Role of the Blood-Brain Barrier in Multiple Sclerosis

Archives of Medical Research

Volumn 45, Issue 8, 2014, Pages 687-697

  Ortiz, Genaro Gabriel ^a   Pacheco Moisés, Fermín Paul ^b   Macías Islas, Miguel Ángel ^c   Flores Alvarado, Luis Javier ^b   Mireles Ramírez, Mario A ^c   González Renovato, Erika Daniela ^a   Hernández Navarro, Vanessa Elizabeth ^a   Sánchez López, Angélica Lizeth ^a   Alatorre Jiménez, Moisés Alejandro ^a  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

^c Hospital de Especialidades   (Mexico)

Author keywords

Blood brain barrier; Central nervous system; Multiple sclerosis; Oxidative stress

Indexed keywords

CYTOKINE; MYELIN; NITRIC OXIDE; PROTEINASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; CELL ADHESION MOLECULE;

ASTROCYTE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN PERICYTE; CENTRAL NERVOUS SYSTEM; CYTOKINE RELEASE; ENDOTHELIUM CELL; HUMAN; IMMUNE RESPONSE; LEUKOCYTE ACTIVATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MULTIPLE SCLEROSIS; NERVE FIBER; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; QUALITY OF LIFE; REVIEW; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; CELL ADHESION; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ASTROCYTES; BLOOD-BRAIN BARRIER; CELL ADHESION; CELL ADHESION MOLECULES; CYTOKINES; ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; LYMPHOCYTES; MACROPHAGES; MULTIPLE SCLEROSIS; OXIDATIVE STRESS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84924813906     PISSN: 01884409     EISSN: 18735487     Source Type: Journal    
DOI: 10.1016/j.arcmed.2014.11.013     Document Type: Review

References (82)

