Nitric oxide mediates hypoxia-induced changes in paracellular permeability of cerebral microvasculature

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 286, Issue 1 55-1, 2004, Pages

  Mark, Karen S ^a   Burroughs, Amanda R ^a   Brown, Rachel C ^a   Huber, Jason D ^a   Davis, Thomas P ^a,b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Blood brain barrier; Endothelial; Nitric oxide synthase; Reoxygenation

Indexed keywords

CARBON 14; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SUCROSE;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN MICROCIRCULATION; CATTLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; GLIA CELL; ISOTOPE LABELING; NERVE CELL; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; REOXYGENATION; STROKE; WESTERN BLOTTING;

EID: 0346998130     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00669.2002     Document Type: Article

References (49)

1. Abbruscato TJ and Davis TP. Combination of hypoxia/aglycemia compromises in vitro blood-brain barrier integrity. J Pharmacol Exp Ther 289: 668-675, 1999.
2. Adachi R, Matsui S, Kinoshita M, Nagaishi K, Sasaki H, Kasahara T, and Suzuki K. Nitric oxide induces chemotaxis of neutrophil-like HL-60 cells and translocation of cofilin to plasma membranes. Int J Immunopharmacol 22: 855-864, 2000.
3. Ali MH, Schlidt SA, Chandel NS, Hynes KL, Schumacker PT, and Gewertz BL. Endothelial permeability and IL-6 production during hypoxia: role of ROS in signal transduction. Am J Physiol Lung Cell Mol Physiol 277: L1057-L1065, 1999.
4. Baldwin AL, Thurston G, and al Naemi H. Inhibition of nitric oxide synthesis increases venular permeability and alters endothelial actin cytoskeleton. Am J Physiol Heart Circ Physiol 274: H1776-H1784, 1998.
5. Betz AL, Yang GY, Kawai N, Fujisawa M, Abdelkarim GE, Ennis SR, and Keep RF. Reperfusion-induced injury of the blood-brain barrer. In: Brain Barrier Systems, edited by Paulson OB, Knudsen GM, and Moos T. Copenhagen, Denmark: Munksgaard, 1999, p. 430-440.
6. Bolanos JP and Almeida A. Roles of nitric oxide in brain hypoxia-ischemia. Biochim Biophys Acta 1411: 415-436, 1999.
7. Burgstahler AD and Nathanson MH. NO modulates the apicolateral cytoskeleton of isolated hepatocytes by a PKC-dependent, cGMP-independent mechanism. Am J Physiol Gastrointest Liver Physiol 269: G789-G799, 1995.
8. Cho MM, Ziats NP, Pal D, Utian WH, and Gorodeski GI. Estrogen modulates paracellular permeability of human endothelial cells by eNOS-and iNOS-related mechanisms. Am J Physiol Cell Physiol 276: C337-C349, 1999.
9. Chryssanthou C, Palaia T, Goldstein G, and Stenger R. Increase in blood-brain barrier permeability by altitude decompression. Aviat Space Environ Med 58: 1082-1086, 1987.
10. Del Zoppo G, Ginis I, Hallenbeck JM, Iadecola C, Wang X, and Feuerstein GZ. Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia. Brain Pathol 10: 95-112, 2000.
11. Deli MA, Descamps L, Dehouck MP, Cecchelli R, Joo F, Abraham CS, and Torpier G. Exposure of tumor necrosis factor-α to luminal membrane of bovine brain capillary endothelial cells co-cultured with astrocytes induces a delayed increase of permeability and cytoplasmic stress fiber formation of actin. J Neurosci Res 41: 717-726, 1995.
12. Demiryurek AT, Karamsetty MR, McPhaden AR, Wadsworth RM, Kane KA, and MacLean MR. Accumulation of nitrotyrosine correlates with endothelial NO synthase in pulmonary resistance arteries during chronic hypoxia in the rat. Pulm Pharmacol Ther 13: 157-165, 2000.
13. Fischer S, Clauss M, Wiesnet M, Renz D, Schaper W, and Karliczek GF. Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO. Am J Physiol Cell Physiol 276: C812-C820, 1999.
14. Fischer S, Wobben M, Marti HH, Renz D, and Schaper W. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc Res 63: 70-80, 2002.
15. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, and Knowles RG. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 272: 4959-4963, 1997.
16. Gonzalez NC and Wood JG. Leukocyte-endothelial interactions in environmental hypoxia. Adv Exp Med Biol 502: 39-60, 2001.
17. Guo Y, Ward ME, Beasjours S, Mori M, and Hussain SN. Regulation of cerebellar nitric oxide production in response to prolonged in vivo hypoxia. J Neurosci Res 49: 89-97, 1997.
18. Hackett PH. High altitude cerebral edema and acute mountain sickness. A pathophysiology update. Adv Exp Med Biol 474: 23-45, 1999.
19. Hanafy KA, Krumenacker JS, and Murad F. NO, nitrotyrosine, and cyclic GMP in signal transduction. Med Sci Monit 7: 801-819, 2001.
20. Huang PL. Mouse models of nitric oxide synthase deficiency. J Am Soc Nephrol 11, Suppl 16: S120-S123, 2000.
21. Iadecola C, Zhang F, and Xu X. Inhibition of inducible nitric oxide synthase ameliorates cerebral ischemic damage. Am J Physiol Regul Integr Comp Physiol 268: R286-R292, 1995.
