Immunolocalization of tight junction proteins in the adult and developing human brain

Histochemistry and Cell Biology

Volumn 122, Issue 1, 2004, Pages 51-59

  Virgintino, Daniela ^a   Errede, Mariella ^a   Robertson, David ^b   Capobianco, Carmen ^a   Girolamo, Francesco ^a   Vimercati, Antonella ^a   Bertossi, Mirella ^c   Roncali, Luisa ^a  

^a UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF FOGGIA   (Italy)

Author keywords

Blood brain barrier; Claudin 5; Human brain development; Occludin; Tight junctions

Indexed keywords

CLAUDIN; CLAUDIN 5; OCCLUDIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTERIOLE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN DEVELOPMENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENDOTHELIUM CELL; GESTATION PERIOD; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; INFANT; MALE; MENINX; MICROVASCULATURE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TELENCEPHALON; TIGHT JUNCTION;

EID: 4043131714     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-004-0665-1     Document Type: Article

References (71)

1. Abbott NJ (2002) Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 200:629-638
2. Balabanov R, Dore-Duffy P (1998) Role of the CNS microvascular pericyte in the blood-brain barrier. J Neurosci Res 53:637-644
3. Bär T (1980) The vascular system of the cerebral cortex. Adv Anat Embryol Cell Biol 59:1-62
4. Bauer H-C, Bauer H (2000) Neural induction of the blood-brain barrier: still an enigma. Cell Mol Neurobiol 20:13-28
5. Bauer H-C, Bauer H, Lametschwandtner A, Amberger A, Ruiz PL, Steiner M (1993) Neovascularization and the appearance of morphological characteristics of the blood-brain barrier in the embryonic mouse central nervous system. Dev Brain Res 75:269-278
6. Bauer H, Sonnleitner U, Lametschwandtner A, Steiner M, Adam H, Bauer H-C (1995) Ontogenic expression of the erythroid-type glucose transporter (GLUT 1) in the telencephalon of the mouse: correlation to the tightening of the blood-brain barrier. Dev Brain Res 86:317-325
7. Bertossi M, Virgintino D, Errede M, Roncali L (1999) Immunohistochemical and ultrastructural characterization of cortical plate microvasculature in the human fetus telencephalon. Microvasc Res 58:49-61
8. Bertossi M, Girolamo F, Errede M, Benagiano V, Virgintino D, Roncali L (2002) Developmental changes of HT7 expression in the microvessels of the chick embryo brain. Anat Embryol 205:229-233
9. Cancilla PA, Bready J, Berliner J (1993) Brain endothelial-astrocyte interactions. In: Pardridge WM (ed) The blood-brain barrier. Cellular and molecular biology. Raven, New York, pp 25-46
10. Cassella JP, Lawrenson JG, Allt G, Firth JA (1996) Ontogeny of four blood-brain barrier markers: an immunocytochemical comparison of pial and cerebral microvessels. J Anat 189:407-415
11. Dobrogowska DH, Vorbrodt AW (1999) Quantitative immunocytochemical study of blood-brain barrier glucose transporter (GLUT-1) in four regions of mouse brain. J Histochem Cytochem 47:1021-1029
12. Dziegielewska KM, Evans CAN, Malinowska DH, Møllgård K, Reynolds JM, Reynolds ML, Sauders NR (1979) Studies of the development of brain barrier systems to lipid insoluble molecules in fetal sheep. J Physiol 292:207-231
13. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM (1998) The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273:29745-29753
14. Furuse M, Tetsuaki H, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777-1788
15. Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S (1998) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141:1539-1550
16. Furuse M, Sasaki H, Tsukita S (1999) Manner of interaction of heterogeneous claudin species within and between tight junction strands. J Cell Biol 147:891-903
17. Gerhart DZ, Le Vasseur RJ, Broderius MA, Drewes LR (1989) Glucose transporter localization in brain using light and electron immunocytochemistry. J Neurosci Res 22:464-472
18. González-Mariscal L, Betanzos A, Nava P, Jaramillo BE (2003) Tight junction proteins. Prog Biophys Mol Biol 81:1-44
19. Goodenough DA (1999) Plugging the leaks. Proc Natl Acad Sci USA 96:319-321
20. Hirase T, Staddon JM, Saitou M, Ando-Akatsuka Y, Itoh M, Furuse M, Fujimoto K, Tsukita S, Rubin LL (1997) Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 110:1603-1613
