From biomarkers to a clue of biology: A computation-aided perspective of immune gene expression profiles in human type 1 diabetes

Frontiers in Immunology

Volumn 3, Issue OCT, 2012, Pages

  Han, Dongmei ^a   Cai, Xiaodong ^b   Wen, Ji ^b   Kenyon, Norma S ^a   Chen, Zhibin ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b University of Miami College of Engineering   (United States)

Author keywords

Autoimmunity; Computation; Diabetes; Gene expression; Human

Indexed keywords

EID: 84874218779     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00320     Document Type: Review

References (67)

1. Anjos, S. M., Shao, W., Marchand, L., and Polychronakos, C. (2005). Allelic effects on gene regulation at the autoimmunity-predisposing CTLA4 locus: a re-evaluation of the 3' +6230G>A polymorphism. Genes Immun. 6,305-311.
2. Bending, D., De La Pena, H., Veld-hoen, M., Phillips, J. M., Uyt-tenhove, C., Stockinger, B., etal. (2009). Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest. 119, 565-572.
3. Beyan, H., Drexhage, R. C., van der Heul Nieuwenhuijsen, L., de Wit, H., Padmos, R. C., Schloot, N. C., etal. (2010). Monocyte gene-expression profiles associated with childhood-onsettype1diabetesanddiseaserisk: astudyofidenticaltwins.Diabetes59, 1751-1755.
4. Bouaziz, J. D., Yanaba, K., Venturi, G. M., Wang, Y., Tisch, R. M., Poe, J. C., etal. (2007). Ther-apeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc. Natl. Acad. Sci. U.S.A. 104, 20878-20883.
5. Chen, Z., Benoist, C., and Mathis, D. (2005). How defects in central tol-erance impinge on a deficiency in regulatory T cells. Proc. Natl. Acad. Sci. U.S.A. 102,14735-14740.
6. Chen, Z., Stockton, J., Mathis, D., and Benoist, C. (2006). Modeling CTLA4-linked autoimmunity with RNA interference in mice. Proc. Natl. Acad. Sci. U.S.A. 103, 16400-16405.
7. Cooke, A. (2006). Th17 cells in inflam-matoryconditions. Rev. Diabet. Stud. 3, 72-75.
8. Cordell, H. J. (2009). Detecting gene-gene interactions that underlie human diseases. Nat. Rev. Genet. 10, 392-404.
9. Cordell, H. J., Todd, J. A., Bennett, S. T., Kawaguchi,Y.,andFarrall,M.(1995). Two-locus maximum lod score anal-ysis of a multifactorial trait: joint considerationofIDDM2andIDDM4 with IDDM1 in type 1 diabetes. Am. J. Hum. Genet. 57,920-934.
10. Duddy, M., Niino, M., Adatia, F., Hebert, S., Freedman, M., Atkins, H., etal. (2007). Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 178,6092-6099.
11. Eisenbarth, G. S., Gianani, R., Yu, L., Pietropaolo, M., Verge, C. F., Chase, H. P., etal. (1998). Dual-parameter model for prediction of type I diabetes mellitus. Proc. Assoc. Am. Physicians 110,126-135.
12. Emamaullee, J. A., Davis, J., Merani, S., Toso,C.,Elliott,J.F.,Thiesen,A.,etal. (2009). Inhibition of Th17 cells reg-ulates autoimmune diabetes in NOD mice. Diabetes 58,1302-1311.
13. Falcone, M., Lee, J., Patstone, G., Yeung, B., and Sarvetnick, N. (1998). B lymphocytes are crucial antigen-presenting cells in the pathogenic autoimmune response to GAD65 antigen in nonobese diabetic mice. J. Immunol. 161,1163-1168.
14. Fan, J., and Li, R. (2001). Variable selection via nonconcave penalized likelihood and its oracle properties. J. Am. Stat. Assoc. 96, 1348-1360.
15. Friedman, J., Hastie, T., and Tibshirani, R. (2010). Regularization paths for generalized linear models via coor-dinate descent. J. Stat. Softw. 33, 1-22.
16. Gallegos,A.M.,andBevan,M.J.(2004). Driven to autoimmunity: the nod mouse. Cell 117, 149-151.
