Expression of properly folded human glutamate decarboxylase 65 as a fusion protein in Escherichia coli

European Journal of Biochemistry

Volumn 246, Issue 2, 1997, Pages 350-359

  Papouchado, Mariana L ^a   Valdez, Silvina N ^a   Ghiringhelli, Daniel ^b   Poskus, Edgardo ^a,c   Ermácora, Mario R ^b,c  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSIDAD NACIONAL DE QUILMES   (Argentina)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Autoantibodies; Biotechnology; Glutamate decarboxylase; Insulin dependent diabetes mellitus; Protein expression

Indexed keywords

GLUTAMATE DECARBOXYLASE; HYBRID PROTEIN;

ARTICLE; CHILD; CONTROLLED STUDY; DIABETES MELLITUS; DRUG MANUFACTURE; ENZYME IMMUNOASSAY; ENZYME STRUCTURE; ESCHERICHIA COLI; GENE CONSTRUCT; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; TECHNIQUE;

EID: 0031006826     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00350.x     Document Type: Article

References (51)

1. Bottazzo, G. F. (1986) Death of a beta cell: homicide or suicide? Diabetic Med. 3, 119-130.
2. Cook, A. (1990) An overview on possible mechanisms of destruction of the insulin-producing beta cell, Curr. Top. Microbiol. Immunol. 164, 125-142.
3. Bækkeskov, S., Nielsen, J. H., Marner, B., Bilde, T., Ludvigsson, J. & Lernmark, Å. (1982) Autoantibodies in newly diagnosed diabetic children immunoprecipitate human pancreatic islet cell proteins, Nature 298, 167-169.
4. Bækkeskov, S., Aanstoot, H.-J., Christgau, S., Reetz, A., Solimena, M., Cascalho, M., Folli, F., Richter-Olesen, H. & De Camilli, P. (1990) Identification of the 64 K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase, Nature 347, 151-156.
5. Atkinson, M. A., Kaufman, D. L., Campbell, L., Gibbs, K. A., Shah, S. C., Bu, D.-F., Erlander, M. G., Tobin, A. J. & Maclaren, N. K. (1992) Response of peripheral-blood mononuclear cells to glutamate decarboxylase in insulin-dependent diabetes, Lancet 339, 458-459.
6. Panina-Bordignon, P., Lang, R., van Endert, P., Benazzi, E., Felix, A. M., Pastore, R. M., Spinas, G. A. & Sinigaglia, F. (1995) Cytotoxic T cells specific for glutamic acid decarboxylase in autoimmune diabetes, J. Exp. Med. 181, 1923-1927.
7. Kaufman, D. L., Clare-Salzler, M., Tian, J., Forsthuber, T., Ting, G. S. P., Robinson, P., Atkinson, M. A., Sercarz, E. E., Tobin, A. J. & Lehmann, P. V. (1993) Spontaneous loss of T-cell tolerance to glutamic acid decarboxylase in murine insulin-dependent diabetes, Nature 366, 69-72.
8. Tisch, R., Yang, X.-D., Singer, S. M., Liblau, R. S., Fugger, L. & McDevitt, H. O. (1993) Immune response to glutamic acid decarboxylase correlates with insulins in non-obese diabetic mice, Nature 366, 72-75.
9. Tisch, R., Yang, X. D., Liblau, R. S. & McDevitt, H. O. (1994) Administering glutamic acid decarboxylase to NOD mice prevents diabetes. J. Autoimmun. 7, 845-850.
10. 67) prevents autoimmune diabetes in NOD mice, Diabetes 43, 1494-1499.
11. Petersen, J. S., Karlsen, A. E., Markholst, H., Worsaae, A., Dyrberg, T. & Michelsen, B. (1994) Neonatal tolerization with glutamic acid decarboxylase but not with bovine serum albumin delays the onset of diabetes in NOD mice, Diabetes 44, 1478-1484.
12. 65), Clin. Immunol. Immunopathol. 76, 90-95.
13. Bu, D.-F., Erlander, M. G., Hitz, B. C., Tillakaratne, N. J. K., Kaufman, D. L., Wagner-McPherson, C. B., Evans, G. A. & Tobin, A. J. (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.
14. Hagopian, W. A., Michelsen, B., Karlsen, A. E., Larsen, F., Moody, A., Grubin, C. E., Rowe, R., Petersen, J., Mcevoy, R. & Lernmark, Å. (1993) Autoantibodies in IDDM primarily recognize the 65000-Mr rather than the 67000-Mr isoform of glutamic acid decarboxylsase, Diabetes 42, 631-636.
