Type 1 diabetes in mice and men: Gene expression profiling to investigate disease pathogenesis

Immunologic Research

Volumn 58, Issue 2-3, 2014, Pages 340-350

  Yip, Linda ^a   Fathman, C Garrison ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenosine a1 receptor (adora1); Deformed epidermal autoregulatory factor 1 (deaf1); Microarray; Nonobese diabetic mice; Type 1 diabetes

Indexed keywords

AUTOANTIBODY; BIOLOGICAL MARKER; TISSUE ANTIGEN; ADENOSINE A1 RECEPTOR; ANTIGEN; DEAF1 PROTEIN, HUMAN; NUCLEAR PROTEIN;

ADORA1 GENE; AGE; ANTIGEN EXPRESSION; CELL STRESS; DEAF1 GENE; DISEASE COURSE; ENVIRONMENTAL FACTOR; GENE; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HUMAN; HYPERGLUCAGONEMIA; IMMUNOLOGICAL TOLERANCE; IMPAIRED GLUCOSE TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE CELL; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREAS ISLET; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; STROMA CELL; TISSUE SPECIFICITY; ALTERNATIVE RNA SPLICING; ANIMAL; ANTIBODY SPECIFICITY; ANTIGEN PRESENTATION; CYTOLOGY; DIABETES MELLITUS, TYPE 1; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; TRANSLATIONAL RESEARCH;

ALTERNATIVE SPLICING; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; NUCLEAR PROTEINS; ORGAN SPECIFICITY; RECEPTOR, ADENOSINE A1; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84901612211     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-014-8501-8     Document Type: Review

References (75)

