative metabolism in essential hypertension: a meta-analysis. J. Hypertens. 1995, 13:653-658.
28. Doba N., Reis D.J. Acute fulminating neurogenic hypertension produced by brainstem lesions in the rat. Circ. Res. 1973, 32:584-593.
29. Doyle C.A., Slater P. Localization of neuronal and endothelial nitric oxide synthase isoforms in human hippocampus. Neuroscience 1997, 76:387-395.
30. Ebnet K., Suzuki A., Ohno S., Vestweber D. Junctional adhesion molecules (JAMs): more molecules with dual functions?. J. Cell Sci. 2004, 117:19-29.
31. Egan B.M. Neurogenic mechanisms initiating essential hypertension. Am. J. Hypertens. 1989, 2:357S-362S.
32. Esler M., Kaye D. Sympathetic nervous system activation in essential hypertension, cardiac failure and psychosomatic heart disease. J. Cardiovasc. Pharmacol. 2000, 35:S1-S7.
33. Friese R.S., Mahboubi P., Mahapatra N.R., Mahata S.K., Schork N.J., Schmid-Schonbein G.W., O'Connor D.T. Common genetic mechanisms of blood pressure elevation in two independent rodent models of human essential hypertension. Am. J. Hypertens. 2005, 18:633-652.
34. Frigero M., Bonagamba L.G., Machado B.H. The gain of the baroreflex bradycardia is reduced by microinjection of NMDA receptor antagonists into the nucleus tractus solitarii of awake rats. J. Auton. Nerv. Syst. 2000, 79:28-33.
35. Fukuda S., Yasu T., Kobayashi N., Ikeda N., Schmid-Schonbein G.W. Contribution of fluid shear response in leukocytes to hemodynamic resistance in the spontaneously hypertensive rat. Circ. Res. 2004, 95:100-108.
36. Funakoshi Y., Ichiki T., Ito K., Takeshita A. Induction of interleukin-6 expression by angiotensin II in rat vascular smooth muscle cells. Hypertension 1999, 34:118-125.
37. Gorbet M.B., Sefton M.V. Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 2004, 25:5681-5703.
38. Gouraud S.S., Waki H., Bhuiyan M.E., Takagishi M., Cui H., Kohsaka A., Paton J.F., Maeda M. Down-regulation of chemokine Ccl5 gene expression in the NTS of SHR may be pro-hypertensive. J. Hypertens. 2011, 29:732-740.
39. Granstam S.O., Granstam E., Fellström B., Lind L. Regional haemodynamic differences between normotensive and spontaneously hypertensive rats - a microsphere study. Physiol. Res. 1998, 47:9-15.
40. Grassi G. Counteracting the sympathetic nervous system in essential hypertension. Curr. Opin. Nephrol. Hypertens. 2004, 13:513-519.
41. Gross P.M. Morphology and physiology of capillary systems in subregions of the subfornical organ and area postrema. Can. J. Physiol. Pharmacol. 1991, 69:1010-1025.
42. Guzik T.J., Hoch N.E., Brown K.A., McCann L.A., Rahman A., Dikalov S., Goronzy J., Weyand C., Harrison D.G. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J. Exp. Med. 2007, 204:2449-2460.
43. Hesselgesser J., Horuk R. Chemokine and chemokine receptor expression in the central nervous system. J. Neurovirol. 1999, 5:13-26.
44. Huber J.D., Egleton R.D., Davis T.P. Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci. 2001, 24:719-725.
45. Intengan H.D., Schiffrin E.L. Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension 2001, 38:581-587.
46. Kang Y.M., Ma Y., Elks C., Zheng J.P., Yang Z.M., Francis J. Cross-talk between cytokines and renin-angiotensin in hypothalamic paraventricular nucleus in heart failure: role of nuclear factor-kappaB. Cardiovasc. Res. 2008, 79:671-678.
47. Kang Y.M., Ma Y., Zheng J.P., Elks C., Sriramula S., Yang Z.M., Francis J. Brain nuclear factor-kappa B activation contributes to neurohumoral excitation in angiotensin II-induced hypertension. Cardiovasc. Res. 2009, 82:503-512.
48. Kannan H., Tanaka Y., Kunitake T., Ueta Y., Hayashida Y., Yamashita H. Activation of sympathetic outflow by recombinant human interleukin-1 beta in conscious rats. Am. J. Physiol. 1996, 270:R479-R485.
