Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis

Journal of Experimental Medicine

Volumn 203, Issue 4, 2006, Pages 1007-1016

  Agrawal, Smriti ^a   Anderson, Per ^a   Durbeej, Madeleine ^b   Van Rooijen, Nico ^c   Ivars, Fredrik ^a   Opdenakker, Ghislain ^d   Sorokin, Lydia M ^a,e  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^e UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; BETA1 INTEGRIN; DYSTROGLYCAN; GELATINASE; GELATINASE A; GELATINASE B; LAMININ 1; MEROSIN; PERLECAN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BASEMENT MEMBRANE; BINDING AFFINITY; BLOOD BRAIN BARRIER; CELL INFILTRATION; CONTROLLED STUDY; ENCEPHALITIS; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; EXTRAVASATION; GLIA CELL; LEUKOCYTE; MACROPHAGE; MONOLAYER CULTURE; MOUSE; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; ANIMAL TISSUE; BRAIN BLOOD VESSEL; DNA CLEAVAGE;

ANIMALS; ASTROCYTES; BASEMENT MEMBRANE; CELLS, CULTURED; DYSTROGLYCANS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GELATINASES; HYDROLYSIS; LEUKOCYTE ROLLING; LEUKOCYTES; MACROPHAGES; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

ANIMALIA;

EID: 33645869560     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20051342     Document Type: Article

References (49)

