Evaluation of in vivoT cell kinetics: Use of heavy isotope labelling in type 1 diabetes

Clinical and Experimental Immunology

Volumn 172, Issue 3, 2013, Pages 363-374

  Bollyky, J B ^a   Long, S A ^a   Fitch, M ^b   Bollyky, P L ^a   Rieck, M ^a   Rogers, R ^a   Samuels, P L ^a   Sanda, S ^a   Buckner, J H ^a   Hellerstein, M K ^b   Greenbaum, C J ^a  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Deuterium oxide; Heavy water; Isotope labelling; Memory T cell; Regulatory T cell; T cell kinetics; Type 1 diabetes

Indexed keywords

DEOXYRIBOSE; DEUTERIUM OXIDE;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL KINETICS; CLINICAL EVALUATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; ISOTOPE LABELING; LYMPHOCYTE PROLIFERATION; MALE; MASS FRAGMENTOGRAPHY; MATHEMATICAL MODEL; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TURNOVER TIME; ADOLESCENT; CASE CONTROL STUDY; CELL PROLIFERATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; KINETICS; METABOLISM; MIDDLE AGED; PATHOLOGY;

ADOLESCENT; ADULT; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DEOXYRIBOSE; DEUTERIUM OXIDE; DIABETES MELLITUS, TYPE 1; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; KINETICS; MALE; MIDDLE AGED; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT;

MLCS; MLOWN;

EID: 84876724582     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12064     Document Type: Article

References (46)

