DOI QR코드

DOI QR Code

Loss of Integrity: Impairment of the Blood-brain Barrier in Heavy Metal-associated Ischemic Stroke

  • 투고 : 2013.08.30
  • 심사 : 2013.09.23
  • 발행 : 2013.09.30

초록

Although stroke is one of the leading causes of death and disability worldwide, preventive or therapeutic options are still limited. Therefore, a better understanding of the pathophysiological characteristics of this life-threatening disease is urgently needed. The incidence and prevalence of ischemic stroke are increased by exposure to certain types of xenobiotics, including heavy metals, suggesting the possible toxicological contribution of these compounds to the onset or aggravation of stroke. Among the potential targets, we have focused on alterations to cerebral endothelial cells (CECs), which play important roles in maintaining the functional integrity of brain tissue.

키워드

참고문헌

  1. O'Donnell, M.J., Xavier, D., Liu, L., Zhang, H., Chin, S.L., Rao-Melacini, P., Rangarajan, S., Islam, S., Pais, P., Mcqueen, M.J., Mondo, C., Damasceno, A., Lopez-Jaramillo, P., Hankey, G.J., Dans, A.L., Yusoff, K., Truelsen, T., Diener, H.C., Sacco, R.L., Ryglewicz, D., Czlonkowska, A., Weimar, C., Wang, X., Yusuf, S. and Investigators, I. (2010) Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet, 376, 112-123. https://doi.org/10.1016/S0140-6736(10)60834-3
  2. Fisher, M. (2011) New approaches to neuroprotective drug development. Stroke, 42, S24-S27. https://doi.org/10.1161/STROKEAHA.110.592394
  3. Savitz, S.I. and Fisher, M. (2007) Future of neuroprotection for acute stroke: in the aftermath of the SAINT trials. Ann. Neurol., 61, 396-402. https://doi.org/10.1002/ana.21127
  4. Roger, V.L., Go, A.S., Lloyd-Jones, D.M., Benjamin, E.J., Berry, J.D., Borden, W.B., Bravata, D.M., Dai, S., Ford, E.S., Fox, C.S., Fullerton, H.J., Gillespie, C., Hailpern, S.M., Heit, J.A., Howard, V.J., Kissela, B.M., Kittner, S.J., Lackland, D.T., Lichtman, J.H., Lisabeth, L.D., Makuc, D.M., Marcus, G.M., Marelli, A., Matchar, D.B., Moy, C.S., Mozaffarian, D., Mussolino, M.E., Nichol, G., Paynter, N.P., Soliman, E.Z., Sorlie, P.D., Sotoodehnia, N., Turan, T.N., Virani, S.S., Wong, N.D., Woo, D., Turner, M.B.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2012) Heart disease and stroke statistics--2012 update: a report from the American Heart Association. Circulation, 125, e2-e220. https://doi.org/10.1161/CIR.0b013e318245fac5
  5. Lo, E.H., Dalkara, T. and Moskowitz, M.A. (2003) Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosci., 4, 399-415.
  6. Dirnagl, U., Iadecola, C. and Moskowitz, M.A. (1999) Patho-biology of ischaemic stroke: an integrated view. Trends Neurosci., 22, 391-397. https://doi.org/10.1016/S0166-2236(99)01401-0
  7. Macdonald, J.F., Xiong, Z.G. and Jackson, M.F. (2006) Paradox of Ca2+ signaling, cell death and stroke. Trends Neurosci., 29, 75-81. https://doi.org/10.1016/j.tins.2005.12.001
  8. Graham, S.H. and Chen, J. (2001) Programmed cell death in cerebral ischemia. J. Cereb. Blood Flow Metab., 21, 99-109. https://doi.org/10.1097/00004647-200102000-00001
  9. Lo, E.H., Moskowitz, M.A. and Jacobs, T.P. (2005) Exciting, radical, suicidal: how brain cells die after stroke. Stroke, 36, 189-192. https://doi.org/10.1161/01.STR.0000153069.96296.fd
  10. Green, A.R. (2008) Pharmacological approaches to acute ischaemic stroke: reperfusion certainly, neuroprotection possibly. Br. J. Pharmacol., 153 Suppl 1, S325-S338.
  11. del Zoppo, G.J. (2006) Stroke and neurovascular protection. N. Engl. J. Med., 354, 553-555. https://doi.org/10.1056/NEJMp058312
