New role for Agrin in T cells and its potential importance in immune system regulation

Arthritis Research and Therapy

Volumn 12, Issue 2, 2010, Pages

  Jury, Elizabeth C ^a   Kabouridis, Panagiotis S ^b  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; CYTOKINE; T LYMPHOCYTE RECEPTOR;

AUTOIMMUNITY; CELL DIFFERENTIATION; CELL MIGRATION; CYTOLOGY; DOWN REGULATION; GENETIC TRANSCRIPTION; GLOMERULUS BASEMENT MEMBRANE; HUMAN; IMMUNE SYSTEM; IMMUNOREGULATION; MEMBRANE PERMEABILITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANTIGEN PRESENTING CELL; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AGRIN; ANTIGEN-PRESENTING CELLS; HUMANS; IMMUNE SYSTEM; IMMUNOLOGICAL SYNAPSES; LYMPHOCYTE ACTIVATION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 77957014341     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2957     Document Type: Review

References (53)

1. Huppa JB, Davis MM. T-cell-antigen recognition and the immunological synapse. Nat Rev Immunol 2003, 3:973-983. 10.1038/nri1245, 14647479.
2. Bromley SK, Burack WR, Johnson KG, Somersalo K, Sims TN, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML. The immunological synapse. Annu Rev Immunol 2001, 19:375-396. 10.1146/annurev.immunol.19.1.375, 11244041.
3. Shaw AS, Allen PM. Kissing cousins: immunological and neurological synapses. Nat Immunol 2001, 2:575-576. 10.1038/89712, 11429536.
4. Kaizuka Y, Douglass AD, Varma R, Dustin ML, Vale RD. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc Natl Acad Sci USA 2007, 104:20296-20301. 2154425, 18077330, 10.1073/pnas.0710258105.
5. Yokosuka T, Sakata-Sogawa K, Kobayashi W, Hiroshima M, Hashimoto-Tane A, Tokunaga M, Dustin ML, Saito T. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat Immunol 2005, 6:1253-1262. 10.1038/ni1272, 16273097.
6. Varma R, Campi G, Yokosuka T, Saito T, Dustin ML. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 2006, 25:117-127. 1626533, 16860761, 10.1016/j.immuni.2006.04.010.
7. Campi G, Varma R, Dustin ML. Actin and agonist MHC-peptide complexdependent T cell receptor microclusters as scaffolds for signaling. J Exp Med 2005, 202:1031-1036. 1373686, 16216891, 10.1084/jem.20051182.
8. Depoil D, Zaru R, Guiraud M, Chauveau A, Harriague J, Bismuth G, Utzny C, Muller S, Valitutti S. Immunological synapses are versatile structures enabling selective T cell polarization. Immunity 2005, 22:185-194. 10.1016/j.immuni.2004.12.010, 15723807.
9. Monks CRF, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998, 395:82-86. 10.1038/25764, 9738502.
10. Davis SJ, Merwe PA. The kinetic-segregation model: TCR triggering and beyond. Nat Immunol 2006, 7:803-809. 10.1038/ni1369, 16855606.
11. Dustin ML. The cellular context of T cell signaling. Immunity 2009, 30:482-492. 10.1016/j.immuni.2009.03.010, 19371714.
12. Lee KH, Dinner AR, Tu C, Campi G, Raychaudhuri S, Varma R, Sims TN, Burack WR, Wu H, Wang J, Kanagawa O, Markiewicz M, Allen PM, Dustin ML, Chakraborty AK, Shaw AS. The immunological synapse balances T cell receptor signaling and degradation. Science 2003, 302:1218-1222. 10.1126/science.1086507, 14512504.
13. Saito T, Yokosuka T. Immunological synapse and microclusters: the site for recognition and activation of T cells. Curr Opin Immunol 2006, 18:305-313. 10.1016/j.coi.2006.03.014, 16616469.
14. Sarris M, Andersen KG, Randow F, Mayr L, Betz AG. Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity 2008, 28:402-413. 2726439, 18328743, 10.1016/j.immuni.2008.01.012.
15. Vincent P, Collette Y, Marignier R, Vuaillat C, Rogemond V, Davoust N, Malcus C, Cavagna S, Gessain A, Machuca-Gayet I, Belin MF, Quach T, Giraudon P. A role for the neuronal protein collapsin response mediator protein 2 in T lymphocyte polarization and migration. J Immunol 2005, 175:7650-7660.