21. Itoh M, Sasaki H, Furuse M, Ozaki H, Kita T, Tsukita S (2001) Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J Cell Biol 154:491-497
22. Ivanov AI, Nusrat A, Parkos CA (2004) Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol Biol Cell 15:176-188
23. Janzer RC, Raff MC (1987) Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325:253-257
24. 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
25. Kniesel U, Wolburg H (2000) Tight junctions of the blood-brain barrier. Cell Mol Neurobiol 20:57-76
26. Kniesel U, Risau W, Wolburg H (1996) Development of blood-brain barrier tight junctions in the rat cortex. Dev Brain Res 96:229-240
27. Lacaz-Vieira F, Jaeger MM, Farshori P, Kachar B (1999) Small synthetic peptides homologous to segments of the first external loop of occludin impair tight junction resealing. J Membr Biol 168:289-297
28. Laterra J, Guerin C, Goldstein GW (1990) Astrocyte induce neural microvascular endothelial cells to form capillary-like structure in vitro. J Cell Physiol 144:204-215
29. Liebner S, Kniesel U, Kalbacher H, Wolburg H (2000) Correlation of tight junction morphology with the expression of tight junction proteins in blood-brain barrier endothelial cells. Eur J Cell Biol 79:707-717
30. Lippoldt A, Liebner S, Andbjer B, Kalbacher H, Wolburg H, Haller H, Fuxe K (2000a) Organization of choroid plexus epithelial and endothelial cell tight junctions and regulation of claudin-1, -2 and -5 expression by protein kinase C. Neuroreport 11:1427-1431
31. Lippoldt A, Kniesel U, Liebner S, Kalbacher H, Kirsch T, Wolburg H, Haller H (2000b) Structural alterations of tight junctions are associated with loss of polarity in stroke-prone spontaneously hypertensive rat blood-brain barrier endothelial cells. Brain Res 885:251-261
32. Marín-Padilla M (1987) Embryogenesis of the early vascularization of the central nervous system. In: Yasargil MG (ed) Microneurosurgery, vol 3. Thieme, Stuttgart, pp 23-44
33. Marín-Padilla M (1995) Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocytes in the human cerebral cortex: a Golgi study. J Comp Neurol 357:554-572
34. Matter K, Balda S (2003) Holey barrier: claudins and the regulation of brain endothelial permeability. J Cell Biol 161:459-460
35. Meyer G, Schaaps JP, Moreau L, Goffinet AM (2000) Embryonic and early fetal development of the human neocortex. J Neurosci 20:1858-1868
36. Møllgård K, Saunders NR (1986) The development of the human blood-brain and blood-CSF barriers. Neuropathol Appl Neurobiol 12:337-358
37. Morcos Y, Hosie MJ, Bauer H-C, Chan-Ling T (2001) Immunolocalization of occludin and claudin-1 to tight junctions in intact CNS vessels of mammalian retina. J Neurocytol 30:107-123
38. Morita K, Furuse M, Fujimoto K, Tsukita S (1999a) Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci U S A 96:511-516
39. Morita K, Sasaki H, Furuse M, Tsukita S (1999b) Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol 147:185-194
40. Nag S (2003) Morphology and molecular properties of cellular components of normal cerebral vessels. In: Nag S (ed) The blood-brain barrier. Biology and research protocols. Humana, Totowa, NJ, pp 3-36
41. Nagy Z, Peters H, Huttner I (1984) Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions. Lab Invest 50:313-322
42. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, Furuse M, Tsukita S (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161:653-660
43. Norman MG, O'Kusky JR (1986) The growth and development of microvasculature in human cerebral cortex. J Neuropathol Exp Neurol 45:222-232
44. Nusrat A, Turner JR, Madara JL (2000) Molecular physiology and pathophysiology of tight junctions. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am J Physiol Gastrointest Liver Physiol 279: G851-G857
45. Papadopoulos MC, Saadoun S, Woodrow CJ, Davies DC, Costa-Martins P, Moss RF, Krishna S, Bell BA (2001) Occludin expression in microvessels of neoplastic and non-neoplastic human brain. Neuropathol Appl Neurobiol 27:384-395
46. Pekny M, Stanness KA, Eliasson C, Betsholtz C, Janigro D (1998) Impaired induction of blood-brain barrier properties in aortic endothelial cells by astrocytes from GFAP-deficient mice. Glia 22:390-400
