Analysis of GAD65 autoantibodies in Stiff-Person syndrome patients

Journal of Immunology

Volumn 175, Issue 11, 2005, Pages 7755-7762

  Raju, Raghavanpillai ^a   Foote, Jefferson ^b   Banga, J Paul ^c   Hall, Tyler R ^d   Padoa, Carolyn J ^e   Dalakas, Marinos C ^a   Ortqvist, Eva ^f   Hampe, Christiane S ^d  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b Arrowsmith Technologies   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; AUTOANTIBODY; EPITOPE; GLUTAMATE DECARBOXYLASE 65 ANTIBODY; GLUTAMIC ACID; MONOCLONAL ANTIBODY; PYRIDOXAL 5 PHOSPHATE;

AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CLINICAL ARTICLE; ENZYME INHIBITION; FEMALE; HUMAN; IMMUNOGENICITY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; PRIORITY JOURNAL; STIFF MAN SYNDROME;

EID: 28344449503     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.11.7755     Document Type: Article

References (64)

1. Moersch, F., and H. Woltman. 1956. Progressive fluctuating muscular rigidity and spasm ("Stiff-Man" syndrome): report of a case and some observations in 13 other cases. Proc. Mayo Clinic 31: 421-427.
2. Toro, C., D. M. Jacobowitz, and M. Hallett. 1994. Stiff-Man syndrome. Semin. Neurol. 14: 154-158.
3. Dalakas, M. C., M. Fujii, M. Li, and B. McElroy. 2000. The clinical spectrum of anti-GAD antibody-positive patients with Stiff-Person syndrome. Neurology 55: 1531-1535.
4. Levy, L. M., M. C. Dalakas, and M. K. Floeter. 1999. The Stiff-Person syndrome: an autoimmune disorder affecting neurotransmission of γ-aminobutyric acid. Ann. Intern. Med. 131: 522-530.
5. Solimena, M., and P. De Camilli. 1991. Autoimmunity to glutamic acid decarboxylase (GAD) in Stiff-Man syndrome and insulin-dependent diabetes mellitus. Trends Neurosci. 14: 452-457.
6. Erlander, M. G., N. J. K. Tillakaratne, S. Feldblum, N. Patel, and A. J. Tobin. 1991. Two genes encode distinct glutamate decarboxylase. Neuron 7: 91-100.
7. Bu, D.-F., M. G. Erlander, B. C. Hitz, N. J. K. Tillakaratne, D. L. Kaufman, C. B. Wanger-McPherson, G. A. Evans, and A. J. Tobin. 1992. Two human glutamate decarboxylases, 65-kDa GAD and 67-kDa GAD, are each encoded by a single gene. Proc. Natl. Acad. Sci. USA 89: 2115-2119.
8. Chen, C. H., G. Battaglioli, D. L. Martin, S. A. Hobart, and W. Colon. 2003. Distinctive interactions in the holoenzyme formation for two isoforms of glutamate decarboxylase. Biochim. Biophys. Acta 1645: 63-71.
9. Kaufman, D. L., C. R. Houser, and A. J. Tobin. 1991. Two forms of the γ-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J. Neurochem. 56: 720-723.
10. Martin. D. L., and K. Rimvall. 1993. Regulation of γ-aminobutyric acid synthesis in the brain. J. Neurochem. 60: 395-407.
11. Condie, B. G., G. Bain, D. I. Gottlieb, and M. R. Capecchi. 1997. Cleft palate in mice with a targeted mutation in the α-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67. Proc. Natl. Acad. Sci. USA 94: 11451-11455.
12. Asada, H., Y. Kawamura, K. Maruyama, H. Kume, R. G. Ding, N. Kanbara, H. Kuzume, M. Sanbo, T. Yagi, and K. Obata. 1997. Cleft palate and decreased brain γ-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA 94: 6496-6499.
13. Kash, S. F., R. S. Johnson, L. H. Tecott, J. L. Noebels, R. D. Mayfield, D. Hanahan, and S. Baekkeskov. 1997. Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA 94: 14060-14065.
14. Giometto, B., D. Miotto, F. Faresin, V. Argentiero, T. Scaravilli, and B. Tavolato. 1996. Anti-gabaergic neuron autoantibodies in a patient with Stiff-Man syndrome and ataxia. J. Neurol. Sci. 143: 57-59.
15. Honnorat, J., P. Trouillas, C. Thivolet, M. Aguera, and M. F. Belin. 1995. Autoantibodies to glutamate decarboxylase in a patient with cerebellar cortical atrophy, peripheral neuropathy, and slow eye movements. Arch. Neurol. 52: 462-468.
