Altered CD161bright CD8+ mucosal associated invariant t (MAIT)-like cell dynamics and increased differentiation states among juvenile type 1 diabetics

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Harms, Robert Z ^a   Lorenzo, Kristina M ^a   Corley, Kevin P ^b   Cabrera, Monina S ^b   Sarvetnick, Nora E ^a,c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b CHILDREN S HOSPITAL AND MEDICAL CENTER   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD161 ANTIGEN; CD27 ANTIGEN; HEMOGLOBIN A1C; INTERLEUKIN 17; GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN A1C PROTEIN, HUMAN; IL17A PROTEIN, HUMAN; KLRB1 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY B;

ADOLESCENT; AGE DISTRIBUTION; AGING; ARTICLE; CD8+ MUCOSAL ASSOCIATED INVARIANT T CELL; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CHILD; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE MUCOSA; LEUKOCYTE; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; MALE; T LYMPHOCYTE ACTIVATION; BLOOD; CASE CONTROL STUDY; CELL DIFFERENTIATION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PRESCHOOL CHILD;

ADOLESCENT; AGE DISTRIBUTION; CASE-CONTROL STUDIES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; FEMALE; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; INTERLEUKIN-17; LYMPHOCYTE COUNT; MALE; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B;

EID: 84921910209     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117335     Document Type: Article

References (58)

1. Sacks DB, Arnold M, Bakris GL, Bruns DE, Horvath AR, et al. (2011) Guidelines and recommendations for laboratory analysis in the diagnosis and management of diabetes mellitus. Diabetes Care 34: e61-e99. doi: 10.1373/clinchem.2010.161596 PMID: 21617108
2. Canivell S, Gomis R (2014) Diagnosis and classification of autoimmune diabetes mellitus. Autoimmunity Reviews 13: 403-407. doi: 10.1016/j.autrev.2014.01.020 PMID: 24424179
3. Reutens AT (2013) Epidemiology of diabetic kidney disease. Med Clin North Am 97: 1-18. doi: 10.1016/j.mcna.2012.10.001 PMID: 23290726
4. Callaghan BC, Cheng HT, Stables CL, Smith AL, Feldman EL (2012) Diabetic neuropathy: Clinical manifestations and current treatments. The Lancet Neurology 11: 521-534. doi: 10.1016/S1474-4422 (12)70065-0 PMID: 22608666
5. Chillaron JJ, Flores Le-Roux JA, Benaiges D, Pedro-Botet J (2014) Type 1 diabetes, metabolic syndrome and cardiovascular risk. Metabolism 63: 181-187. doi: 10.1016/j.metabol.2013.10.002 PMID: 24274980
6. The DIAMOND Project Group (2006) Incidence and trends of childhood type 1 diabetes worldwide 1990-1999. Diabetic Med 23: 857-866. doi: 10.1111/j.1464-5491.2006.01925.x PMID: 16911623
7. Soltesz G, Patterson C, Dahlquist G, EURODIAB Study Group (2007) Worldwide childhood type 1 diabetes incidence: what can we learn from epidemiology? Pediatric Diabetes 8: 6-14. doi: 10.1111/j. 1399-5448.2007.00280.x PMID: 17727380
8. Burton PR, Clayton DG, Cardon LR, Craddock N, Deloukas P, et al. (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447: 661-678. doi: 10.1038/nature05911
9. Barrett JC, Clayton DG, Concannon P, Akolkar B, Cooper JD, et al. (2009) Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 41: 703-707. doi: 10.1038/ng.381 PMID: 19430480
10. Ilonen J, Sjoroos M, Knip M, Veijola R, Simell O, et al. (2002) Estimation of genetic risk for type 1 diabetes. Am J Med Genet 115: 30-36. doi: 10.1002/ajmg.10341 PMID: 12116174