16. Nitkin RM, Smith MA, Magill C, Fallon JR, Yao YM, Wallace BG, McMahan UJ. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J Cell Biol 1987, 105:2471-2478. 2114709, 2826489, 10.1083/jcb.105.6.2471.
17. Ruegg MA, Bixby JL. Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci 1998, 21:22-27. 10.1016/S0166-2236(97)01154-5, 9464682.
18. Bezakova G, Ruegg MA. New insights into the roles of agrin. Nat Rev Mol Cell Biol 2003, 4:295-308. 10.1038/nrm1074, 12671652.
19. Burgess RW, Skarnes WC, Sanes JR. Agrin isoforms with distinct amino termini: differential expression, localization, and function. J Cell Biol 2000, 151:41-52. 2189804, 11018052, 10.1083/jcb.151.1.41.
20. Neumann FR, Bittcher G, Annies M, Schumacher B, Kroger S, Ruegg MA. An alternative amino-terminus expressed in the central nervous system converts agrin to a type II transmembrane protein. Mol Cell Neurosci 2001, 17:208-225. 10.1006/mcne.2000.0932, 11161480.
21. Gesemann M, Denzer AJ, Ruegg MA. Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J Cell Biol 1995, 128:625-636. 2199893, 7860635, 10.1083/jcb.128.4.625.
22. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 1996, 85:525-535. 10.1016/S0092-8674(00)81253-2, 8653788.
23. Ksiazek I, Burkhardt C, Lin S, Seddik R, Maj M, Bezakova G, Jucker M, Arber S, Caroni P, Sanes JR, Bettler B, Ruegg MA. Synapse loss in cortex of agrindeficient mice after genetic rescue of perinatal death. J Neurosci 2007, 27:7183-7195. 10.1523/JNEUROSCI.1609-07.2007, 17611272.
24. Barber AJ, Lieth E. Agrin accumulates in the brain microvascular basal lamina during development of the blood-brain barrier. Dev Dyn 1997, 208:62-74. 10.1002/(SICI)1097-0177(199701)208:1<62::AID-AJA6>3.0.CO;2-#, 8989521.
25. Khan AA, Bose C, Yam LS, Soloski MJ, Rupp F. Physiological regulation of the immunological synapse by agrin. Science 2001, 292:1681-1686. 10.1126/science.1056594, 11349136.
26. Jury EC, Flores-Borja F, Kabouridis PS. Lipid rafts in T cell signalling and disease. Semin Cell Dev Biol 2007, 18:608-615. 2596300, 17890113, 10.1016/j.semcdb.2007.08.002.
27. Zhang J, Wang Y, Chu Y, Su L, Gong Y, Zhang R, Xiong S. Agrin is involved in lymphocytes activation that is mediated by alpha-dystroglycan. FASEB J 2006, 20:50-58. 10.1096/fj.04-3303com, 16394267.
28. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, Shark KB, Grande WJ, Hughes KM, Kapur V, Gregersen PK, Behrens TW. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA 2003, 100:2610-2615. 151388, 12604793, 10.1073/pnas.0337679100.
29. Banchereau J, Pascual V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 2006, 25:383-392. 10.1016/j.immuni.2006.08.010, 16979570.
30. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, Pascual V. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med 2003, 197:711-723. 2193846, 12642603, 10.1084/jem.20021553.
31. Pascual V, Farkas L, Banchereau J. Systemic lupus erythematosus: all roads lead to type I interferons. Curr Opin Immunol 2006, 18:676-682. 10.1016/j.coi.2006.09.014, 17011763.
32. Jury EC, Eldridge J, Isenberg DA, Kabouridis PS. Agrin signalling contributes to cell activation and is overexpressed in T lymphocytes from lupus patients. J Immunol 2007, 179:7975-7983. 2596879, 18025246.
33. Dustin ML, Cooper JA. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat Immunol 2000, 1:23-29. 10.1038/76877, 10881170.
34. Alfsen A, Yu H, Magerus-Chatinet A, Schmitt A, Bomsel M. HIV-1-infected blood mononuclear cells form an integrin- and agrin-dependent viral synapse to induce efficient HIV-1 transcytosis across epithelial cell monolayer. Mol Biol Cell 2005, 16:4267-4279. 1196336, 15975901, 10.1091/mbc.E05-03-0192.
35. Hausser HJ, Ruegg MA, Brenner RE, Ksiazek I. Agrin is highly expressed by chondrocytes and is required for normal growth. Histochem Cell Biol 2007, 127:363-374. 10.1007/s00418-006-0258-2, 17186266.