16. Saiz, A., J. Arpa, A. Sagasta, R. Casamitjana, J. J. Zarranz, E. Tolosa, and F. Graus. 1997. Autoantibodies to glutamic acid decarboxylase in three patients with cerebellar ataxia, late-onset insulin-dependent diabetes mellitus, and polyendocrine autoimmunity. Neurology 49: 1026-1030.
17. Giometto, B., P. Nicolao, M. Macucci, B. Tavolato, R. Foxon, and G. F. Bottazzo. 1998. Temporal-lobe epilepsy associated with glutamic-acid- decarboxylase autoantibodies. Lancet 352: 457.
18. Peltola, J., P. Kulmala, J. Isojarvi, A. Saiz, K. Latvala, J. Palmio, K. Savola, M. Knip, T. Keranen, and F. Graus. 2000. Autoantibodies to glutamic acid decarboxylase in patients with therapy-resistant epilepsy. Neurology 55: 46-50.
19. Nemni, R., S. Braghi, M. G. Natali-Sora, V. Lampasona, E. Bonifacio, G. Comi. and N. Canal. 1994. Autoantibodies to glutamic acid decarboxylase in palatal myoclonus and epilepsy. Ann. Neurol. 36: 665-667.
20. Vianello, M., B. Tavolato, M. Armani, and B. Giometto. 2003. Cerebellar ataxia associated with anti-glutamic acid decarboxylase autoantibodies. Cerebellum 2: 77-79.
21. Bjork, E., L. A. Velloso, O. Kampe, and F. A. Karlsson. 1994. GAD autoantibodies in IDDM, Stiff-Man syndrome, and autoimmune polyendocrine syndrome type 1 recognize different epitopes. Diabetes 43: 161-165.
22. Daw, K., and A. C. Powers. 1995. Two distinct glutamic acid decarboxylase auto-antibody specificities in IDDM target difference epitopes. Diabetes 44: 216-220.
23. Daw, K., N. Ujihara, M. Atkinson, and A. C. Powers. 1996. Glutamic acid decarboxylase autoantibodies in Stiff-Man syndrome and insulin-dependent diabetes mellitus exhibit similarities and differences in epitope recognition. J. Immunol. 156: 818-825.
24. Tuomi, T., M. J. Rowley, W. J. Knowles, Q. Y. Chen, T. McAnally, P. Z. Zimmet, and I. R. Mackay. 1994. Autoantigenic properties of native and denatured glutamic acid decarboxylase: evidence for a conformational epitope. Clin. Immunol. Immunopathol. 71: 53-59.
25. Dinkel, K., H. Meinck, K. M. Jury, W. Karges, and W. Richter. 1998. Inhibition of γ-aminobutyric acid synthesis by glutamic acid decarboxylase autoantibodies in Stiff-Man syndrome. Ann. Neurol. 44: 194-201.
26. Kobayashi, T., S. Tanaka, M. Okubo, K. Nakanishi, T. Murase, and ?. Lernmark. 2003. Unique epitopes of glutamic acid decarboxylase autoantibodies in slowly progressive type 1 diabetes. J. Clin. Endocrinol. Metab. 88: 4768-4775.
27. Dalakas, M. C., M. Li, M. Fujii, and D. M. Jacobowitz. 2001. Stiff-Person syndrome: quantification, specificity, and intrathecal synthesis of GAD65 antibodies. Neurology 57: 780-784.
28. Honnorat, J., A. Saiz, B. Giometto, A. Vincent, L. Brieva, C. de Andres, J. Maestre, N. Fabien, A. Vighetto, R. Casamitjana, et al. 2001. Cerebellar ataxia with anti-glutamic acid decarboxylase antibodies: study of 14 patients. Arch. Neurol. 58: 225-230.
29. Takenoshita, H., M. Shizuka-Ikeda, H. Mitoma, S. Song, Y. Harigaya, Y. Igeta, M. Yaguchi, K. Ishida, M. Shoji, M. Tanaka, et al. 2001. Presynaptic inhibition of cerebellar GABAergic transmission by glutamate decarboxylase autoantibodies in progressive cerebellar ataxia. J. Neurol. Neurosurg. Psychiatry 70: 386-389.
30. Ellis, T. M., and M. A. Atkinson. 1996. The clinical significance of an autoimmune response against glutamic acid decarboxylase. Nat. Med. 2: 148-153.
31. Mitoma, H., S. Y. Song, K. Ishida, T. Yamakuni, T. Kobayashi, and H. Mizusawa. 2000. Presynaptic impairment of cerebellar inhibitory synapses by an autoantibody to glutamate decarboxylase. J. Neurol. Sci. 175: 40-44.
