The role of oxidative stress in cerebral aneurysm formation and rupture

Current Neurovascular Research

Volumn 10, Issue 3, 2013, Pages 247-255

  Starke, Robert M ^a,b   Chalouhi, Nohra ^a   Ali, Muhammad S ^a   Jabbour, Pascal M ^a   Tjoumakaris, Stavropoula I ^a   Gonzalez, L Fernando ^a   Rosenwasser, Robert H ^a   Koch, Walter J ^c   Dumont, Aaron S ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aneurysm; Inflammation; NADPH oxidase; Oxidative stress; Reactive oxygen species; Subarachnoid hemorrhage

Indexed keywords

CELL ADHESION MOLECULE; CHEMOKINE; FREE RADICAL; MATRIX METALLOPROTEINASE; REACTIVE NITROGEN SPECIES;

APOPTOSIS; ARTICLE; BRAIN ARTERY ANEURYSM; BRAIN ARTERY ANEURYSM RUPTURE; BRAIN ATHEROSCLEROSIS; CELL INVASION; ENDOTHELIUM INJURY; GENE SWITCHING; HEMODYNAMIC STRESS; HUMAN; HYPERTENSION; INFLAMMATORY CELL; LIPID PEROXIDATION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; UPREGULATION;

EID: 84880253553     PISSN: 15672026     EISSN: 18755739     Source Type: Journal    
DOI: 10.2174/15672026113109990003     Document Type: Article

References (115)

1. Rinkel GJ: Natural history, epidemiology and screening of unruptured intracranial aneurysms. J Neuroradiol 2008, 35(2):99-103.
2. Komotar RJ, Zacharia BE, Mocco J, Connolly ES, Jr.: Controversies in the surgical treatment of ruptured intracranial aneurysms: the First Annual J. Lawrence Pool Memorial Research Symposium-controversies in the management of cerebral aneurysms. Neurosurgery 2008, 62(2):396-407; discussion 405-397.
3. van Gijn J, Kerr RS, Rinkel GJ: Subarachnoid haemorrhage. Lancet 2007, 369(9558):306-318.
4. Kassell NF, Torner JC: The International Cooperative Study on Timing of Aneurysm Surgery-an update. Stroke 1984, 15(3):566-570.
5. Schievink WI: Intracranial aneurysms. N Engl J Med 1997, 336(1):28-40.
6. Ronkainen A, Miettinen H, Karkola K, Papinaho S, Vanninen R, Puranen M et al: Risk of harboring an unruptured intracranial aneurysm. Stroke 1998, 29(2):359-362.
7. Ingall T, Asplund K, Mahonen M, Bonita R: A multinational comparison of subarachnoid hemorrhage epidemiology in the WHO MONICA stroke study. Stroke 2000, 31(5):1054-1061.
8. Brown RD, Jr., Huston J, Hornung R, Foroud T, Kallmes DF, Kleindorfer D et al: Screening for brain aneurysm in the Familial Intracranial Aneurysm study: frequency and predictors of lesion detection. J Neurosurg 2008, 108(6):1132-1138.
9. Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ: Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a metaanalysis. Lancet Neurol 2009, 8(7):635-642.
10. Rosenorn J, Eskesen V, Schmidt K, Espersen JO, Haase J, Harmsen A et al: Clinical features and outcome in 1076 patients with ruptured intracranial saccular aneurysms: a prospective consecutive study. Br J Neurosurg 1987, 1(1):33-45.
11. Saveland H, Sonesson B, Ljunggren B, Brandt L, Uski T, Zygmunt S et al: Outcome evaluation following subarachnoid hemorrhage. J Neurosurg 1986, 64(2):191-196.
12. Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF, Rosenwasser RH et al: Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab 2012, 32(9):1659-1676.
13. Hasan DM, Chalouhi N, Jabbour P, Dumont AS, Kung DK, Magnotta VA et al: Evidence that acetylsalicylic acid attenuates inflammation in the walls of human cerebral aneurysms: preliminary results. J Am Heart Assoc 2013, 2(1):e000019.
14. Hasan D, Chalouhi N, Jabbour P, Dumont AS, Kung DK, Magnotta VA et al: Early change in ferumoxytol-enhanced magnetic resonance imaging signal suggests unstable human cerebral aneurysm: a pilot study. Stroke 2012, 43(12):3258-3265.
