In Vitro Assessment of Tobacco Smoke Toxicity at the BBB: Do Antioxidant Supplements Have a Protective Role?

BMC Neuroscience

Volumn 12, Issue , 2011, Pages

  Hossain, Mohammed ^a   Mazzone, Peter ^a   Tierney, William ^b   Cucullo, Luca ^c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GELATINASE A; GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 6; NITRIC OXIDE; PADGEM PROTEIN; TOBACCO SMOKE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; ANTIOXIDANT; NEUROPROTECTIVE AGENT;

ARTICLE; BLOOD BRAIN BARRIER; CELL VIABILITY; CLINICAL ASSESSMENT; CYTOKINE RELEASE; ENZYME ACTIVITY; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LEUKOCYTE COUNT; LIPID PEROXIDATION; MACROPHAGE; MONOCYTE; NEUROPROTECTION; NEUTROPHIL; OXIDATIVE STRESS; VASCULAR ENDOTHELIUM; VITAMIN SUPPLEMENTATION; ASTROCYTE; CYTOLOGY; ENDOTHELIUM CELL; METABOLISM; PASSIVE SMOKING; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANTIOXIDANTS; ASTROCYTES; BLOOD-BRAIN BARRIER; CELL LINE, TUMOR; ENDOTHELIAL CELLS; HUMANS; MONOCYTES; NEUROPROTECTIVE AGENTS; TOBACCO SMOKE POLLUTION;

EID: 80053175211     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-12-92     Document Type: Article

References (97)

1. Adams MR, Jessup W, Celermajer DS. Cigarette smoking is associated with increased human monocyte adhesion to endothelial cells: reversibility with oral L-arginine but not vitamin C. J Am Coll Cardiol 1997, 29:491-497. 10.1016/S0735-1097(96)00537-2, 9060883.
2. Brennan JA, Boyle JO, Koch WM, Goodman SN, Hruban RH, Eby YJ, Couch MJ, Forastiere AA, Sidransky D. Association between cigarette smoking and mutation of the p53 gene in squamous-cell carcinoma of the head and neck. N Engl J Med 1995, 332:712-717. 10.1056/NEJM199503163321104, 7854378.
3. Chen HW, Chien ML, Chaung YH, Lii CK, Wang TS. Extracts from cigarette smoke induce DNA damage and cell adhesion molecule expression through different pathways. Chem Biol Interact 2004, 150:233-241. 10.1016/j.cbi.2004.09.014, 15560890.
4. Davis JW. Some acute effects of smoking on endothelial cells and platelets. Adv Exp Med Biol 1990, 273:107-118.
5. Freed BM, Ouyang Y, McCue JM. Mechanisms of altered transcription by cigarette smoke. Toxicol Sci 2001, 59:1-2. 10.1093/toxsci/59.1.1, 11134538.
6. Freeman DJ, Packard CJ. Smoking and plasma lipoprotein metabolism. Clin Sci (Lond) 1995, 89:333-342.
7. Henningfield JE, Stapleton JM, Benowitz NL, Grayson RF, London ED. Higher levels of nicotine in arterial than in venous blood after cigarette smoking. Drug Alcohol Depend 1993, 33:23-29. 10.1016/0376-8716(93)90030-T, 8370337.
8. Li XY, Rahman I, Donaldson K, MacNee W. Mechanisms of cigarette smoke induced increased airspace permeability. Thorax 1996, 51:465-471. 10.1136/thx.51.5.465, 473589, 8711672.
9. Morrison D, Rahman I, Lannan S, MacNee W. Epithelial permeability, inflammation, and oxidant stress in the air spaces of smokers. Am J Respir Crit Care Med 1999, 159:473-479.
10. Nagy J, Demaster EG, Wittmann I, Shultz P, Raij L. Induction of endothelial cell injury by cigarette smoke. Endothelium 1997, 5:251-263. 10.3109/10623329709052590, 9588817.
11. Noronha-Dutra AA, Epperlein MM, Woolf N. Effect of cigarette smoking on cultured human endothelial cells. Cardiovasc Res 1993, 27:774-778. 10.1093/cvr/27.5.774, 8394208.
12. Raij L, Demaster EG, Jaimes EA. Cigarette smoke-induced endothelium dysfunction: role of superoxide anion. J Hypertens 2001, 19:891-897. 10.1097/00004872-200105000-00009, 11393672.