1. Concannon P, Rich SS, Nepom GT. Genetics of type 1A diabetes. N Engl J Med. 2009;360:1646-54.
2. Noble JA, Erlich HA. Genetics of type 1 diabetes. Cold Spring Harb Perspect Med. 2012;2:a007732.
3. Pociot F, Akolkar B, Concannon P, Erlich HA, Julier C, Morahan G, et al. Genetics of type 1 diabetes: what's next? Diabetes. 2010;59:1561-71.
4. Leiter EH. Nonobese diabetic mice and the genetics of diabetes susceptibility. Curr Diabetes Rep. 2005;5:141-8. (Pubitemid 40823498)
5. Suri A, Walters JJ, Gross ML, Unanue ER. Natural peptides selected by diabetogenic DQ8 and murine I-A(g7) molecules show common sequence specificity. J Clin Investig. 2005;115:2268-76. (Pubitemid 41135930)
6. Young EF, Hess PR, Arnold LW, Tisch R, Frelinger JA. Islet lymphocyte subsets in male and female NOD mice are qualitatively similar but quantitatively distinct. Autoimmunity. 2009;42:678-91.
7. Yaacob NS, Goh KS, Norazmi MN. Male and female NOD mice differentially express peroxisome proliferator-activated receptors and pathogenic cytokines. Exp Toxicol Pathol. 2012;64:127-31.
8. Enomoto A, Hasegawa M, Komine S. Spleen cells derived from male non-obese diabetic mice are capable of suppressing the autoantigen-specific production of interferon-gamma of female cells in vitro. Biosci Biotechnol Biochem. 2005;69:2312-8. (Pubitemid 43004359)
9. Bao M, Yang Y, Jun HS, Yoon JW. Molecular mechanisms for gender differences in susceptibility to T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Immunol. 2002;168:5369-75. (Pubitemid 34496006)
10. Whitacre CC. Sex differences in autoimmune disease. Nat Immunol. 2001;2:777-80.
11. Ronningen KS. Type 1 diabetes: prospective cohort studies for identification of the environmental trigger. Arch Immunol Ther Exp (Warsz). 2013;61:459-68.
12. Knip M, Simell O. Environmental triggers of type 1 diabetes. Cold Spring Harb Perspect Med. 2012;2:a007690.
13. Barbeau WE. What is the key environmental trigger in type 1 diabetes - is it viruses, or wheat gluten, or both? Autoimmun Rev. 2012;12:295-9.
14. Larsson PG, Lakshmikanth T, Svedin E, King C, Flodstrom-Tullberg M. Previous maternal infection protects offspring from enterovirus infection and prevents experimental diabetes development in mice. Diabetologia. 2013;56:867-74.
15. Hyoty H. Enterovirus infections and type 1 diabetes. Ann Med. 2002;34:138-47. (Pubitemid 34804186)
16. Myers MA, Hettiarachchi KD, Ludeman JP, Wilson AJ, Wilson CR, Zimmet PZ. Dietary microbial toxins and type 1 diabetes. Ann N Y Acad Sci. 2003;1005:418-22. (Pubitemid 38507798)
17. Furuse M, Kimura C, Takahashi H, Okumura J. Influence of dietary sorbose on diabetes in nonobese diabetic mice. Comp Biochem Physiol Comp Physiol. 1994;108:123-7. (Pubitemid 24201214)
18. Hermitte L, Atlan-Gepner C, Payan MJ, Mehelleb M, Vialettes B. Dietary protection against diabetes in NOD mice: lack of a major change in the immune system. Diabete Metab. 1995;21:261-8.
19. Marietta EV, Gomez AM, Yeoman C, Tilahun AY, Clark CR, Luckey DH, et al. Low incidence of spontaneous type 1 diabetes in non-obese diabetic mice raised on gluten-free diets is associated with changes in the intestinal microbiome. PLoS One. 2013;8:e78687.
20. Funda DP, Kaas A, Tlaskalova-Hogenova H, Buschard K. Glu-ten- free but also gluten-enriched (gluten+) diet prevent diabetes in NOD mice; the gluten enigma in type 1 diabetes. Diabetes Metab Res Rev. 2008;24:59-63. (Pubitemid 351176001)
21. MacFarlane AJ, Strom A, Scott FW. Epigenetics: deciphering how environmental factors may modify autoimmune type 1 diabetes. Mamm Genome. 2009;20:624-32.
22. Luo FL, Yuan F, Peng Z, Zhou W, Fang L, Cai JF. Regulation different network analysis of rheumatoid arthritis (RA) and osteoarthritis (OA). Eur Rev Med Pharmacol Sci. 2013;17:2504-11.
23. Armananzas R, Calvo B, Inza I, Lopez-Hoyos M, Martinez-Taboada V, Ucar E, et al. Microarray analysis of autoimmune diseases by machine learning procedures. IEEE Trans Inf Technol Biomed. 2009;13:341-50.
24. Dutta R. Gene expression changes underlying cortical pathology: clues to understanding neurological disability in multiple sclerosis. Mult Scler J. 2013;19:1249-54.
25. Yip L, Taylor C, Whiting CC, Fathman CG. Diminished adenosine A1 receptor expression in pancreatic alpha cells may contribute to the pathology of type 1 diabetes. Diabetes. 2013;62:4208-19.
26. Kodama K, Butte AJ, Creusot RJ, Su L, Sheng D, Hartnett M, et al. Tissue- and age-specific changes in gene expression during disease induction and progression in NOD mice. Clin Immunol. 2008;129:195-201.
27. Vang T, Congia M, Macis MD, Musumeci L, Orru V, Zavattari P, et al. Autoimmune-associated lymphoid tyrosine phosphatase is a gain-of-function variant. Nat Genet. 2005;37:1317-9. (Pubitemid 41722185)
28. Long A, Buckner JH. Intersection between genetic polymorphisms and immune deviation in type 1 diabetes. Curr Opin Endocrinol Diabetes Obes. 2013;20:285-91.
29. Maine CJ, Hamilton-Williams EE, Cheung J, Stanford SM, Bottini N, Wicker LS, et al. PTPN22 alters the development of regulatory T cells in the thymus. J Immunol. 2012;188:5267-75.
