Increased neutrophil elastase and proteinase 3 and augmented NETosis are closely associated with β-cell autoimmunity in patients with type 1 diabetes

Diabetes

Volumn 63, Issue 12, 2014, Pages 4239-4248

  Wang, Yudong ^a,b   Xiao, Yang ^c   Zhong, Ling ^a,b   Ye, Dewei ^a,b   Zhang, Jialiang ^a,b   Tu, Yiting ^c   Bornstein, Stefan R ^d   Zhou, Zhiguang ^c   Lam, Karen S L ^a,b   Xu, Aimin ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ANTIGEN; LEUKOCYTE ELASTASE; MYELOBLASTIN; SERINE PROTEINASE; ALPHA 1 ANTITRYPSIN; AUTOANTIBODY; SERPINA1 PROTEIN, HUMAN;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; AUTOIMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE DURATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NEUTROPHIL GRANULE; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOGENESIS; PROTEIN ANALYSIS; ANIMAL; CASE CONTROL STUDY; CELL DEATH; CHILD; ENZYMOLOGY; EXTRACELLULAR TRAP; IMMUNOLOGY; LEUKOCYTE COUNT; METABOLISM; NEUTROPHIL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONOBESE DIABETIC MOUSE; YOUNG ADULT;

ADOLESCENT; ALPHA 1-ANTITRYPSIN; ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; CASE-CONTROL STUDIES; CELL DEATH; CHILD; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; EXTRACELLULAR TRAPS; FEMALE; HUMANS; INSULIN-SECRETING CELLS; LEUKOCYTE COUNT; LEUKOCYTE ELASTASE; MALE; MICE; MICE, INBRED NOD; MYELOBLASTIN; NEUTROPHILS; YOUNG ADULT;

EID: 84911922929     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0480     Document Type: Article

References (50)