13. Tsuchiya M, Asada A, Kasahara E, Sato EF, Shindo M, Inoue M. Smoking a single cigarette rapidly reduces combined concentrations of nitrate and nitrite and concentrations of antioxidants in plasma. Circulation 2002, 105:1155-1157. 10.1161/hc1002.105935, 11889006.
14. Howard G, Wagenknecht LE, Cai J, Cooper L, Kraut MA, Toole JF. Cigarette smoking and other risk factors for silent cerebral infarction in the general population. Stroke 1998, 29:913-917. 10.1161/01.STR.29.5.913, 9596234.
15. Shinton R, Beevers G. Meta-analysis of relation between cigarette smoking and stroke. BMJ 1989, 298:789-794. 10.1136/bmj.298.6676.789, 1836102, 2496858.
16. Mannami T, Iso H, Baba S, Sasaki S, Okada K, Konishi M, Tsugane S. Cigarette smoking and risk of stroke and its subtypes among middle-aged Japanese men and women: the JPHC Study Cohort I. Stroke 2004, 35:1248-1253. 10.1161/01.STR.0000128794.30660.e8, 15118170.
17. Miller GJ, Bauer KA, Cooper JA, Rosenberg RD. Activation of the coagulant pathway in cigarette smokers. Thromb Haemost 1998, 79:549-553.
18. Mast H, Thompson JL, Lin IF, Hofmeister C, Hartmann A, Marx P, Mohr JP, Sacco RL. Cigarette smoking as a determinant of high-grade carotid artery stenosis in Hispanic, black, and white patients with stroke or transient ischemic attack. Stroke 1998, 29:908-912. 10.1161/01.STR.29.5.908, 9596233.
19. Gill JS, Shipley MJ, Tsementzis SA, Hornby R, Gill SK, Hitchcock ER, Beevers DG. Cigarette smoking. A risk factor for hemorrhagic and nonhemorrhagic stroke. Arch Intern Med 1989, 149:2053-2057. 10.1001/archinte.149.9.2053, 2774782.
20. Epperlein MM, Nourooz-Zadeh J, Noronha-Dutra AA, Woolf N. Nitric oxide in cigarette smoke as a mediator of oxidative damage. Int J Exp Pathol 1996, 77:197-200.
21. Baldeiras I, Santana I, Proenca MT, Garrucho MH, Pascoal R, Rodrigues A, Duro D, Oliveira CR. Oxidative Damage and Progression to Alzheimer's Disease in Patients with Mild Cognitive Impairment. J Alzheimers Dis 2010,
22. Seet RC, Lee CY, Lim EC, Tan JJ, Quek AM, Chong WL, Looi WF, Huang SH, Wang H, Chan YH, et al. Oxidative damage in Parkinson disease: Measurement using accurate biomarkers. Free Radic Biol Med 2010, 48:560-566. 10.1016/j.freeradbiomed.2009.11.026, 19969070.
23. Dal Pizzol F, Ritter C, Cassol-Jr OJ, Rezin GT, Petronilho F, Zugno AI, Quevedo J, Streck EL. Oxidative mechanisms of brain dysfunction during sepsis. Neurochem Res 2010, 35:1-12. 10.1007/s11064-009-0043-4, 19680806.
24. Stangherlin EC, Luchese C, Ardais AP, Nogueira CW. Passive smoke exposure induces oxidative damage in brains of rat pups: Protective role of diphenyl diselenide. Inhal Toxicol 2009, 21:868-874. 10.1080/08958370802526881, 19225963.
25. Hossain M, Sathe T, Fazio V, Mazzone P, Weksler B, Janigro D, Rapp E, Cucullo L. Tobacco smoke: a critical etiological factor for vascular impairment at the blood-brain barrier. Brain Res 2009, 1287:192-205. 2831230, 19539613.
26. Schreibelt G, Kooij G, Reijerkerk A, van Doorn R, Gringhuis SI, van der PS, Weksler BB, Romero IA, Couraud PO, Piontek J, et al. Reactive oxygen species alter brain endothelial tight junction dynamics via RhoA, PI3 kinase, and PKB signaling. FASEB J 2007, 21:3666-3676. 10.1096/fj.07-8329com, 17586731.
