Agrin accumulates in the brain microvascular basal lamina during development of the blood-brain barrier

Developmental Dynamics

Volumn 208, Issue 1, 1997, Pages 62-74

  Barber, Alistair J ^a   Lieth, Erich ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

agrin; astrocyte; basal lamina; blood brain barrier; chick; development; endothelial cell; microvessel; rat

Indexed keywords

AGRIN;

ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN DEVELOPMENT; BRAIN MICROCIRCULATION; CHICK EMBRYO; EMBRYO; EMBRYO DEVELOPMENT; HUMAN; IMMUNOBLOTTING; MICROVASCULATURE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SYNAPTOGENESIS; TISSUE DISTRIBUTION;

EID: 0031015296     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1097-0177(199701)208:1<62::aid-aja6>3.0.co;2-%23     Document Type: Article

References (59)

1. Arthur, F.E., Shivers, R.R., and Bownam, P.D. (1987) Astrocyte mediated induction of tight junctions in brain capillary endothelium: An efficient in vitro model. Dev. Brain Res. 36:155-159.
2. Bar, T. (1980) The vascular system of the cerebral cortex. Adv. Anat. Embryol. Cell Biol. 59:1-62.
3. Barber, A., and Lieth, E. (1995) Agrin expression on brain capillaries develops simultaneously with the blood-brain barrier. Soc. Neurosci. Abst. 25:826.
4. Betz, A.L., Csejtey, J., and Goldstein, G.W. (1979) Hexose transport and phosphorylation by capillaries isolated from rat brain. Am. J. Physiol. 236:C96-C102.
5. Biroc, S.L., Payan, D.G., and Fisher, J.M. (1993) Isoforms of agrin are widely expressed in the developing rat and may function as protease inhibitors. Dev. Brain Res. 75:119-129.
6. Bowe, M.A., Deyst, K.A., Leszyk, J.D., and Fallon, J.R. (1994) Identification and purification of an agrin receptor from torpedo postsynaptic membranes: A heteromeric complex related to the dystroglycans. Neuron 12:1173-1180.
7. Cagliero, E., Roth, T., Roy, S., and Lorenzi, M. (1991) Characteristics and mechanisms of high-glucose-induced overexpression of basement membrane components in cultured human endothelial cells. Diabetes 40:102-110.
8. Campanelli, J.T., Hoch, W., Rupp, F., Kreiner, T., and Scheller, R.H. (1991) Agrin mediates cell contact-induced acetylcholine receptor clustering. Cell 67:909-916.
9. Campbell, K.P., and Kahl, S.D. (1989) Association of dystrophin and an integral membrane glycoprotein. Nature 338:259-262.
10. Cancilla, P.A., Bready, J., and Berliner, J. (1993) Brain Endothelial-Astrocyte Interactions. In: "The Blood-Brain Barrier." Pardridge, W.M. (ed). New York: Raven Press, Ltd., pp. 25-46.
11. DeBault, L., and Cancilla, P.A. (1980) Gamma-glutamyl transpeptidase in isolated brain endothelial cells: Induction by glial cells in vitro. Science 207:635-645.
12. Delorme, P., Gayet, J., and Grignon, G. (1970) Ultrastructural study on transcapillary exchanges in the developing telencephalon in the chicken. Brain Res. 22:2269-2283.
13. Ervasti, J.M., Ohlendieck, K., Kahl, S.D., Gaver, M.G., and Campbell, K.P. (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345:315-319.
14. Estrada, C., Bready, J.V., Berliner, J.A., Pardridge, W.M., and Cancilla, P.A. (1990) Astrocyte growth stimulation by a soluble factor produced by cerebral endothelial cells in vitro. J. Neuropathol. Exp. Neurol. 49:539-549.
15. Ferns, M., Hoch, W., Campanelli, J.T., Rupp, F., Hall, Z.W., and Scheller, R.H. (1992) RNA splicing regulated agrin-mediated acetylcholine receptor clustering activity on cultured myotubes. Neuron 8:1079-1086.
16. Gay, D., and Esiri, M. (1991) Blood-brain barrier damage in acute multiple sclerosis plaques. Brain 114:557-572.
17. Gee, S.H., Blacher, R.W., Douville, P.J., Provost, P.R., Yurchenco, P.D., and Carbonetto, S. (1993) Laminin-binding protein 120 from brain is closely related to the dystrophin-associated glycoprotein, dystroglycan, and bind with high affinity to the major heparin binding domain of laminin. J. Biol. Chem. 268:14972-14980.
