Angiotensin II controls occludin function and is required for blood-brain barrier maintenance: Relevance to multiple sclerosis

Journal of Neuroscience

Volumn 27, Issue 34, 2007, Pages 9032-9042

  Wosik, Karolina ^a   Cayrol, Romain ^a   Dodelet Devillers, Aurore ^a   Berthelet, France ^b   Bernard, Monique ^a   Moumdjian, Robert ^b   Bouthillier, Alain ^b   Reudelhuber, Timothy L ^b   Prat, Alexandre ^a,b,c  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Astrocytes; CNS; Human; Immune privilege; Lipid rafts; Lymphocytes; Mouse; Neuroinflammation; Renin angiotensin system; Tight junctions

Indexed keywords

ANGIOTENSIN II; GAMMA INTERFERON; OCCLUDIN; PLASMINOGEN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MALE; MULTIPLE SCLEROSIS; PRIORITY JOURNAL;

EID: 34548145190     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2088-07.2007     Document Type: Article

References (52)

1. Abbott NJ (2002) Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 200:629-638.
2. Abbott NJ, Ronnback L, Hansson E (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7:41-53.
3. Alter A, Duddy M, Hebert S, Biernacki K, Prat A, Antel JP, Yong VW, Nuttall RK, Pennington CJ, Edwards DR, Bar-Or A (2003) Determinants of human B cell migration across brain endothelial cells. J Immunol 170:4497-4505.
4. Arthur FE, Shivers RR, Bowman PD (1987) Astrocyte-mediated induction of tight junctions in brain capillary endothelium: an efficient in vitro model. Brain Res 433:155-159.
5. Biernacki K, Prat A, Blain M, Antel JP (2004) Regulation of cellular and molecular trafficking across human brain endothelial cells by Th1- and Th2-polarized lymphocytes. J Neuropathol Exp Neurol 63:223-232.
6. Blezer EL, Nicolay K, Koomans HA, Joles JA (2001) Losartan versus enalapril on cerebral edema and proteinuria in stroke-prone hypertensive rats. Am J Hypertens 14:54-61.
7. Clemens DL, Clauser E, Celio MR, Inagami T (1986) Generation of angiotensinogen by cultured neuroblastoma and glioma cells. Brain Res 364:205-211.
8. Cooper WO, Hernandez-Diaz S, Arbogast PG, Dudley JA, Dyer S, Gideon PS, Hall K, Ray WA (2006) Major congenital malformations after first-trimester exposure to ACE inhibitors. N Engl J Med 354:2443-2451.
9. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T (2000) International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 52:415-472.
10. Deschepper CF, Bouhnik J, Ganong WF (1986) Colocalization of angiotensinogen and glial fibrillary acidic protein in astrocytes in rat brain. Brain Res 374:195-198.
11. D'Souza S, Alinauskas K, McCrea E, Goodyer C, Antel JP (1995) Differential susceptibility of human CNS-derived cell populations to TNF-dependent and independent immune-mediated injury. J Neurosci 15:7293-7300.
12. Farshori P, Kachar B (1999) Redistribution and phosphorylation of occludin during opening and resealing of tight junctions in cultured epithelial cells. J Membr Biol 170:147-156.
13. Ghandour MS, Langley OK, Labourdette G, Vincendon G, Gombos G (1981) Specific and artefactual cellular localizations of S 100 protein: an astrocyte marker in rat cerebellum. Dev Neurosci 4:66-78.
14. Hansson L (2000) Results of the STOP-Hypertension-2 trial. Blood Press Suppl 2:17-20.
15. Hirase T, Kawashima S, Wong EY, Ueyama T, Rikitake Y, Tsukita S, Yokoyama M, Staddon JM (2001) Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms. J Biol Chem 276:10423-10431.