49. Kotani A., Hori T., Matsumura Y., Uchiyama T. Signaling of gp34 (OX40 ligand) induces vascular endothelial cells to produce a CC chemokine RANTES/CCL5. Immunol. Lett. 2002, 84:1-7.
50. Laffer C.L., Elijovich F. Inflammation and therapy for hypertension. Curr. Hypertens. Rep. 2010, 12:233-242.
51. Lee D.L., Sturgis L.C., Labazi H., Osborne J.B., Fleming C., Pollock J.S., Manhiani M., Imig J.D., Brands M.W. Angiotensin II hypertension is attenuated in interleukin-6 knockout mice. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H935-H940.
52. Li J.J., Chen J.L. Inflammation may be a bridge connecting hypertension and atherosclerosis. Med. Hypotheses 2005, 64:925-929.
53. Lo W.C., Lu P.J., Ho W.Y., Hsiao M., Tseng C.J. Induction of heme oxygenase-1 is involved in carbon monoxide-mediated central cardiovascular regulation. J. Pharmacol. Exp. Ther. 2006, 318:8-16.
54. Lo W.C., Hsiao M., Tung C.S., Tseng C.J. The cardiovascular effects of nitric oxide and carbon monoxide in the nucleus tractus solitarii of rats. J. Hypertens. 2004, 22:1182-1190.
55. Lohmeier T.E., Iliescu R., Dwyer T.M., Irwin E.D., Cates A.W., Rossing M.A. Sustained suppression of sympathetic activity and arterial pressure during chronic activation of the carotid baroreflex. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H402-H409.
56. Lonergan T., Teschemacher A.G., Hwang D.Y., Kim K.S., Pickering A.E., Kasparov S. Targeting brain stem centers of cardiovascular control using adenoviral vectors: impact of promoters on transgene expression. Physiol. Genomics 2005, 20:165-172.
57. Luster A.D. Chemokines: chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 1998, 338:436-444.
58. Machado B.H. Neurotransmission of the cardiovascular reflexes in the nucleus tractus solitarii of awake rats. Ann. N. Y. Acad. Sci. 2001, 940:179-196.
59. Marvar P.J., Thabet S.R., Guzik T.J., Lob H.E., McCann L.A., Weyand C., Gordon F.J., Harrison D.G. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ. Res. 2010, 107:263-270.
60. Mendelsohn F.A., Allen A.M., Clevers J., Denton D.A., Tarjan E., McKinley M.J. Localization of angiotensin II receptor binding in rabbit brain by in vitro autoradiography. J. Comp. Neurol. 1988, 270:372-384.
61. Min J., Jin Y.M., Moon J.S., Sung M.S., Jo S.A., Jo I. Hypoxia-induced endothelial NO synthase gene transcriptional activation is mediated through the tax-responsive element in endothelial cells. Hypertension 2006, 47:1189-1196.
62. Miyoshi M., Miyano K., Moriyama N., Taniguchi M., Watanabe T. Angiotensin type 1 receptor antagonist inhibits lipopolysaccharide-induced stimulation of rat microglial cells by suppressing nuclear factor kappaB and activator protein-1 activation. Eur. J. Neurosci. 2008, 27:343-351.
63. Mo Z.L., Katafuchi T., Hori T. Effects of IL-1 beta on neuronal activities in the dorsal motor nucleus of the vagus in rat brain slices. Brain Res. Bull. 1996, 41:249-255.
64. Musante V., Longordo F., Neri E., Pedrazzi M., Kalfas F., Severi P., Raiteri M., Pittaluga A. RANTES modulates the release of glutamate in human neocortex. J. Neurosci. 2008, 28:12231-12240.
65. Naik U.P., Ehrlich Y.H., Kornecki E. Mechanisms of platelet activation by a stimulatory antibody: cross-linking of a novel platelet receptor for monoclonal antibody F11 with the Fc gamma RII receptor. Biochem. J. 1995, 310:155-162.
66. O'Dell T.J., Huang P.L., Dawson T.M., Dinerman J.L., Snyder S.H., Kandel E.R., Fishman M.C. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 1994, 265:542-546.
67. Okamoto K., Aoki K. Development of a strain of spontaneously hypertensive rats. Jpn. Circ. J. 1963, 27:282-293.
68. Oseka M., Koźniewska E. Dependence of basal cerebral blood flow and cerebral vascular resistance in spontaneously hypertensive rats upon vasoconstrictor prostanoids. Acta Neurochir. Suppl. 1997, 70:228-230.
