Regulation of cathepsin G reduces the activation of proinsulin-reactive T cells from type 1 diabetes patients

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Zou, Fang ^a   Schäfer, Nadja ^a   Palesch, David ^a   Brücken, Ruth ^a   Beck, Alexander ^b,f   Sienczyk, Marcin ^c   Kalbacher, Hubert ^d   Sun, ZiLin ^e   Boehm, Bernhard O ^a   Burster, Timo ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b PANATecs   (Germany)

^c WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e SOUTHEAST UNIVERSITY   (China)

^f SOLVIAS AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC PROTEINASE; CATHEPSIN; CATHEPSIN D; CATHEPSIN G; CATHEPSIN S; CATHEPSIN V; CYSTEINE PROTEINASE; EPITOPE; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 22; PROINSULIN; SERINE PROTEINASE; TUMOR NECROSIS FACTOR ALPHA; ALOXISTATIN; CARRIER PROTEIN; DRUG DERIVATIVE; LEUCINE; PENETRATIN; PEPSTATIN;

ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; MYELOID DENDRITIC CELL; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN PROCESSING; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; METABOLISM; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BLOTTING, WESTERN; CARRIER PROTEINS; CATHEPSIN G; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; LEUCINE; PEPSTATINS; POLYMERASE CHAIN REACTION; PROINSULIN; T-LYMPHOCYTES;

EID: 79961135430     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022815     Document Type: Article

References (39)