1. Wolf, K., R. Muller, S. Borgmann, E.B. Brocker, and P. Friedl. 2003. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood. 102:3262-3269.
2. Yadav, R., K.Y. Larbi, R.E. Young, and S. Nourshargh. 2003. Migration of leukocytes through the vessel wall and beyond. Thromb. Haemost. 90:598-606.
3. Engelhardt, B. 1997. Lymphocyte trafficking through the central nervous system. In Adhesion Molecules and Chemokines in Lymphocyte Trafficking. A. Hamann, editor. Harwood Academic Publishers, Amsterdam. 173-200.
4. Kawakami, N., U.V. Nagerl, F. Odoardi, T. Bonhoeffer, H. Wekerle, and A. Flugel. 2005. Live imaging of effector cell trafficking and autoantigen recognition within the unfolding autoimmune encephalomyelitis lesion. J. Exp. Med. 201:1805-1814.
5. Sixt, M., B. Engelhardt, F. Pausch, R. Hallmann, O. Wendler, and L.M. Sorokin. 2001. Endothelial cell laminin isoforms, laminin 8 and 10, play decisive roles in T-cell recruitment across the blood-brain-barrier in an EAE model. J. Cell Biol. 153:933-945.
6. Reese, T., and M. Karnovsky. 1967. Fine structure localization of a blood-brain barrier to endogenous peroxidase. J. Cell Biol. 34:207-217.
7. Tian, M., C. Jacobson, S.H. Gee, K.P. Campbell, S. Carbonetto, and M. Jucker. 1996. Dystroglycan in the cerebellum is a laminin α2-chain binding protein at the glial-vascular interface and is expressed in Purkinje cells. Eur. J. Neurosci. 8:2739-2747.
8. Zaccaria, M.L., F. Di Tommaso, A. Brancaccio, P. Paggi, and T.C. Petrucci. 2001. Dystroglycan distribution in adult mouse brain: a light and electron microscopy study. Neuroscience. 104:311-324.
9. Durbeej, M., M. Henry, and K.P. Campbell. 1998. Dystroglycan in development and disease. Curr. Opin. Cell Biol. 10:594-601.
10. Talts, J.F., Z. Andac, W. Göhring, A. Brancaccio, and R. Timpl. 1999. Binding of G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan and several extracellular matrix proteins. EMBO J. 18:863-870.
11. Sugita, S., F. Saito, J. Tang, J. Satz, K. Campbell, and T.C. Sudhof. 2001. A stoichiometric complex of neurexins and dystroglycan in brain. J. Cell Biol. 154:435-445.
12. Moore, S.A., F. Saito, J. Chen, D.E. Michele, M.D. Henry, A. Messing, R.D. Cohn, S.E. Ross-Barta, S. Westra, R.A. Williamson, et al. 2002. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature. 418:422-425.
13. Tran, E.H., K. Hoekstra, N. v. Rooijen, C.D. Dijkstra, and T. Owens. 1998. Immune evasion of the CNS parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice. J. Immunol. 161:3767-3775.
14. Körner, H., D.S. Riminton, D.H. Strickland, F.A. Lemckert, J.D. Pollard, and J.D. Sedgwick. 1997. Critical points of tumor necrosis factor action in CNS autoimmune inflammation defined by gene targeting. J. Exp. Med. 186:1585-1590.
15. Grewal, I.S., H.G. Foellmer, K.D. Grewal, H. Wang, W.P. Lee, D. Tumas, C.A. Janeway Jr., and R.A. Flavell. 2001. CD62L is required on effector cells for local interactions in the CNS to cause myelin damage in experimental allergic encephalomyelitis. Immunity. 14:291-302.
16. Graesser, D., S. Mahooti, and J. Madri. 2000. Distinct roles for MMP-2 and α4 integrin in autoimmune T cell extravsastion and residency in brain parenchyma during EAE. J. Neuroimmunol. 109:121-131.
17. Gijbels, K., P. Proost, S. Masure, H. Carton, A. Billiau, and G. Opdenakker. 1993. Gelatinase B is present in the cerebrospinal fluid during EAE and cleaves myelin basic protein. J. Neurosci. Res. 36:432-440.
18. Larsen, P.H., J.E. Wells, W.B. Stallcup, G. Opdenakker, and V.W. Yong. 2003. MMP-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J. Neurosci. 23:11127-11135.
19. Van den Steen, P.E., P. Proost, A. Wuyts, J. Van Damme, and G. Opdenakker. 2000. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood. 96:2673-2681.
20. McQuibban, G.A., J.H. Gong, E.M. Tam, C.A. McCulloch, I. Clark-Lewis, and C.M. Overall. 2000. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science. 289:1202-1206.
21. Gearing, A.J., P. Beckett, M. Christodoulou, M. Churchill, J. Clements, A.H. Davidson, A.H. Drummond, W.A. Galloway, R. Gilbert, J.L. Gordon, et al. 1994. Processing of TNF-α precursor by metalloproteinases. Nature. 370:555-557.
22. Dubois, B., S. Masure, U. Hurtenbach, L. Paemen, H. Heremans, J. van der Oord, R. Sciot, T. Meinhardt, G. Hämmerling, G. Opdenakker, and B. Arnold. 1999. Resistance of young gelatinase B-deficient mice to EAE and necrotizing tail lesions. J. Clin. Invest. 104:1507-1515.
23. Kieseier, B.C., R. Kiefer, J.M. Clements, K. Miller, G.M. Wells, T. Schweitzer, A.J. Gearing, and H.P. Hartung. 1998. MMP-9 and -7 are regulated in EAE. Brain. 121:159-166.
24. Nygardas, P., and A. Hinkkanen. 2002. Up-regulation of MMP-8 and MMP-9 activity in the BALB/c mouse spinal cord correlates with the severity of EAE. Clin. Exp. Immunol. 128:245-254.
25. Gijbels, K., R.E. Galardy, and L. Steinman. 1994. Reversal of EAE with a hydroxamate inhibitor of MMPs. J. Clin. Invest. 94:2177-2182.