  12. Ballabh, P., Braun, A. and Nedergaard, M. (2004) The bloodbrain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis., 16, 1-13. https://doi.org/10.1016/j.nbd.2003.12.016
  13. Lai, C.H., Kuo, K.H. and Leo, J.M. (2005) Critical role of actin in modulating BBB permeability. Brain Res. Brain Res. Rev., 50, 7-13. https://doi.org/10.1016/j.brainresrev.2005.03.007
  14. Wolburg, H. and Lippoldt, A. (2002) Tight junctions of the blood-brain barrier: development, composition and regulation. Vasc. Pharmacol., 38, 323-337. https://doi.org/10.1016/S1537-1891(02)00200-8
  15. Matter, K. and Balda, M.S. (2003) Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol., 4, 225-236. https://doi.org/10.1038/nrm1055
  16. Hawkins, B.T. and Davis, T.P. (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev., 57, 173-185. https://doi.org/10.1124/pr.57.2.4
  17. Oldendorf, W.H., Cornford, M.E. and Brown, W.J. (1977) The large apparent work capability of the blood-brain barrier: a study of the mitochondrial content of capillary endothelial cells in brain and other tissues of the rat. Ann. Neurol., 1, 409-417. https://doi.org/10.1002/ana.410010502
  18. del Zoppo, G.J. and Mabuchi, T. (2003) Cerebral microvessel responses to focal ischemia. J. Cereb. Blood Flow Metab., 23, 879-894. https://doi.org/10.1097/01.WCB.0000078322.96027.78
  19. Petty, M.A. and Wettstein, J.G. (2001) Elements of cerebral microvascular ischaemia. Brain Res. Brain Res. Rev., 36, 23-34. https://doi.org/10.1016/S0165-0173(01)00062-5
  20. Mark, K.S. and Davis, T.P. (2002) Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am. J. Physiol. Heart Circ. Physiol., 282, H1485-H1494. https://doi.org/10.1152/ajpheart.00645.2001
  21. Denes, A., Ferenczi, S. and Kovacs, K.J. (2011) Systemic inflammatory challenges compromise survival after experimental stroke via augmenting brain inflammation, bloodbrain barrier damage and brain oedema independently of infarct size. J. Neuroinflammation, 8, 164. https://doi.org/10.1186/1742-2094-8-164
  22. Kahles, T., Luedike, P., Endres, M., Galla, H.J., Steinmetz, H., Busse, R., Neumann-Haefelin, T. and Brandes, R.P. (2007) NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke, 38, 3000-3006. https://doi.org/10.1161/STROKEAHA.107.489765
  23. Belayev, L., Busto, R., Zhao, W. and Ginsberg, M.D. (1996) Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res., 739, 88-96. https://doi.org/10.1016/S0006-8993(96)00815-3
  24. Strbian, D., Durukan, A., Pitkonen, M., Marinkovic, I., Tatlisumak, E., Pedrono, E., Abo-Ramadan, U. and Tatlisumak, T. (2008) The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience, 153, 175-181. https://doi.org/10.1016/j.neuroscience.2008.02.012
  25. Abo-Ramadan, U., Durukan, A., Pitkonen, M., Marinkovic, I., Tatlisumak, E., Pedrono, E., Soinne, L., Strbian, D. and Tatlisumak, T. (2009) Post-ischemic leakiness of the bloodbrain barrier: a quantitative and systematic assessment by Patlak plots. Exp. Neurol., 219, 328-333. https://doi.org/10.1016/j.expneurol.2009.06.002
  26. Sandoval, K.E. and Witt, K.A. (2008) Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol. Dis., 32, 200-219. https://doi.org/10.1016/j.nbd.2008.08.005
  27. Rosenberg, G.A., Estrada, E.Y. and Dencoff, J.E. (1998) Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke, 29, 2189-2195. https://doi.org/10.1161/01.STR.29.10.2189
  28. Ramos-Fernandez, M., Bellolio, M.F. and Stead, L.G. (2011) Matrix metalloproteinase-9 as a marker for acute ischemic stroke: a systematic review. J. Stroke Cerebrovasc. Dis., 20, 47-54. https://doi.org/10.1016/j.jstrokecerebrovasdis.2009.10.008
