ICA 512, an autoantigen of type I diabetes, is an intrinsic membrane protein of neurosecretory granules

EMBO Journal

Volumn 15, Issue 9, 1996, Pages 2102-2114

  Solimena, Michele ^a   Dirkx Jr , Ronald ^a   Hermel, Jean Michel ^a   Pleasic Williams, Susan ^b   Shapiro, Jeffrey A ^b   Caron, Laurent ^a   Rabin, Daniel U ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYER CORPORATION   (United States)

Author keywords

1A 2; Autoantigens; Insulin dependent diabetes mellitus; Neurosecretory granules; Protein tyrosine phosphatase

Indexed keywords

AUTOANTIGEN; MEMBRANE PROTEIN; PROTEIN TYROSINE PHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; GOLGI COMPLEX; HUMAN; IMMUNOPRECIPITATION; INSULIN DEPENDENT DIABETES MELLITUS; NEUROSECRETORY CELL; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RABBIT; RAT; SECRETORY GRANULE; SEQUENCE HOMOLOGY;

EID: 0029940504     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00564.x     Document Type: Article

References (59)

1. Atkinson, M.A., Bowman, M.A., Campbell, L., Darrow, B.L., Kaufman, D.L. and Maclaren, N.K. (1994) Cellular immunity to a determinant common to glutamate decarboxylase and Coxsackie virus in insulin-dependent diabetes. J. Clin. Invest., 94, 2125-2129.
2. Bækkeskov, S., Aanstoot, H.J., Christgau, S., Reetz, A., Solimena, M , Cascalho, M., Folli, F., Richter-Olesen, H. and De Camilli, P. (1990) Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature, 347, 151-156.
3. Banker, G.A and Cowan, W.M. (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res., 126, 397-425.
4. Bergman, B. and Haskins, K. (1994) Islet-specific T-cell clones from the NOD mouse respond to beta-granule antigen. Diabetes, 43, 197-203.
5. Bottazzo, G.F., Dean, B.M., McNally, J.M., MacKay, E H., Swift, P.G. and Gamble, D.R. (1985) In situ characterization of autoimmune phenomena and expression of HLA molecules in the pancreas in diabetic insulitis. New Engl. J. Med., 313, 353-360.
6. Brady-Kalnay, S.M. and Tonks, N.K (1994) Identification of the homophilic binding site of the receptor protein tyrosine phosphatase PTPμ. J. Biol. Chem., 269, 28472-28477.
7. Brand, S.H. and Castle, J.D. (1993) SCAMP 37, a new marker within the general cell surface recycling system. EMBO J., 12, 3753-3761.
8. Brand, S.H., Laurie, S.M , Mixon, M.B and Castle J.D. (1991) Secretory carrier membrane proteins 31-35 define a common protein composition among secretory carrier membranes. J. Biol. Chem., 266, 18949-18957.
9. Buckley, K.M., Floor, E. and Kelly, R.B. (1987) Cloning and sequence analysis of cDNA encoding p38, a major synaptic vesicle protein. J. Cell Biol., 105, 2447-2456.
10. Castano, L., Russo, E., Zhou, L., Lipes, M.A. and Eisenbarth, G.S. (1991) Identification and cloning of a granule autoantigen (carboxypeptidase-H) associated with type I diabetes. J. Clin. Endocrinol. Metab., 73, 1197-1201.
11. Chavrier, P., Parton, R.G., Hauri, H.P., Simons, K. and Zerial, M. (1990) Localization of the low molecular weight GTP-binding proteins to exocytic and endocytic compartments. Cell, 62, 317-329.
12. Chilcote, T.J., Galli, T , Mundigl, O., Edelmann, L., McPherson, P.S., Takei, K. and De Camilli, P. (1995) Cellubrevin and synaptobrevins: similar subcellular localization and biochemical properties in PC12 cells. J. Cell Biol., 129, 219-231
13. Clift-O'Grady, L., Linstedt, A.D , Lowe, A.W., Grote, E. and Kelly, R.B. (1990) Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC-12 J. Cell Biol , 110, 1693-1703.
14. De Camilli, P., Cameron, R. and Greengard, P. (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell Biol., 96, 1337-1354.
15. De Camilli, P., Benfenati, F., Valtorta, F. and Greengard, P. (1990) The synapsins. Annu. Rev. Cell Biol., 6, 433-460.
16. Eipper, B.A., Milgram, S.L., Husten, E.J., Yun, H.Y. and Mains, R.E. (1993) Peptidylglycine alpha-amidating monooxygenase: a multifunctional protein with catalytic, processing, and routing domains. Protein Sci., 2, 489-497.
17. Erickson, J.D., Eiden, L.E. and Hoffman, B.J. (1992) Expression cloning of a reserpine-sensitive vesicular monoamine transporter. Proc. Natl Acad. Sci. USA, 89, 10993-10997