27. Rao R. Oxidative stress-induced disruption of epithelial and endothelial tight junctions. Front Biosci 2008, 13:7210-7226.
28. Zou N, Hong J, Dai QY. Passive cigarette smoking induces inflammatory injury in human arterial walls. Chin Med J (Engl ) 2009, 122:444-448.
29. Westbrook DG, Anderson PG, Pinkerton KE, Ballinger SW. Perinatal tobacco smoke exposure increases vascular oxidative stress and mitochondrial damage in non-human primates. Cardiovasc Toxicol 2010, 10:216-226. 10.1007/s12012-010-9085-8, 2926475, 20668962.
30. Haorah J, Ramirez SH, Schall K, Smith D, Pandya R, Persidsky Y. Oxidative stress activates protein tyrosine kinase and matrix metalloproteinases leading to blood-brain barrier dysfunction. J Neurochem 2007, 101:566-576. 10.1111/j.1471-4159.2006.04393.x, 17250680.
31. Hutamekalin P, Farkas AE, Orbok A, Wilhelm I, Nagyoszi P, Veszelka S, Deli MA, Buzas K, Hunyadi-Gulyas E, Medzihradszky KF, et al. Effect of nicotine and polyaromtic hydrocarbons on cerebral endothelial cells. Cell Biol Int 2008, 32:198-209. 10.1016/j.cellbi.2007.08.026, 17920942.
32. Pun PB, Lu J, Moochhala S. Involvement of ROS in BBB dysfunction. Free Radic Res 2009, 43:348-364. 10.1080/10715760902751902, 19241241.
33. Van der GA, Wouters D, Van Der Pol SM, Huizinga R, Ronken E, Adamson P, Greenwood J, Dijkstra CD, de Vries HE. Reactive oxygen species enhance the migration of monocytes across the blood-brain barrier in vitro. FASEB J 2001, 15:1852-1854.
34. Whincup PH, Gilg JA, Emberson JR, Jarvis MJ, Feyerabend C, Bryant A, Walker M, Cook DG. Passive smoking and risk of coronary heart disease and stroke: prospective study with cotinine measurement. BMJ 2004, 329:200-205. 10.1136/bmj.38146.427188.55, 487731, 15229131.
35. Paulson JR, Yang T, Selvaraj PK, Mdzinarishvili A, Van der Schyf CJ, Klein J, Bickel U, Abbruscato TJ. Nicotine exacerbates brain edema during in vitro and in vivo focal ischemic conditions. J Pharmacol Exp Ther 2010, 332:371-379. 10.1124/jpet.109.157776, 2812118, 19889792.
36. Djordjevic VB. Free radicals in cell biology. Int Rev Cytol 2004, 237:57-89.
37. Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol 2010, 38:96-109. 10.1177/0192623309356453, 20019356.
38. Kong Q, Lin CL. Oxidative damage to RNA: mechanisms, consequences, and diseases. Cell Mol Life Sci 2010, 67:1817-1829. 10.1007/s00018-010-0277-y, 3010397, 20148281.
39. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: How are they linked?. Free Radic Biol Med 2010,
40. Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009, 7:65-74. 10.2174/157015909787602823, 2724665, 19721819.
41. Tabet N, Mantle D, Orrell M. Free radicals as mediators of toxicity in Alzheimer's disease: a review and hypothesis. Adverse Drug React Toxicol Rev 2000, 19:127-152.
42. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J. Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 2004, 266:37-56.
43. Pryor WA, Stone K, Zang LY, Bermudez E. Fractionation of aqueous cigarette tar extracts: fractions that contain the tar radical cause DNA damage. Chem Res Toxicol 1998, 11:441-448. 10.1021/tx970159y, 9585474.
44. DeMarini DM. Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res 2004, 567:447-474. 10.1016/j.mrrev.2004.02.001, 15572290.
45. Fang YZ, Yang S, Wu G. Free radical homeostasis. Sheng Li Ke Xue Jin Zhan 2004, 35:199-204.
46. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007, 39:44-84. 10.1016/j.biocel.2006.07.001, 16978905.
47. Varela-Carver A, Parker H, Kleinert C, Rimoldi O. Adverse effects of cigarette smoke and induction of oxidative stress in cardiomyocytes and vascular endothelium. Curr Pharm Des 2010, 16:2551-2558. 10.2174/138161210792062830, 20550505.
