The Relationship Between Aquaporin-4 Expression and Blood-Brain and Spinal Cord Barrier Permeability Following Experimental Autoimmune Encephalomyelitis in the Rat

Anatomical Record

Volumn 294, Issue 1, 2011, Pages 46-54

  Huang, Xiang Nan ^a   Wang, Wei Zhi ^a   Fu, Jin ^a   Wang, Hua Bing ^b  

^a THE SECOND AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

AQP4; Blood central nervous system barrier; Multiple sclerosis; Occludin

Indexed keywords

AQUAPORIN 4; EVANS BLUE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CEREBELLUM; CONTROLLED STUDY; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD; TIGHT JUNCTION; WESTERN BLOTTING;

ANIMALS; AQUAPORIN 4; BLOOD-BRAIN BARRIER; CELL MEMBRANE PERMEABILITY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GUINEA PIGS; INFLAMMATION MEDIATORS; RATS; RATS, INBRED LEW; SPINAL CORD; UP-REGULATION;

RATTUS;

EID: 78650119727     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21286     Document Type: Article

References (48)

1. Abbott NJ. 2000. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell Mol Neurobiol 20: 131-147.
2. Amiry-Moghaddam M, Ottersen OP. 2003. The molecular basis of water transport in the brain. Nat Rev Neurosci 4: 991-1001.
3. Balda MS, Whitney JA, Flores C, González S, Cereijido M, Matter K. 1996. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol 134: 1031-1049.
4. Bloch O, Auguste KI, Manley GT, Verkman AS. 2006. Accelerated progression of kaolin-induced hydrocephalus in aquaporin-4-deficient mice. J Cereb Blood Flow Metab 26: 1527-1537.
5. Bloch O, Papadopoulos MC, Manley GT, Verkman AS. 2005. Aquaporin-4 gene deletion in mice increases focal edema associated with staphylococcal brain abscess. J Neurochem 95: 254-262.
6. Chen Y, Merzdorf C, Paul DL. 1997. Goodenough, COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos. J Cell Biol 138: 891-899.
7. Diane MM, Michael PP, Judith MG. 2005. Blood-brain barrier disruption and lesion localisation in experimental autoimmune encephalomyelitis with predominant cerebellar and brainstem involvement. J Neuroimmunol 160: 162-169.
8. Engelhardt B, Ransohoff R. 2005. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 26: 485-495.
9. Fabis MJ, Scott GS, Kean RB, Koprowski H, Hooper DC. 2007. Loss of blood-brain barrier integrity in the spinal cord is common to experimental allergic encephalomyelitis in knockout mouse models. Proc Natl Acad Sci USA 104: 5656-5661.
10. Gary AR. 2002. Matrix metalloproteinases in neuroinflammation. Glia 39: 279-291.
11. Inmaculada R, Alberto M, Josefina C, Jose' LV. 2008. Intracerebral VEGF injection highly upregulates AQP4 mRNA and protein in the perivascular space and glia limitans externa. Neurochem Int 52: 897-903.
12. Katsuichi M, Naomi N, Mayumi M, Kazuo K, Susumu K. 2009. Upregulation of water channel aquaporin-4 in experimental autoimmune encephalomyelitis. J Neurol Sci 276: 103-107.
13. Kean RB, Spitsin SV, Mikheeva T, Scott GS, Hooper DC. 2000. The peroxynitrite scavenger uric acid prevents inflammatory cell invasion into the central nervous system in experimental allergic encephalomyelitis through maintenance of blood-central nervous system barrier integrity. J Immunol 165: 6511-6518.
14. Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, Bernard M, Giuliani F, Arbour N, Becher B, Prat A. 2007. Human T H 17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 13: 1173-1175.
15. Kirk J, Plumb J, Mirakhur M, McQuaid S. 2003. 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 201: 319-327.
16. Leech S, Kirk J, Plumb J, McQuaid S. 2006. Persistent endothelial abnormalities and blood-brain barrier leak in primary and secondary progressive multiple sclerosis. Neuropathol Appl Neurobiol (in press).
17. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR. 2005. IgG marker of opticspinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 202: 473-477.
18. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K. 2004. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364: 2106-2112.
19. Lihua L, Hua Z, Verkman AS. 2009. Greatly attenuated experimental autoimmune encephalomyelitis in aquaporin-4 knockout mice. BMC Neurosci 10: 94.
20. Man S, Ubogu EE, Ransohoff RM. 2007. Inflammatory cell migration into the central nervous system: a few new twists on an old tale. Brain Pathol 17: 243-250.
21. Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW. 2000. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 6: 159-163.
22. Matsuoka T, Matsushita T, Kawano Y, Osoegawa M, Ochi H, Ishizu T. 2007. Heterogeneity of aquaporin-4 autoimmunity and spinal cord lesions in multiple sclerosis in Japanese. Brain 130: 1206-1223.
