The protective effects of bioactive (RS)-glucoraphanin on the permeability of the mice blood-brain barrier following experimental autoimmune encephalomyelitis

European Review for Medical and Pharmacological Sciences

Volumn 18, Issue 2, 2014, Pages 194-204

  Giacoppo, S ^a   Galuppo, M ^a   Iori, R ^b   De Nicola, G R ^b   Bramanti, P ^a   Mazzon, E ^a  

^a IRCCS CENTRO NEUROLESI BONINO PULEJO   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

Apoptosis; Blood brain barrier; Inflammation; Multiple sclerosis; Tight junctions

Indexed keywords

CASPASE 3; CLAUDIN 1; CLAUDIN 3; CLAUDIN 5; GLUCORAPHANIN; GLUCOSINOLATE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PERTUSSIS TOXIN; PROTEIN ZO1; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CLDN1 PROTEIN, MOUSE; CLDN5 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; IMIDOESTER; NEUROPROTECTIVE AGENT; TJP1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BORDETELLA PERTUSSIS; BRAIN TISSUE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNIZATION; INFLAMMATION; MALE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PERTUSSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TIGHT JUNCTION; TREATMENT RESISTANT DEPRESSION; WESTERN BLOTTING; ANIMAL; APOPTOSIS; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; EMBRYOLOGY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; METABOLISM; PERMEABILITY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BLOOD-BRAIN BARRIER; CASPASE 3; CLAUDIN-1; CLAUDIN-3; CLAUDIN-5; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FORKHEAD TRANSCRIPTION FACTORS; GLUCOSINOLATES; IMIDOESTERS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; PERMEABILITY; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84896911307     PISSN: 11283602     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. SOSPEDRA M, MARTIN R. Immunology of multiple sclerosis. Annu Rev Immunol 2005; 23: 683-747.
2. DHIB-JALBUT S. Pathogenesis of myelin/oligodendrocyte damage in multiple sclerosis. Neurology 2007; 68: S13-21.
3. HOLMOY T, HESTVIK AL. Multiple sclerosis: immunopathogenesis and controversies in defining the cause. Curr Opin Infect Dis 2008; 21: 271-278.
4. LISAK RP. Neurodegeneration in multiple sclerosis: defining the problem. Neurology 2007; 68: S5-12.
5. TSUKITA S, FURUSE M, ITOH M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001; 2: 285-293.
6. SHIN K, FOGG VC, MARGOLIS B.Tight junctions and cell polarity. Annu Rev Cell Dev Biol 2006; 22: 207-235.
7. VORBRODT AW, DOBROGOWSKA DH. Molecular anatomy of intercellular junctions in brain endothelial and epithelial barriers: electron microscopist's view. Brain Res Brain Res Rev 2003; 42: 221-242.
8. BALLABH P, BRAUN A, NEDERGAARD M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16: 1-13.
9. LUISSINT AC, FEDERICI C, GUILLONNEAU F, CHRETIEN F, CAMOIN L, GLACIAL F, GANESHAMOORTHY K, COURAUD PO. Guanine nucleotide-binding protein Galphai2: a new partner of claudin-5 that regulates tight junction integrity in human brain endothelial cells. J Cereb Blood Flow Metab 2012; 32: 860-873.
10. MINAGAR A, ALEXANDER JS. Blood-brain barrier disruption in multiple sclerosis. Mult Scler 2003; 9: 540-549.
11. MINAGAR A, JY W, JIMENEZ JJ, ALEXANDER JS. Multiple sclerosis as a vascular disease. Neurol Res 2006; 28: 230-235.
12. BEDNARCZYK J, LUKASIUK K. Tight junctions in neurological diseases. Acta Neurobiol Exp (Wars) 2011; 71: 393-408.
13. KIRK J, PLUMB J, MIRAKHUR M, MCQUAID S. Tight junctional abnormality in multiple sclerosis white matter affects all calibres of vessel and is associated with blood-brain barrier leakage and active demyelination. J Pathol 2003; 201: 319-327.
14. LUCCARINI I, BALLERINI C, BIAGIOLI T, BIAMONTE F, BELLUCCI A, ROSI MC, GROSSI C, MASSACESI L, CASAMENTI F. Combined treatment with atorvastatin and minocycline suppresses severity of EAE. Exp Neurol 2008; 211: 214-226.
15. GOLD R, LININGTON C, LASSMANN H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006; 129: 1953-1971.