15. Hasan D, Chalouhi N, Jabbour P, Hashimoto T: Macrophage imbalance (M1 vs. M2) and upregulation of mast cells in wall of ruptured human cerebral aneurysms: preliminary results. J Neuroinflammation 2012, 9:222.
16. Hasan DM, Mahaney KB, Brown RD, Jr., Meissner I, Piepgras DG, Huston J et al: Aspirin as a promising agent for decreasing incidence of cerebral aneurysm rupture. Stroke 2011, 42(11):3156-3162.
17. Griendling KK, FitzGerald GA: Oxidative stress and cardiovascular injury: Part I: basic mechanisms and in vivo monitoring of ROS. Circulation 2003, 108(16):1912-1916.
18. Stocker R, Keaney JF, Jr.: Role of oxidative modifications in atherosclerosis. Physiol Rev 2004, 84(4):1381-1478.
19. Papaharalambus CA, Griendling KK: Basic mechanisms of oxidative stress and reactive oxygen species in cardiovascular injury. Trends Cardiovasc Med 2007, 17(2):48-54.
20. Griendling KK, FitzGerald GA: Oxidative stress and cardiovascular injury: Part II: animal and human studies. Circulation 2003, 108(17):2034-2040.
21. Miller AA, Drummond GR, Sobey CG: Reactive oxygen species in the cerebral circulation: are they all bad? Antioxid Redox Signal 2006, 8(7-8):1113-1120.
22. Olmez I, Ozyurt H: Reactive oxygen species and ischemic cerebrovascular disease. Neurochem Int 2012, 60(2):208-212.
23. Brandes RP, Kreuzer J: Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 2005, 65(1):16-27.
24. Didion SP, Hathaway CA, Faraci FM: Superoxide levels and function of cerebral blood vessels after inhibition of CuZn-SOD. Am J Physiol Heart Circ Physiol 2001, 281(4):H1697-1703.
25. Faraci FM, Sobey CG, Chrissobolis S, Lund DD, Heistad DD, Weintraub NL: Arachidonate dilates basilar artery by lipoxygenase-dependent mechanism and activation of K(+) channels. Am J Physiol Regul Integr Comp Physiol 2001, 281(1):R246-253.
26. Rouzer CA, Marnett LJ: Cyclooxygenases: structural and functional insights. J Lipid Res 2009, 50 Suppl:S29-34.
27. Dobrian AD, Lieb DC, Cole BK, Taylor-Fishwick DA, Chakrabarti SK, Nadler JL: Functional and pathological roles of the 12-and 15-lipoxygenases. Prog Lipid Res 2011, 50(1):115-131.
28. Hasan D, Hashimoto T, Kung D, Macdonald RL, Winn HR, Heistad D: Upregulation of cyclooxygenase-2 (COX-2) and microsomal prostaglandin E2 synthase-1 (mPGES-1) in wall of ruptured human cerebral aneurysms: preliminary results. Stroke 2012, 43(7):1964-1967.
29. Forstermann U, Li H: Therapeutic effect of enhancing endothelial nitric oxide synthase (eNOS) expression and preventing eNOS uncoupling. Br J Pharmacol 2011, 164(2):213-223.
30. Walford G, Loscalzo J: Nitric oxide in vascular biology. J Thromb Haemost 2003, 1(10):2112-2118.
31. Puca AA, Carrizzo A, Ferrario A, Villa F, Vecchione C: Endothelial nitric oxide synthase, vascular integrity and human exceptional longevity. Immun Ageing 2012, 9(1):26.
32. Seimetz M, Parajuli N, Pichl A, Veit F, Kwapiszewska G, Weisel FC et al: Inducible NOS inhibition reverses tobacco-smokeinduced emphysema and pulmonary hypertension in mice. Cell 2011, 147(2):293-305.
33. Xia Y, Tsai AL, Berka V, Zweier JL: Superoxide generation from endothelial nitric-oxide synthase. A Ca2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. J Biol Chem 1998, 273(40):25804-25808.
34. Alp NJ, Channon KM: Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler Thromb Vasc Biol 2004, 24(3):413-420.
35. Fukuda S, Hashimoto N, Naritomi H, Nagata I, Nozaki K, Kondo S et al: Prevention of rat cerebral aneurysm formation by inhibition of nitric oxide synthase. Circulation 2000, 101(21):2532-2538.
36. Sadamasa N, Nozaki K, Hashimoto N: Disruption of gene for inducible nitric oxide synthase reduces progression of cerebral aneurysms. Stroke 2003, 34(12):2980-2984.