69. Pascual O., Morin-Surun M.P., Barna B., Denavit-Saubié M., Peqquignot J.M., Champagnat J. Progesterone reverses the neuronal responses to hypoxia in rat nucleus tractus solitarius in vitro. J. Physiol. 2002, 544:511-520.
70. Paton J.F. The Sharpey-Schafer prize lecture: nucleus tractus solitarii: integrating structures. Exp. Physiol. 1999, 84:815-833.
71. Paton J.F.R., Deuchars J., Ahmad Z., Wong L.F., Murphy D., Kasparov S. Adeno viral vector demonstrates that angiotensin II induced depression of the cardiac baroreflex is mediated by endothelial nitric oxide synthase in the nucleus tractus solitarii. J. Physiol. 2001, 531:445-458.
72. Paton J.F.R., Kasparov S., Paterson D.J. Site-specific differential modulation of cardiac autonomic control by nitric oxide. TINS 2002, 25:626-631.
73. Paton J.F.R., Lonergan T., Deuchars J., James P.E., Kasparov S. Detection of angiotensin II mediated nitric oxide release within the nucleus of the solitary tract using electron-paramagnetic resonance (EPR) spectroscopy. Auton. Neurosci. 2006, 126-127:193-201.
74. Paton J.F.R., Waki H., Abdala A.P., Dickinson J., Kasparov S. Vascular-brain signaling in hypertension: role of angiotensin II and nitric oxide. Curr. Hypertens. Rep. 2007, 9:242-247.
75. Paton J.F.R., Wang S., Polson J.W., Kasparov S. Signalling across the blood brain barrier by angiotensin II: novel implications for neurogenic hypertension. J. Mol. Med. 2008, 86:705-710.
76. Paton J.F.R., Dickinson C.J., Mitchell G. Harvey Cushing and the regulation of blood pressure in giraffe, rat and man: introducing 'Cushing's mechanism'. Exp. Physiol. 2009, 94:11-17.
77. Powell F.L., Kim B.C., Johnson S.R., Fu Z. Oxygen sensing in the brain - invited article. Adv. Exp. Med. Biol. 2009, 648:369-376.
78. Powell F.L., Fu Z. HIF-1 and ventilatory acclimatization to chronic hypoxia. Respir. Physiol. Neurobiol. 2008, 164:282-287.
79. Rostène W., Kitabgi P., Parsadaniantz S.M. Chemokines: a new class of neuromodulator?. Nat. Rev. Neurosci. 2007, 8:895-903.
80. Rodriguez-Pallares J., Rey P., Parga J.A., Muñoz A., Guerra M.J., Labandeira-Garcia J.L. Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS. Neurobiol. Dis. 2008, 31:58-73.
81. Sadoshima S., Fujii K., Yao H., Kusuda K., Ibayashi S., Fujishima M. Regional cerebral blood flow autoregulation in normotensive and spontaneously hypertensive rats - effects of sympathetic denervation. Stroke 1986, 17:981-984.
82. Savoia C., Schiffrin E.L. Inflammation in hypertension. Curr. Opin. Nephrol. Hypertens. 2006, 15:152-158.
83. Seidel B., Stanarius A., Wolf G. Differential expression of neuronal and endothelial nitric oxide synthase in blood vessels of the rat brain. Neurosci. Lett. 1997, 239:109-112.
84. Shi P., Diez-Freire C., Jun J.Y., Qi Y., Katovich M.J., Li Q., Sriramula S., Francis J., Sumners C., Raizada M.K. Brain microglial cytokines in neurogenic hypertension. Hypertension 2010, 56:297-303.
85. Sriramula S., Haque M., Majid D.S., Francis J. Involvement of tumor necrosis factor-alpha in angiotensin II-mediated effects on salt appetite, hypertension, and cardiac hypertrophy. Hypertension 2008, 51:1345-1351.
86. Silva C.C., Almeida V.A., Haibara A.S., Johnson R.A., Colombari E. Role of carbon monoxide in l-glutamate-induced cardiovascular responses in nucleus tractus solitarius of conscious rats. Brain Res. 1999, 824:147-152.