48. Valavanidis A, Vlachogianni T, Fiotakis K. Tobacco smoke: involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. Int J Environ Res Public Health 2009, 6:445-462. 10.3390/ijerph6020445, 2672368, 19440393.
49. Pryor WA, Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci 1993, 686:12-27. 10.1111/j.1749-6632.1993.tb39148.x, 8512242.
50. Sobczak A, Golka D, Szoltysek-Boldys I. The effects of tobacco smoke on plasma alpha- and gamma-tocopherol levels in passive and active cigarette smokers. Toxicol Lett 2004, 151:429-437. 10.1016/j.toxlet.2004.03.010, 15261987.
51. Dietrich M, Block G, Norkus EP, Hudes M, Traber MG, Cross CE, Packer L. Smoking and exposure to environmental tobacco smoke decrease some plasma antioxidants and increase gamma-tocopherol in vivo after adjustment for dietary antioxidant intakes. Am J Clin Nutr 2003, 77:160-166.
52. Willcox JK, Ash SL, Catignani GL. Antioxidants and prevention of chronic disease. Crit Rev Food Sci Nutr 2004, 44:275-295. 10.1080/10408690490468489, 15462130.
53. Kelly G. The interaction of cigarette smoking and antioxidants. Part III: ascorbic acid. Altern Med Rev 2003, 8:43-54.
54. Kelly GS. The interaction of cigarette smoking and antioxidants. Part 2: alpha-tocopherol. Altern Med Rev 2002, 7:500-511.
55. Kelly GS. The interaction of cigarette smoking and antioxidants. Part I: diet and carotenoids. Altern Med Rev 2002, 7:370-388.
56. Traber MG, van d V, Reznick AZ, Cross CE. Tobacco-related diseases. Is there a role for antioxidant micronutrient supplementation?. Clin Chest Med 2000, 21:173-87. x., 10.1016/S0272-5231(05)70016-2, 10763098.
57. Preedy VR, Watson RR, Sherma Z. 2010, Humana Press.
58. Johnston CS, Martin LJ, Cai X. Antihistamine effect of supplemental ascorbic acid and neutrophil chemotaxis. J Am Coll Nutr 1992, 11:172-176.
59. van Horssen J, Schreibelt G, Drexhage J, Hazes T, Dijkstra CD, van d V, de Vries HE. Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 2008, 45:1729-1737. 10.1016/j.freeradbiomed.2008.09.023, 18930811.
60. Montecinos V, Guzman P, Barra V, Villagran M, Munoz-Montesino C, Sotomayor K, Escobar E, Godoy A, Mardones L, Sotomayor P, et al. Vitamin C is an essential antioxidant that enhances survival of oxidatively stressed human vascular endothelial cells in the presence of a vast molar excess of glutathione. J Biol Chem 2007, 282:15506-15515. 10.1074/jbc.M608361200, 17403685.
61. Smith AR, Visioli F, Hagen TM. Vitamin C matters: increased oxidative stress in cultured human aortic endothelial cells without supplemental ascorbic acid. FASEB J 2002, 16:1102-1104.
62. Panda K, Chattopadhyay R, Ghosh MK, Chattopadhyay DJ, Chatterjee IB. Vitamin C prevents cigarette smoke induced oxidative damage of proteins and increased proteolysis. Free Radic Biol Med 1999, 27:1064-1079. 10.1016/S0891-5849(99)00154-9, 10569639.
63. van Dam B, van Hinsbergh VW, Stehouwer CD, Versteilen A, Dekker H, Buytenhek R, Princen HM, Schalkwijk CG. Vitamin E inhibits lipid peroxidation-induced adhesion molecule expression in endothelial cells and decreases soluble cell adhesion molecules in healthy subjects. Cardiovasc Res 2003, 57:563-571. 10.1016/S0008-6363(02)00699-5, 12566129.
64. Wagner BA, Buettner GR, Burns CP. Vitamin E slows the rate of free radical-mediated lipid peroxidation in cells. Arch Biochem Biophys 1996, 334:261-267. 10.1006/abbi.1996.0454, 8900400.
65. Brown KM, Morrice PC, Duthie GG. Vitamin E supplementation suppresses indexes of lipid peroxidation and platelet counts in blood of smokers and nonsmokers but plasma lipoprotein concentrations remain unchanged. Am J Clin Nutr 1994, 60:383-387.