  29. Cunningham, L.A., Wetzel, M. and Rosenberg, G.A. (2005) Multiple roles for MMPs and TIMPs in cerebral ischemia. Glial, 50, 329-339. https://doi.org/10.1002/glia.20169
  30. Koto, T., Takubo, K., Ishida, S., Shinoda, H., Inoue, M., Tsubota, K., Okada, Y. and Ikeda, E. (2007) Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells. Am. J. Pathol., 170, 1389-1397. https://doi.org/10.2353/ajpath.2007.060693
  31. Song, L., Ge, S. and Pachter, J.S. (2007) Caveolin-1 regulates expression of junction-associated proteins in brain microvascular endothelial cells. Blood, 109, 1515-1523. https://doi.org/10.1182/blood-2006-07-034009
  32. Liu, J., Jin, X., Liu, K.J. and Liu, W. (2012) Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. J. Neurosci., 32, 3044-3057. https://doi.org/10.1523/JNEUROSCI.6409-11.2012
  33. Fischer, S., Wobben, M., Marti, H.H., Renz, D. and Schaper, W. (2002) Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc. Res., 63, 70-80. https://doi.org/10.1006/mvre.2001.2367
  34. Andras, I.E., Deli, M.A., Veszelka, S., Hayashi, K., Hennig, B. and Toborek, M. (2007) The NMDA and AMPA/KA receptors are involved in glutamate-induced alterations of occludin expression and phosphorylation in brain endothelial cells. J. Cereb. Blood Flow Metab., 27, 1431-1443. https://doi.org/10.1038/sj.jcbfm.9600445
  35. Zlokovic, B.V. (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron, 57, 178-201. https://doi.org/10.1016/j.neuron.2008.01.003
  36. Gasche, Y., Copin, J.C., Sugawara, T., Fujimura, M. and Chan, P.H. (2001) Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab., 21, 1393-1400. https://doi.org/10.1097/00004647-200112000-00003
  37. Heo, J.H., Han, S.W. and Lee, S.K. (2005) Free radicals as triggers of brain edema formation after stroke. Free Radical Biol. Med., 39, 51-70. https://doi.org/10.1016/j.freeradbiomed.2005.03.035
  38. Rosenberg, G.A. and Yang, Y. (2007) Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cere bral ischemia. Neurosurg. Focus, 22, E4.
  39. Kastrup, A., Groschel, K., Ringer, T.M., Redecker, C., Cordesmeyer, R., Witte, O.W. and Terborg, C. (2008) Early disruption of the blood-brain barrier after thrombolytic therapy predicts hemorrhage in patients with acute stroke. Stroke, 39, 2385-2387. https://doi.org/10.1161/STROKEAHA.107.505420
  40. Krysl, D., Deykun, K., Lambert, L., Pokorny, J. and Mares, J. (2012) Perifocal and remote blood-brain barrier disruption in cortical photothrombotic ischemic lesion and its modulation by the choice of anesthesia. J. Physiol. Pharmacol., 63, 127-132.
  41. Fagan, S.C., Hess, D.C., Hohnadel, E.J., Pollock, D.M. and Ergul, A. (2004) Targets for vascular protection after acute ischemic stroke. Stroke, 35, 2220-2225. https://doi.org/10.1161/01.STR.0000138023.60272.9e
  42. Ivens, S., Kaufer, D., Flores, L.P., Bechmann, I., Zumsteg, D., Tomkins, O., Seiffert, E., Heinemann, U. and Friedman, A. (2007) TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain, 130, 535-547. https://doi.org/10.1093/brain/awl317
  43. Seiffert, E., Dreier, J.P., Ivens, S., Bechmann, I., Tomkins, O., Heinemann, U. and Friedman, A. (2004) Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J. Neurosci., 24, 7829-7836. https://doi.org/10.1523/JNEUROSCI.1751-04.2004
  44. Bernal-Pacheco, O. and Roman, G.C. (2007) Environmental vascular risk factors: new perspectives for stroke prevention. J. Neurol. Sci., 262, 60-70. https://doi.org/10.1016/j.jns.2007.06.026