11. Altobelli E, Blasetti A, Petrocelli R, Tumini S, Azzarone R, et al. (2005) HLA DR/DQ alleles and risk of type I diabetes in childhood: A population-based case-control study. Clinical and Experimental Medicine 5: 72-79. doi: 10.1007/s10238-005-0069-0 PMID: 16096857
12. Borchers AT, Uibo R, Gershwin ME (2010) The geoepidemiology of type 1 diabetes. Autoimmunity Reviews 9: A355-A365. doi: 10.1016/j.autrev.2009.12.003 PMID: 19969107
13. de Goffau MC, Luopajarvi K, Knip M, Ilonen J, Ruohtula T, et al. (2013) Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes 62: 1238-1244. doi: 10.2337/db12-0526 PMID: 23274889
14. Endesfelder D, Zu Castell W, Ardissone A, Davis-Richardson AG, Achenbach P, et al. (2014) Compromised gut microbiota networks in children with anti-islet cell autoimmunity. Diabetes 63: 2006-2014. doi: 10.2337/db13-1676 PMID: 24608442
15. Giongo A, Gano KA, Crabb DB, Mukherjee N, Novelo LL, et al. (2011) Toward defining the autoimmune microbiome for type 1 diabetes. ISME J 5: 82-91. doi: 10.1038/ismej.2010.92 PMID: 20613793
16. Bosi E, Molteni L, Radaelli MG, Folini L, Fermo I, et al. (2006) Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 49: 2824-2827. doi: 10.1007/s00125-006-0465-3 PMID: 17028899
17. Oresic M, Simell S, Sysi-Aho M, Nanto-Salonen K, Seppanen-Laakso T, et al. (2008) Dysregulation of lipid and amino acid metabolism precedes islet autoimmunity in children who later progress to type 1 diabetes. J Exp Med 205: 2975-2984. doi: 10.1084/jem.20081800 PMID: 19075291
18. Murri M, Leiva I, Gomez-Zumaquero JM, Tinahones FJ, Cardona F, et al. (2013) Gut microbiota in children with type 1 diabetes differs from that in healthy children: A case-control study. BMC Med 11: 46. doi: 10.1186/1741-7015-11-46 PMID: 23433344
19. Soyucen E, Gulcan A, Aktuglu-Zeybek AC, Onal H, Kiykim E, et al. (2014) Differences in the gut microbiota of healthy children and those with type 1 diabetes. Pediatrics International 56: 336-343. doi: 10.1111/ped.12243 PMID: 24475780
20. Mejía-León ME, Petrosino JF, Ajami NJ, Domínguez-Bello MG, Calderón de la Barca AM (2014) Fecal microbiota imbalance in mexican children with type 1 diabetes. Scientific Reports 4: 3814. doi: 10.1038/srep03814 PMID: 24448554
21. Damci T, Nuhoglu I, Devranoglu G, Osar Z, Demir M, et al. (2003) Increased intestinal permeability as a cause of fluctuating postprandial blood glucose levels in type 1 diabetic patients. Eur J Clin Invest 33: 397-401. doi: 10.1046/j.1365-2362.2003.01161.x PMID: 12713453
22. Sapone A, de Magistris L, Pietzak M, Clemente MG, Tripathi A, et al. (2006) Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 55: 1443-1449. doi: 10.2337/db05-1593 PMID: 16644703
23. Secondulfo M, Iafusco D, Carratù R, deMagistris L, Sapone A, et al. (2004) Ultrastructural mucosal alterations and increased intestinal permeability in non-celiac, type I diabetic patients. Digestive and Liver Disease 36: 35-45. doi: 10.1016/j.dld.2003.09.016 PMID: 14971814
24. Savilahti E, Ormala T, Saukkonen T, Sandini-Pohjavuori U, Kantele JM, et al. (1999) Jejuna of patients with insulin-dependent diabetes mellitus (IDDM) show signs of immune activation. Clin Exp Immunol 116: 70-77. doi: 10.1046/j.1365-2249.1999.00860.x PMID: 10209507
25. Westerholm-Ormio M, Vaarala O, Pihkala P, Ilonen J, Savilahti E (2003) Immunologic activity in the small intestinal mucosa of pediatric patients with type 1 diabetes. Diabetes 52: 2287-2295. doi: 10.2337/diabetes.52.9.2287 PMID: 12941768
26. Thaiss CA, Levy M, Suez J, Elinav E (2014) The interplay between the innate immune system and the microbiota. Curr Opin Immunol 26: 41-48. doi: 10.1016/j.coi.2013.10.016 PMID: 24556399