1. Kakalacheva K., Lünemann J.D. Enviromental triggers of multiple sclerosis. FEBS Lett 2011, 585:3724-3729.
2. Chitnis T. Role of puberty in multiple sclerosis risk and course. Clin Immunol 2013, 149:192-200.
3. Franciotta D., Salvetti M., Lolli F., et al. B cells and multiple sclerosis. Lancet Neurol 2008, 7:852-858.
4. Fletcher J.M., Lalor S.J., Sweeney C.M., et al. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin Exp Immunol 2010, 162:1-11.
5. Markovic-Plese S., Pinilla C., Martin R. The initiation of the autoimmune response in multiple sclerosis. Clin Neurol Neurosurg 2004, 106:218-222.
6. Lassmann H., Brück W., Lucchinetti C., et al. Remyelination in multiple sclerosis. Mult Scler 1997, 3:133-136.
7. Ramagopalan S.V., Maugeri N.J., Handunnetthi L., et al. Expression of the multiple sclerosis-associated MHC class II allele HLA-DRB1*1501 is regulated by vitamin D. PLoS Genet 2009, 5:e1000369.
8. Ransohoff R.M., Engelhardt B. The anatomical and cellular basis of immune surveillance in the central nervous system. Nat Rev Immunol 2012, 12:623-635.
9. Odoardi F., Sie C., Streyl K., et al. T cells become licensed in the lung to enter the central nervous system. Nature 2012, 30(488):675-679.
10. Dodelet-Devillers A., Cayrol R., van Horssen J., et al. Functions of lipid raft membrane microdomains at the blood-brain barrier. J Mol Med 2009, 87:765-774.
11. Shrenik P.S. Drug delivery to the central nervous system: a review. JPharm Pharm Sci 2003, 62:252-273.
12. Upadhyay R.K. Drug delivery systems, CNS protection, and the blood brain barrier. BioMed Res Int 2014, 2014:1-37.
13. Spuch C., Navarro C. Transport mechanisms at the blood-cerebrospinal-fluid barrier: role of megalin (LRP2). Recent Patents Endocr Metab Immune Drug Disc 2010, 4:1-16.
14. Herald N. Microglia: a cellular vehicle for CNS gene therapy. J Clin Invest 2006, 116:2857-2860.
15. Loch-Neckel G., Koepp J. The blood-brain barrier and the drug delivery in the central nervous system. Rev Neurol 2010, 51:165-174.
16. Salama N.N., Eddington N.D., Fasano A. Tight junction modulation and its relationship to drug delivery. Adv Drug Deliv Rev 2006, 58:15-28.
17. Rostami A., Ciric B. Role of Th17 cells in the pathogenesis of CNS inflammatory demyelination. J Neurol Sci 2013, 333:76-87.
18. Jolanda M.E., Williams A. Promoting remyelination in multiple sclerosis-recent advances. Drugs 2013, 73:2017-2029.
19. Cramer S.P., Simonsen H., Frederiksen J.L., et al. Abnormal blood-brain barrier permeability in normal appearing white matter in multiple sclerosis investigated by MRI. Neuroimage Clin 2014, 4:182-189.
20. Neumann H., Cavalie A., Jenne D.E., et al. Induction of MHC class I genesin neurons. Science 1995, 269:549-552.
21. Cassan C., Liblau R.S. Immune tolerance and control of CNS autoimmunity: from animal models to MS patients. J Neurochem 2007, 100:883-892.
22. Nair A., Frederick T.J., Miller S.D. Astrocytes in multiple sclerosis: a product of their environment. Cell Mol Life Sci 2008, 65:2702-2720.
23. Wilson E.H., Weninger W., Hunter C.A. Trafficking of immune cells in the central nervous system. J Clin Invest 2010, 120:1368-1379.
24. Barreiro O., Sánchez-Madrid F. Molecular basis of leukocyte-endothelium interactions during the inflammatory response. Rev Esp Cardiol 2009, 62:552-562.
25. Hernández-Pedro N.Y., Espinosa-Ramirez G., Pérez de la Cruz V., et al. Initial immunopathogenesis of multiple sclerosis: innate immune response. Clin Dev Immunol 2013, 2013:1-15.
26. Alvarez J.I., Cayrol R., Prat A. Disruption of central nervous system barriers in multiple sclerosis. Biochim Biophys Acta 2011, 1812:252-264.
27. Holmana D.W., Kleina R.S., Ransohoffd R.M. The blood-brain barrier, chemokines and multiple sclerosis. Biochim Biophys Acta 2011, 1812:220-230.
28. Losy J. Is MS an inflammatory or primary degenerative disease?. J Neural Transm 2013, 120:1459-1462.
29. Ricci G.L., Pasq V.L. Astrocyte-neuron interactions in neurological disorders. J Biol Phys 2009, 35:317-336.
30. Wink D.A., Hines H.B., Cheng R.Y.S., et al. Nitric oxide and redox mechanisms in the immune response. J Leukocyte Biol 2011, 89:873-891.
31. Costantino C.M., Hutton J., Baecher-Allan C., et al. Multiple sclerosis and regulatory T cells. J Clin Immunol 2008, 6:697-706.