16. Huber JD, Egleton RD, Davis TP (2001) Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24:719-725.
17. Ifergan I, Wosik K, Cayrol R, Kebir H, Auger C, Bernard M, Bouthillier A, Moumdjian R, Duquette P, Prat A (2006) Statins reduce human blood-brain barrier permeability and restrict leukocyte migration: relevance to multiple sclerosis. Ann Neurol 60:45-55.
18. Intebi AD, Flaxman MS, Ganong WF, Deschepper CF (1990) Angiotensinogen production by rat astroglial cells in vitro and in vivo. Neuroscience 34:545-554.
19. Ito H, Takemori K, Suzuki T (2001) Role of angiotensin II type 1 receptor in the leucocytes and endothelial cells of brain microvessels in the pathogenesis of hypertensive cerebral injury. J Hypertens 19:591-597.
20. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A, Antel JP (2005) TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 175:4320-4330.
21. Juillerat-Jeanneret L, Celerier J, Chapuis BC, Nguyen G, Wostl W, Maerki HP, Janzer RC, Corvol P, Gasc JM (2004) Renin and angiotensinogen expression and functions in growth and apoptosis of human glioblastoma. Br J Cancer 90:1059-1068.
22. Kacem K, Lacombe P, Seylaz J, Bonvento G (1998) Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 23:1-10.
23. Kago T, Takagi N, Date I, Takenaga Y, Takagi K, Takeo S (2006) Cerebral ischemia enhances tyrosine phosphorylation of occludin in brain capillaries. Biochem Biophys Res Commun 339:1197-1203.
24. Kakinuma Y, Hama H, Sugiyama F, Yagami K, Goto K, Murakami K, Fukamizu A (1998) Impaired blood-brain barrier function in angiotensinogen-deficient mice. Nat Med 4:1078-1080.
25. Kucuk M, Kaya M, Kalayci R, Cimen V, Kudat H, Arican N, Elmas I, Korkut F (2002) Effects of losartan on the blood-brain barrier permeability in long-term nitric oxide blockade-induced hypertensive rats. Life Sci 71:937-946.
26. Lampugnani MG, Corada M, Andriopoulou P, Esser S, Risau W, Dejana E (1997) Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells. J Cell Sci 110:2065-2077.
27. Lochard N, Silversides DW, van Kats JP, Mercure C, Reudelhuber TL (2003) Brain-specific restoration of angiotensin II corrects renal defects seen in angiotensinogen-deficient mice. J Biol Chem 278:2184-2189.
28. Lou M, Blume A, Zhao Y, Gohlke P, Deuschl G, Herdegen T, Culman J (2004) Sustained blockade of brain AT1 receptors before and after focal cerebral ischemia alleviates neurologic deficits and reduces neuronal injury, apoptosis, and inflammatory responses in the rat. J Cereb Blood Flow Metab 24:536-547.
29. Lynch KR, Hawelu-Johnson CL, Guyenet PG (1987) Localization of brain angiotensinogen mRNA by hybridization histochemistry. Brain Res 388:149-158.
30. Methot D, vanKats JP, Lochard N, Tremblay F, Silversides DW, Reudelhuber TL (2001) Development and application of a biological peptide pump for the study of the in vivo actions of angiotensin peptides. Am J Hypertens 14:38S-43S.
31. Morimoto S, Sigmund CD (2002) Angiotensin mutant mice: a focus on the brain renin-angiotensin system. Neuropeptides 36:194-200.
32. Mungall BA, Shinkel TA, Sernia C (1995) Immunocytochemical localization of angiotensinogen in the fetal and neonatal rat brain. Neuroscience 67:505-524.
33. Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26:523-530.
34. Neuhaus J, Risau W, Wolburg H (1991) Induction of blood-brain barrier characteristics in bovine brain endothelial cells by rat astroglial cells in transfilter coculture. Ann NY Acad Sci 633:578-580.