47. Plate KH (1999) Mechanisms of angiogenesis in the brain. J Neuropathol Exp Neurol 58:313-320
48. 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
49. Risau W (1993) Development of the vascular system of organs and tissues. In: Schaper W, Schaper J (eds) Collateral circulation. Kluwer Academic, Norwell, pp 17-28
50. Risau W (1997) Mechanisms of angiogenesis. Nature 386:671-674
51. Roncali L, Nico B, Ribatti D, Bertossi M, Mancini L (1986) Microscopical and ultrastructural investigation on the development of the blood-brain barrier in the chick embryo optic tectum. Acta Neuropathol 70:193-201
52. Rubin LL, Staddon JM (1999) The cell biology of the blood-brain barrier. Annu Rev Neurosci 22:11-28
53. Saitou M, Furuse M, Sasaki H, Schulzke J-D, Fromm M, Takano H, Noda T, Tsukita S (2000) Complex phenotype of mice lacking occludin, a component of tight junction strands. Am Soc Cell Biol 11:4131-4142
54. Sasaki H, Matsui C, Furuse K, Mimori-Kiyosue Y, Furuse M, Tsukita S (2003) Dynamic behavior of paired claudin strands within apposing plasma membranes. Proc Natl Acad Sci U S A 100:3971-3976
55. Saunders NR (1977) Ontogeny of the blood-brain barrier. Exp Eye Res S25:523-550
56. Savettieri G, Di Liegro I, Catania C, Licata L, Pitarresi GL, D'Agostino S, Schiera G, De Caro V, Giandalia G, Giannola LI, Cestelli A (2000) Neurons and ECM regulate occludin localization in brain endothelial cells. Neuroreport 11:1081-1084
57. Smart IHM, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12:37-53
58. Sobue K, Yamamoto N, Yoneda K, Hodgson ME, Yamashiro K, Tsuruoka N, Tsuda T, Katsuya H, Miura Y, Asai K, Kato T (1999) Induction of blood-brain barrier properties in immortalized bovine brain endothelial cells by astrocytic factors. Neurosci Res 35:155-164
59. Tagami M, Yamagata K, Fujino H, Kubota A, Nara Y, Yamori Y (1992) Morphological differentiation of endothelial cells co-cultured with astrocytes on type-I or type-IV collagen. Cell Tissue Res 268:225-232
60. Tilling T, Korte D, Hoheisel D, Galla HJ (1998) Basement membrane proteins influence brain capillary endothelial barrier function in vitro. J Neurochem 71:1151-1157
61. Tsukita S, Furuse M (1999) Occludin and claudins in tight-junction strands: leading or supporting players? Trends Cell Biol 9:268-273
62. Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285-293
63. Virgintino D, Robertson D, Monaghan P, Errede M, Ambrosi G, Roncali L, Bertossi M (1998a) Glucose transporter GLUT1 localization in human foetus telencephalon. Neurosci Lett 256:147-150
64. Virgintino D, Maiorano E, Errede M, Vimercati A, Greco P, Selvaggi L, Roncali L, Bertossi M (1998b) Astroglia-microvessel relationship in the developing human telencephalon. Int J Dev Biol 42:1165-1168
65. Virgintino D, Robertson D, Benagiano V, Errede M, Bertossi M, Ambrosi G, Roncali L (2000) Immunogold cytochemistry of the blood-brain barrier glucose transporter GLUT1 and endogenous albumin in the developing human brain. Dev Brain Res 123:95-101
66. Vorbrodt A, Dobrogowska DH (1994) Immunocytochemical evaluation of blood-brain barrier to endogenous albumin in adult, newborn and aged mice. Folia Histochem Cytobiol 32:63-70
67. Vorbrodt A, Dobrogowska DH (2003) Molecular anatomy of intercellular junctions in brain endothelial and epithelial barriers: electron microscopist's view. Brain Res Rev 42:221-242
68. Vorbrodt A, Dobrogowska DH, Tarnawski M (2001) Immunogold study of interendothelial junction-associated and glucose transporter proteins during postnatal maturation of the mouse blood-brain barrier. J Neurocytol 30:705-716
69. Willis CL, Nolan CC, Reith SN, Lister T, Prior MJW, Guerin CJ, Mavroudis G, Ray DE (2004) Focal astrocyte loss is followed by microvascular damage, with subsequent repair of the blood-brain barrier in the apparent absence of direct astrocytic contact. Glia 45:325-337
70. Wolburg H, Lippoldt A (2002) Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 38:323-337
71. Wolburg H, Wolburg-Buchholz K, Kraus J, Rascher-Eggstein G, Liebner S, Hamm S, Duffner F, Grote E-H, Risau W, Engelhardt B (2003) 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 105:586-592