15. Velloso, L. A., Kämpe, O., Hallberg, A., Christmanson, L., Betsholtz, C. & Anders Karlsson, F. (1993) Demonstration of GAD-65 as the main immunogenic isoform of glutamate decarboxylase in type 1 diabetes and determination of autoantibodies using a radioligand produced by eukaryotic expression, J. Clin. Invest. 91, 2084-2090.
16. Ujihara, N., Daw, K., Gianani, R., Boel, E., Yu, L. & Powers, A. C. (1994) Identification of glutamic acid decarboxylase autoantibody heterogeneity and epitope regions in type I diabetes, Diabetes 43, 968-975.
17. 65 antibodies in diabetes and other autimmune diseases using a simple radioligand assay, Diabetes 43, 459-467.
18. Verge, C. E., Howard, N. J., Rowley, M. J., Mackay, I. R., Zimmet, P. Z., Egan, M., Hulinska, H., Hulinsky, I., Silvestrini, R. A., Kamath, S., Sharp. A., Arundel, T. & Silink, M. (1994) Antiglutamate decarboxylase and other antibodies at the onset of childhood IDDM: a population-based study, Diabetologia 37, 1113-1120.
19. Yano, M., Moriuchi, R., Kawasaki, E., Watanabe, M., Saito, K., Takino, H., Akazawa, S., Miyamoto, T. & Nagataki, S. (1995) Autoantibodies against glutamic acid decarboxylase 65 in Japanese patients with insulin-dependent diabetes mellitus (IDDM), J. Autoimmun. 8, 83-96.
20. Richter, W., Shi, Y. & Bækkeskov, S. (1993) Autoreactive epitopes defined by diabetes-associated human monoclonal antibodies are localized in the middle and C-terminal domains of the smaller form of glutamate decarboxylase, Proc. Natl Acad. Sci. USA 90, 2832-2836.
21. Tuomi, T., Rowley, M. J., Knowles, W. J., Chen, Q.-Y., McAnally, T, Zimmet, P. Z. & Mackay, I. R. (1994) Autoantigenic properties of native and denatured glutamic acid decarboxylase: evidence for a conformational epitope, Clin. Immunol. Immunopathol. 71, 53-59.
22. Papouchado, M. L., Ermácora, M. R. & Poskus, E. (1996) Detection of glutamic acid decarboxylase (GAD) autoantibodies by indirect immunofluorescence using CHO cells expressing recombinant human GAD65, J. Autoimmun. 9, 689-697.
23. 65, J. Cell. Biol. 124, 927-934.
24. Chang, Y.-C. & Gottlieb, D. I. (1988) Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase, J. Neurosci. 8, 2123-2130.
25. Nathan, B., Bao, J., Hsu, C.-C., Aguilar, P., Wu, R., Yarom, M., Kuo, C.-Y. & Wu, J.-Y. (1994) A membrane form of brain L-glutamate decarboxylase: identification, isolation and its relation to insulin-dependent diabetes mellitus, Proc. Natl Acad. Sci. USA 91, 242-246.
26. Mauch, L., Seissler, J., Haubruck, H., Cook, N. J., Abney, C. C., Berthold, H., Wirbelauer, C., Liedvogel, B., Scherbaum, W. A. & Northemann, W. (1993) Baculovirus-mediated expression of human 65 kDa and 67 kDa glutamic acid decarboxylases in SF9 insect cells and their relevance in diagnosis of insulin-dependent diabetes mellitus, J. Biochem. (Tokyo) 113, 699-704.
27. Moody, A. J., Hejnæs, K. R., Marshall, M. O., Larsen, F. S., Boel, E., Svendsen, I., Mortensen, E. & Dyrberg, T. (1995) Isolation by anion-exchange of immunologically and enzymatically active human islet glutamic acid decarboxylase 65 overexpressed in Sf9 insect cells, Diabetologia 38, 14-23.
28. Mauch, L., Abney, C. C., Berg, H., Scherbaum, W. A., Liedvogel, B. & Northemann, W. (1993) Characterization of a linear epitope within the human pancreatic 64-kDa glutamic acid decarboxylase and its autoimmune recognition by sera from insulin-dependent diabetes mellitus patients, Eur, J. Biochem. 212, 597-603.
29. Georgiou, G. & Valax, P. (1996) Expression of correctly folded proteins in Escherichia coli, Curr. Opin. Biotechnol. 7, 190-197.
30. National Diabetes Data Group (1979) Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance, Diabetes 28, 1039-1057.
31. Shägger, H. & von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal. Biochem. 166, 368-379.
32. Read, S. M. & Northcote, D. H. (1981) Minimization of variation in the response to different proteins of the Coomassie Blue G dye-binding assay for protein, Anal. Biochem. 116, 53-64.
33. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor NY.
34. Karlsen, A. E., Hagopian, W. A., Petersen, J. S., Boel, E., Dyrberg, T., Grubin, C. E., Michelsen, B. K., Madsen, O. D. & Lernmark, Å. (1992) Recombinant glutamic acid decarboxylase (representing the single isoform expressed in human islets) detects IDDM-associated 64000-Mr autoantibodies, Diabetes 41, 1355-1359.
35. Karlsen, A. E., Hagopian, W. A., Grubin, C. E., Dube, S., Disteche, C. M., Adler, D. A., Bårmeier, H., Mathewes, S., Grant, F. J., Foster, D. & Lernmark, Å. (1991) Cloning and primary structure of a human islet isoform of glutamic acid decarboxylase from chromosome 10. Proc. Natl Acad. Sci. USA 88, 8337-8341.
36. Ellerby, L. M., Escobar, W. A., Fink, A. L., Mitchinson, C. & Wells, J. A. (1990) The role of lysine-234 in β-lactamase catalysis probed by site-directed mutagenesis, Biochemistry 29, 5797-5806.
37. Wu, J.-Y, Matsuda, T. & Roberts, E. (1973) Purification and characterization of glutamate decarboxylase from mouse brain, J. Biol. Chem. 248, 3029-3034.
38. Matsudaira, P. (1987) Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes, J. Biol. Chem. 262, 10035-10038.
39. Ermácora, M. R., Ledman, D. W., Hellinga, H. W., Hsu, G. W. & Fox, R. O. (1994) Mapping staphylococcal nuclease conformation using an EDTA-Fe derivative attached to genetically engineered cysteine residues, Biochemistry 33, 13 625-13 641.
40. Grubin, C. E., Daniels, T., Toivola, B., Landin-Olsson, M., Hagopian, W. A., Li, L., Karlsen, A. E., Boel, E., Michelsen, B. & Lernmark, Å. (1994) A novel radioligand binding assay to determine diagnostic accuracy of isoform-specific glutamic acid decarboxylase antibodies in childhood IDDM, Diabetologia 37, 344-350.
41. Rodbard, D. & Frazier, G. R. (1975) Statistical analysis of radioligand assay data, Methods Enzymol. 37, 3-22.
42. De Boer, H. A. & Hui, A. S. (1991) Sequences within ribosome binding site affecting messenger RNA translatibility and method to direct ribosomes to single messenger RNA species, in Gene expression technology (Goeddel, D. V., Emr, S. D., Henner, D. J., Gold, L. & Levinson, A. D., eds) pp. 103-115, Academic Press, San Diego.
43. Wang, G, Liu, N. & Yang, K. (1995) High-level expression of prochymosin in Escherichia coli: effect of the secondary structure of the ribosome binding site, Protein Expr. Purif. 6, 284-290.
44. Uhlén, M. & Moks, T. (1991) Gene fusion for purpose of expression: an introduction, in Gene expression technology (Goeddel, D. V., Emr, S. D., Henner, D. J., Gold, L. & Levinson, A. D., eds) pp. 129-143, Academic Press, San Diego.
45. Better, M., Chang, C. P., Robinson, R. R. & Horwitz, A. H. (1988) Escherichia coli secretion of an active chimeric antibody fragment, Science 240, 1041-1043.
46. LaVallie, E. R., DiBlasio, E. A., Kovacic, S., Grant, K. L., Schendel, P. F. & McCoy, J. M. (1993) A thioredoxin gene fusion expression system that circunvents inclusion body formation in the E. coli cytoplasm, Biotechnology 11, 187-193.
47. Chopra, A. K., Brasier, A. R., Das, M., Xu, X. J. & Peterson, J. W. (1994) Improved synthesis of Salmonella typhimurium enterotoxin using gene fusion systems, Gene 144, 81-85.
48. Wilkinson, D. L., Ma, N. T., Haught, C. & Harrison, R. G. (1995) Purification by immobilized metal affinity chromatography of human atrial natriuretic peptide expressed in a novel thioredoxin fusion protein, Biotechnol. Prog. 11, 265-269.
49. De Aizpurua, H. J., Wilson, Y. M. & Harrison, L. C. (1992) Glutamic acid decarboxylase in preclinical insulin-dependent diabetes, Proc. Natl Acad. Sci. USA 89, 9841-9845.
50. 65 autoantibodies, a key risk-assessment marker for insulin-dependent diabetes mellitus, Clin. Chem. 42, 263-269.
51. 2-terminal region of the 65-kDa isoform of glutamic acid decarboxylase, J. Biol. Chem. 270, 2241-2246.