37. Tulamo R, Frosen J, Hernesniemi J, Niemela M: Inflammatory changes in the aneurysm wall: a review. J Neurointerv Surg 2010, 2(2):120-130.
38. 2-from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J Biol Chem 2003, 278(47):47291-47298.
39. 2, and iron are required for TNF-alpha-induced MCP-1 gene expression in endothelial cells: role of Rac1 and NADPH oxidase. Am J Physiol Heart Circ Physiol 2004, 286(3):H1001-1007.
40. Juric V, Chen CC, Lau LF: TNFalpha-induced apoptosis enabled by CCN1/CYR61: pathways of reactive oxygen species generation and cytochrome c release. PLoS One 2012, 7(2):e31303.
41. Jamous MA, Nagahiro S, Kitazato KT, Tamura T, Aziz HA, Shono M et al: Endothelial injury and inflammatory response induced by hemodynamic changes preceding intracranial aneurysm formation: experimental study in rats. J Neurosurg 2007, 107(2):405-411.
42. Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF, Rosenwasser RH et al: Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab 2012.
43. Tada Y, Yagi K, Kitazato KT, Tamura T, Kinouchi T, Shimada K et al: Reduction of endothelial tight junction proteins is related to cerebral aneurysm formation in rats. J Hypertens 2010, 28(9):1883-1891.
44. Lum H, Roebuck KA: Oxidant stress and endothelial cell dysfunction. Am J Physiol Cell Physiol 2001, 280(4):C719-741.
45. McCormick ML, Gavrila D, Weintraub NL: Role of oxidative stress in the pathogenesis of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 2007, 27(3):461-469.
46. Montezano AC, Touyz RM: Reactive oxygen species and endothelial function-role of nitric oxide synthase uncoupling and Nox family nicotinamide adenine dinucleotide phosphate oxidases. Basic Clin Pharmacol Toxicol 2012, 110(1):87-94.
47. Kvietys PR, Granger DN: Role of reactive oxygen and nitrogen species in the vascular responses to inflammation. Free Radic Biol Med 2012, 52(3):556-592.
48. Marumo T, Schini-Kerth VB, Fisslthaler B, Busse R: Plateletderived growth factor-stimulated superoxide anion production modulates activation of transcription factor NF-kappaB and expression of monocyte chemoattractant protein 1 in human aortic smooth muscle cells. Circulation 1997, 96(7):2361-2367.
49. Aoki T, Kataoka H, Ishibashi R, Nozaki K, Egashira K, Hashimoto N: Impact of monocyte chemoattractant protein-1 deficiency on cerebral aneurysm formation. Stroke 2009, 40(3):942-951.
50. Kanematsu Y, Kanematsu M, Kurihara C, Tada Y, Tsou TL, van Rooijen N et al: Critical roles of macrophages in the formation of intracranial aneurysm. Stroke 2011, 42(1):173-178.
51. Aoki T, Kataoka H, Morimoto M, Nozaki K, Hashimoto N: Macrophage-derived matrix metalloproteinase-2 and -9 promote the progression of cerebral aneurysms in rats. Stroke 2007, 38(1):162-169.
52. Aoki T, Kataoka H, Ishibashi R, Nozaki K, Hashimoto N: Cathepsin B, K, and S are expressed in cerebral aneurysms and promote the progression of cerebral aneurysms. Stroke 2008, 39(9):2603-2610.
53. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S: p47phoxdependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res 2005, 97(6):533-540.
54. Martinez-Lemus LA, Zhao G, Galinanes EL, Boone M: Inward remodeling of resistance arteries requires reactive oxygen speciesdependent activation of matrix metalloproteinases. Am J Physiol Heart Circ Physiol 2011, 300(6):H2005-2015.
55. Sousa-Santos O, Neto-Neves EM, Ferraz KC, Ceron CS, Rizzi E, Gerlach RF et al: Antioxidant treatment protects against matrix metalloproteinase activation and cardiomyocyte injury during acute pulmonary thromboembolism. Naunyn Schmiedebergs Arch Pharmacol 2012, 385(7):685-696.
56. Acilan C, Serhatli M, Kacar O, Adiguzel Z, Tuncer A, Hayran M et al: Smooth muscle cells isolated from thoracic aortic aneurysms exhibit increased genomic damage, but similar tendency for apoptosis. DNA Cell Biol 2012, 31(10):1523-1534.
57. Pollman MJ, Hall JL, Gibbons GH: Determinants of vascular smooth muscle cell apoptosis after balloon angioplasty injury. Influence of redox state and cell phenotype. Circ Res 1999, 84(1):113-121.