23. Maureen P, Susie L, Beverly C, John K, Brenda B, Stephen McQ. 2006. Differences in expression of junctional adhesion molecule-A and β-catenin in multiple sclerosis brain tissue: increasing evidence for the role of tight junction pathology. Acta Neuropathologica (This is from Springer-Verlag).
24. Minagar A, Alexander JS. 2003. Blood-brain barrier disruption in multiple sclerosis. Mult Scler 9: 540-549.
25. Misu T, Fujihara K, Nakashima I, Miyazawa I, Okita N, Takase S. 2002. Pure opticospinal form of multiple sclerosis in Japan. Brain 125: 2460-2468.
26. Miyamoto K, Nagaosa N, Motoyama M, Kataoka K, Kusunoki S. 2009. Upregulation of water channel aquaporin-4 in experimental autoimmune encephalomyeritis. J Neurol Sci 276: 103-107.
27. Morgan L, Shah B, Rivers LE, Barden L, Groom AJ, Chung R, Higazi D, Esmond H, Smith T, Staddon JM. 2007. Inflammation and dephosphorylation of the tight junction protein occludin in an experimental model of multiple sclerosis. Neuroscience 147: 664-673.
28. Nicchia GP, Frigeri A, Liuzzi GM, Svelto M. 2003. Inhibition of aquaporin-4 expression in astrocytes by RNAi determines alteration in cell morphology, growth, and water transport and induces changes in ischemia-related genes. Faseb J 17: 1508-1510.
29. Nicchia GP, Nico B, Camassa LMA, Mola MG, Loh N, Dermietzel R, Spray DC, Svelto M, Frigeri A. 2004. The role of aquaporin-4 in the blood-brain barrier development and integrity: studies in animal and cell culture models. Neuroscience 129: 935-945.
30. Nico B, Cardelli P, Fiori A, Riccetelli L, Giglio RM, Strom R, Sassoè-Pognetto M, Cantino D, Bertossi M, Ribatti D, Roncali L. 1997. Developmental study of ultrastructural and biochemical changes in isolated chick brain microvessels. Microvasc Res 53: 79-91.
31. Nico B, Quondamatteo F, Herken R, Marzullo A, Corsi P, Bertossi M, Russo G, Ribatti D, Roncali L. 1999. Developmental expression of ZO-1 antigen in the mouse blood-brain barrier. Dev Brain Res 114: 161-169.
32. Nico B, Quondamatteo F, Ribatti D, Bertossi M, Russo G, Herken R, Roncalli L. 1998. Ultrastructural localization of lectin binding sites in the developing brain microvasculature. Anat Embryol 197: 305-315.
33. Oshio K, Binder DK, Yang B, Schecter S, Verkman AS, Manley GT. 2004. Expression of aquaporin water channels in mouse spinal cord. Neuroscience 127: 685-693.
34. Papadopoulos MC, Manley GT, Krishna S, Verkman AS. 2004. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. Faseb J 18: 1291-1293.
35. Papadopoulos MC, Verkman AS. 2005. Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis. J Biol Chem 280: 13906-13912.
36. Papadopoulos MC, Verkman AS. 2007. Aquaporin-4 and brain edema. Pediatr Nephrol 22: 778-784.
37. Plumb J, McQuaid S, Mirakhur M, Kirk J. 2002. Abnormal endothelial tight junctions in active lesions and normal-appearing white matter in multiple sclerosis. Brain Pathol 12: 154-169.
38. Pozza M. 2000. Further evidence for a role of nitric oxide in experimental allergic encephalomyelitis: aminoguanidine treatment modifies its clinical evolution. Brain Res 855: 39-46.
39. Ransohoff RM, Kivisakk P, Kidd G. 2003. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 3: 569-581.
40. Rash JE, Yasumura T, Hudson CS. 1998. Direct immunogold labeling of aquapann-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci USA 95: 11981-11986.
41. Saadoun S, Tait MJ, Reza A, Davies DC, Bell BA, Verkman AS, Papadopoulos MC. 2009. AQP4 gene deletion in mice does not alter bloodbrain barrier integrity or brain morphology. Neuroscience. Doi: 10.1016/j.neuroscience.2009.03.069.
42. Scott GS, Hake P, Kean RB, Virág L, Szabó C, Hooper DC. 2001. Role of poly(ADP-ribose) synthetase activation in the development of experimental allergic encephalomyelitis. J Neuroimmunol 117: 78-86.
43. Simone AT, Ana AV, Simone MB, Marcelo NM. 2005. Experimental autoimmune encephalomyelitis: a heterogeneous group of animal models to study human multiple sclerosis. Drug Discovery Today 2: 127-134.
44. Solenov E, Watanabe H, Manley GT, Verkman AS. 2004. Seven fold reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 286: C426-C432.
45. Stockinger B, Veldhoen M. 2007. Differentiation and function of Th17 T cells. Curr Opin Immunol 19: 281-286.
46. Tait MJ, Saadoun S, Bell BA, Papadopoulos MC. 2008. Water movements in the brain: role of aquaporins. Trends Neurosci 31: 37-43.
47. Vajda Z, Pedersen M, Docxi T. 2004. Studies of mdx mice. J Neurosci 129: 993-998.
48. Wong V, Gumbiner BM. 1997. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 136: 399-409.