18. Glass, D.J., Bowen, D.C., Stitt, T.N., Radziejiewski, C., Bruno, J., Ryan, T.E., Gies, D.R., Shah, S., Mattsson, K., Burden, S.J., DiStefano, P.S., Valenzuela, D.M., DeChiara, T.M., and Yancopoulos, G.D. (1996) Agrin acts via a MuSK receptor complex. Cell 85:513-523.
19. Godfrey, E.W., Dietz, M.E., Morstad, A.L., Wallskog, P.A., and Yorde, D.E. (1988) Acetylcholine receptor-aggregating proteins are associated with the extracellular matrix of many tissues in Torpedo. J. Cell Biol. 106:1263-1272.
20. Hoch, W., Ferns, M., Campanelli, J.T., Hall, Z.W., and Scheller, R.H. (1993) Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11:479-490.
21. Hoch, W., Campanelli, J.T., Harrison, S., and Scheller, R.H. (1994) Structural domains of agrin required for clustering of nicotinic acetylcholine receptors. EMBO J. 13:2814-2821.
22. Hoyer, L.W., de los Santos, R.P., and Hoyer, J.R. (1973) Antihemophiliac factor antigen: Localization in endothelia by immunofluorescent microscopy. J. Clin. Invest. 52:2737-2744.
23. Hunter, D.D., Shah, V., Merlie, J.P., and Sanes, J.R. (1989) A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338:229-234.
24. Hunter, D.D., Llinas, R., Ard, M., Merlie, J.P., and Sanes, J.R. (1992) Expression of s-laminin and laminin in the developing rat central nervous system. J. Comp. Neurol. 323:238-251.
25. Ibraghimov-Beskrovnaya, O., Milatovich, A., Ozcelik, T., Yang, B., Koepnick, K., Francke, U., and Campbell, K.P. (1993) Human dystroglycan: Skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum. Mol. Genet. 2:1651-1657.
26. Johanson, C.E. (1980) Permeability and vascularity of the developing brain: Cerebellum vs. cerebral cortex. Brain Res. 190:3-16.
27. Khurana, T.S., Watkins, S.C., and Kunkel, L.M. (1992) The subcellular distribution of chromosome 6-encoded dystrophin-related protein in the brain. J. Cell Biol. 119:357-366.
28. Kolodziej, P.A., and Young, R.A. (1991) Epitope tagging and protein surveillance. Meth. Enzymol. 194:508-519.
29. Kramarcy, N.R., Vidai, A., Froehner, S.C., and Sealock, R. (1994) Association of utrophin and multiple dystrophin short forms with the mammalian Mr 58,000 dystrophin-associated protein (syntrophin). J. Biol. Chem. 269:2870-2876.
30. Lee, V.M.-Y., Page, C.D., Wu, H.-L., and Schlaepfer, W.W. (1984) Monoclonal antibodies to gel-excised glial filament protein and their reactivities with other intermediate filament proteins. J. Neurochem. 42:25-32.
31. Lieth, E., Cardasis, C.A., and Fallen, J.R. (1992) Muscle-derived agrin in cultured myotubes: Expression in the basal lamina and at induced acetylcholine receptor clusters. Dev. Biol. 149:41-54.
32. Lieth, E., Barber, A., and Gardner, T.W. (1995) Astrocyte expression of brain microvascular agrin-related protein is induced by endothelial cells. Mol. Biol. Cell. 6:337a.
33. Magill-Solc, C., and McMahan, U.J. (1988) Motor neurons contain agrin-like molecules. J. Cell Biol. 107:1825-1833.
34. Maher, F., Simpson, I.A., and Vannucci, S.J. (1993) Alterations in brain glucose transporter proteins, GLUT1 and GLUT3, in streptozotocin diabetic rats. In "Frontiers in Cerebral Vascular Biology: Transport and Its Regulation." Drewes, L.R., and Beta, A.L. (eds). New York; Plenum Press, pp. 9-12.
35. Matsumura, K., and Campbell, K.P. (1993) Deficiency of dystrophinassociated proteins: A common mechanism leading to muscle cell necrosis in severe childhood muscular dystrophies. Neuromusc. Disord. 3:109-118.
36. Maxwell, K., Berliner, J., and Cancilla, P.A. (1989) Stimulation of glucose analogue uptake by cerebral microvessel endothelial cells by a product released by astrocytes. J. Neuropathol. Exp. Neurol. 48:69-80.
37. McMahan, U.J. (1990) The agrin hypothesis. CSH Symp. Quant. Biol. 55:407-418.
38. Montanaro, F., Carbonetto, S., Campbell, K.P., and Lindenbaum, M. (1995) Dystroglycan expression in the wild type and mdx mous neural retina: Synaptic colocalization with dystrophin, dystrophin-related protein, but not laminin. J. Neurosci. Res. 42:528-538.