1. Jasinski JM, Eisenbarth GS, (2005) Insulin as a primary autoantigen for type 1A diabetes. Clin Dev Immunol 12: 181-186.
2. Burster T, Boehm BO, (2010) Processing and presentation of (pro)-insulin in the MHC class II pathway: the generation of antigen-based immunomodulators in the context of type 1 diabetes mellitus. Diabetes Metab Res Rev 26: 227-238.
3. Fissolo N, Kraus M, Reich M, Ayturan M, Overkleeft H, et al. (2008) Dual inhibition of proteasomal and lysosomal proteolysis ameliorates autoimmune central nervous system inflammation. Eur J Immunol 38: 2401-2411.
4. Burster T, Macmillan H, Hou T, Boehm BO, Mellins ED, (2010) Cathepsin G: roles in antigen presentation and beyond. Mol Immunol 47: 658-665.
5. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES, (2005) Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307: 1630-1634.
6. Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C, et al. (2007) Differential antigen processing by dendritic cell subsets in vivo. Science 315: 107-111.
7. Burster T, Beck A, Tolosa E, Marin-Esteban V, Rotzschke O, et al. (2004) Cathepsin G, and not the asparagine-specific endoprotease, controls the processing of myelin basic protein in lysosomes from human B lymphocytes. J Immunol 172: 5495-5503.
8. Colbert JD, Matthews SP, Miller G, Watts C, (2009) Diverse regulatory roles for lysosomal proteases in the immune response. Eur J Immunol.
9. Chapman HA, (2006) Endosomal proteases in antigen presentation. Curr Opin Immunol 18: 78-84.
10. Zavasnik-Bergant T, Turk B, (2006) Cysteine cathepsins in the immune response. Tissue Antigens 67: 349-355.
11. Rudensky A, Beers C, (2006) Lysosomal cysteine proteases and antigen presentation. Ernst Schering Res Found Workshop pp. 81-95.
12. van Endert P, Villadangos JA, (2007) Antigen processing and recognition. Curr Opin Immunol 19: 63-65.
13. Maehr R, Mintern JD, Herman AE, Lennon-Dumenil AM, Mathis D, et al. (2005) Cathepsin L is essential for onset of autoimmune diabetes in NOD mice. J Clin Invest 115: 2934-2943.
14. Hsing LC, Kirk EA, McMillen TS, Hsiao SH, Caldwell M, et al. (2010) Roles for cathepsins S, L, and B in insulitis and diabetes in the NOD mouse. J Autoimmun 34: 96-104.
15. Oleksyszyn J, Powers JC, (1991) Irreversible inhibition of serine proteases by peptide derivatives of (alpha-aminoalkyl)phosphonate diphenyl esters. Biochemistry 30: 485-493.
16. Reich M, Lesner A, Legowska A, Sienczyk M, Oleksyszyn J, et al. (2009) Application of specific cell permeable cathepsin G inhibitors resulted in reduced antigen processing in primary dendritic cells. Mol Immunol 46: 2994-2999.
17. Zaidi N, Burster T, Sommandas V, Herrmann T, Boehm BO, et al. (2007) A novel cell penetrating aspartic protease inhibitor blocks processing and presentation of tetanus toxoid more efficiently than pepstatin A. Biochem Biophys Res Commun 364: 243-249.
18. Tamai M, Matsumoto K, Omura S, Koyama I, Ozawa Y, et al. (1986) In vitro and in vivo inhibition of cysteine proteinases by EST, a new analog of E-64. J Pharmacobiodyn 9: 672-677.
19. Lang Y, Forquet F, Speck E, Blum J, Delovitch TL, (1996) Major histocompatibility complex class II molecules function as a template for the processing of a partially processed insulin peptide into a T-cell epitope. Diabetes 45: 1711-1719.
20. Raymond WW, Trivedi NN, Makarova A, Ray M, Craik CS, et al. (2010) How Immune Peptidases Change Specificity: Cathepsin G Gained Tryptic Function but Lost Efficiency during Primate Evolution. J Immunol 185: 5360-5368.
21. Ettinger RA, Kwok WW, (1998) A peptide binding motif for HLA-DQA1*0102/DQB1*0602, the class II MHC molecule associated with dominant protection in insulin-dependent diabetes mellitus. J Immunol 160: 2365-2373.
22. Durinovic-Bello I, Boehm BO, Ziegler AG, (2002) Predominantly recognized proinsulin T helper cell epitopes in individuals with and without islet cell autoimmunity. J Autoimmun 18: 55-66.
23. Arif S, Tree TI, Astill TP, Tremble JM, Bishop AJ, et al. (2004) Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health. J Clin Invest 113: 451-463.
24. Sercarz EE, Maverakis E, (2003) Mhc-guided processing: binding of large antigen fragments. Nat Rev Immunol 3: 621-629.
25. Delovitch TL, Semple JW, Naquet P, Bernard NF, Ellis J, et al. (1988) Pathways of processing of insulin by antigen-presenting cells. Immunol Rev 106: 195-222.
26. Riese RJ, Wolf PR, Bromme D, Natkin LR, Villadangos JA, et al. (1996) Essential role for cathepsin S in the MHC class II-associated invariant chain proecessing and peptide loading. Immunity 4: 450-453.
27. Villadangos JA, Riese RJ, Peters C, Chapman HA, Ploegh HL, (1997) Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J Exp Med 186: 549-560.
28. Reich M, Zou F, Boehm BO, Burster T, (2011) Cell Immunol.
29. Mathieu C, Badenhoop K, (2005) Vitamin D and type 1 diabetes mellitus: state of the art. Trends Endocrinol Metab 16: 261-266.
30. Penna G, Adorini L, (2000) 1 Alpha,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Immunol 164: 2405-2411.
31. Jeffery LE, Burke F, Mura M, Zheng Y, Qureshi OS, et al. (2009) 1,25-Dihydroxyvitamin D3 and IL-2 combine to inhibit T cell production of inflammatory cytokines and promote development of regulatory T cells expressing CTLA-4 and FoxP3. J Immunol 183: 5458-5467.
32. Mathieu C, Gysemans C, Giulietti A, Bouillon R, (2005) Vitamin D and diabetes. Diabetologia 48: 1247-1257.
33. Pitocco D, Crino A, Di Stasio E, Manfrini S, Guglielmi C, et al. (2006) The effects of calcitriol and nicotinamide on residual pancreatic beta-cell function in patients with recent-onset Type 1 diabetes (IMDIAB XI). Diabet Med 23: 920-923.
34. Miyata J, Tani K, Sato K, Otsuka S, Urata T, et al. (2007) Cathepsin G: the significance in rheumatoid arthritis as a monocyte chemoattractant. Rheumatol Int 27: 375-382.
35. Shimoda N, Fukazawa N, Nonomura K, Fairchild RL, (2007) Cathepsin g is required for sustained inflammation and tissue injury after reperfusion of ischemic kidneys. Am J Pathol 170: 930-940.
36. Koulmanda M, Bhasin M, Hoffman L, Fan Z, Qipo A, et al. (2008) Curative and beta cell regenerative effects of alpha1-antitrypsin treatment in autoimmune diabetic NOD mice. Proc Natl Acad Sci U S A 105: 16242-16247.
37. Tausch L, Henkel A, Siemoneit U, Poeckel D, Kather N, et al. (2009) Identification of human cathepsin G as a functional target of boswellic acids from the anti-inflammatory remedy frankincense. J Immunol 183: 3433-3442.
38. Palesch D, Sienczyk M, Oleksyszyn J, Reich M, Wieczerzak E, et al. (2011) Was the serine protease cathepsin G discovered by S. G. Hedin in 1903 in bovine spleen? Acta Biochim Pol 58: 39-44.
39. Tolosa E, Li W, Yasuda Y, Wienhold W, Denzin LK, et al. (2003) Cathepsin V is involved in the degradation of invariant chain in human thymus and is overexpressed in myasthenia gravis. J Clin Invest 112: 517-526.