58. Killer-Oberpfalzer M, Aichholzer M, Weis S, Richling B, Jones R, Virmani R et al: Histological analysis of clipped human intracranial aneurysms and parent arteries with short-term followup. Cardiovasc Pathol 2012, 21(4):299-306.
59. Kosierkiewicz TA, Factor SM, Dickson DW: Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J Neuropathol Exp Neurol 1994, 53(4):399-406.
60. Chalouhi N, Chitale R, Jabbour P, Tjoumakaris S, Dumont AS, Rosenwasser R et al: The case for family screening for intracranial aneurysms. Neurosurg Focus 2011, 31(6):E8.
61. Woo D, Khoury J, Haverbusch MM, Sekar P, Flaherty ML, Kleindorfer DO et al: Smoking and family history and risk of aneurysmal subarachnoid hemorrhage. Neurology 2009, 72(1):69-72.
62. Asano H, Horinouchi T, Mai Y, Sawada O, Fujii S, Nishiya T et al: Nicotine-and tar-free cigarette smoke induces cell damage through reactive oxygen species newly generated by PKC-dependent activation of NADPH oxidase. J Pharmacol Sci 2012, 118(2):275-287.
63. Talukder MA, Johnson WM, Varadharaj S, Lian J, Kearns PN, El-Mahdy MA et al: Chronic cigarette smoking causes hypertension, increased oxidative stress, impaired NO bioavailability, endothelial dysfunction, and cardiac remodeling in mice. American journal of physiology Heart and circulatory physiology 2011, 300(1):H388-396.
64. Ambrose JA, Barua RS: The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 2004, 43(10):1731-1737.
65. Chalouhi N, Ali MS, Starke RM, Jabbour PM, Tjoumakaris SI, Gonzalez LF et al: Cigarette smoke and inflammation: role in cerebral aneurysm formation and rupture. Mediators Inflamm 2012, 2012:271582.
66. Barua RS, Ambrose JA, Srivastava S, DeVoe MC, Eales-Reynolds LJ: Reactive oxygen species are involved in smoking-induced dysfunction of nitric oxide biosynthesis and upregulation of endothelial nitric oxide synthase: an in vitro demonstration in human coronary artery endothelial cells. Circulation 2003, 107(18):2342-2347.
67. Heitzer T, Just H, Munzel T: Antioxidant vitamin C improves endothelial dysfunction in chronic smokers. Circulation 1996, 94(1):6-9.
68. Fennessy FM, Moneley DS, Wang JH, Kelly CJ, Bouchier-Hayes DJ: Taurine and vitamin C modify monocyte and endothelial dysfunction in young smokers. Circulation 2003, 107(3):410-415.
69. Khanna AK, Xu J, Mehra MR: Antioxidant N-acetyl cysteine reverses cigarette smoke-induced myocardial infarction by inhibiting inflammation and oxidative stress in a rat model. Lab Invest 2012, 92(2):224-235.
70. Nyunoya T, March TH, Tesfaigzi Y, Seagrave J: Antioxidant diet protects against emphysema, but increases mortality in cigarette smoke-exposed mice. COPD 2011, 8(5):362-368.
71. Yang T, Luo F, Shen Y, An J, Li X, Liu X et al: Quercetin attenuates airway inflammation and mucus production induced by cigarette smoke in rats. Int Immunopharmacol 2012, 13(1):73-81.
72. Juvela S: Prevalence of and risk factors for intracranial aneurysms. Lancet Neurol 2011, 10(7):595-597.
73. Juvela S, Poussa K, Porras M: Factors affecting formation and growth of intracranial aneurysms: a long-term follow-up study. Stroke 2001, 32(2):485-491.
74. Qin L, Crews FT: NADPH oxidase and reactive oxygen species contribute to alcohol-induced microglial activation and neurodegeneration. J Neuroinflammation 2012, 9:5.
75. Brooks PJ: Brain atrophy and neuronal loss in alcoholism: a role for DNA damage? Neurochem Int 2000, 37(5-6):403-412.
76. Reddy VD, Padmavathi P, Kavitha G, Saradamma B, Varadacharyulu N: Alcohol-induced oxidative/nitrosative stress alters brain mitochondrial membrane properties. Mol Cell Biochem 2013, 375(1-2):39-47.
