Trimming of two major type 1 diabetes driving antigens, GAD65 and IA-2, allows for successful expression in Lactococcus lactis

Beneficial Microbes

Volumn 6, Issue 4, 2015, Pages 591-601

  Robert, S ^a   Van Huynegem, K ^b   Gysemans, C ^a   Mathieu, C ^a   Rottiers, P ^b   Steidler, L ^b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b ActoGeniX NV   (Belgium)

Author keywords

Oral tolerance; Recombinant bacteria; Secretion efficiency

Indexed keywords

GLUTAMATE DECARBOXYLASE 65; INTERLEUKIN 10; PROBIOTIC AGENT; PROTEIN TYROSINE PHOSPHATASE; TYROSINE PHOSPHATASE LIKE PROTEIN ICA512; UNCLASSIFIED DRUG; AUTOANTIGEN; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 2; IL10 PROTEIN, HUMAN; MUTANT PROTEIN; PTPRN PROTEIN, HUMAN; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; IMMUNOBLOTTING; INSULIN DEPENDENT DIABETES MELLITUS; LACTOCOCCUS LACTIS; MOUSE; NONHUMAN; PLASMID; PROTEIN EXPRESSION; PROTEIN SECRETION; TRANSGENIC ORGANISM; DIABETES MELLITUS, TYPE 1; GENE DELETION; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; SECRETION (PROCESS);

AUTOANTIGENS; DIABETES MELLITUS, TYPE 1; GENE EXPRESSION; GLUTAMATE DECARBOXYLASE; HUMANS; INTERLEUKIN-10; LACTOCOCCUS LACTIS; MUTANT PROTEINS; PLASMIDS; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 8; RECOMBINANT PROTEINS; SEQUENCE DELETION;

EID: 84931384340     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2014.0083     Document Type: Article

References (48)