32. Anderson A.C., Anderson D.E., Bregoli L., et al. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 2007, 318:1141-1143.
33. Rosenberg G.A. Neurological diseases in relation to the blood-brain barrier. J Cereb Blood Flow Metab 2012, 32:1139-1151.
34. Furuse M., Furuse K., Sasaki H., et al. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol 2001, 153:263-272.
35. Tsukita S., Furuse M. The structure and function of claudins, cell adhesion molecules at tight junctions. Ann N Y Acad Sci 2000, 915:129-135.
36. Furuse M., Fujita K., Hiiragi T., et al. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 1998, 141:1539-1550.
37. Liebner S., Fischmann A., Rascher G., et al. Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol 2000, 100:323-331.
38. Wolburg H., Wolburg-Buchholz K., Kraus J., et al. Localization of claudin-3 in tight junctions of the blood-brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol 2003, 105:586-592.
39. Gonçalves A., Ambrósio A.F., Fernandes R. Regulation of claudins in blood-tissue barriers under physiological and pathological states. Tissue Barriers 2013, 1:3.
40. Friederike P., Shafer J., Engelhardt B. Claudin-1 induced sealing of blood-brain barrier tight junctions ameliorates chronic experimental autoimmune encephalomyelitis. Acta Neuropathol 2011, 122:601-614.
41. Halliwell B. Reactive oxygen species and the central nervous system. J Neurochem 1992, 59:1609-1623.
42. Léwen A., Matz P., Chan P.H. Free radical pathways in CNS injury. Neurotrauma 2000, 17:871-889.
43. Korhonen R., Lahti A., Kankaanranta H., et al. Nitric oxide production and signaling in inflammation. Curr Drug Targets Inflamm Allergy 2005, 4:471-479.
44. Vaz A.R., Silva S.L., Barateiro A., et al. Proinflammatory cytokines intensify the activation of NO/NOS, JNK1/2 and caspase cascades in immature neurons exposed to elevated levels of unconjugated bilirubin. Exp Neurol 2011, 229:381-390.
45. Hartung H.P., Jung S., Stoll G., et al. Inflammatory mediators in demyelinating disorders of the CNS and PNS. J Neuroimmunol 1992, 40:197-210.
46. Bonda D.J., Wang X., Perry G., et al. Oxidative stress in Alzheimer disease: a possibility for prevention. Neuropharmacology 2010, 59:290-294.
47. Stefani I.C., Wright D., Polizzi K.M., et al. The role of ER stress-induced apoptosis in neurodegeneration. Curr Alzheimer Res 2012, 9:373-378.
48. Ortiz G.G., Macias-Islas M.A., Pacheco-Moises F.P., et al. Oxidative stress is increased in serum from Mexican patients with relapsing-remitting multiple sclerosis. Dis Markers 2009, 26:35-39.
49. Smith K.J., Kapoor R., Felts P.A. Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathol 1999, 9:69-92.
50. Calabrese V., Scapagnini G., Ravagna A., et al. Nitric oxide synthase is present in the cerebrospinal fluid of patients with active multiple sclerosis and is associated with increases in cerebrospinal fluid protein nitrotyrosine and S-nitrosothiols and with changes in glutathione levels. J Neurosci Res 2002, 70:580-587.
51. Hill K.E., Zollinger L.V., Watt H.E., et al. Inducible nitric oxide synthase in chronic active multiple sclerosis plaques: distribution, cellular expression and association with myelin damage. J Neuroimmunol 2004, 151:171-179.
52. van der Goes A., Wouters D., Wouters S.M., et al. Reactive oxygen species enhance the migration of monocytes across the blood-brain barrier invitro. FASEB J 2001, 15:1852-1854.
53. Schreibelt G., Musters R.J., Reijerkerk A., et al. Lipoic acid affects cellular migration into the central nervous system and stabilizes blood-brain barrier integrity. J Immunol 2006, 177:2630-2637.
54. van der Goes A., Brouwer J., Hoekstra K., et al. Reactive oxygen species are required for the phagocytosis of myelin by macrophages. J Neuroimmunol 1998, 92:67-75.
55. van Meeteren M.E., Hendriks J.J., Dijkstra C.D., et al. Dietary compounds prevent oxidative damage and nitric oxide production by cells involved in demyelinating disease. Biochem Pharmacol 2004, 67:967-975.
56. Hendriks J.J., Teunissen C.E., de Vries H.E. Macrophages and neurodegeneration. Brain Res Rev 2005, 48:185-195.
57. Giovannoni G., Heales S.J., Land J.M., et al. The potential role of nitric oxide in multiple sclerosis. Mult Scler 1998, 4:212-216.