17. Giordano, C., De Maria, R., Stassi, G., Todaro, M., Richiusa, P., Gior-dano, M., etal. (1995). Defective expression of the apoptosis-inducing CD95 (Fas/APO-1) molecule on T andBcellsinIDDM.Diabetologia38, 1449-1454.
18. Halminen,M.,Simell,O.,Knip,M.,and Ilonen,J. (2001).Cytokineexpression in unstimulated PBMC of children withtype1diabetesandsubjectspos-itive for diabetes-associated autoan-tibodies. Scand. J. Immunol. 53, 510-513.
19. Han, D., Cai, X., Wen, J., Matheson, D., Skyler, J. S., Kenyon, N. S., etal. (2012). Innate and adaptive immune gene expression profiles as biomark-ers in human type 1 diabetes. Clin. Exp. Immunol. 170,131-138.
20. Han, D., Leith, J., Alejandro, R., Bolton, W., Ricordi, C., and Kenyon, N. S. (2005). Peripheral blood cytotoxic lymphocytegenetranscriptlevelsdif-fer in patients with long-term type 1 diabetes compared to normal con-trols. Cell Transplant. 14, 403-409.
21. Han, D., Leyva, C. A., Matheson, D., Mineo, D., Messinger, S., Blomberg, B. B., etal. (2011). Immune pro-filing by multiple gene expression analysis in patients at-risk and with type 1 diabetes. Clin. Immunol. 139, 290-301.
22. Harris, D. P., Goodrich, S., Gerth, A. J., Peng, S. L., and Lund, F. E. (2005a). Regulation of IFN-gamma produc-tion by B effector 1 cells: essential roles for T-bet and the IFN-gamma receptor. J. Immunol. 174, 6781-6790.
23. Harris, D. P., Goodrich, S., Mohrs, K., Mohrs, M., and Lund, F. E. (2005b). Cutting edge: the development of IL-4-producingBcells(Beffector2cells) is controlled by IL-4, IL-4 receptor alpha,andTh2cells. J. Immunol. 175, 7103-7107.
24. Haseda, F., Imagawa, A., Murase-Mishiba, Y., Sano, H., Hirano-Kuwata, S., Ueda, H., etal. (2011). Low CTLA-4 expression in CD4+ helper T-cells in patients with fulminant type 1 diabetes. Immunol. Lett. 139,80-86.
25. Hedman, M., Ludvigsson, J., and Faresjo, M. K. (2006). Nicotinamide reduces high secretion of IFN-gamma in high-risk relatives even though it does not prevent type 1 diabetes. J. Interferon Cytokine Res. 26, 207-213.
26. Honkanen, J., Nieminen, J. K., Gao, R., Luopajarvi, K., Salo, H. M., Ilonen, J., etal. (2010). IL-17 immunity in human type 1 diabetes. J. Immunol. 185,1959-1967.
27. Hussain, M. J., Peakman, M., Gallati, H., Lo, S. S., Hawa, M., Viberti, G. C., etal. (1996). Elevated serum lev-els of macrophage-derived cytokines precede and accompany the onset of IDDM. Diabetologia 39,60-69.
28. Ide, A., Kawasaki, E., Abiru, N., Sun, F., Kobayashi, M., Fukushima, T., etal. (2004). Association between IL-18genepromoterpolymorphisms and CTLA-4 gene 49A/G polymor-phism in Japanese patients with type 1 diabetes. J. Autoimmun. 22, 73-78.
29. Ise, W., Kohyama, M., Nutsch, K. M., Lee, H. M., Suri, A., Unanue, E. R., etal. (2010). CTLA-4 suppresses the pathogenicity of self antigen-specific T cells by cell-intrinsic and cell-extrinsicmechanisms.Nat.Immunol. 11, 129-135.
30. Jain, N., Nguyen, H., Chambers, C., and Kang, J. (2010). Dual function of CTLA-4 in regulatory T cells and conventional T cells to prevent mul-tiorgan autoimmunity. Proc. Natl. Acad. Sci. U.S.A. 107,1524-1528.
31. Kallmann, B. A., Huther, M., Tubes, M., Feldkamp, J., Bertrams, J., Gries, F. A., etal. (1997). Systemic bias of cytokine production toward cell-mediated immune regulation in IDDM and toward humoral immu-nity in Graves' disease. Diabetes 46, 237-243.
32. Karlsson Faresjo, M. G., Ernerudh, J., and Ludvigsson, J. (2004). Cytokine profile in children during the first 3 months after the diagnosis of type 1 diabetes. Scand. J. Immunol. 59, 517-526.