1. Aramaki, Y., Fujii, Y., Suda, H., Suzuki, I., Yadomae, T. and Tsuchiya, S., 1994. Induction of oral tolerance after feeding of ragweed pollen extract in mice. Immunology Letters 40: 21-25.
2. Atkinson, M.A., Maclaren, N.K., Scharp, D.W., Lacy, P.E. and Riley, W.J., 1990. 64,000 Mr autoantibodies as predictors of insulin-dependent diabetes. The Lancet 335: 1357-1360.
3. Bjork, E., Kampe, O., Karlsson, F.A., Pipeleers, D.G., Andersson, A., Hellerstrom, C. and Eizirik, D.L., 1992. Glucose regulation of the autoantigen GAD65 in human pancreatic islets. Journal of Clinical Endocrinology and Metabolism 75: 1574-1576.
4. Braat, H., Rottiers, P., Hommes, D.W., Huyghebaert, N., Remaut, E., Remon, J.P., Van Deventer, S.J., Neirynck, S., Peppelenbosch, M.P. and Steidler, L., 2006. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clinical Gastroenterology and Hepatology 4: 754-759.
5. Chaillous, L., Lefevre, H., Thivolet, C., Boitard, C., Lahlou, N., Atlan-Gepner, C., Bouhanick, B., Mogenet, A., Nicolino, M., Carel, J.C., Lecomte, P., Marechaud, R., Bougneres, P., Charbonnel, B. and Sai, P., 2000. Oral insulin administration and residual beta-cell function in recent-onset type 1 diabetes: a multicentre randomised controlled trial. Diabete Insuline Orale group. The Lancet 356: 545-549.
6. Chatel, J.M., Langella, P., Adel-Patient, K., Commissaire, J., Wal, J.M. and Corthier, G., 2001. Induction of mucosal immune response after intranasal or oral inoculation of mice with Lactococcus lactis producing bovine beta-lactoglobulin. Clinical and Diagnostic Laboratory Immunology 8: 545-551.
7. Daniel, D. and Wegmann, D.R., 1996. Protection of nonobese diabetic mice from diabetes by intranasal or subcutaneous administration of insulin peptide B-(9-23). Proceedings of the National Academy of sciences of the USA 93: 956-960.
8. De Vos, W.M., 2011. Systems solutions by lactic acid bacteria: from paradigms to practice. Microbiological Cell Factories 10 Suppl. 1: S2.
9. Di Lorenzo, T.P., Peakman, M. and Roep, B.O., 2007. Translational mini-review series on type 1 diabetes: Systematic analysis of T cell epitopes in autoimmune diabetes. Clinical and Experimental Immunology 148: 1-16.
10. Ergun-Longmire, B., Marker, J., Zeidler, A., Rapaport, R., Raskin, P., Bode, B., Schatz, D., Vargas, A., Rogers, D., Schwartz, S., Malone, J., Krischer, J. and Maclaren, N.K., 2004. Oral insulin therapy to prevent progression of immune-mediated (type 1) diabetes. Annals of the New York Academy of Sciences 1029: 260-277.
11. Fenalti, G., Hampe, C.S., Arafat, Y., Law, R.H., Banga, J.P., Mackay, I.R., Whisstock, J.C., Buckle, A.M. and Rowley, M.J., 2008. COOHterminal clustering of autoantibody and T-cell determinants on the structure of GAD65 provide insights into the molecular basis of autoreactivity. Diabetes 57: 1293-1301.
12. Fowler, E. and Weiner, H.L., 1997. Oral tolerance: elucidation of mechanisms and application to treatment of autoimmune diseases. Biopolymers 43: 323-335.
13. Higgins, P.J. and Weiner, H.L., 1988. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein and its fragments. Journal of Immunology 140: 440-445.
14. Holo, H. and Nes, I.F., 1989. High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Applied and Environmental Microbiology 55: 3119-3123.
15. Huibregtse, I.L., Marietta, E.V., Rashtak, S., Koning, F., Rottiers, P., David, C.S., Van Deventer, S.J. and Murray, J.A., 2009. Induction of antigen-specific tolerance by oral administration of Lactococcus lactis delivered immunodominant DQ8-restricted gliadin peptide in sensitized nonobese diabetic Abo Dq8 transgenic mice. Journal of Immunology 183: 2390-2396.
16. Huibregtse, I.L., Snoeck, V., De Creus, A., Braat, H., De Jong, E.C., Van Deventer, S.J. and Rottiers, P., 2007. Induction of ovalbumin-specific tolerance by oral administration of Lactococcus lactis secreting ovalbumin. Gastroenterology 133: 517-528.