35. Nissen SE, Tuzcu EM, Libby P, Thompson PD, Ghali M, Garza D, Berman L, Shi H, Buebendorf E, Topol EJ (2004) Effect of antihypertensive agents on cardiovascular events in patients with coronary disease and normal blood pressure: the CAMELOT study: a randomized controlled trial. JAMA 292:2217-2225.
36. Nusrat A, Parkos CA, Verkade P, Foley CS, Liang TW, Innis-Whitehouse W, Eastburn KK, Madara JL (2000) Tight junctions are membrane microdomains. J Cell Sci 113: 1771-1781.
37. Ovbiagele B, Kidwell CS, Starkman S, Selco SL, Rajajee V, Razinia T, Saver JL (2005) Angiotensin 2 type 2 receptor activity and ischemic stroke severity. Neurology 65:851-854.
38. Petty MA, Lo EH (2002) Junctional complexes of the blood- brain barrier: permeability changes in neuroinflammation. Prog Neurobiol 68:311-323.
39. Pike LJ (2004) Lipid rafts: heterogeneity on the high seas. Biochem J 378:281-292.
40. Prat A, Biernacki K, Becher B, Antel JP (2000) B7 expression and antigen presentation by human brain endothelial cells: requirement for proinflammatory cytokines. J Neuropathol Exp Neurol 59:129-136.
41. Prat A, Biernacki K, Wosik K, Antel JP (2001) Glial cell influence on the human blood- brain barrier. Glia 36:145-155.
42. Prat A, Biernacki K, Lavoie JF, Poirier J, Duquette P, Antel JP (2002) Migration of multiple sclerosis lymphocytes through brain endothelium. Arch Neurol 59:391-397.
43. Rubin LL, Barbu K, Bard F, Cannon C, Hall DE, Horner H, Janatpour M, Liaw C, Manning K, Morales J, Porter S, Tanner L, Tomasellli K, Yednock T (1991) Differentiation of brain endothelial cells in cell culture. Ann NY Acad Sci 633:420-425.
44. Saavedra JM (2005) Brain angiotensin II: new developments, unanswered questions and therapeutic opportunities. Cell Mol Neurobiol 25:485-512.
45. Stanimirovic D, Shapiro A, Wong J, Hutchison J, Durkin J (1997) The induction of ICAM-1 in human cerebromicrovascular endothelial cells (HCEC) by ischemia-like conditions promotes enhanced neutrophil/HCEC adhesion. J Neuroimmunol 76:193-205.
46. Stanimirovic DB, Ball R, Durkin JP (1995) Evidence for the role of protein kinase C in astrocyte-induced proliferation of rat cerebromicrovascular endothelial cells. Neurosci Lett 197:219-222.
47. Stornetta RL, Hawelu-Johnson CL, Guyenet PG, Lynch KR (1988) Astrocytes synthesize angiotensinogen in brain. Science 242:1444-1446.
48. Tao-Cheng JH, Brightman MW (1988) Development of membrane interactions between brain endothelial cells and astrocytes in vitro. Int J Dev Neurosci 6:25-37.
49. Vianello B, Clauser E, Corvol P, Monnot C (1998) Functional interactions of L-162,313 with angiotensin II receptor subtypes and mutants. Eur J Pharmacol 347:113-118.
50. Wachtel M, Frei K, Ehler E, Fontana A, Winterhalter K, Gloor SM (1999) Occludin proteolysis and increased permeability in endothelial cells through tyrosine phosphatase inhibition. J Cell Sci 112:4347-4356.
51. Wosik K, Becher B, Ezman A, Nalbantoglu J, Antel JP (2001) Caspase 8 expression and signaling in Fas injury-resistant human fetal astrocytes. Glia 33:217-224.
52. Yanai K, Saito T, Kakinuma Y, Kon Y, Hirota K, Taniguchi-Yanai K, Nishijo N, Shigematsu Y, Horiguchi H, Kasuya Y, Sugiyama F, Yagami K, Murakami K, Fukamizu A (2000) Renin-dependent cardiovascular functions and renin-independent blood- brain barrier functions revealed by renin-deficient mice. J Biol Chem 275:5-8.