77. Shiu C, Barbier E, Di Cello F, Choi HJ, Stins M: HIV-1 gp120 as well as alcohol affect blood-brain barrier permeability and stress fiber formation: involvement of reactive oxygen species. Alcohol Clin Exp Res 2007, 31(1):130-137.
78. Haorah J, Ramirez SH, Floreani N, Gorantla S, Morsey B, Persidsky Y: Mechanism of alcohol-induced oxidative stress and neuronal injury. Free Radic Biol Med 2008, 45(11):1542-1550.
79. Vlak MH, Algra A, Brandenburg R, Rinkel GJ: Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis. Lancet Neurol 2011, 10(7):626-636.
80. Lassegue B, Griendling KK: Reactive oxygen species in hypertension; An update. Am J Hypertens 2004, 17(9):852-860.
81. Touyz RM: Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: what is the clinical significance? Hypertension 2004, 44(3):248-252.
82. Montezano AC, Touyz RM: Molecular mechanisms of hypertension-reactive oxygen species and antioxidants: a basic science update for the clinician. Can J Cardiol 2012, 28(3):288-295.
83. Montezano AC, Touyz RM: Oxidative stress, Noxs, and hypertension: experimental evidence and clinical controversies. Ann Med 2012, 44 Suppl 1:S2-16.
84. Nagata I, Handa H, Hashimoto N, Hazama F: Experimentally induced cerebral aneurysms in rats: Part VI. Hypertension. Surg Neurol 1980, 14(6):477-479.
85. Morimoto M, Miyamoto S, Mizoguchi A, Kume N, Kita T, Hashimoto N: Mouse model of cerebral aneurysm: experimental induction by renal hypertension and local hemodynamic changes. Stroke 2002, 33(7):1911-1915.
86. Aoki T, Kataoka H, Ishibashi R, Nozaki K, Hashimoto N: Gene expression profile of the intima and media of experimentally induced cerebral aneurysms in rats by laser-microdissection and microarray techniques. Int J Mol Med 2008, 22(5):595-603.
87. Aoki T, Nishimura M, Matsuoka T, Yamamoto K, Furuyashiki T, Kataoka H et al: PGE(2) -EP(2) signalling in endothelium is activated by haemodynamic stress and induces cerebral aneurysm through an amplifying loop via NF-kappaB. Br J Pharmacol 2011, 163(6):1237-1249.
88. Koide M, Kawahara Y, Tsuda T, Nakayama I, Yokoyama M: Expression of nitric oxide synthase by cytokines in vascular smooth muscle cells. Hypertension 1994, 23(1 Suppl):I45-48.
89. Morris SM, Jr., Billiar TR: New insights into the regulation of inducible nitric oxide synthesis. Am J Physiol 1994, 266(6 Pt 1):E829-839.
90. Nathan C, Xie QW: Nitric oxide synthases: roles, tolls, and controls. Cell 1994, 78(6):915-918.
91. Ross R: Atherosclerosis-an inflammatory disease. N Engl J Med 1999, 340(2):115-126.
92. Inci S, Spetzler RF: Intracranial aneurysms and arterial hypertension: a review and hypothesis. Surg Neurol 2000, 53(6):530-540; discussion 540-532.
93. Kondo S, Hashimoto N, Kikuchi H, Hazama F, Nagata I, Kataoka H: Apoptosis of medial smooth muscle cells in the development of saccular cerebral aneurysms in rats. Stroke 1998, 29(1):181-188; discussion 189.
94. Hara A, Yoshimi N, Mori H: Evidence for apoptosis in human intracranial aneurysms. Neurol Res 1998, 20(2):127-130.
95. Gimbrone MA, Jr.: Endothelial dysfunction, hemodynamic forces, and atherosclerosis. Thromb Haemost 1999, 82(2):722-726.
96. Tamura T, Jamous MA, Kitazato KT, Yagi K, Tada Y, Uno M et al: Endothelial damage due to impaired nitric oxide bioavailability triggers cerebral aneurysm formation in female rats. J Hypertens 2009, 27(6):1284-1292.
97. Aoki T, Nishimura M, Kataoka H, Ishibashi R, Nozaki K, Hashimoto N: Reactive oxygen species modulate growth of cerebral aneurysms: a study using the free radical scavenger edaravone and p47phox(-/-) mice. Lab Invest 2009, 89(7):730-741.
98. Aoki T, Kataoka H, Shimamura M, Nakagami H, Wakayama K, Moriwaki T et al: NF-kappaB is a key mediator of cerebral aneurysm formation. Circulation 2007, 116(24):2830-2840.