16. FLETCHER JM, LALOR SJ, SWEENEY CM, TUBRIDY N, MILLS KH. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin Exp Immunol 2010; 162: 1-11.
17. CANISTRO D, BARILLARI J, MELEGA S, SAPONE A, IORI R, SPERONI E, PAOLINI M. Black cabbage seed extract affects rat Cyp-mediated biotransformation: organ and sex related differences. Food Chem Toxicol 2012; 50: 2612-2621.
18. VERHOEVEN DT, VERHAGEN H, GOLDBOHM RA, VAN DEN BRANDT PA, VAN POPPEL G. A review of mechanisms underlying anticarcinogenicity by brassica vegetables. Chem Biol Interact 1997; 103: 79-129.
19. LEONI O, IORI R, PALMIERI S. Hydrolysis of glucosinolates using nylon-immobilized myrosinase to produce pure bioactive molecules. Biotechnol Bioeng 2000; 68: 660-664.
20. LISI L, NAVARRA P, CIROCCHI R, SHARP A, STIGLIANO E, FEINSTEIN DL, DELLO RUSSO C. Rapamycin reduces clinical signs and neuropathic pain in a chronic model of exper imental autoimmune encephalomyelitis. J Neuroimmunol 2012; 243: 43-51.
21. RODRIGUES DH, VILELA MC, BARCELOS LS, PINHO V, TEIXEIRA MM, TEIXEIRA AL. Absence of PI3Kgamma leads to increased leukocyte apoptosis and diminished severity of experimental autoimmune encephalomyelitis. J Neuroimmunol 2010; 222: 90-94.
22. ABDULL RAZIS AF, BAGATTA M, DE NICOLA GR, IORI R, IOANNIDES C. Intact glucosinolates modulate hepatic cytochrome P450 and phase II conjugation activities and may contribute directly to the chemopreventive activity of cruciferous vegetables. Toxicology 2010; 277: 74-85.
23. WAGNER AE, ERNST I, IORI R, DESEL C, RIMBACH G. Sulforaphane but not ascorbigen, indole-3-carbinole and ascorbic acid activates the transcription factor Nrf2 and induces phase-2 and antioxidant enzymes in human keratinocytes in culture. Exp Dermatol 2010; 19: 137-144.
24. EEC Regulation 1864/90, Enclosure VIII.
25. PESSINA A, THOMAS RM, PALMIERI S, LUISI PL. An improved method for the purification of myrosinase and its physicochemical characterization. Arch Biochem Biophys 1990; 280: 383-389.
26. FURUSE M, SASAKI H, TSUKITA S. Manner of interaction of heterogeneous claudin species within and between tight junction strands. J Cell Biol 1999; 147: 891-903.
27. MINETA K, YAMAMOTO Y, YAMAZAKI Y, TANAKA H, TADA Y, SAITO K, TAMURA A, IGARASHI M, ENDO T, TAKEUCHI K, TSUKITA S. Predicted expansion of the claudin multigene family. FEBS Lett 2011; 585: 606-612.
28. FURUSE M, FUJITA K, HIIRAGI T, FUJIMOTO K, TSUKITA S. 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.
29. ITOH M, FURUSE M, MORITA K, KUBOTA K, SAITOU M, TSUKITA S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 1999; 147: 1351-1363.
30. MORITA K, SASAKI H, FURUSE M, TSUKITA S. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol 1999; 147: 185-194.
31. PIONTEK J, WINKLER L, WOLBURG H, MULLER SL, ZULEGER N, PIEHL C, WIESNER B, KRAUSE G, BLASIG IE. Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J 2008; 22: 146-158.
32. PIEHL C, PIONTEK J, CORDING J, WOLBURG H, BLASIG IE. Participation of the second extracellular loop of claudin-5 in paracellular tightening against ions, small and large molecules. Cell Mol Life Sci 2010; 67: 2131-2140.
33. ZHANG J, PIONTEK J, WOLBURG H, PIEHL C, LISS M, OTTEN C, CHRIST A, WILLNOW TE, BLASIG IE, ABDELILAHSEYFRIED S. Establishment of a neuroepithelial bar- rier by Claudin5a is essential for zebrafish brain ventricular lumen expansion. Proc Natl Acad Sci U S A 2010; 107: 1425-1430.
34. FURUSE M, HATA M, FURUSE K, YOSHIDA Y, HARATAKE A, SUGITANI Y, NODA T, KUBO A, TSUKITA S. Claudinbased tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 2002; 156: 1099-1111.
35. KRAUSE G, WINKLER L, MUELLER SL, HASELOFF RF, PIONTEK J, BLASIG IE. Structure and function of claudins. Biochim Biophys Acta 2008; 1778: 631-645.
36. WOLBURG H, WOLBURG-BUCHHOLZ K, KRAUS J, RASCHEREGGSTEIN G, LIEBNER S, HAMM S, DUFFNER F, GROTE EH, RISAU W, ENGELHARDT B. 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.