58. Bagasra O., Michaels F.H., Zheng Y.M. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc Natl Acad Sci U S A 1995, 92:12041-12045.
59. Kevil C.G., Okayama N., Alexander J.S. H(2)O(2)-mediated permeability II: importance of tyrosine phosphatase and kinase activity. Am J Physiol, Cell Physiol 2001, 281:1940-1947.
60. Griendling K.K., Sorescu D., Lassegue B., et al. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol 2000, 20:2175-2183.
61. Kamata H., Manabe T., Kakuta J., et al. Multiple redox regulation of the cellular signaling system linked to AP-1 and NFkappaB: effects of N-acetylcysteine and H2O2 on the receptor tyrosine kinases, the MAP kinase cascade, and IkappaB kinases. Ann NY Acad Sci 2002, 973:419-422.
62. Scott G.S., Hake P., Kean R.B., et al. Role of poly(ADP-ribose) synthetase activation in the development of experimental allergic encephalomyelitis. J Neuroimmunol 2001, 117:78-86.
63. Smith K.J., Lassman H. The role of nitric oxide in multiple sclerosis. Lancet Neurol 2002, 1:233-239.
64. Ibarra-Alvarado C., Galle J., Melichar V.O., et al. Phosphorylation of blood vessel vasodilator stimulated phosphoprotein at serine 239 as a functional biochemical marker of endothelial nitric oxide/cyclic GMP signaling. Mol Pharmacol 2002, 61:312-319.
65. Wink D.A., Miranda K.M., Espey M.G., et al. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal 2001, 3:203-213.
66. Marcus J.S., Karackattu S.L., Fleegal M.A., et al. Cytokine stimulated inducible nitric oxide synthase expression in astroglia: role of Erk mitogen-activated protein kinase and NF-kappaB. Glia 2003, 41:152-160.
67. Cucullo L., Mohammed H., Puvenna V., et al. The role of shear stress in blood-brain barrier endothelial physiology. BMC Neurosci 2011, 12:40.
68. Baker D.E. Natalizumab: overview of its pharmacology and safety. Rev Gastroenterol Disord 2007, 7:38-46.
69. Masserini M. Nanoparticles for brain drug delivery. ISRN Biochem 2013, 2013:18.
70. Bellavance M.A., Blanchette M., Fortin D. Recent advances in blood-brain barrier disruption as a CNS delivery strategy. AAPS J 2008, 10:166-177.
71. Pardridge W.M. Drug transport across the blood-brain barrier. J Cereb Blood Flow Metab 2012, 32:1959-1972.
72. Minn A., Leclerc S., Heydel J.M., et al. Drug transport into the mammalian brain: the nasal pathway and its specific metabolic barrier. J Drug Target 2002, 10:285-296.
73. Ross T.M., Martinez P.M., Renner J.C., et al. Intranasal administration of interferon beta bypasses the blood-brain barrier to target the central nervous system and cervical lymph nodes: a non-invasive treatment strategy for multiple sclerosis. J Neuroimmunol 2004, 151:66-77.
74. Ben-Zvi A., Lacoste B., Kur E., et al. Mfsd2a is critical for the formation and function of the blood-brain barrier. Nature 2014, 509:507-511.
75. Perez J.H., Branch W., Smith J., et al. Investigation of endosomal compartments involved in endocytosis and transcytosis of polymeric immunoglobulin a by subcellular fractionation of perfused isolated rat liver. Biochem J 1988, 25:763-770.
76. Engelhardt B., Kappo L. Natalizumab: targeting alpha4-integrins in multiple sclerosis. Neurodegener Dis 2008, 5:16-17.
77. Steinman L. Blocking adhesion molecules as therapy for multiple sclerosis: natalizumab. Nat Rev Drug Discov 2005, 4:510-511.
78. Ransohoff R.M. Thinking without thinking about natalizumab and PML. J Neurol Sci 2007, 259:50-51.
79. Sadowski T., Steinmeyer J. Effects of tetracyclines on the production of matrix metalloproteinases and plasminogen activators as well as of their natural inhibitors, tissue inhibitor of metalloproteinases-1 and plasminogen activator inhibitor-1. Inflamm Res 2001, 50:175-182.
80. Waubant E., Goodkin D., Bostrom A., et al. IFNbeta lowers MMP-9/TIMP-1 ratio, which predicts new enhancing lesions in patients with SPMS. Neurology 2003, 60:52-57.
81. Gelati M., Corsini E., De Rossi M., et al. Methylprednisolone acts on peripheral blood mono-nuclear cells and endothelium in inhibiting migration phenomena in patients with multiple sclerosis. Arch Neurol 2002, 59:774-780.
82. Shinto L., Marracci G., Baldauf-Wagner S., et al. Omega-3 fatty acid supplementation decreases matrix metalloproteinase-9 production in relapsing-remitting multiple sclerosis. Prostaglandins Leukot Essent Fatty Acids 2009, 80:131-136.