66. Cucullo L, Hossain M, Rapp E, Manders T, Janigro D. Development of a humanized in vitro blood-brain barrier model to screen for brain penetration of antiepileptic drugs. Epilepsia 2006,
67. Cucullo L, McAllister M, Kight K, Krizanac-Bengez L, Marroni M, Mayberg M, Stanness K, Janigro D. A new dynamic in vitro model for the multidimensional study of astrocyte-endothelial cell interactions at the blood-brain barrier. Brain Res 2002, 951:243. 10.1016/S0006-8993(02)03167-0, 12270503.
68. Santaguida S, Janigro D, Hossain M, Oby E, Rapp E, Cucullo L. Side by side comparison between dynamic versus static models of blood-brain barrier in vitro: A permeability study. Brain Res 2006, 1109:1-13. 10.1016/j.brainres.2006.06.027, 16857178.
69. Nakayama T, Church DF, Pryor WA. Quantitative analysis of the hydrogen peroxide formed in aqueous cigarette tar extracts. Free Radic Biol Med 1989, 7:9-15. 10.1016/0891-5849(89)90094-4, 2753397.
70. Takanami Y, Moriyama T, Kosaka Y, Nakayama T. Analysis of hydrogen peroxide in an aqueous extract of cigarette smoke and effect of pH on the yield. Biosci Biotechnol Biochem 2009, 73:2222-2225. 10.1271/bbb.90324, 19809177.
71. Cucullo L, Hossain M, Puvenna V, Marchi N, Janigro D. The role of shear stress in Blood-Brain Barrier endothelial physiology. BMC Neurosci 2011, 12:40. 10.1186/1471-2202-12-40, 3103473, 21569296.
72. Bernacki J, Dobrowolska A, Nierwinska K, Malecki A. Physiology and pharmacological role of the blood-brain barrier. Pharmacol Rep 2008, 60:600-622.
73. Weiss N, Miller F, Cazaubon S, Couraud PO. The blood-brain barrier in brain homeostasis and neurological diseases. Biochim Biophys Acta 2009, 1788:842-857. 10.1016/j.bbamem.2008.10.022, 19061857.
74. Abbott NJ, Revest PA, Romero IA. Astrocyte-endothelial interaction: physiology and pathology. Neuropathol Appl Neurobiol 1992, 18:424-433. 10.1111/j.1365-2990.1992.tb00808.x, 1454132.
75. Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 2009,
76. Vajdovich P. Free radicals and antioxidants in inflammatory processes and ischemia-reperfusion injury. Vet Clin North Am Small Anim Pract 2008, 38:31-123. v., 10.1016/j.cvsm.2007.11.008, 18249244.
77. Khanna AK, Xu J, Uber PA, Burke AP, Baquet C, Mehra MR. Tobacco smoke exposure in either the donor or recipient before transplantation accelerates cardiac allograft rejection, vascular inflammation, and graft loss. Circulation 2009, 120:1814-1821. 10.1161/CIRCULATIONAHA.108.840223, 19841304.
78. Nordskog BK, Blixt AD, Morgan WT, Fields WR, Hellmann GM. Matrix-degrading and pro-inflammatory changes in human vascular endothelial cells exposed to cigarette smoke condensate. Cardiovasc Toxicol 2003, 3:101-117. 10.1385/CT:3:2:101, 14501029.
79. Masubuchi T, Koyama S, Sato E, Takamizawa A, Kubo K, Sekiguchi M, Nagai S, Izumi T. Smoke extract stimulates lung epithelial cells to release neutrophil and monocyte chemotactic activity. Am J Pathol 1998, 153:1903-1912. 10.1016/S0002-9440(10)65704-5, 1866325, 9846980.
80. Verma S, Wang CH, Li SH, Dumont AS, Fedak PW, Badiwala MV, Dhillon B, Weisel RD, Li RK, Mickle DA, et al. A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis. Circulation 2002, 106:913-919. 10.1161/01.CIR.0000029802.88087.5E, 12186793.
81. Rahman I, MacNee W. Role of oxidants/antioxidants in smoking-induced lung diseases. Free Radic Biol Med 1996, 21:669-681. 10.1016/0891-5849(96)00155-4, 8891669.