17. Huibregtse, I.L., Zaat, S.A., Kapsenberg, M.L., Sartori da Silva, M.A., Peppelenbosch, M.P., Van Deventer, S.J. and Braat, H., 2012. Genetically modified Lactococcus lactis for delivery of human interleukin-10 to dendritic cells. Gastroenterology Research and Practice 2012: 639291.
18. Jing, H., Yong, L., Haiyan, L., Yanjun, M., Yun, X., Yu, Z., Taiming, L., Rongyue, C., Liang, J., Jie, W., Li, Z. and Jingjing, L., 2011. Oral administration of Lactococcus lactis delivered heat shock protein 65 attenuates atherosclerosis in low-density lipoprotein receptordeficient mice. Vaccine 29: 4102-4109.
19. Jun, H.S., Khil, L.Y. and Yoon, J.W., 2002. Role of glutamic acid decarboxylase in the pathogenesis of type 1 diabetes. Cellular and Molecular Life Sciences 59: 1892-1901.
20. Kyte, J. and Doolittle, R.F., 1982. A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157: 105-132.
21. Lan, M.S., Wasserfall, C., Maclaren, N.K. and Notkins, A.L., 1996. IA-2, a transmembrane protein of the protein tyrosine phosphatase family, is a major autoantigen in insulin-dependent diabetes mellitus. Proceedings of the National Academy of Sciences of the USA 93: 6367-6370.
22. Le, L.Y., Gruss, A., Ehrlich, S.D. and Langella, P., 1998. A nineresidue synthetic propeptide enhances secretion efficiency of heterologous proteins in Lactococcus lactis. Journal of Bacteriology 180: 1895-1903.
23. Leahy, S.C., Higgins, D.G., Fitzgerald, G.F. and Van Sinderen D., 2005. Getting better with bifidobacteria. Journal of Applied Microbiology 98: 1303-1315.
24. Limaye, S.A., Haddad, R.I., Cilli, F., Sonis, S.T., Colevas, A.D., Brennan, M.T., Hu, K.S. and Murphy, B.A., 2013. Phase 1b, multicenter, single blinded, placebo-controlled, sequential dose escalation study to assess the safety and tolerability of topically applied AG013 in subjects with locally advanced head and neck cancer receiving induction chemotherapy. Cancer 119: 4268-4276.
25. Maron, R., Guerau-de-Arellano, M., Zhang, X. and Weiner, H.L., 2001. Oral administration of insulin to neonates suppresses spontaneous and cyclophosphamide induced diabetes in the NOD mouse. Journal of Autoimmunity 16: 21-28.
26. Moriyama, H., Abiru, N., Paronen, J., Sikora, K., Liu, E., Miao, D., Devendra, D., Beilke, J., Gianani, R., Gill, R.G. and Eisenbarth, G.S., 2003. Evidence for a primary islet autoantigen (preproinsulin 1) for insulitis and diabetes in the nonobese diabetic mouse. Proceedings of the National Academy of Sciences of the USA 100: 10376-10381.
27. Murai, M., Turovskaya, O., Kim, G., Madan, R., Karp, C.L., Cheroutre, H. and Kronenberg, M., 2009. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nature Immunology 10: 1178-1184.
28. Nagler-Anderson, C., Bober, L.A., Robinson, M.E., Siskind, G.W. and Thorbecke, G.J., 1986. Suppression of type II collagen-induced arthritis by intragastric administration of soluble type II collagen. Proceedings of the National Academy of Sciences of the USA 83: 7443-7446.
29. Ng, D.T. and Sarkar, C.A., 2013. Engineering signal peptides for enhanced protein secretion from Lactococcus lactis. Applied and Environmental Microbiology 79: 347-356.
30. Nguyen, T.N., Gourdon, M.H., Hansson, M., Robert, A., Samuelson, P., Libon, C., Andreoni, C., Nygren, P.A., Binz, H., Uhlen, M. and Stahl, S., 1995. Hydrophobicity engineering to facilitate surface display of heterologous gene products on Staphylococcus xylosus. Journal of Biotechnology 42: 207-219.
31. Passini, N., Larigan, J.D., Genovese, S., Appella, E., Sinigaglia, F. and Rogge, L., 1995. The 37/40-kilodalton autoantigen in insulindependent diabetes mellitus is the putative tyrosine phosphatase IA-2. Proceedings of the National Academy of Sciences of the USA 92: 9412-9416.
32. Payton, M.A., Hawkes, C.J. and Christie, M.R., 1995. Relationship of the 37,000-and 40,000-M(r) tryptic fragments of islet antigens in insulin-dependent diabetes to the protein tyrosine phosphataselike molecule IA-2 (ICA512). Journal of Clinical Investigation 96: 1506-1511.