  45. Mateen, F.J. and Brook, R.D. (2011) Air pollution as an emerging global risk factor for stroke. JAMA, 305, 1240-1241. https://doi.org/10.1001/jama.2011.352
  46. Kromhout, D. (1988) Blood lead and coronary heart disease risk among elderly men in Zutphen, The Netherlands. Environ. Health Perspect., 78, 43-46. https://doi.org/10.1289/ehp.887843
  47. Elliott, P., Arnold, R., Cockings, S., Eaton, N., Jarup, L., Jones, J., Quinn, M., Rosato, M., Thornton, I., Toledano, M., Tristan, E. and Wakefield, J. (2000) Risk of mortality, cancer incidence, and stroke in a population potentially exposed to cadmium. Occup. Environ. Med., 57, 94-97. https://doi.org/10.1136/oem.57.2.94
  48. Moller, L. and Kristensen, T.S. (1992) Blood lead as a cardiovascular risk factor. Am. J. Epidemiol., 136, 1091-1100. https://doi.org/10.1093/oxfordjournals.aje.a116574
  49. Schober, S.E., Mirel, L.B., Graubard, B.I., Brody, D.J. and Flegal, K.M. (2006) Blood lead levels and death from all causes, cardiovascular disease, and cancer: results from the NHANES III mortality study. Environ. Health Perspect., 114, 1538-1541.
  50. Navas-Acien, A., Selvin, E., Sharrett, A.R., Calderon-Aranda, E., Silbergeld, E. and Guallar, E. (2004) Lead, cadmium, smoking, and increased risk of peripheral arterial disease. Circulation, 109, 3196-3201. https://doi.org/10.1161/01.CIR.0000130848.18636.B2
  51. Menke, A., Muntner, P., Batuman, V., Silbergeld, E.K. and Guallar, E. (2006) Blood lead below 0.48 micromol/L (10 microg/dL) and mortality among US adults. Circulation, 114, 1388-1394. https://doi.org/10.1161/CIRCULATIONAHA.106.628321
  52. Lustberg, M. and Silbergeld, E. (2002) Blood lead levels and mortality. Arch. Intern. Med., 162, 2443-2449. https://doi.org/10.1001/archinte.162.21.2443
  53. Peters, J.L., Perlstein, T.S., Perry, M.J., Mcneely, E. and Weuve, J. (2010) Cadmium exposure in association with history of stroke and heart failure. Environ. Res., 110, 199-206. https://doi.org/10.1016/j.envres.2009.12.004
  54. Garcia Gomez, M., Boffetta, P., Caballero Klink, J.D., Espanol, S. and Gomez Quintana, J. (2007) [Cardiovascular mortality in mercury miners]. Med. Clin. (Barcelona), 128, 766-771. https://doi.org/10.1157/13106327
  55. Lisabeth, L.D., Ahn, H.J., Chen, J.J., Sealy-Jefferson, S., Burke, J.F. and Meliker, J.R. (2010) Arsenic in drinking water and stroke hospitalizations in Michigan. Stroke, 41, 2499-2504. https://doi.org/10.1161/STROKEAHA.110.585281
  56. Chiou, H.Y., Huang, W.I., Su, C.L., Chang, S.F., Hsu, Y.H. and Chen, C.J. (1997) Dose-response relationship between prevalence of cerebrovascular disease and ingested inorganic arsenic. Stroke, 28, 1717-1723. https://doi.org/10.1161/01.STR.28.9.1717
  57. Dietrich, W.D., Alonso, O. and Busto, R. (1993) Moderate hyperglycemia worsens acute blood-brain barrier injury after forebrain ischemia in rats. Stroke, 24, 111-116. https://doi.org/10.1161/01.STR.24.1.111
  58. Chi, O.Z., Hunter, C., Liu, X. and Weiss, H.R. (2009) Effects of exogenous excitatory amino acid neurotransmitters on blood-brain barrier disruption in focal cerebral ischemia. Neurochem. Res., 34, 1249-1254. https://doi.org/10.1007/s11064-008-9902-7
  59. Zheng, W., Aschner, M. and Ghersi-Egea, J.F. (2003) Brain barrier systems: a new frontier in metal neurotoxicological research. Toxicol. Appl. Pharmacol., 192, 1-11. https://doi.org/10.1016/S0041-008X(03)00251-5
  60. Goldstein, G.W., Asbury, A.K. and Diamond, I. (1974) Pathogenesis of lead encephalopathy. Uptake of lead and reaction of brain capillaries. Arch. Neurol., 31, 382-389. https://doi.org/10.1001/archneur.1974.00490420048005