27. Goto Y, Ivanov II (2013) Intestinal epithelial cells as mediators of the commensal-host immune crosstalk. Immunol Cell Biol 91: 204-214. doi: 10.1038/icb.2012.80 PMID: 23318659
28. Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, et al. (2011) Human MAIT cells are xenobioticresistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 117: 1250-1259. doi: 10.1182/blood-2010-08-303339 PMID: 21084709
29. Le Bourhis L, Martin E, Peguillet I, Guihot A, Froux N, et al. (2010) Antimicrobial activity of mucosalassociated invariant T cells. Nat Immunol 11: 701-708. doi: 10.1038/ni.1890 PMID: 20581831
30. Le Bourhis L, Mburu YK, Lantz O (2013) MAIT cells, surveyors of a new class of antigen: Development and functions. Curr Opin Immunol 25: 174-180. doi: 10.1016/j.coi.2013.01.005 PMID: 23422835
31. McCarthy NE, Bashir Z, Vossenkamper A, Hedin CR, Giles EM, et al. (2013) Proinflammatory Vδ2+ T cells populate the human intestinal mucosa and enhance IFN-γ production by colonic αβ T cells. The Journal of Immunology 191: 2752-2763. doi: 10.4049/jimmunol.1202959 PMID: 23904167
32. Huber S, Gagliani N, Flavell RA (2012) Life, death, and miracles: Th17 cells in the intestine. Eur J Immunol 42: 2238-2245. doi: 10.1002/eji.201242619 PMID: 22949322
33. Costa VS, Mattana TC, da Silva ME (2010) Unregulated IL-23/IL-17 immune response in autoimmune diseases. Diabetes Res Clin Pract 88: 222-226. doi: 10.1016/j.diabres.2010.03.014 PMID: 20392505
34. Korsgren S, Molin Y, Salmela K, Lundgren T, Melhus A, et al. (2012) On the etiology of type 1 diabetes: A new animal model signifying a decisive role for bacteria eliciting an adverse innate immunity response. Am J Pathol 181: 1735-1748. doi: 10.1016/j.ajpath.2012.07.022 PMID: 22944599
35. Donath MY, Hess C, Palmer E (2014) What is the role of autoimmunity in type 1 diabetes? A clinical perspective. Diabetologia 57: 653-655. doi: 10.1007/s00125-013-3153-0 PMID: 24389751
36. Skog O, Korsgren S, Melhus A, Korsgren O (2013) Revisiting the notion of type 1 diabetes being a T-cell-mediated autoimmune disease. Curr Opin Endocrinol Diabetes Obes 20: 118-123. doi: 10.1097/MED.0b013e32835edb89 PMID: 23422243
37. Sorini C, FalconeM (2013) Shaping the (auto)immune response in the gut: The role of intestinal immune regulation in the prevention of type 1 diabetes. Am J Clin Exp Immunol 2: 156-171. PMID: 23885333
38. Walker LJ, Kang YH, Smith MO, Tharmalingham H, Ramamurthy N, et al. (2012) Human MAIT and CD8αα cells develop from a pool of type-17 precommitted CD8+ T cells. Blood 119: 422-433. doi: 10.1182/blood-2011-05-353789 PMID: 22086415
39. Cengiz E, Connor CG, Ruedy KJ, Beck RW, Kollman C, et al. (2014) Pediatric diabetes consortium T1D new onset (NeOn) study: Clinical outcomes during the first year following diagnosis. Pediatric Diabetes 15: 287-293. doi: 10.1111/pedi.12068 PMID: 23944865
40. Mortensen HB, Swift PG, Holl RW, Hougaard P, Hansen L, et al. (2009) Multinational study in children and adolescents with newly diagnosed type 1 diabetes: Association of age, ketoacidosis, HLA status, and autoantibodies on residual beta-cell function and glycemic control 12 months after diagnosis. Pediatric Diabetes 11: 218-226. doi: 10.1111/j.1399-5448.2009.00566.x PMID: 19708904
41. Agner T, Damm P, Binder C (1987) Remission in IDDM: Prospective study of basal C-peptide and insulin dose in 268 consecutive patients. Diabetes Care 10: 164-169. doi: 10.2337/diacare.10.2.164 PMID: 3556104