32. Mitoma, H., K. Ishida, M. Shizuka-Ikeda, and H. Mizusawa. 2003. Dual impairment of GABAA- and GABAB-receptor-mediated synaptic responses by autoantibodies to glutamic acid decarboxylase. J. Neurol. Sci. 208: 51-56.
33. Marner, B., ?. Lernmark, J. Ludvigsson, P. MacKay, I. Matsuba, J. Nerup, and A. Rabinovitch. 1985. Islet cell antibodies in insulin-dependent (type 1) diabetic children treated with plasmapheresis. Diabetes Res. 2: 231-236.
34. Bonifacio, E., R. L. Dawkins, and ?. Lernmark. 1987. Immunology and diabetes workshops: report of the Second International Workshop on the Standardization of Cytoplasmic Islet Cell Antibodies. Diabetologia 30: 273.
35. Schmidli, R. S., P. G. Colman, E. Bonifacio, G. F. Bottazzo, and L. C. Harrison. 1994. High level of concordance between assays for glutamic acid decarboxylase antibodies: the First International Glutamic Acid Decarboxylase Antibody Workshop. Diabetes 43: 1005-1009.
36. Mire-Sluis, A. R., R. G. Das, and A. Lernmark. 1999. The development of a World Health Organization international standard for islet cell antibodies: the aims and design of an international collaborative study. Diabetes Metab. Res. Rev. 15: 72-77.
37. Mire-Sluis, A. R., R. G. Das, and A. Lernmark. 2000. The World Health Organization International Collaborative Study for Islet Cell Antibodies. Diabetologia 43: 1282-1292.
38. Li, L., W. A. Hagopian, H. R. Brashear, T., Daniels, and A. Lernmark. 1994. Identification of autoantibody epitopes of glutamic acid decarboxylase in Stiff-Man syndrome patients. J. Immunol. 152: 930-934.
39. Hampe, C. S., P. Lundgren, D. T. L., L. P. Hammerle, S. M. Marcovina, and A. Lernmark. 2001. A novel monoclonal antibody specific for the N-terminal end of GAD65. J. Neuroimmunol. 113: 63-71.
40. Ziegler, B., M. Schlosser, F. Luhder, M. Strebelow, P. Augstein, W. Northemann, A. C. Powers, and M. Ziegler. 1996. Murine monoclonal glutamic acid decarboxylase (GAD)65 antibodies recognize autoimmune-associated GAD epitope regions targeted in patients with type 1 diabetes mellitus and Stiff-Man syndrome. Acta Diabetol. 33: 225-231.
41. Madec, A. M., F. Rousset, S. Ho, F. Robert, C. Thivolet, J. Orgiazzi, and S. Lebecque. 1996. Four IgG anti-islet human monoclonal antibodies isolated from a type 1 diabetes patient recognize distinct epitopes of glutamic acid decarboxylase 65 and are somatically mutated. J. Immunol. 156: 3541-3549.
42. Jaume, J. C., S. L. Parry, A. M. Madec, G. Sonderstrup, and S. Baekkeskov. 2002. Suppressive effect of glutamic acid decarboxylase 65-specific autoimmune B lymphocytes on processing of T cell determinants located within the antibody epitope. J. Immunol. 169: 665-672.
43. Schwartz, H. L., J. M. Chandonia, S. F. Kash, J. Kanaani, E. Tunnell, A. Domingo, F. E. Cohen, J. P. Banga, A. M. Madec, W. Richter, and S. Baekkeskov. 1999. High-resolution autoreactive epitope mapping and structural modeling of the 65 kDa form of human glutamic acid decarboxylase. J. Mol. Biol. 287: 983-999.
44. Tremble, J., N. G. Morgenthaler, A. Vlug, A. C. Powers, M. R. Christie, W. A. Scherbaum, and J. P. Banga. 1997. Human B cells secreting immunoglobulin G to glutamic acid decarboxylase-65 from a nondiabetic patient with multiple autoantibodies and Graves' disease: a comparison with those present in type diabetes. J. Clin. Endocrinol. Metab. 82: 2664-2670.
45. Carter, P., R. F. Kelley, M. L. Rodrigues, B. Snedecor, M. Covarrubias, M. D. Velligan, W. L. Wong, A. M. Rowland, C. E. Kotts, and M. E. Carver. 1992. High level Escherichia coli expression and production of a bivalent humanized antibody fragment. Biotechnology 10: 163-167.
46. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119: 736-747.