  61. Struzynska, L., Walski, M., Gadamski, R., Dabrowska-Bouta, B. and Rafalowska, U. (1997) Lead-induced abnormalities in blood-brain barrier permeability in experimental chronic toxicity. Mol. Chem. Neuropathol., 31, 207-224. https://doi.org/10.1007/BF02815125
  62. Toews, A.D., Kolber, A., Hayward, J., Krigman, M.R. and Morell, P. (1978) Experimental lead encephalopathy in the suckling rat: concentration of lead in cellular fractions enriched in brain capillaries. Brain Res., 147, 131-138. https://doi.org/10.1016/0006-8993(78)90777-1
  63. Dyatlov, V.A., Platoshin, A.V., Lawrence, D.A. and Carpenter, D.O. (1998) Lead potentiates cytokine- and glutamatemediated increases in permeability of the blood-brain barrier. Neurotoxicology, 19, 283-291.
  64. Shukla, A., Shukla, G.S. and Srimal, R.C. (1996) Cadmiuminduced alterations in blood-brain barrier permeability and its possible correlation with decreased microvessel antioxidant potential in rat. Hum. Exp. Toxicol., 15, 400-405. https://doi.org/10.1177/096032719601500507
  65. Jung, Y.S., Jeong, E.M., Park, E.K., Kim, Y.M., Sohn, S., Lee, S.H., Baik, E.J. and Moon, C.H. (2008) Cadmium induces apoptotic cell death through p38 MAPK in brain microvessel endothelial cells. Eur. J. Pharmacol., 578, 11-18. https://doi.org/10.1016/j.ejphar.2007.08.049
  66. Jeong, E.M., Moon, C.H., Kim, C.S., Lee, S.H., Baik, E.J., Moon, C.K. and Jung, Y.S. (2004) Cadmium stimulates the expression of ICAM-1 via NF-kappaB activation in cerebrovascular endothelial cells. Biochem. Biophys. Res. Commun., 320, 887-892. https://doi.org/10.1016/j.bbrc.2004.05.218
  67. Clarkson, T.W. (1993) Mercury: major issues in environmental health. Environ. Health Perspect., 100, 31-38. https://doi.org/10.1289/ehp.9310031
  68. Peterson, E.W. and Cardoso, E.R. (1983) The blood-brain barrier following experimental subarachnoid hemorrhage. Part 2: Response to mercuric chloride infusion. J. Neurosurg., 58, 345-351. https://doi.org/10.3171/jns.1983.58.3.0345
  69. Chiou, J.M., Wang, S.L., Chen, C.J., Deng, C.R., Lin, W. and Tai, T.Y. (2005) Arsenic ingestion and increased microvascular disease risk: observations from the south-western arseniasis-endemic area in Taiwan. Int. J. Epidemiol., 34, 936-943. https://doi.org/10.1093/ije/dyi108
  70. Chen, S.C., Tsai, M.H., Wang, H.J., Yu, H.S. and Chang, L.W. (2004) Vascular permeability alterations induced by arsenic. Hum. Exp. Toxicol., 23, 1-7. https://doi.org/10.1191/0960327104ht407oa
  71. Reyes, J.L., Molina-Jijon, E., Rodriguez-Munoz, R., Bautista-Garcia, P., Debray-Garcia, Y. and Namorado Mdel, C. (2013) Tight junction proteins and oxidative stress in heavy metalsinduced nephrotoxicity. Biomed. Res. Int., 2013, 730789.
  72. Wong, E.W. and Cheng, C.Y. (2011) Impacts of environmental toxicants on male reproductive dysfunction. Trends Pharmacol. Sci., 32, 290-299. https://doi.org/10.1016/j.tips.2011.01.001

피인용 문헌

  1. Impact of commercial cigarette smoke condensate on brain tissue co-cultured with astrocytes and blood–brain barrier endothelial cells vol.80, pp.10-12, 2017, https://doi.org/10.1080/15287394.2017.1355863
  2. Role of Autophagy in Endothelial Damage and Blood–Brain Barrier Disruption in Ischemic Stroke vol.49, pp.6, 2018, https://doi.org/10.1161/STROKEAHA.117.017287
  3. Chronic Oral Arsenic Exposure and Its Correlation with Serum S100B Concentration pp.1559-0720, 2019, https://doi.org/10.1007/s12011-018-1463-2
  4. Association between heavy metal levels and acute ischemic stroke vol.25, pp.1, 2018, https://doi.org/10.1186/s12929-018-0446-0