99. Ali M, Jabbour P, Tjoumarkaris S, Gonzalez LF, Rosenwasser RH, Koch JH et al: Tumor Necrosis Factor-alpha Induces Phenotypic Modulation in Cerebral Vascular Smooth Muscle Cells via KLF4: Implications for Cerebral Aneurysm Pathology In: International Stroke Conference. 2012.
100. Ali M, Jabbour P, Tjoumarkaris S, Gonzalez LF, Rosenwasser RH, Koch JH et al: Regulation of Nox1 and Nox2 In Cerebral Vascular Smooth Muscle Cells: A Role of Oxidative Stress in Cerebral Aneurysm Formation In: Arteriosclerosis, Thrombosis, Vascular Biology 2012.
101. Marchese E, Vignati A, Albanese A, Nucci CG, Sabatino G, Tirpakova B et al: Comparative evaluation of genome-wide gene expression profiles in ruptured and unruptured human intracranial aneurysms. Journal of biological regulators and homeostatic agents, 24(2):185-195.
102. Roder C, Kasuya H, Harati A, Tatagiba M, Inoue I, Krischek B: Meta-analysis of microarray gene expression studies on intracranial aneurysms. Neuroscience, 201:105-113.
103. Pera J, Korostynski M, Krzyszkowski T, Czopek J, Slowik A, Dziedzic T et al: Gene expression profiles in human ruptured and unruptured intracranial aneurysms: what is the role of inflammation? Stroke, 41(2):224-231.
104. Li L, Yang X, Jiang F, Dusting GJ, Wu Z: Transcriptome-wide characterization of gene expression associated with unruptured intracranial aneurysms. Eur Neurol 2009, 62(6):330-337.
105. Krischek B, Kasuya H, Tajima A, Akagawa H, Sasaki T, Yoneyama T et al: Network-based gene expression analysis of intracranial aneurysm tissue reveals role of antigen presenting cells. Neuroscience 2008, 154(4):1398-1407.
106. Shi C, Awad IA, Jafari N, Lin S, Du P, Hage ZA et al: Genomics of human intracranial aneurysm wall. Stroke 2009, 40(4):1252-1261.
107. Kurki MI, Hakkinen SK, Frosen J, Tulamo R, von und zu Fraunberg M, Wong G et al: Upregulated signaling pathways in ruptured human saccular intracranial aneurysm wall: an emerging regulative role of Toll-like receptor signaling and nuclear factorkappaB, hypoxia-inducible factor-1A, and ETS transcription factors. Neurosurgery, 68(6):1667-1675; discussion 1675-1666.
108. Hasan D, Hashimoto T, Kung D, Macdonald RL, Winn HR, Heistad D: Upregulation of cyclooxygenase-2 (COX-2) and microsomal prostaglandin E2 synthase-1 (mPGES-1) in wall of ruptured human cerebral aneurysms: preliminary results. Stroke, 43(7):1964-1967.
109. Gaetani P, Pasqualin A, Rodriguez y Baena R, Borasio E, Marzatico F: Oxidative stress in the human brain after subarachnoid hemorrhage. J Neurosurg 1998, 89(5):748-754.
110. Lin CL, Hsu YT, Lin TK, Morrow JD, Hsu JC, Hsu YH et al: Increased levels of F2-isoprostanes following aneurysmal subarachnoid hemorrhage in humans. Free Radic Biol Med 2006, 40(8):1466-1473.
111. Marzatico F, Gaetani P, Tartara F, Bertorelli L, Feletti F, Adinolfi D et al: Antioxidant status and alpha1-antiproteinase activity in subarachnoid hemorrhage patients. Life Sci 1998, 63(10):821-826.
112. Okamoto K, Horisawa R: The joint effect of oxidative stress and antioxidants on the risk of an aneurysmal rupture subarachnoid hemorrhage: a case-control study in Japan. Ann Epidemiol 2007, 17(5):359-363.
113. Okamoto K: Habitual green tea consumption and risk of an aneurysmal rupture subarachnoid hemorrhage: a case-control study in Nagoya, Japan. Eur J Epidemiol 2006, 21(5):367-371.
114. Okamoto K, Horisawa R: Dietary antioxidant intake and risk of an aneurysmal rupture subarachnoid hemorrhage in Japan. Eur J Clin Nutr 2007, 61(9):1140-1142.
115. Lambeth JD, Krause KH, Clark RA: NOX enzymes as novel targets for drug development. Semin Immunopathol 2008, 30(3):339-363.