1. Hummel K, McFann KK, Realsen J, Messer LH, Klingensmith GJ, Chase HP. The increasing onset of type 1 diabetes in children. J Pediatr 2012;161:652-657, e1
2. Tuomilehto J. The emerging global epidemic of type 1 diabetes. Curr Diab Rep 2013;13:795-804
3. van Belle TL, Coppieters KT, von Herrath MG. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 2011;91:79-118
4. Skyler JS, Sosenko JM. The evolution of type 1 diabetes. JAMA 2013;309:2491-2492
5. Gan MJ, Albanese-O'Neill A, Haller MJ. Type 1 diabetes: current concepts in epidemiology, pathophysiology, clinical care, and research. Curr Probl Pediatr Adolesc Health Care 2012;42:269-291
6. Pihoker C, Gilliam LK, Hampe CS, Lernmark A. Autoantibodies in diabetes. Diabetes 2005;54(Suppl. 2):S52-S61
7. Miao D, Yu L, Eisenbarth GS. Role of autoantibodies in type 1 diabetes. Front Biosci 2007;12:1889-1898
8. Richardson SJ, Willcox A, Bone AJ, Morgan NG, Foulis AK. Immunopathology of the human pancreas in type-I diabetes. Semin Immunopathol 2011;33:9-21
9. Diana J, Simoni Y, Furio L, et al. Crosstalk between neutrophils, B-1a cells and plasmacytoid dendritic cells initiates autoimmune diabetes. Nat Med 2013;19:65-73
10. Harsunen MH, Puff R, D'Orlando O, et al. Reduced blood leukocyte and neutrophil numbers in the pathogenesis of type 1 diabetes. Horm Metab Res 2013;45:467-470
11. Valle A, Giamporcaro GM, Scavini M, et al. Reduction of circulating neutrophils precedes and accompanies type 1 diabetes. Diabetes 2013;62:2072-2077
12. Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol 2004;172:2731-2738
13. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013;13:159-175
14. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004;303:1532-1535
15. Mócsai A. Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J Exp Med 2013;210:1283-1299
16. Korkmaz B, Moreau T, Gauthier F. Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions. Biochimie 2008;90:227-242
17. Wiedow O, Meyer-Hoffert U. Neutrophil serine proteases: potential key regulators of cell signalling during inflammation. J Intern Med 2005;257:319-328
18. Pham CT. Neutrophil serine proteases fine-tune the inflammatory response. Int J Biochem Cell Biol 2008;40:1317-1333
19. Meyer-Hoffert U, Wiedow O. Neutrophil serine proteases: mediators of innate immune responses. Curr Opin Hematol 2011;18:19-24
20. Korkmaz B, Horwitz MS, Jenne DE, Gauthier F. Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol Rev 2010;62:726-759
21. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2013;36(Suppl. 1):S67-S74
22. Xiao Y, Xu A, Law LS, et al. Distinct changes in serum fibroblast growth factor 21 levels in different subtypes of diabetes. J Clin Endocrinol Metab 2012;97:E54-E58
23. Yang L, Luo S, Huang G, et al. The diagnostic value of zinc transporter 8 autoantibody (ZnT8A) for type 1 diabetes in Chinese. Diabetes Metab Res Rev 2010;26:579-584
24. Wiesner O, Litwiller RD, Hummel AM, et al. Differences between human proteinase 3 and neutrophil elastase and their murine homologues are relevant for murine model experiments. FEBS Lett 2005;579:5305-5312
25. Labow RS, Erfle DJ, Santerre JP. Elastase-induced hydrolysis of synthetic solid substrates: poly(ester-urea-urethane) and poly(ether-urea-urethane). Biomaterials 1996;17:2381-2388
26. Kessenbrock K, Krumbholz M, Schönermarck U, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009;15:623-625
27. Villanueva E, Yalavarthi S, Berthier CC, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol 2011;187:538-552
28. Naegele M, Tillack K, Reinhardt S, Schippling S, Martin R, Sospedra M. Neutrophils in multiple sclerosis are characterized by a primed phenotype. J Neuroimmunol 2012;242:60-71
29. Lande R, Ganguly D, Facchinetti V, et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med 2011;3:73ra19
30. Garcia-Romo GS, Caielli S, Vega B, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011;3:73ra20
31. Zhang S, Zhong J, Yang P, Gong F, Wang CY. HMGB1, an innate alarmin, in the pathogenesis of type 1 diabetes. Int J Clin Exp Pathol 2009;3:24-38
32. Knight JS, Carmona-Rivera C, Kaplan MJ. Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front Immunol 2012;3:380
33. Dwivedi N, Radic M. Citrullination of autoantigens implicates NETosis in the induction of autoimmunity. Ann Rheum Dis 2014;73:483-491
34. Ziegler AG, Hummel M, Schenker M, Bonifacio E. Autoantibody appearance and risk for development of childhood diabetes in offspring of parents with type 1 diabetes: the 2-year analysis of the German BABYDIAB Study. Diabetes 1999;48:460-468
35. Lebastchi J, Herold KC. Immunologic and metabolic biomarkers of β-cell destruction in the diagnosis of type 1 diabetes. Cold Spring Harb Perspect Med 2012;2:a007708
36. Atkinson MA. The pathogenesis and natural history of type 1 diabetes. Cold Spring Harb Perspect Med 2012;2:a007641
37. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 2006;6:541-550
38. Meyer-Hoffert U. Neutrophil-derived serine proteases modulate innate immune responses. Front Biosci (Landmark Ed) 2009;14:3409-3418
39. Coeshott C, Ohnemus C, Pilyavskaya A, et al. Converting enzyme-independent release of tumor necrosis factor alpha and IL-1beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc Natl Acad Sci U S A 1999;96:6261-6266
40. Sugawara S, Uehara A, Nochi T, et al. Neutrophil proteinase 3-mediated induction of bioactive IL-18 secretion by human oral epithelial cells. J Immunol 2001;167:6568-6575
41. Walsh DE, Greene CM, Carroll TP, et al. Interleukin-8 up-regulation by neutrophil elastase is mediated by MyD88/IRAK/TRAF-6 in human bronchial epithelium. J Biol Chem 2001;276:35494-35499
42. Devaney JM, Greene CM, Taggart CC, Carroll TP, O'Neill SJ, McElvaney NG. Neutrophil elastase up-regulates interleukin-8 via toll-like receptor 4. FEBS Lett 2003;544:129-132
43. Grieco FA, Vendrame F, Spagnuolo I, Dotta F. Innate immunity and the pathogenesis of type 1 diabetes. Semin Immunopathol 2011;33:57-66
44. Padgett LE, Broniowska KA, Hansen PA, Corbett JA, Tse HM. The role of reactive oxygen species and proinflammatory cytokines in type 1 diabetes pathogenesis. Ann N Y Acad Sci 2013;1281:16-35
45. Talukdar S, Oh Y, Bandyopadhyay G, et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012;18:1407-1412
46. Bae S, Choi J, Hong J, et al. Neutrophil proteinase 3 induces diabetes in a mouse model of glucose tolerance. Endocr Res 2012;37:35-45
47. Song S, Goudy K, Campbell-Thompson M, et al. Recombinant adeno-associated virus-mediated alpha-1 antitrypsin gene therapy prevents type I diabetes in NOD mice. Gene Ther 2004;11:181-186
48. Lu Y, Tang M, Wasserfall C, et al. Alpha1-antitrypsin gene therapy modulates cellular immunity and efficiently prevents type 1 diabetes in nonobese diabetic mice. Hum Gene Ther 2006;17:625-634
49. Janciauskiene SM, Bals R, Koczulla R, Vogelmeier C, Köhnlein T, Welte T. The discovery of a1-antitrypsin and its role in health and disease. Respir Med 2011;105:1129-1139
50. Stoller JK, Aboussouan LS. Alpha1-antitrypsin deficiency. Lancet 2005;365:2225-2236