1. Makhlouf L, Grey ST, Dong V etal. Depleting anti-CD4 monoclonal antibody cures new-onset diabetes, prevents recurrent autoimmune diabetes, and delays allograft rejection in nonobese diabetic mice. Transplantation 2004; 77:990-997.
2. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG. Analysis of islet inflammation in human type 1 diabetes. Clin Exp Immunol 2009; 155:173-181.
3. Segurado OG, Arnaiz-Villena A, Wank R, Schendel DJ. The multifactorial nature of MHC-linked susceptibility to insulin-dependent diabetes. Autoimmunity 1993; 15:85-89.
4. Mikulkova Z, Praksova P, Stourac P etal. Numerical defects in CD8+. Cell Immunol 2010; 262:75-79.
5. Petersen LD, Duinkerken G, Bruining GJ, van Lier RA, de Vries RR, Roep BO. Increased numbers of in vivo activated T cells in patients with recent onset insulin-dependent diabetes mellitus. J Autoimmun 1996; 9:731-737.
6. Hedman M, Faresjo M, Axelsson S, Ludvigsson J, Casas R. Impaired CD4 and CD8 T cell phenotype and reduced chemokine secretion in recent-onset type 1 diabetic children. Clin Exp Immunol 2008; 153:360-368.
7. Peakman M, Mahalingam M, Leslie RD, Vergani D. Co-expression of CD45RA (naive) and CD45R0 (memory) T-cell markers. Lancet 1994; 343:424.
8. Wildin RS, Freitas A. IPEX and FOXP3: clinical and research perspectives. J Autoimmun 2005; 25 (Suppl.):56-62.
9. Brusko T, Wasserfall C, McGrail K etal. No alterations in the frequency of FOXP3+ regulatory T-cells in type 1 diabetes. Diabetes 2007; 56:604-612.
10. Tree TI, Roep BO, Peakman M. A mini meta-analysis of studies on CD4+CD25+ T cells in human type 1 diabetes: report of the Immunology of Diabetes Society T Cell Workshop. Ann NY Acad Sci 2006; 1079:9-18.
11. Kukreja A, Cost G, Marker J etal. Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest 2002; 109:131-140.
12. Long SA, Cerosaletti K, Bollyky PL etal. Defects in IL-2R signaling contribute to diminished maintenance of FOXP3 expression in CD4(+)CD25(+) regulatory T-cells of type 1 diabetic subjects. Diabetes 2010; 59:407-415.
13. Alcina A, Fedetz M, Ndagire D etal. IL2RA/CD25 gene polymorphisms: uneven association with multiple sclerosis (MS) and type 1 diabetes (T1D). PloS ONE 2009; 4:e4137.
14. Dendrou CA, Wicker LS. The IL-2/CD25 pathway determines susceptibility to T1D in humans and NOD mice. J Clin Immunol 2008; 28:685-696.
15. Hakonarson H, Qu HQ, Bradfield JP etal. A novel susceptibility locus for type 1 diabetes on Chr12q13 identified by a genome-wide association study. Diabetes 2008; 57:1143-1146.
16. Todd JA, Walker NM, Cooper JD etal. Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes. Nat Genet 2007; 39:857-864.
17. Chen Q, Kim YC, Laurence A, Punkosdy GA, Shevach EM. IL-2 controls the stability of Foxp3 expression in TGF-beta-induced Foxp3+ T cells in vivo. J Immunol 2011; 186:6329-6337.
18. Koenecke C, Czeloth N, Bubke A etal. Alloantigen-specific de novo-induced Foxp3+ Treg revert in vivo and do not protect from experimental GVHD. Eur J Immunol 2009; 39:3091-3096.
19. Buckner JH. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat Rev Immunol 2010; 10:849-859.
20. Setoguchi R, Hori S, Takahashi T, Sakaguchi S. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 2005; 201:723-735.
21. Schwartz RH. Natural regulatory T cells and self-tolerance. Nat Immunol 2005; 6:327-330.
22. Delovitch TL, Singh B. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 1997; 7:727-738.
23. Vukmanovic-Stejic M, Zhang Y, Cook JE etal. Human CD4+ CD25hi Foxp3+ regulatory T cells are derived by rapid turnover of memory populations in vivo. J Clin Invest 2006; 116:2423-2433.
24. Hellerstein M, Hanley MB, Cesar D etal. Directly measured kinetics of circulating T lymphocytes in normal and HIV-1-infected humans. Nat Med 1999; 5:83-89.
25. Hellerstein MK, Hoh RA, Hanley MB etal. Subpopulations of long-lived and short-lived T cells in advanced HIV-1 infection. J Clin Invest 2003; 112:956-966.
26. Neese RA, Misell LM, Turner S etal. Measurement in vivo of proliferation rates of slow turnover cells by 2H2O labeling of the deoxyribose moiety of DNA. Proc Natl Acad Sci USA 2002; 99:15345-15350.
27. Mohri H, Perelson AS, Tung K etal. Increased turnover of T lymphocytes in HIV-1 infection and its reduction by antiretroviral therapy. J Exp Med 2001; 194:1277-1287.
28. Defoiche J, Debacq C, Asquith B etal. Reduction of B cell turnover in chronic lymphocytic leukaemia. Br J Haematol 2008; 143:240-247.
29. Defoiche J, Zhang Y, Lagneaux L, Willems L, Macallan DC. In vivo ribosomal RNA turnover is down-regulated in leukaemic cells in chronic lymphocytic leukaemia. Br J Haematol 2010; 151:192-195.
30. Akbar AN, Vukmanovic-Stejic M, Taams LS, Macallan DC. The dynamic co-evolution of memory and regulatory CD4+ T cells in the periphery. Nat Rev Immunol 2007; 7:231-237.
31. Vukmanovic-Stejic M, Agius E, Booth N etal. The kinetics of CD4+Foxp3+ T cell accumulation during a human cutaneous antigen-specific memory response in vivo. J Clin Invest 2008; 118:3639-3650.
32. Asquith B, Debacq C, Macallan DC, Willems L, Bangham CR. Lymphocyte kinetics: the interpretation of labelling data. Trends Immunol 2002; 23:596-601.
33. Busch R, Neese RA, Awada M, Hayes GM, Hellerstein MK. Measurement of cell proliferation by heavy water labeling. Nat Protoc 2007; 2:3045-3057.
34. Collins ML, Eng S, Hoh R, Hellerstein MK. Measurement of mitochondrial DNA synthesis in vivo using a stable isotope-mass spectrometric technique. J Appl Physiol 2003; 94:2203-2211.
35. Macallan DC, Fullerton CA, Neese RA, Haddock K, Park SS, Hellerstein MK. Measurement of cell proliferation by labeling of DNA with stable isotope-labeled glucose: studies in vitro, in animals, and in humans. Proc Natl Acad Sci USA 1998; 95:708-713.
36. Vrisekoop N, den Braber I, de Boer AB etal. Sparse production but preferential incorporation of recently produced naive T cells in the human peripheral pool. Proc Natl Acad Sci USA 2008; 105:6115-6120.
37. Asquith B, Borghans JA, Ganusov VV, Macallan DC. Lymphocyte kinetics in health and disease. Trends Immunol 2009; 30:182-189.
38. Macallan DC, Asquith B, Zhang Y etal. Measurement of proliferation and disappearance of rapid turnover cell populations in human studies using deuterium-labeled glucose. Nat Protoc 2009; 4:1313-1327.
39. Macallan DC, Wallace D, Zhang Y etal. Rapid turnover of effector-memory CD4(+) T cells in healthy humans. J Exp Med 2004; 200:255-260.
40. Wallace DL, Zhang Y, Ghattas H etal. Direct measurement of T cell subset kinetics in vivo in elderly men and women. J Immunol 2004; 173:1787-1794.
41. Park SO, Han YW, Aleyas AG etal. Low-dose antigen-experienced CD4+ T cells display reduced clonal expansion but facilitate an effective memory pool in response to secondary exposure. Immunology 2008; 123:426-437.
42. Sun JC, Williams MA, Bevan MJ. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 2004; 5:927-933.
43. Swain SL, Bradley LM, Croft M etal. Helper T-cell subsets: phenotype, function and the role of lymphokines in regulating their development. Immunol Rev 1991; 123:115-144.
44. Schneider A, Rieck M, Sanda S, Pihoker C, Greenbaum C, Buckner JH. The effector T cells of diabetic subjects are resistant to regulation via CD4+ FOXP3+ regulatory T cells. J Immunol 2008; 181:7350-7355.
45. Miyara M, Yoshioka Y, Kitoh A etal. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 2009; 30:899-911.
46. Booth NJ, McQuaid AJ, Sobande T etal. Different proliferative potential and migratory characteristics of human CD4+ regulatory T cells that express either CD45RA or CD45RO. J Immunol 2010; 184:4317-4326.