Activity of childhood lupus nephritis is linked to altered T cell and cytokine homeostasis

Journal of Clinical Immunology

Volumn 32, Issue 3, 2012, Pages 477-487

  Edelbauer, Monika ^a   Kshirsagar, Sudhir ^a   Riedl, Magdalena ^a   Billing, Heiko ^b   Tönshoff, Burkhard ^b   Haffner, Dieter ^c   Cortina, Gerard ^a   Amon, Oliver ^d   Ross, Sophia ^e   Dötsch, Jörg ^f   Wechselberger, Gottfried ^a   Weber, Lutz T ^g   Dablander, Martin ^h   Anliker, Markus ^h   Griesmacher, Andrea ^h   Steichen Gersdorf, Elisabeth ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^e UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^f UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^g LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^h UNIVERSITY HOSPITAL INNSBRUCK   (Austria)

Author keywords

Childhood; cytokines; effector T cells; lupus nephritis; regulatory T cells

Indexed keywords

ANTIBODY; CD28 ANTIBODY; CD3 ANTIBODY; CD4 ANTIGEN; CD45RO ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; CYCLOPHOSPHAMIDE; CYCLOSPORIN; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 17; INTERLEUKIN 23; MONOCYTE CHEMOTACTIC PROTEIN 1; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PREDNISONE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CD4 CD8 RATIO; CELLULAR DISTRIBUTION; CHILD; CHILDHOOD DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DRUG PULSE THERAPY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FOCAL GLOMERULOSCLEROSIS; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; INFANT; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHOCYTE DIFFERENTIATION; MALE; MEMORY T LYMPHOCYTE; MINIMAL CHANGE GLOMERULONEPHRITIS; NEPHROTIC SYNDROME; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCORING SYSTEM; SYSTEMIC LUPUS ERYTHEMATOSUS DISEASE ACTIVITY INDEX 2000 UPDATE; T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ADOLESCENT; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHEMOKINE CCL2; CHILD; CYTOKINES; FEMALE; HOMEOSTASIS; HUMANS; IMMUNOPHENOTYPING; LEUKOCYTES, MONONUCLEAR; LUPUS NEPHRITIS; MALE; RECEPTORS, CCR2; RECEPTORS, CXCR3; RECEPTORS, CYTOKINE;

EID: 84861481620     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-011-9637-0     Document Type: Article

References (33)