87. Smith P.A., Graham L.N., Mackintosh A.F., Stoker J.B., Mary D.A. Sympathetic neural mechanisms in white-coat hypertension. J. Am. Coll. Cardiol. 2002, 40:126-132.
88. Suematsu M., Suzuki H., Delano F.A., Schmid-Schönbein G.W. The inflammatory aspect of the microcirculation in hypertension: oxidative stress, leukocytes/endothelial interaction, apoptosis. Microcirculation 2002, 9:259-276.
89. Szelényi J. Cytokines and the central nervous system. Brain Res. Bull. 2001, 54:329-338.
90. Takagishi M., Waki H., Bhuiyan M.E., Gouraud S.S., Kohsaka A., Cui H., Yamazaki T., Paton J.F., Maeda M. IL-6 microinjected in the nucleus tractus solitarii attenuates cardiac baroreceptor reflex function in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R183-R190.
91. Talman W.T., Perrone M.H., Reis D.J. Acute hypertension after the local injection of kainic acid into the nucleus tractus solitarii of rats. Circ. Res. 1981, 48:292-298.
92. Tan P.S., Killinger S., Horiuchi J., Dampney R.A. Baroreceptor reflex modulation by circulating angiotensin II is mediated by AT1 receptors in the nucleus tractus solitarius. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R2267-R2278.
93. Thrasher T.N. Unloading arterial baroreceptors causes neurogenic hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 282:R1044-R1053.
94. Thrasher T.N. Arterial baroreceptor input contributes to long-term control of blood pressure. Curr. Hypertens. Rep. 2006, 8:249-254.
95. 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.
96. Waki H., Kasparov S., Wong L.F., Murphy D., Shimizu T., Paton J.F. Chronic inhibition of eNOS activity in NTS enhances baroreceptor reflex in conscious rats. J. Physiol. 2003, 546:233-242.
97. Waki H., Kasparov S., Miyake M., Katahira K., Liu B., Murphy D., Paton J.F. Gene expression profiles in the nucleus tractus solitarii of the spontaneously hypertensive rat. J. Physiol. 2004, 560P:PC6.
98. Waki H., Katahira K., Polson J.W., Kasparov S., Murphy D., Paton J.F. Automation of analysis of cardiovascular autonomic function from chronic measurements of arterial pressure in conscious rats. Exp. Physiol. 2006, 91:201-213.
99. Waki H., Murphy D., Yao S., Kasparov S., Paton J.F. Endothelial nitric oxide synthase in the nucleus tractus solitarii contributes to the hypertension in the spontaneously hypertensive rat. Hypertension 2006, 48:644-650.
100. Waki H., Liu B., Miyake M., Katahira K., Murphy D., Kasparov S., Paton J.F. Junctional adhesion molecule-1 is upregulated in spontaneously hypertensive rats: evidence for a prohypertensive role within the brain stem. Hypertension 2007, 49:1321-1327.
101. Waki H., Gouraud S.S., Maeda M., Paton J.F. Evidence of specific inflammatory condition in nucleus tractus solitarii of spontaneously hypertensive rats. Exp. Physiol. 2010, 95:595-600.
102. Wang S., Teschemacher A.G., Paton J.F., Kasparov S. Mechanism of nitric oxide action on inhibitory GABAergic signaling within the nucleus tractus solitarii. FASEB J. 2006, 20:1537-1539.
103. Wang S., Paton J.F., Kasparov S. Differential sensitivity of excitatory and inhibitory synaptic transmission to modulation by nitric oxide in rat nucleus tractus solitarii. Exp. Physiol. 2007, 92:371-382.
104. Waki, H., Bhuiyan, M.E., Gouraud, S.S., Takagishi, M., Hatada, A., Kohsaka, A., Paton, J.F., Maeda, M. Acute reductions in blood flow restricted to the dorsomedial medulla induce a pressor response in rats. J. Hypertens., in press.
105. Whitehead G.S., Wang T., DeGraff L.M., Card J.W., Lira S.A., Graham G.J., Cook D.N. The chemokine receptor D6 has opposing effects on allergic inflammation and airway reactivity. Am. J. Respir. Crit. Care Med. 2007, 175:243-249.
106. Wu L., Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol. Rev. 2005, 57:585-630.
107. Yokomizo T., Izumi T., Shimizu T. Leukotriene B4: metabolism and signal transduction. Arch. Biochem. Biophys. 2001, 385:231-241.