18. Feany, M.B., Lee, S., Edwards, R.H. and Buckley, K.M. (1992) The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell, 70, 861-867.
19. Fischer von Mollard, G., Stahl, B., Walch-Solimena, C., Takei, K., Daniels, L., Khoklatchev, A., De Camilli, P., Sudhof, T.C. and Jahn, R. (1994) Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur. J. Cell Biol., 65, 319-326.
20. Harrison, L C., De Aizpurua, H., Loudovaris, T., Campbell, I.L., Cebon, J.S., Tait, B D. and Colman, P.G. (1991) Reactivity to human islets and fetal pig proislets by peripheral blood mononuclear cells from subjects with preclinical and clinical insulin-dependent diabetes. Diabetes, 40, 1128-1133.
21. Jahn, R., Schiebler, W., Ouimet, C. and Greengard, P. (1985) A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc. Natl Acad Sci USA, 82, 4137-4141.
22. Jiang, Y.P., Wang, H., D'Eustachio, P., Musacchio, J.M., Schlessinger, J. and Sap, J (1993) Cloning and characterization of R-PTP-kappa, a new member of the receptor protein tyrosine phosphatase family with a proteolytically cleaved cellular adhesion molecule-like extracellular region. Mol. Cell. Biol., 13, 2942-2951.
23. Keller, R.J. (1990) Cellular immunity to human insulin in individuals at high risk for the development of type I diabetes mellitus. J. Autoimmun., 3, 321-327.
24. Kostron, H., Winkler, H., Peer, L.J. and Konig, P. (1977) Uptake of adenosine triphosphate by isolated adrenal chromaffin granules: a carrier-mediated transport. Neuroscience, 2, 159-166.
25. Krueger, N.X., Streuli, M and Saito, H. (1990) Structural diversity and evolution of human receptor-like protein tyrosine phosphatases. EMBO J., 9, 3241-3252.
26. Lan, M.S., Lu, J., Goto, Y. and Notkins, A.L. (1994) Molecular cloning and identification of a receptor-type protein tyrosine phosphatase, IA-2, from human insulinoma. DNA Cell Biol., 13, 505-514.
27. Lowe, A.W , Madeddu, L and Kelly, R.B. (1988) Endocrine secretory granules and neuronal synaptic vesicles have three integral membrane proteins in common. J. Cell Biol., 106, 51-59
28. Lu, J., Notkins, A.L. and Lan, M.S. (1994) Isolation, sequence and expression of a novel mouse brain cDNA, mIA-2, and its relatedness to members of the protein tyrosine phosphatase family. Biochem Biophys. Res. Commun , 204, 930-936.
29. Miller, B J., Appel, M.C , O'Neil, J.J. and Wicker, L.S. (1988) Both the Lyt-2+ and L3T4+ T cell subsets are required for the transfer of diabetes in nonobese diabetic mice. J Immunol., 140, 52-58.
30. Mundigl, O., Matteoli, M., Daniell, L., Thomas-Reetz, A., Metcalf, A., Jahn, R and De Camilli, P. (1993) Synaptic vesicle proteins and early endosomes in cultured hippocampal neurons: differential effects of Brefeldin A in axon and dendrites. J Cell Biol., 122, 1207-1221.
31. Navone, F., Di Gioia, G., Jahn, R., Browning, M., Greengard, P and De Camilli, P. (1989) Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J. Cell Biol., 109, 3425-3433.
32. Nelson, N. and Lill, H. (1994) Porters and neurotransmitter transporters. J. Exp Biol. 196, 213-228.
33. Obendorf, D., Schwarzenbrunner, U., Fischer-Colbrie, R., Laslop, A. and Winkler, H. (1988) Immunological characterization of a membrane glycoprotein of chromaffin granules, its presence in endocrine and exocrine tissues. Neuroscience, 25, 343-351.
34. O'Farrell, P.H. (1975) High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem., 250, 4007-4021.
35. Orci, L., Ravazzola, M., Storch, M.J., Anderson, R.G., Vassalli, J.D. and Perrelet, A. (1987) Proteolytic maturation of insulin is a post-Golgi event which occurs in acidifying clathrin-coated secretory vesicles. Cell, 49, 865-868.
36. Palmer, J.P., Asplin, C.M., Clemons, P , Lyen, K., Tatpati, O., Raghu, P.K. and Paquette, T.L. (1983) Insulin antibodies in insulin-dependent diabetics before insulin treatment. Science, 222, 1337-1339.
37. Panina-Bordignon, P. Lang, R., Van Endert, P., Benazzi, E., Felix, A M., Pastore, R.M., Spinas, G.A. and Sinigaglia, F. (1995) Cytotoxic T-cells specific for glutamic acid decarboxylase in autoimmune diabetes. J. Exp. Med., 181, 1923-1927.
38. Pietropaolo, M., Castano, L., Babu, S , Buelow, R., Kuo, Y.L., Martin, S., Martin, A., Powers, A.C., Prochazka, M., Naggert, J., Leiter, E.H. and Eisenbarth, G.S. (1993) Islet cell autoantigen 69 kDa (ICA69). Molecular cloning and characterization of a novel diabetes-associated autoantigen. J. Clin Invest., 92, 359-371.