39. Murata, T., Ishibashi, T., and Inomata, H. (1992) Immunohistochemical detection of extravasated fibrinogen (fibrin) in human diabetic retina. Graefe's Arch. Clin. Exp. Ophthalmol. 230:428-431.
40. Nastuk, M.A., Lieth, E., Ma, J., Cardasis, C.A., Moynihan, E.B., McKechnie, B.A., and Fallon, J.R. (1991) The putative agrin receptor binds ligand in a calcium-dependent manner and aggregates during agrin-induced acetylcholine receptor clustering. Neuron 7:807-818.
41. Nitkin, R.M., Smith, M.A., Magill, C., Fallon, J.R., Yao, Y.M., Wallace, B.G., and McMahan, U.J. (1987) Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J. Cell Biol. 105:2471-2478.
42. Osterby, R. (1983) Basement membrane morphology in diabetes mellitus. In: "Diabetes Mellitus, Theory and Practice." Ellenberg M., and Rifkin, H. (eds). New Hyde Park, NY: Medical Examiner, pp. 323-341.
43. Pasternak, C., Wong, S., and Elson, E.L. (1995) Mechanical function of dystrophin in muscle cells. J. Cell Biol. 128:355-361.
44. Purdy, J.L., and Bondy, S.C. (1976) Blood-brain barrier: Selective changes during maturation. Neuroscience 1:125-129.
45. Reist, N.E., Magill, C., and McMahan, U.J. (1987) Agrin-like molecules at synaptic sites in normal, denervated, and damaged skeletal muscles. J. Cell Biol. 105:2557-2469.
46. Risau, W., and Lemmon, V. (1988) Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev. Biol. 125:441-450.
47. Rosenberg, G.A., Kornfeld, M., Extrada, E., Kelley, R.O., Liotta, L.A., and Stetler-Stevenson, W.G. (1992) TIMP-2 reduces proteolytic opening of blood-brain barrier by type IV collagenase. Brain Res. 576:203-207.
48. Rosenberg, G.A., Estrada, E., Kelley, R.O., and Kornfeld, M. (1993) Bacterial collagenase disrupts extracellular matrix and opens blood-brain barrier in rat. Neurosci Lett 160:117-119.
49. Rupp, F., Payan, D.G., Magill-Solc, C., Cowan, D.M., and Scheller, R.H. (1991) Structure and expression of a rat agrin. Neuron 6:811-823.
50. Sanes, J.R., Hunter, D.D., Green, T.L., and Merlie, J.P. (1990) S-Laminin. Cold Spring Harbor Symp Quant Biol 55:419-430.
51. Stone, D.M., and Nikolics, K. (1995) Tissue-and age-specific expression patterns of alternatively spliced agrin mRNA transcripts in embryonic rat suggest novel developmental roles. J. Neurosci. 15: 6767-6778.
52. Sugiyama, J., Bowen, D.C., and Hall, Z.W. (1994) Dystroglycan binds nerve and muscle agrin. Neuron 13:103-115.
53. Theilen, H., and Kuschinsky, W. (1992) Fluorescence labeling of the capillary network in rat brains. J. Cereb. Blood Flow Metab. 12: 347-350.
54. Tsen, G., Halfter, W., Kroger, S., and Cole, G.J. (1995a) Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270:3392-3399.
55. Tsen, G., Napier, A., Halfter, W., and Cole, G.J. (1995b) Identification of a novel alternatively spliced agrin mRNA that is preferentially expressed in non-neuronal cells. J. Biol. Chem. 270:15934-15937.
56. Valenzuela, D.M., Stitt, T.N., DiStefano, P.S., Rojas, E., Mattsson, K., Compton, D.L., Nunez, L., Par, J.S., Stark, J.L., Gies, D.R., Thomas, S., Le Beau, M.M., Fernald, A.A., Copeland, N.G., Jenkins, N.A., Burden, S.J., Glass, D.J., and Yancopoulos, G.D. (1995) Receptor tyrosine kinase specific for the skeletal muscle lineage: Expression of embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15:573-584.
57. Vannucci, S.J. (1994) Developmetnal expression of GLUT1 and GLUT3 glucose transporters in rat brain. J. Neurochem. 62:240-246.
58. Vinores, S.A., Campochiaro, P.A., Lee, A., McGehee, R., Gadegbeku, C., and Green, W.R. (1990) Localization of blood-retinal barrier breakdown in human pathologic specimens by immunohistochemical staining for albumin. Lab. Invest. 62:742-750.
59. Watson, P.M., Anderson, J.M., Vanltallie, C.M., and Doctrow, S.R. (1991) The tight-junction-specific protein ZO-1 is a component of the human and rat blood-brain barriers. Neurosci. Lett. 129:6-10.