33. King,C.,Ilic,A.,Koelsch,K.,andSarvet-nick, N. (2004). Homeostatic expansion of T cells during immune insufficiency generates autoimmunity.Cell 117,265-277.
34. Kreuwel, H. T., Morgan, D. J., Krahl, T., Ko, A., Sarvetnick, N., and Sherman, L. A. (1999). Comparing the relative role of perforin/granzyme versus Fas/Fas ligand cytotoxic path-ways in CD8+ T cell-mediated insulin-dependent diabetes mellitus. J. Immunol. 163,4335-4341.
35. Kreuwel, H. T., and Sherman, L. A. (2001).TheroleofFas-FasLinCD8+ T-cell-mediated insulin-dependent diabetes mellitus (IDDM). J. Clin. Immunol. 21, 15-18.
36. Kristiansen, O. P., Larsen, Z. M., and Pociot,F. (2000). CTLA-4 in autoimmune diseases-ageneralsuscepti-bility gene to autoimmunity? Genes Immun. 1, 170-184.
37. Kucharska, A. M., Gorska, E., Wasik, M., Pyrzak, B., and Demkow, U. (2009).ExpressionofCD152(CTLA-4) in children with autoimmune thy-roiditis and +49 A/G polymorphism of exon 1 of the CTLA-4 gene. J. Physiol. Pharmacol. 60(Suppl. 5), 77-80.
38. Lehuen, A., Diana, J., Zaccone, P., and Cooke, A. (2010). Immune cell crosstalk in type 1 diabetes. Nat. Rev. Immunol. 10, 501-513.
39. Lu,Y., Suzuki, J., Guillioli, M., Umland, O., and Chen, Z. (2011). Induc-tion of self-antigen-specific Foxp3(+ regulatory T cells in the periph-ery by lymphodepletion treatment with anti-mouse thymocyte glob-ulin in mice. Immunology 134, 50-59.
40. Luczynski, W., Wawrusiewicz-Kurylonek, N., Stasiak-Barmuta, A., Urban, R., Ilendo, E., Urban, M., etal. (2009). Diminished expression of ICOS, GITR and CTLA-4 at the mRNA level in T regulatory cells of children with newly diagnosed type 1 diabetes. Acta Biochim. Pol. 56, 361-370.
41. Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., etal. (2009). Finding the missing heritability of complex diseases. Nature 461,747-753.
42. Martin-Orozco, N., Chung, Y., Chang, S. H., Wang, Y. H., and Dong, C. (2009). Th17 cells promote pancre-atic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur. J. Immunol. 39,216-224.
43. Marwaha, A. K., Crome, S. Q., Pana-Giotopoulos, C., Berg, K. B., Qin, H., Ouyang, Q., etal. (2010). Cut-ting edge: Increased IL-17-secreting T cells in children with new-onset type 1 diabetes. J. Immunol. 185, 3814-3818.
44. Mathis,D.,and Benoist,C. (2010). Lev-ees of immunological tolerance. Nat. Immunol. 11,3-6.
45. Miska, J., Bas, E., Devarajan, P., and Chen, Z. (2012). Autoimmunity-mediated antitumor immunity: tumor as an immunoprivileged self. Eur. J. Immunol. 42,2584-2596.
46. Moriwaki, M., Itoh, N., Miyagawa, J., Yamamoto, K., Imagawa, A., Yam-agata, K., etal. (1999). Fas and Fas ligand expression in inflamed islets in pancreas sections of patients with recentonset Type I diabetes mellitus. Diabetologia 42, 1332-1340.
47. Nicoletti, F., Conget, I., Di Mauro, M., Di Marco, R., Mazzarino, M. C., Bendtzen, K., etal. (2002). Serum concentrations of the interferon-gamma-inducible chemokine IP-10/CXCL10 are augmented in both newly diagnosed Type I dia-betes mellitus patients and subjects at risk of developing the disease. Diabetologia 45,1107-1110.
48. O'Neill,S. K.,Liu,E.,and Cambier,J. C. (2009). Change you can B(cell)eive in: recent progress confirms a critical roleforBcellsintype1diabetes.Curr. Opin. Endocrinol. Diabetes Obes. 16, 293-298.
49. Padmos, R. C., Schloot, N. C., Beyan, H., Ruwhof, C., Staal, F. J., de Ridder, D., etal. (2008). Distinct monocytegene-expressionprofilesin autoimmune diabetes. Diabetes 57, 2768-2773.