39. Rabin, D.U., Pleasic, S.M., Palmer-Crocker, R. and Shapiro, J.A. (1992) Cloning and expression of IDDM-specific human autoantigens. Diabetes, 41, 183-186.
40. Rabin, D.U., Pleasic, S.M., Shapiro, J.A., Yoo-Warren, H., Oles, J., Hicks, J.M., Goldstein, D.E. and Rae, P.M. (1994) Islet cell antigen 512 is a diabetes-specific islet autoantigen related to protein tyrosine phosphatases. J. Immunol., 152, 3183-3188.
41. Reetz, A., Solimena, M., Matteoli, M., Folli, F., Takei, K. and De Camilli, P. (1991) GABA and pancreatic beta-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J., 10, 1275-1284.
42. Reich, E.P., Sherwin, R.S., Kanagawa, O. and Janeway, C.A ,Jr (1989) An explanation for the protective effect of the MHC class II I-E molecule in murine diabetes. Nature, 341, 326-328.
43. Roep, B.O., Arden, S.D., de Vries, R.R. and Hutton, J.C. (1990) T-cell clones from a type-1 diabetes patient respond to insulin secretory granule proteins. Nature, 345, 632-634.
44. Roep, B.O., Kallan, A.A., Duinkerken, G., Arden, S.D., Hutton, J.C., Bruining, G.J. and de Vries, R.R. (1995) T-cell reactivity to beta-cell membrane antigens associated with beta-cell destruction in IDDM. Diabetes, 44, 278-283.
45. Ronnet, G.V., Hester, L.D. and Snyder, S.H. (1991) Primary culture of neonatal rat olfactory neurons. J. Neurosci., 11, 1243-1255.
46. Rosa, P , Hille, A., Lee, R.W., Zanini, A , De Camilli, P. and Huttner, W.B. (1985) Secretogranins I and II: two tyrosine-sulfated secretory proteins common to a variety of cells secreting peptides by the regulated pathway J. Cell Biol., 101, 1999-2011.
47. Saito, H., Streuli, M., Krueger, N.X., Itoh, M. and Tsai, A.Y. (1992) CD45 and a family of receptor-linked protein tyrosine phosphatases. Biochem. Soc Trans., 20, 165-169.
48. Seidah, N.G , Chretien, M. and Day, R. (1994) The family of subtilisin/ kexin like pro-protein and pro-hormone convertases: divergent or shared functions. Biochimie, 76, 197-209
49. Serra-Pages, C., Saito, H. and Streuli, M. (1994) Mutational analysis of proprotein processing, subunit association, and shedding of the LAR transmembrane protein tyrosine phosphatase. J. Biol. Chem., 269, 23632-23641.
50. Sibley, R.K., Sutherland, D.E., Goetz, F. and Michael, A.F. (1985) Recurrent diabetes mellitus in the pancreas iso- and allograft. A light and electron microscopic and immunohistochemical analysis of four cases. Lab. Invest., 53, 132-144.
51. Silsand, T. and Flatmark, T (1974) Purification of cytochrome b-561. An integral heme protein of the adrenal chromaffin granule membrane. Biochim. Biophys Acta, 359, 257-266.
52. Sohmena, M. and De Camilli, P. (1994) Diabetes. Spotlight on a neuronal enzyme. Nature, 366, 15-17
53. Streuli, M., Krueger, N.X., Arintello, P.D., Tang, M., Munro, J.M., Blattler, W.A , Adler, D.A., Disteche, C.M. and Saito, H. (1992) Expression of the receptor-linked protein tyrosine phosphatase LAR: proteolytic cleavage and shedding of the CAM-like extracellular region EMBO J., 11, 897-907.
54. Walch-Solimena, C., Takei, K., Marek, K L., Midyett, K., Sudhof, T.C., De Camilli, P. and Jahn, R. (1993) Synaptotagmin: a membrane constituent of neuropeptide-containing large dense-core vesicles. J. Neurosci., 13, 3895-3903.
55. Webster, P., Vanacore, L., Naim, A C. and Marino, C.R. (1994) Subcellular localization of CFTR to endosomes in a ductal epithelium. Am. J. Physiol., 267, C340-C348.
56. Wiedenmann, B. and Franke, W.W (1985) Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles Cell, 41, 1017-1028
57. Xu, T. Caron, L., Fehon, G. and Artavanis-Tsakonas, S (1992) The involvement of the Notch locus in Drosophila oogenesis. Development, 115, 913-922.
58. Yamashita, S. and Yasuda, K. (1992) Monoclonal antibody to a common antigen of secretory granule membranes: intracellular localization and recycling of the antigen after secretion. J. Histochem. Cytochem., 40, 793-806.
59. Zhang, Z-Y., Wang, Y. and Dixon, J.E. (1994) Dissecting the catalytic mechanism of protein tyrosine phosphatases. Proc Natl Acad. Sci USA, 91, 1624-1627.