82. Pincemail J, Vanbelle S, Degrune F, Cheramy-Bien JP, Charlier C, Chapelle JP, Giet D, Collette G, Albert A, Defraigne JO. Lifestyle Behaviours and Plasma Vitamin C and beta-Carotene Levels from the ELAN Population (Liege, Belgium). J Nutr Metab 2011, 2011:494370. 3062067, 21437178.
83. Sharma MK, Buettner GR. Interaction of vitamin C and vitamin E during free radical stress in plasma: an ESR study. Free Radic Biol Med 1993, 14:649-653. 10.1016/0891-5849(93)90146-L, 8392021.
84. Abbruscato TJ, Lopez SP, Mark KS, Hawkins BT, Davis TP. Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. J Pharm Sci 2002, 91:2525-2538. 10.1002/jps.10256, 12434396.
85. Darley-Usmar VM, Hogg N, O'Leary VJ, Wilson MT, Moncada S. The simultaneous generation of superoxide and nitric oxide can initiate lipid peroxidation in human low density lipoprotein. Free Radic Res Commun 1992, 17:9-20. 10.3109/10715769209061085, 1332919.
86. Su Y, Han W, Giraldo C, De Li Y, Block ER. Effect of cigarette smoke extract on nitric oxide synthase in pulmonary artery endothelial cells. Am J Respir Cell Mol Biol 1998, 19:819-825.
87. Toda N, Toda H. Nitric oxide-mediated blood flow regulation as affected by smoking and nicotine. Eur J Pharmacol 2010, 649:1-13. 10.1016/j.ejphar.2010.09.042, 20868673.
88. Leone A. Does Smoking Act as a Friend or Enemy of Blood Pressure? Let Release Pandora's Box. Cardiol Res Pract 2011, 2011:264894. 3034987, 21318159.
89. Chalon S, Moreno H, Benowitz NL, Hoffman BB, Blaschke TF. Nicotine impairs endothelium-dependent dilatation in human veins in vivo. Clin Pharmacol Ther 2000, 67:391-397. 10.1067/mcp.2000.105153, 10801248.
90. Jensen EX, Fusch C, Jaeger P, Peheim E, Horber FF. Impact of chronic cigarette smoking on body composition and fuel metabolism. J Clin Endocrinol Metab 1995, 80:2181-2185. 10.1210/jc.80.7.2181, 7608276.
91. Gorman D, Drewry A, Huang YL, Sames C. The clinical toxicology of carbon monoxide. Toxicology 2003, 187:25-38. 10.1016/S0300-483X(03)00005-2, 12679050.
92. Stoller KP. Hyperbaric oxygen and carbon monoxide poisoning: a critical review. Neurol Res 2007, 29:146-155. 10.1179/016164107X181770, 17439699.
93. Shimosegawa E, Hatazawa J, Nagata K, Okudera T, Inugami A, Ogawa T, Fujita H, Itoh H, Kanno I, Uemura K. Cerebral blood flow and glucose metabolism measurements in a patient surviving one year after carbon monoxide intoxication. J Nucl Med 1992, 33:1696-1698.
94. Rizzo MR, Abbatecola AM, Barbieri M, Vietri MT, Cioffi M, Grella R, Molinari A, Forsey R, Powell J, Paolisso G. Evidence for anti-inflammatory effects of combined administration of vitamin E and C in older persons with impaired fasting glucose: impact on insulin action. J Am Coll Nutr 2008, 27:505-511.
95. Meyer J, Tauh J, Galla HG. The susceptibility of cerebral endothelial cells to astroglial induction of blood-brain barrier enzymes depends on their proliferative state. J Neurochem 1991, 57:1971-1977. 10.1111/j.1471-4159.1991.tb06411.x, 1719132.
96. Barth A, Newell DW, Nguyen LB, Winn HR, Wender R, Meno JR, Janigro D. Neurotoxicity in organotypic hippocampal slices mediated by adenosine analogues and nitric oxide. Brain Res 1997, 762:79-88. 10.1016/S0006-8993(97)00348-X, 9262161.
97. Janigro D, Nguyen TS, Gordon EL, Winn HR. Physiological properties of ATP-activated cation channels in rat brain microvascular endothelial cells. Am J Physiol 1996, 270:H1423-H1434.