47. Grubin, C., T. Daniels, A. E. Karlsen, E. Boel, W. A. Hagopian, and A. Lernmark. 1992. The cDNA-directed, in vitro-synthesized nascent peptide of glutamic acid decarboxylase (GAD2) is the autoantigen in insulin-dependent diabetes. Clin. Res. 40: 299A.
48. Padoa, C. J., J. P. Banga, A. M. Madec, M. Ziegler, M. Schlosser, E. Ortqvist, T. Kockum, J. Palmer, O. Rolandsson, K. A. Binder, et al. 2003. Recombinant Fabs of human monoclonal antibodies specific to the middle epitope of GAD65 inhibit type 1 diabetes-specific GAD65Abs. Diabetes 52: 2689-2695.
49. Hampe, C. S., L. P. Hammerle, A. Falorni, J. Robertson, and A. Lernmark. 2001. Site-directed mutagenesis of K396R of the 65 kDa glutamic acid decarboxylase active site obliterates enzyme activity but not antibody binding. FEBS Lett. 488: 185-189.
50. Hwang, W. Y., and J. Foote. 2005. Immunogenicity of engineered antibodies. Methods 36: 3-10.
51. Al-Lazikani, B., A. M. Lesk, and C. Chothia. 1997. Standard conformations for the canonical structures of immunoglobulins. J. Mol. Biol. 273: 927-948.
52. Lautner-Rieske, A., C. Huber, A. Meindl, W. Pargent, K. F. Schable, R. Thiebe, T. Zocher, and H. G. Zachau. 1992. The human immunoglobulin κ locus: characterization of the duplicated A regions. Eur. J. Immunol. 22: 1023-1029.
53. Matsuda, F., K. Ishii, P. Bourvagnet, K. Kuma, H. Hayashida, T. Miyata, and T. Honjo. 1998. The complete nucleotide sequence of the human immunoglobulin heavy chain variable region locus. J. Exp. Med. 188: 2151-2162.
54. Rakocevic, G., R. Raju, and M. C. Dalakas. 2004. Anti-glutamic acid decarboxylase antibodies in the serum and cerebrospinal fluid of patients with Stiff-Person syndrome: correlation with clinical severity. Arch. Neurol. 61: 902-904.
55. Baekkeskov, S., H. J. Aanstoot, S. Christgau, A. Reetz, M. Solimena, M. Cascalho, F. Folli, H. Richter-Olesen, and P. De Camilli. 1990. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature 347: 151-156.
56. Persson, H., M. Pelto-Huikko, M. Metsis, O. S"der, S. Bren, S. Skog, T. H"kfelt, and M. Ritz, N. 1990. Expression of the neurotransmitter- synthesizing enzyme glutamic acid decarboxylase in male germ cells. Mol. Cell. Biol. 10: 4701-4711.
57. Erd", S. L., F. Joo, and J. R. Wolff. 1989. Immunohistochemical localization of glutamate decarboxylase in the rat oviduct and ovary: further evidence for non-neural GABA system. Cell Tissue Res. 255: 431-434.
58. Tillakaratne, N. J., M. G. Erlander, M. W. Collard, K. F. Greif, and A. J. Robin, 1992. Glutamate decarboxylases in nonneural cells of rat testis and oviduct: differential expression of GAD65 and GAD67. J. Neurochem. 58: 618-627.
59. 2-terminal epitope in the autoantigen GAD65, distinguish Stiff-Man syndrome from insulin-dependent diabetes mellitus. J. Exp. Med. 180: 595-606.
60. Piquer, S., Belloni, C., Lampasona, V., Bazzigaluppi. E., Vianello, M., Giometto, B., Bosi, E., Bottazzo, G. F., and E. Bonifacio. 2005. Humoral autoimmune responses to glutamic acid decarboxylase have similar target epitopes and subclass that show titer-dependent disease association. Clin. Immunol. 117: 31-35.
61. Riechmann, L., M. Clark, H. Waldmann, and G. Winter. 1988. Reshaping human antibodies for therapy. Nature 332: 323-327.
62. Hao, W., C. Davis, I. B. Hirsch, L. J. Eng, T. Daniels, D. Walsh, and A. Lernmark. 1999. Plasmapheresis and immunosuppression in Stiff-Man syndrome with type 1 diabetes: a two-year study. J. Neurol. 246: 731-735.
63. Vicari, A., F. Folli, G. Pozza, G. C. Comi, M. Comola, N. Canal, C. Besana, A. Borri, M. Tresoldi, M. Solimena, and P. De Camili. 1989. Plasmapheresis in the treatment of Stiff-Man syndrome. N. Engl. J. Med. 320: 1499.
64. Brashear, H. R., and L. H. Phillips, 2nd. 1991. Autoantibodies to GABAergic neurons and response to plasmapheresis in Stiff-Man syndrome. Neurology 41: 1588-1592.