26. Hewson, A.K., T. Smith, J.P. Leonard, and M.L. Cuzner. 1995. Suppression of experimental allergic encephalomyelitis in the Lewis rat by the MMP inhibitor Ro31-9790. Inflamm. Res. 44:345-349.
27. Kjeldsen, L., D.F. Bainton, H. Sengelov, and N. Borregaard. 1993. Structural and functional heterogeneity among peroxidase-negative granules in human neutrophils: identification of a distinct gelatinase-containing granule subset by combined immunocytochemistry and subcellular fractionation. Blood. 82:3183-3191.
28. Moll, J., P. Barzaghi, S. Lin, G. Bezakova, H. Lochmuller, E. Engvall, U. Muller, and M.A. Ruegg. 2001. An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature. 413:302-307.
29. Herzog, C., C. Has, C.W. Franzke, F.G. Echtermeyer, U. Schlotzer-Schrehardt, S. Kroger, E. Gustafsson, R. Fässler, and L. Bruckner-Tuderman. 2004. Dystroglycan in skin and cutaneous cells: β-subunit is shed from the cell surface. J. Invest. Dermatol. 122:1372-1380.
30. Parks, W.C., C.L. Wilson, and Y.S. Lopez-Boado. 2004. MMPs as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 4:617-629.
31. Ford, A.L., A.L. Goodsall, W.F. Hickey, and J.D. Sedgwick. 1995. Normal adult ramified microglia separated from other CNS macrophages by flow cytometric sorting. J. Immunol. 154:4309-4321.
32. Nikolic, T., S. Geutskens, N. Van Rooijen, H. Drexhage, and P. Leenan. 2005. Dendritic cells and macrophages are essential for the retention of lymphocytes in (peri)-insulitis of the nonobese diabetic mouse: a phagocyte depletion study. Lab. Invest. 85:487-501.
33. Teesalu, T., A.E. Hinkkanen, and A. Vaheri. 2001. Coordinated induction of extracellular proteolysis systems during EAE in mice. Am. J. Pathol. 159:2227-2237.
34. Archambault, A.S., J. Sim, M.A. Gimenez, and J.H. Russell. 2005. Defining antigen-dependent stages of T cell migration from the blood to the CNS parenchyma. Eur. J. Immunol. 35:1076-1085.
35. Flügel, A., T. Berkowicz, T. Ritter, M. Labeur, D.E. Jenne, Z. Li, J.W. Ellwart, M. Willem, H. Lassmann, and H. Wekerle. 2001. Migratory activity and functional changes of green fluorescent effector cells before and during EAE. Immunity. 14:547-560.
36. Greter, M., F.L. Heppner, M.P. Lemos, B.M. Odermatt, N. Goebels, T. Laufer, R.J. Noelle, and B. Becher. 2005. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat. Med. 11:328-334.
37. Tam, E.M., C.J. Morrison, Y.I. Wu, M.S. Stack, and C.M. Overall. 2004. Membrane protease proteomics: isotope-coded affinity tag MS identification of undescribed MT1-MMP substrates. Proc. Natl. Acad. Sci. USA. 101:6917-6922.
38. Montanaro, F., and S. Carbonetto. 2003. Targeting dystroglycan in the brain. Neuron. 37:193-196.
39. Yamada, H., F. Saito, H. Fukuta-Ohi, D. Zhong, A. Hase, K. Arai, A. Okuyama, R. Maekawa, T. Shimizu, and K. Matsumura. 2001. Processing of β-dystroglycan by MMP disrupts the link between the extracellular matrix and cell membrane via the dystroglycan complex. Hum. Mol. Genet. 10:1563-1569.
40. Singh, J., Y. Itahana, S. Knight-Krajewski, M. Kanagawa, K.P. Campbell, M.J. Bissell, and J. Muschler. 2004. Proteolytic enzymes and altered glycosylation modulate dystroglycan function in carcinoma cells. Cancer Res. 64:6152-6159.
41. Esparza, J., M. Kruse, J. Lee, M. Michaud, and J.A. Madri. 2004. MMP-2 null mice exhibit an early onset and severe EAE due to an increase in MMP-9 expression and activity. FASEB J. 18:1682-1691.
42. Matsumura, S., S. Iwanaga, S. Mochizuki, H. Okamoto, S. Ogawa, and Y. Okada. 2005. Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice. J. Clin. Invest. 115:559-609.
43. Fernandez, F.G., L.G. Campbell, W. Liu, J.M. Shipley, S. Itohara, G.A. Patterson, R.M. Senior, T. Mohanakumar, and A. Jaramillo. 2005. Inhibition of obliterative airway disease development in murine tracheal allografts by MMP-9 deficiency. Am. J. Transplant. 5:671-683.
44. Campbell, L.G., S. Ramachandran, W. Liu, J.M. Shipley, S. Itohara, J.G. Rogers, N. Moazami, R.M. Senior, and A. Jaramillo. 2005. Different roles for MMP-2 and MMP-9 in the pathogenesis of cardiac allograft rejection. Am. J. Transplant. 5:517-528.
45. Itoh, T., T. Ikeda, H. Gomi, S. Nakao, T. Suzuki, and S. Itohara. 1997. Unaltered secretion of β-amyloid precursor protein in gelatinase A (MMP-2)-deficient mice. J. Biol. Chem. 272:22389-22392.
46. Dubois, B., S. Masure, U. Hurtenbach, L. Paemen, H. Heremans, J. van den Oord, R. Sciot, T. Meinhardt, G. Hammerling, G. Opdenakker, and B. Arnold. 1999. Resistance of young gelatinase B-deficient mice to EAE and necrotizing tail lesions. J. Clin. Invest. 104:1507-1515.
47. Oh, L.Y., P.H. Larsen, C.A. Krekoski, D.R. Edwards, F. Donovan, Z. Werb, and V.W. Yong. 1999. MMP-9/gelatinase B is required for process outgrowth by oligodendrocytes. J. Neurosci. 19:8464-8475.
48. Eusebio, A., F. Oliveri, P. Barzaghi, and M.A. Ruegg. 2003. Expression of mouse agrin in normal, denervated and dystrophic muscle. Neuromuscul. Disord. 13:408-415.
49. Gawlik, K., Y. Miyagoe-Suzuki, P. Ekblom, S. Takeda, and M. Durbeej. 2004. Laminin α1 chain reduces muscular dystrophy in laminin α2 chain deficient mice. Hum. Mol. Genet. 13:1775-1784.