1. Crispin JC, Tsokos GC. Novel molecular targets in the treatment of systemic lupus erythematosus. Autoimmun Rev. 2008;7(3):256-61. doi:10.1016/j.autrev.2007.11.020.
2. Alexopoulos E, Seron D, Hartley RB, Cameron JS. Lupus nephritis: correlation of interstitial cells with glomerular function. Kidney Int. 1990;37(1):100-9. (Pubitemid 20023773)
3. Crispin JC, Kyttaris VC, Juang YT, Tsokos GC. How signaling and gene transcription aberrations dictate the systemic lupus erythematosus T cell phenotype. Trends Immunol. 2008;29(3):110-5.
4. Crispin JC, Oukka M, Bayliss G, Cohen RA, Van Beek CA, Stillman IE, et al. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J Immunol. 2008;181(12):8761-6.
5. Rajagopalan S, Zordan T, Tsokos GC, Datta SK. Pathogenic anti- DNA autoantibody-inducing T helper cell lines from patients with active lupus nephritis: isolation of CD4-8- T helper cell lines that express the gamma delta T-cell antigen receptor. Proc Natl Acad Sci U S A. 1990;87(18):7020-4.
6. Dolff S, Quandt D, Wilde B, Feldkamp T, Hua F, Cai X, et al. Increased expression of costimulatory markers CD134 and CD80 on interleukin-17 producing T cells in patients with systemic lupus erythematosus. Arthritis Res Ther. 12(4):R150. doi:10.1186/ar3100.
7. Steinmetz OM, Turner JE, Paust HJ, Lindner M, Peters A, Heiss K, et al. CXCR3 mediates renal Th1 and Th17 immune response in murine lupus nephritis. J Immunol. 2009;183(7):4693-704. doi:10.4049/jimmunol.0802626.
8. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell. 2008;133(5):775-87. doi:10.1016/j.cell.2008.05.009. (Pubitemid 351707693)
9. Humrich JY, Morbach H, Undeutsch R, Enghard P, Rosenberger S, Weigert O, et al. Homeostatic imbalance of regulatory and effector T cells due to IL-2 deprivation amplifies murine lupus. Proc Natl Acad Sci U S A. 107(1):204-9. doi:10.1073/pnas.0903158107.
10. La Cava A. The busy life of regulatory T cells in systemic lupus erythematosus. Discov Med. 2009;8(40):13-7.
11. Brunner HI, Gladman DD, Ibanez D, Urowitz MD, Silverman ED. Difference in disease features between childhood-onset and adultonset systemic lupus erythematosus. Arthritis Rheum. 2008;58 (2):556-62. (Pubitemid 351294890)
12. Bartosh SM, Fine RN, Sullivan EK. Outcome after transplantation of young patients with systemic lupus erythematosus: a report of the North American pediatric renal transplant cooperative study. Transplantation. 2001;72(5):973-8. (Pubitemid 32879884)
13. Doria A, Vesco P, Zulian F, Gambari PF. The 1982 ARA/ACR criteria for the classification of systemic lupus erythematosus in pediatric and adult patients. Clin Exp Rheumatol. 1994;12(6):689-90.
14. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725. doi:10.1002/1529-0131(199709)40:9<1725::AID- ART29>3.0.CO;2-Y.
15. Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol. 2004;15(2):241-50. (Pubitemid 38140764)
16. Gladman DD, Ibanez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002;29(2):288-91. (Pubitemid 34118775)
17. Brunner HI, Feldman BM, Bombardier C, Silverman ED. Sensitivity of the Systemic Lupus Erythematosus Disease Activity Index, British Isles Lupus Assessment Group Index, and Systemic Lupus Activity Measure in the evaluation of clinical change in childhood-onset systemic lupus erythematosus. Arthritis Rheum. 1999;42(7):1354-60. doi :10.1002/1529-0131(199907)42:7<1354::AID- ANR8>3.0.CO;2-4.
18. Croft M, So T, Duan W, Soroosh P. The significance of OX40 and OX40L to T-cell biology and immune disease. Immunol Rev. 2009;229(1):173-91. doi:10.1111/j.1600-065X.2009.00766.x.
19. Vu MD, Xiao X, Gao W, Degauque N, Chen M, Kroemer A, et al. OX40 costimulation turns off Foxp3+ Tregs. Blood. 2007;110 (7):2501-10. doi:10.1182/blood-2007-01-070748. (Pubitemid 47523172)
20. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401(6754):708-12. doi:10.1038/44385.
21. Worbs T, Forster R. A key role for CCR7 in establishing central and peripheral tolerance. Trends Immunol. 2007;28(6):274-80. doi:10.1016/j.it.2007. 04.002. (Pubitemid 46810350)
22. Davalos-Misslitz AC, Rieckenberg J, Willenzon S, Worbs T, Kremmer E, Bernhardt G, et al. Generalized multi-organ autoimmunity in CCR7-deficient mice. Eur J Immunol. 2007;37(3):613-22. doi:10.1002/eji.200636656. (Pubitemid 46916929)
23. Kulkarni O, Anders HJ. Chemokines in lupus nephritis. Front Biosci. 2008;13:3312-20. (Pubitemid 351594684)
24. El-Shehaby A, Darweesh H, El-Khatib M, Momtaz M, Marzouk S, El-Shaarawy N, et al. Correlations of urinary biomarkers, TNF-like weak inducer of apoptosis (TWEAK), osteoprotegerin (OPG), monocyte chemoattractant protein-1 (MCP-1), and IL-8 with lupus nephritis. J Clin Immunol. 2011;31(5):848-56. doi:10.1007/s10875-011-9555-1.
25. Summers SA, Steinmetz OM, Li M, Kausman JY, Semple T, Edgtton KL, et al. Th1 and Th17 cells induce proliferative glomerulonephritis. J Am Soc Nephrol. 2009;20(12):2518-24. doi:10.1681/ASN.2009030337.
26. Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol. 2009;21 (3):274-80. doi:10.1016/j.coi.2009. 05.021.
27. Gorelik L, Flavell RA. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity. 2000;12(2):171-81. (Pubitemid 30398631)
28. Manel N, Unutmaz D, Littman DR. The differentiation of human T (H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol. 2008;9(6):641-9. doi:10.1038/ni.1610. (Pubitemid 351714729)
29. Xu L, Kitani A, Fuss I, Strober W. Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol. 2007;178(11):6725-9. (Pubitemid 46847395)
30. McGeachy MJ, Chen Y, Tato CM, Laurence A, Joyce-Shaikh B, Blumenschein WM, et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol. 2009;10(3):314-24. doi:10.1038/ni.1698.
31. Zhang Z, Kyttaris VC, Tsokos GC. The role of IL-23/IL-17 axis in lupus nephritis. J Immunol. 2009;183(5):3160-9. doi:10.4049/jimmunol.0900385.
32. Hirota K, Duarte JH, Veldhoen M, Hornsby E, Li Y, Cua DJ, et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol. 2011;12(3):255-63. doi:10.1038/ni.1993.
33. Damsker JM, Hansen AM, Caspi RR. Th1 and Th17 cells: adversaries and collaborators. Ann N Y Acad Sci. 2010;1183:211-21. doi:10.1111/j.1749-6632.2009. 05133.x.