42. Lee O, Cho Y, Kee S, Kim M, Jin H, et al. (2014) Circulating mucosal-associated invariant T cell levels and their cytokine levels in healthy adults. Exp Gerontol 49: 47-54. doi: 10.1016/j.exger.2013.11.003 PMID: 24269212
43. Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, et al. (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491: 717-723. doi: 10.1038/nature11605 PMID: 23051753
44. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108 Suppl 1: 4578-4585. doi: 10.1073/pnas.1000081107 PMID: 20668239
45. Cosgrove C, Ussher JE, Rauch A, Gartner K, Kurioka A, et al. (2013) Early and nonreversible decrease of CD161++/MAIT cells in HIV infection. Blood 121: 951-961. doi: 10.1182/blood-2012-06-436436 PMID: 23255555
46. Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, et al. (2003) Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422: 164-169. doi: 10.1038/nature01433 PMID: 12634786
47. Gaglia JL, Guimaraes AR, Harisinghani M, Turvey SE, Jackson R, et al. (2011) Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients. J Clin Invest 121: 442-445. doi: 10.1172/JCI44339 PMID: 21123946
48. Campbell-Thompson M, Wasserfall C, Montgomery EL, Atkinson MA, Kaddis JS (2012) Pancreas organ weight in individuals with disease-associated autoantibodies at risk for type 1 diabetes. JAMA 308: 2337-2339. doi: 10.1001/jama.2012.15008 PMID: 23232891
49. Charlton M, Ahlman B, Nair KS (2000) The effect of insulin on human small intestinal mucosal protein synthesis. Gastroenterology 118: 299-306. doi: 10.1016/S0016-5085(00)70212-5 PMID: 10648458
50. Heptulla RA, Rodriguez LM, Mason KJ, Haymond MW(2008) Gastric emptying and postprandial glucose excursions in adolescents with type 1 diabetes. Pediatric Diabetes 9: 561-566. doi: 10.1111/j.1399-5448.2008.00430.x PMID: 18761650
51. Martin E, Treiner E, Duban L, Guerri L, Laude H, et al. (2009) Stepwise development of MAIT cells in mouse and human. PLoS Biol 7: e54. doi: 10.1371/journal.pbio.1000054 PMID: 19278296
52. Leeansyah E, Ganesh A, Quigley MF, Sonnerborg A, Andersson J, et al. (2013) Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 121: 1124-1135. doi: 10.1182/blood-2012-07-445429 PMID: 23243281
53. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E (2013) The who's who of T-cell differentiation: Human memory T-cell subsets. Eur J Immunol 43: 2797-2809. doi: 10.1002/eji.201343751 PMID: 24258910
54. Corbett AJ, Eckle SB, Birkinshaw RW, Liu L, Patel O, et al. (2014) T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 509: 361-365. doi: 10.1038/nature13160 PMID: 24695216
55. Esposito K, Nappo F, Marfella R, Giugliano G, Giugliano F, et al. (2002) Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: Role of oxidative stress. Circulation 106: 2067-2072. doi: 10.1161/01.CIR.0000034509.14906.AE PMID: 12379575
56. Altinova AE, Yetkin I, Akbay E, Bukan N, Arslan M (2008) Serum IL-18 levels in patients with type 1 diabetes: Relations to metabolic control and microvascular complications. Cytokine 42: 217-221. doi: 10.1016/j.cyto.2008.02.006 PMID: 18359638
57. Katakami N, Kaneto H, Matsuhisa M, Yoshiuchi K, Kato K, et al. (2007) Serum interleukin-18 levels are increased and closely associated with various soluble adhesion molecule levels in type 1 diabetic patients. Diabetes Care 30: 159-161. doi: 10.2337/dc06-1768 PMID: 17192354
58. Ussher JE, Bilton M, Attwod E, Shadwell J, Richardson R, et al. (2014) CD161++CD8+T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner. Eur J Immunol 44: 195-203. doi: 10.1002/eji.201343509 PMID: 24019201