33. Pozzilli, P., Pitocco, D., Visalli, N., Cavallo, M.G., Buzzetti, R., Crino, A., Spera, S., Suraci, C., Multari, G., Cervoni, M., Manca Bitti, M.L., Matteoli, M.C., Marietti, G., Ferrazzoli, F., Cassone Faldetta, M.R., Giordano, C., Sbriglia, M., Sarugeri, E. and Ghirlanda, G., 2000. No effect of oral insulin on residual beta-cell function in recent-onset type I diabetes (the IMDIAB VII). IMDIAB Group. Diabetologia 43: 1000-1004.
34. Robert, S., Gysemans, C., Takiishi, T., Korf, H., Spagnuolo, I., Sebastiani, G., Van, H.K., Steidler, L., Caluwaerts, S., Demetter, P., Wasserfall, C.H., Atkinson, M.A., Dotta, F., Rottiers, P., Van Belle, T.L. and Mathieu, C., 2014. Oral delivery of glutamic acid decarboxylase (GAD)-65 and IL10 by Lactococcus lactis reverses diabetes in recentonset NOD mice. Diabetes 63: 2876-2887.
35. Schotte, L., Steidler, L., Vandekerckhove, J. and Remaut, E., 2000. Secretion of biologically active murine interleukin-10 by Lactococcus lactis. Enzyme and Microbial Technology 27: 761-765.
36. Skyler, J.S., Krischer, J.P., Wolfsdorf, J., Cowie, C., Palmer, J.P., Greenbaum, C., Cuthbertson, D., Rafkin-Mervis, L.E., Chase, H.P. and Leschek, E., 2005. Effects of oral insulin in relatives of patients with type 1 diabetes: the Diabetes Prevention Trial-Type 1. Diabetes Care 28: 1068-1076.
37. Steidler, L., Hans, W., Schotte, L., Neirynck, S., Obermeier, F., Falk, W., Fiers, W. and Remaut, E., 2000. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289: 1352-1355.
38. Steidler, L., Neirynck, S., Huyghebaert, N., Snoeck, V., Vermeire, A., Goddeeris, B., Cox, E., Remon, J.P. and Remaut, E., 2003. Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10. Nature Biotechnology 21: 785-789.
39. Takiishi, T., Korf, H., Van Belle, T.L., Robert, S., Grieco, F.A., Caluwaerts, S., Galleri, L., Spagnuolo, I., Steidler, L., Van, H.K., Demetter, P., Wasserfall, C., Atkinson, M.A., Dotta, F., Rottiers, P., Gysemans, C. and Mathieu, C., 2012. Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice. Journal of Clinical Investigation 122: 1717-1725.
40. Tian, J., Atkinson, M.A., Clare-Salzler, M., Herschenfeld, A., Forsthuber, T., Lehmann, P.V. and Kaufman, D.L., 1996. Nasal administration of glutamate decarboxylase (GAD65) peptides induces Th2 responses and prevents murine insulin-dependent diabetes. Journal of Experimental Medicine 183: 1561-1567.
41. Tisch, R., Yang, X.D., Singer, S.M., Liblau, R.S., Fugger, L. and McDevitt, H.O., 1993. Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice. Nature 366: 72-75.
42. Torii, S., 2009. Expression and function of IA-2 family proteins, unique neuroendocrine-specific protein-tyrosine phosphatases. Endocrine Journal 56: 639-648.
43. Van Asseldonk M., Rutten, G., Oteman, M., Siezen, R.J., De Vos, W.M. and Simons, G., 1990. Cloning of usp45, a gene encoding a secreted protein from Lactococcus lactis subsp. lactis MG1363. Gene 95: 155-160.
44. Van Belle, T.L., Coppieters, K.T. and Von Herrath, M.G., 2011. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiological Reviews 91: 79-118.
45. Wegmann, U., O'Connell-Motherway, M., Zomer, A., Buist, G., Shearman, C., Canchaya, C., Ventura, M., Goesmann, A., Gasson, M.J., Kuipers, O.P., Van Sinderen D. and Kok, J., 2007. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. Journal of Bacteriology 189: 3256-3270.
46. Weiner, H.L., Da Cunha, A.P., Quintana, F. and Wu, H., 2011. Oral tolerance. Immunological Reviews 241: 241-259.
47. Yu, L., Robles, D.T., Abiru, N., Kaur, P., Rewers, M., Kelemen, K. and Eisenbarth, G.S., 2000. Early expression of antiinsulin autoantibodies of humans and the NOD mouse: evidence for early determination of subsequent diabetes. Proceedings of the National Academy of Sciences of the USA 97: 1701-1706.
48. Zhang, Z.J., Davidson, L., Eisenbarth, G. and Weiner, H.L., 1991. Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin. Proceedings of the National Academy of Sciences of the USA 88: 10252-10256.