36. Groffen AJ, Ruegg MA, Dijkman H, Velden TJ, Buskens CA, Born J, Assmann KJ, Monnens LA, Veerkamp JH, Heuvel LP. Agrin is a major heparan sulfate proteoglycan in the human glomerular basement membrane. J Histochem Cytochem 1998, 46:19-27.
37. Raats CJ, Bakker MA, Hoch W, Tamboer WP, Groffen AJ, Heuvel LP, Berden JH, Born J. Differential expression of agrin in renal basement membranes as revealed by domain-specific antibodies. J Biol Chem 1998, 273:17832-17838. 10.1074/jbc.273.28.17832, 9651386.
38. Raats CJ, Born J, Bakker MA, Oppers-Walgreen B, Pisa BJ, Dijkman HB, Assmann KJ, Berden JH. Expression of agrin, dystroglycan, and utrophin in normal renal tissue and in experimental glomerulopathies. Am J Pathol 2000, 156:1749-1765. 1876919, 10793086.
39. Rops AL, Vlag J, Lensen JF, Wijnhoven TJ, Heuvel LP, van Kuppevelt TH, Berden JH. Heparan sulfate proteoglycans in glomerular inflammation. Kidney Int 2004, 65:768-785. 10.1111/j.1523-1755.2004.00451.x, 14871397.
40. Hoven MJ, Rops AL, Bakker MA, Aten J, Rutjes N, Roestenberg P, Goldschmeding R, Zcharia E, Vlodavsky I, Vlag J, Berden JH. Increased expression of heparanase in overt diabetic nephropathy. Kidney Int 2006, 70:2100-2108.
41. Goldberg S, Harvey SJ, Cunningham J, Tryggvason K, Miner JH. Glomerular filtration is normal in the absence of both agrin and perlecan-heparan sulfate from the glomerular basement membrane. Nephrol Dial Transplant 2009, 24:2044-2051. 10.1093/ndt/gfn758, 19144998.
42. Harvey SJ, Jarad G, Cunningham J, Rops AL, Vlag J, Berden JH, Moeller MJ, Holzman LB, Burgess RW, Miner JH. Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol 2007, 171:139-152. 1941581, 17591961, 10.2353/ajpath.2007.061116.
43. Wijnhoven TJ, Lensen JF, Wismans RG, Lamrani M, Monnens LA, Wevers RA, Rops AL, Vlag J, Berden JH, Heuvel LP, van Kuppevelt TH. In vivo degradation of heparan sulfates in the glomerular basement membrane does not result in proteinuria. J Am Soc Nephrol 2007, 18:823-832. 10.1681/ASN.2006070692, 17251387.
44. Cotman SL, Halfter W, Cole GJ. Identification of extracellular matrix ligands for the heparan sulfate proteoglycan agrin. Exp Cell Res 1999, 249:54-64. 10.1006/excr.1999.4463, 10328953.
45. Sugiyama J, Bowen DC, Hall ZW. Dystroglycan binds nerve and muscle agrin. Neuron 1994, 13:103-115. 10.1016/0896-6273(94)90462-6, 8043271.
46. Denzer AJ, Brandenberger R, Gesemann M, Chiquet M, Ruegg MA. Agrin binds to the nerve-muscle basal lamina via laminin. J Cell Biol 1997, 137:671-683. 2139873, 9151673, 10.1083/jcb.137.3.671.
47. Sanes JR, Apel ED, Gautam M, Glass D, Grady RM, Martin PT, Nichol MC, Yancopoulos GD. Agrin receptors at the skeletal neuromuscular junction. Ann N Y Acad Sci 1998, 841:1-13. 10.1111/j.1749-6632.1998.tb10905.x, 9668217.
48. Storms SD, Kim AC, Tran BH, Cole GJ, Murray BA. NCAM-mediated adhesion of transfected cells to agrin. Cell Adhes Commun 1996, 3:497-509. 10.3109/15419069609081026, 8807193.
49. Martin PT, Sanes JR. Integrins mediate adhesion to agrin and modulate agrin signaling. Development 1997, 124:3909-3917.
50. Hilgenberg LG, Su H, Gu H, O'Dowd DK, Smith MA. Alpha3Na+/K+-ATPase is a neuronal receptor for agrin. Cell 2006, 125:359-369. 10.1016/j.cell.2006.01.052, 16630822.
51. Hilgenberg LG, Pham B, Ortega M, Walid S, Kemmerly T, O'Dowd DK, Smith MA. Agrin regulation of alpha3 sodium-potassium ATPase activity modulates cardiac myocyte contraction. J Biol Chem 2009, 284:16956-16965. 10.1074/jbc.M806855200, 19376779.
52. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, Huang JH, Hubbard SR, Dustin ML, Burden SJ. Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 2008, 135:334-342. 10.1016/j.cell.2008.10.002, 18848351.
53. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L. LRP4 serves as a coreceptor of agrin. Neuron 2008, 60:285-297. 2743173, 18957220, 10.1016/j.neuron.2008.10.006.