50. Peggs, K. S., Quezada, S. A., Cham-Bers, C. A., Korman, A. J., and Allison, J. P. (2009). Blockade of CTLA-4 on both effector and regula-toryTcellcompartmentscontributes to the antitumor activity of anti-CTLA-4 antibodies. J. Exp. Med. 206, 1717-1725.
51. Pescovitz, M. D., Greenbaum, C. J., Krause-Steinrauf, H., Becker, D. J., Gitelman, S. E., Goland, R., etal. (2009). Rituximab, Blymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med. 361, 2143-2152.
52. Pociot, F., Akolkar, B., Concannon, P., Erlich, H. A., Julier, C., Morahan, G., etal. (2010). Genetics of type 1 diabetes: what's next? Diabetes 59, 1561-1571.
53. Pruitt, S. K., Boczkowski, D., de Rosa, N., Haley, N. R., Morse, M. A., Tyler, D. S., etal. (2011). Enhancement of antitumor immunity through local modulation of CTLA-4 and GITR by dendritic cells. Eur. J. Immunol. 41, 3553-3563.
54. Purohit, S., and She, J. X. (2008). Biomarkers for type 1 diabetes. Int. J. Clin. Exp. Med. 1,98-116.
55. Reynier, F., Pachot, A., Paye, M., Xu, Q., Turrel-Davin, F., Petit, F., etal. (2010). Specific gene expression signature associated with development of autoimmune type-I diabetes using whole-blood microar-ray analysis. Genes Immun. 11, 269-278.
56. Ryden, A., Bolmeson, C., Jonson, C. O., Cilio, C. M., and Faresjo, M. (2012). Low expression and secretion of circulating soluble CTLA-4 in peripheral blood mononuclear cells and sera from type 1 diabetic chil-dren. Diabetes Metab. Res. Rev. 28, 84-96.
57. Schuetz, C., Niehues, T., Friedrich, W., and Schwarz, K. (2010). Autoim-munity, autoinflammation and lym-phoma in combined immunodefi-ciency (CID). Autoimmun. Rev. 9, 477-482.
58. Serreze, D. V., Bridgett, M., Chap-Man, H. D., Chen, E., Richard, S. D., and Leiter, E. H. (1998). Sub-congenic analysis of the Idd13 locus in NOD/Lt mice: evidence for several susceptibility genes including a possible diabetogenic role for beta 2-microglobulin. J. Immunol. 160, 1472-1478.
59. Silveira, P. A., and Grey, S. T. (2006). B cells in the spotlight: innocent bystanders or major players in the pathogenesis of type 1 diabetes. Trends Endocrinol. Metab. 17, 128-135.
60. Stechova,K.,Kolar,M.,Blatny,R.,Halb-Huber, Z., Vcelakova, J., Hubackova, M., etal. (2011). Healthy first degree relatives of patients with type 1 dia-betes exhibit significant differences in basal gene expression pattern of immunocompetentcellscomparedto controls:expressionpatternasprede-terminant of autoimmune diabetes. Scand. J. Immunol. 75,210-219.
61. Suzuki, J., Ricordi, C., and Chen, Z. (2010). Immune tolerance induction by integrating innate and adaptive immune regulators. Cell Transplant. 19, 253-268.
62. Teft, W. A., Kirchhof, M. G., and Madrenas,J. (2006).Amolecularper-spective of CTLA-4 function. Annu. Rev. Immunol. 24, 65-97.
63. Ueda, H., Howson, J. M., Esposito, L., Heward, J., Snook, H., Chamberlain, G., etal. (2003). Association of the T-cell regulatory gene CTLA4 with susceptibilitytoautoimmunedisease. Nature 423, 506-511.
64. Wing, K., Onishi, Y., Prieto-Martin, P., Yamaguchi,T.,Miyara,M.,Fehervari, Z.,etal. (2008). CTLA-4 control over Foxp3+ regulatory T cell function. Science 322,271-275.
65. Wong, F. S., Wen, L., Tang, M., Ramanathan,M.,Visintin,I.,Daugh-erty, J., etal. (2004). Investigation of the role of B-cells in type 1 dia-betesintheNODmouse.Diabetes53, 2581-2587.
66. Yoon,J.W.,andJun,H.S. (2001).Cellu-larandmolecularpathogenicmecha-nisms of insulin-dependent diabetes mellitus. Ann. N. Y. Acad. Sci. 928, 200-211.
67. Zou,H.,and Trevor,T. (2005). Regular-ization and variable selection via the elastic net. J. R. Stat. Soc. Ser. B 67, 301-320.