22. Ioroi T, Yonetani M, and Nakamura H. Effects of hypoxia and reoxygenation on nitric oxide production and cerebral blood flow in developing-rat striatum. Pediatr Res 43: 733-737, 1998.
23. Jung F, Palmer LA, Zhou N, and Johns RA. Hypoxic regulation of inducible nitric oxide synthase via hypoxia inducible factor-1 in cardiac myocytes. Circ Res 86: 319-325, 2000.
24. Kelm M. Nitric oxide metabolism and breakdown. Biochim Biophys Acta 1411: 273-289, 1999.
25. Kish PE and Ueda T. Calcium-dependent release of accumulated glutamate from synaptic vesicles within permeabilized nerve terminals. Neurosci Lett 122: 179-182, 1991.
26. Kristian T and Siesjo BK. Calcium in ischemic cell death. Stroke 29: 705-718, 1998.
27. Liang M and Knox FG. Production and functional roles of nitric oxide in the proximal tubule. Am J Physiol Regul Integr Comp Physiol 278: R1117-R1124, 2000.
28. Lum H, Barr DA, Shaffer JR, Gordon RJ, Ezrin AM, and Malik AB. Reoxygenation of endothelial cells increases permeability by oxidant-dependent mechanisms. Circ Res 70: 991-998, 1992.
29. Maccarrone M, Putti S, and Finazzi Agro A. Nitric oxide donors activate the cyclo-oxygenase and peroxidase activities of prostaglandin H synthase. FEBS Lett 410: 470-476, 1997.
30. Mark KS and Davis TP. Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am J Physiol Heart Circ Physiol 282: H1485-H1494, 2002.
31. Mason RB, Pluta RM, Walbridge S, Wink DA, Oldfield EH, and Boock RJ. Production of reactive oxygen species after reperfusion in vitro and in vivo: protective effect of nitric oxide. J Neurosurg 93: 99-107, 2000.
32. Mayhan WG. Role of nitric oxide in disruption of the blood-brain barrier during acute hypertension. Brain Res 686: 99-103, 1995.
33. Miller DW, Audus KL, and Borchardt RT. Application of cultured endothelial cells of the brain microvasculature in the study of the blood-brain barrier. J Tiss Cult Meth 14: 217-224, 1992.
34. Murray IA, Danlels I, Coupland K, Smith JA, and Long RG. Increased activity and expression of iNOS in human duodenal enterocytes from patients with celiac disease. Am J Physiol Gastrointest Liver Physiol 283: G319-G326, 2002.
35. i in rat brain microvacular endothelial cells. Eur J Pharmacol 361: 119-127, 1998.
36. Ogawa S, Koga S, Kuwabara K, Brett J, Morrow B, Morris SA, Bilezikian JP, Silverstein SC, and Stern D. Hypoxia-induced increased permeability of endothelial monolayers occurs through lowering of cellular cAMP levels. Am J Physiol Cell Physiol 262: C546-C554, 1992.
37. Palmer LA, Semenza GL, Stoler MH, and Johns RA. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am J Physiol Lung Cell Mol Physiol 274: L212-L219, 1998.
38. Parmentier S, Bohme GA, Lerouet D, Damour D, Stutzmann JM, Margaill I, and Plotkine M. Selective inhibition of inducible nitric oxide synthase prevents ischaemic brain injury. Br J Pharmacol 127: 546-552, 1999.
39. Raychaudhuri B, Dweik R, Connors MJ, Buhrow L, Malur A, Drazba J, Arroliga AC, Erzurum SC, Kavuru MS, and Thomassen MJ. Nitric oxide blocks nuclear factor-β activation in alveolar macrophages. Am J Respir Cell Mol Biol 21: 311-316, 1999.
40. Rosenberg GA. Ischemic brain edema. Prog Cardiovasc Dis 42: 209-216, 1999.
41. Samdani AF, Dawson TM, and Dawson VL. Nitric oxide synthase in models of focal ischemia. Stroke 28: 1283-1288, 1997.
42. Schoch HJ, Fischer S, and Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 125: 2549-2557, 2002.
43. Shinnou M, Ueno M, Sakamoto H, and Ide M. Blood-brain barrier damage in reperfusion following ischemia in the hippocampus of the mongolian gerbil. Acta Neural Scand 98: 406-411, 1998.
44. Stanimirovic D and Satoh K. Inflammatory mediators of cerebral endothelium: a role in ischemic brain inflammation. Brain Pathol 10: 113-126, 2000.
45. Utepbergenov DI, Mertsch K, Sporbert A, Tenz K, Paul M, Haseloff RF, and Blasig IE. Nitric oxide protects blood-brain barrier in vitro from hypoxia/reoxygenation-mediated injury. FEBS Lett 424: 197-201, 1998.
46. Xu J, He L, Ahmed SH, Chen SW, Goldberg MP, Beckman JS, and Hsu CY. Oxygen-glucose deprivation induces inducible nitric oxide synthase and nitrotyrosine expression in cerebral endothelial cells. Stroke 31: 1744-1751, 2000.
47. Xu XP, Pollock JS, Tanner MA, and Myers PR. Hypoxia activates nitric oxide synthase and stimulates nitric oxide production in porcine coronary resistance arteriolar endothelial cells. Cardiovasc Res 30: 841-847, 1995.
48. Yang GY and Betz AL. Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke 25: 1658-1665, 1994.
49. Zech JC, Pouvreau I, Cotinet A, Goureau O, Le Varlet B, and de Kozak Y. Effect of cytokines and nitric oxide on tight junctions in cultured rat retinal pigment epithelium. Invest Ophthalmol Vis Sci 39: 1600-1608, 1998.