37. GONZALEZ-MARISCAL L, BETANZOS A, AVILA-FLORES A. MAGUK proteins: structure and role in the tight junction. Semin Cell Dev Biol 2000; 11: 315-324.
38. GUILLEMOT L, PASCHOUD S, PULIMENO P, FOGLIA A, CITI S. The cytoplasmic plaque of tight junctions: a scaffolding and signalling center. Biochim Biophys Acta 2008; 1778: 601-613.
39. 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.
40. CHEN ML, POTHOULAKIS C, LAMONT JT. Protein kinase C signaling regulates ZO-1 translocation and increased paracellular flux of T84 colonocytes exposed to Clostridium difficile toxin A. J Biol Chem 2002; 277: 4247-4254.
41. LIU DZ, LECLUYSE EL, THAKKER DR. Dodecylphosphocholine-mediated enhancement of paracellular permeability and cytotoxicity in Caco-2 cell monolayers. J Pharm Sci 1999; 88: 1161-1168.
42. HOLLANDE F, BLANC EM, BALI JP, WHITEHEAD RH, PELEGRIN A, BALDWIN GS, CHOQUET A. HGF regulates tight junctions in new nontumorigenic gastric epithelial cell line. Am J Physiol Gastrointest Liver Physiol 2001; 280: G910-921.
43. BLUM MS, TONINELLI E, ANDERSON JM, BALDA MS, ZHOU J, O'DONNELL L, PARDI R, BENDER JR. Cytoskeletal rearrangement mediates human microvascular endothelial tight junction modulation by cytokines. Am J Physiol 1997; 273: H286-294.
44. FISCHER S, WOBBEN M, MARTI HH, RENZ D, SCHAPER W. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc Res 2002; 63: 70-80.
45. PROESCHOLDT MA, JACOBSON S, TRESSER N, OLDFIELD EH, MERRILL MJ. Vascular endothelial growth factor is expressed in multiple sclerosis plaques and can induce inflammatory lesions in experimental allergic encephalomyelitis rats. J Neuropathol Exp Neurol 2002; 61: 914-925.
46. SAKAGUCHI S, YAMAGUCHI T, NOMURA T, ONO M. Regulatory T cells and immune tolerance. Cell 2008; 133: 775-787.
47. ZIEGLER SF. FOXP3: of mice and men. Annu Rev Immunol 2006; 24: 209-226.
48. SAKAGUCHI S, SAKAGUCHI N. Regulatory T cells in immunologic self-tolerance and autoimmune disease. Int Rev Immunol 2005; 24: 211-226.
49. FRANSSON M, BURMAN J, LINDQVIST C, ATTERBY C, FAGIUS J, LOSKOG A. T regulatory cells lacking CD25 are increased in MS during relapse. Autoimmunity 2010; 43: 590-597.
50. VENKEN K, HELLINGS N, THEWISSEN M, SOMERS V, HENSEN K, RUMMENS JL, MEDAER R, HUPPERTS R, STINISSEN P. Compromised CD4+ CD25(high) regulatory T-cell function in patients with relapsing-remitting multiple sclerosis is correlated with a reduced frequency of FOXP3-positive cells and reduced FOXP3 expression at the single-cell level. Immunology 2008; 123: 79-89.
51. BUCKNER JH. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat Rev Immunol 2010; 10: 849-859.
52. READ S, MALMSTROM V, POWRIE F. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J Exp Med 2000; 192: 295-302.
53. KOHM AP, CARPENTIER PA, ANGER HA, MILLER SD. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J Immunol 2002; 169: 4712-4716.
54. DE KEULENAER GW, USHIO-FUKAI M, YIN Q, CHUNG AB, LYONS PR, ISHIZAKA N, RENGARAJAN K, TAYLOR WR, ALEXANDER RW, GRIENDLING KK. Convergence of redox-sensitive and mitogen-activated protein kinase signaling pathways in tumor necrosis factoralpha-mediated monocyte chemoattractant protein-1 induction in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2000; 20: 385-391.
55. CHEN Z, GIBSON TB, ROBINSON F, SILVESTRO L, PEARSON G, XU B, WRIGHT A, VANDERBILT C, COBB MH. MAP kinases. Chem Rev 2001; 101: 2449-2476.
56. PLATANIAS LC. Map kinase signaling pathways and hematologic malignancies. Blood 2003; 101: 4667-4679.
57. ALLAN SM, ROTHWELL NJ. Cytokines and acute neurodegeneration. Nat Rev Neurosci 2001; 2: 734-744.
58. MARTINEZ E. Multi-protein complexes in eukaryotic gene transcription.Plant Mol Biol 2002; 50: 925-947.
59. CHEUNG EC, SLACK RS. Emerging role for ERK as a key regulator of neuronal apoptosis. Sci STKE 2004; 2004: PE45.
60. LU Z, XU S. ERK1/2 MAP kinases in cell survival and apoptosis. IUBMB Life 2006; 58: 621-631.
61. PORTER AG, JANICKE RU. Emerging roles of caspase-3 in apoptosis.Cell Death Differ 1999; 6: 99-104.