30. Vang T, Liu WH, Delacroix L, Wu S, Vasile S, Dahl R, et al. LYP inhibits T-cell activation when dissociated from CSK. Nat Chem Biol. 2012;8:437-46.
31. Welch JS, Escoubet-Lozach L, Sykes DB, Liddiard K, Greaves DR, Glass CK. TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J Biol Chem. 2002;277:42821-9. (Pubitemid 35285658)
32. Arora M, Chen L, Paglia M, Gallagher I, Allen JE, Vyas YM, et al. Simvastatin promotes Th2-type responses through the induction of the chitinase family member Ym1 in dendritic cells. Proc Natl Acad Sci USA. 2006;103:7777-82.
33. Yoshida Y. F-box proteins that contain sugar-binding domains. Biosci Biotechnol Biochem. 2007;71:2623-31. (Pubitemid 350164244)
34. Gagnerault MC, Luan JJ, Lotton C, Lepault F. Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J Exp Med. 2002;196:369-77. (Pubitemid 34875666)
35. Kuttenkeuler D, Pelte N, Ragab A, Gesellchen V, Schneider L, Blass C, et al. A large-scale RNAi screen identifies Deaf1 as a regulator of innate immune responses in Drosophila. J Innate Immun. 2010;2:181-94.
36. Reed DE, Huang XM, Wohlschlegel JA, Levine MS, Senger K. DEAF-1 regulates immunity gene expression in Drosophila. Proc Natl Acad Sci USA. 2008;105:8351-6. (Pubitemid 351904759)
37. Huggenvik JI, Michelson RJ, Collard MW, Ziemba AJ, Gurley P, Mowen KA. Characterization of a nuclear deformed epidermal autoregulatory factor-1 (DEAF-1)-related (NUDR) transcriptional regulator protein. Mol Endocrinol. 1998;12:1619-39. (Pubitemid 30663442)
38. Wojciak JM, Clubb RT. Finding the function buried in SAND. Nat Struct Biol. 2001;8:568-70. (Pubitemid 32612997)
39. Anderson MS, Venanzi ES, Klein L, Chen Z, Berzins SP, Turley SJ, et al. Projection of an immunological self shadow within the thymus by the aire protein. Science. 2002;298:1395-401. (Pubitemid 35346134)
40. Gavanescu I, Benoist C, Mathis D. B cells are required for Airedeficient mice to develop multi-organ autoinflammation: a therapeutic approach for APECED patients. Proc Natl Acad Sci USA. 2008;105:13009-14.
41. Lee JW, Epardaud M, Sun J, Becker JE, Cheng AC, Yonekura AR, et al. Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat Immunol. 2007;8:181-90. (Pubitemid 46152649)
42. Yip L, Su L, Sheng D, Chang P, Atkinson M, Czesak M, et al. Deaf1 isoforms control the expression of genes encoding peripheral tissue antigens in the pancreatic lymph nodes during type 1 diabetes. Nat Immunol. 2009;10:1026-33.
43. Yip L, Creusot RJ, Pager CT, Sarnow P, Fathman CG. Reduced DEAF1 function during type 1 diabetes inhibits translation in lymph node stromal cells by suppressing Eif4g3. J Mol Cell Biol. 2013;5:99-110.
44. Gradi A, Imataka H, Svitkin YV, Rom E, Raught B, Morino S, et al. A novel functional human eukaryotic translation initiation factor 4G. Mol Cell Biol. 1998;18:334-42. (Pubitemid 28021044)
45. Marissen WE, Gradi A, Sonenberg N, Lloyd RE. Cleavage of eukaryotic translation initiation factor 4GII correlates with translation inhibition during apoptosis. Cell Death Differ. 2000;7:1234-43. (Pubitemid 32042231)
46. Larsen SL, Pedersen LO, Buus S, Stryhn A. T cell responses affected by aminopeptidase N (CD13)-mediated trimming of major histocompatibility complex class II-bound peptides. J Exp Med. 1996;184:183-9. (Pubitemid 26247228)
47. Eizirik DL, Sammeth M, Bouckenooghe T, Bottu G, Sisino G, Igoillo-Esteve M, et al. The human pancreatic islet transcriptome: expression of candidate genes for type 1 diabetes and the impact of pro-inflammatory cytokines. PLoS Genet. 2012;8:e1002552.
48. van Lummel M, Zaldumbide A, Roep BO. Changing faces, unmasking the beta-cell: post-translational modification of antigens in type 1 diabetes. Curr Opin Endocrinol Diabetes Obes. 2013;20:299-306.
49. Cheng JT, Chi TC, Liu IM. Activation of adenosine A1 receptors by drugs to lower plasma glucose in streptozotocin-induced diabetic rats. Auton Neurosci. 2000;83:127-33.
50. Johansson SM, Salehi A, Sandstrom ME, Westerblad H, Lundquist I, Carlsson PO, et al. A1 receptor deficiency causes increased insulin and glucagon secretion in mice. Biochem Pharmacol. 2007;74:1628-35. (Pubitemid 47614964)
51. Ohneda A, Kobayashi T, Nihei J, Nishikawa K. Glucagon in spontaneously diabetic KK mice. Horm Metab Res. 1981;13:207-11. (Pubitemid 11104329)
52. Ohneda A, Kobayashi T, Nihei J, Tochino Y, Kanaya H, Makino S. Secretion of glucagon in spontaneously diabetic NOD mice. J Jpn Diabet Soc. 1981;24:202.
53. Ohneda A, Kobayashi T, Nihei J, Tochino Y, Kanaya H, Makino S. Insulin and glucagon in spontaneously diabetic non-obese mice. Diabetologia. 1984;27:460-3. (Pubitemid 14022685)
54. Yang GK, Fredholm BB, Kieffer TJ, Kwok YN. Improved blood glucose disposal and altered insulin secretion patterns in adenosine A(1) receptor knockout mice. Am J Physiol Endocrinol Metab. 2012;303:E180-90.
55. Salehi A, Parandeh F, Fredholm BB, Grapengiesser E, Hellman B. Absence of adenosine A1 receptors unmasks pulses of insulin release and prolongs those of glucagon and somatostatin. Life Sci. 2009;85:470-6.
56. Burton AR, Vincent E, Arnold PY, Lennon GP, Smeltzer M, Li CS, et al. On the pathogenicity of autoantigen-specific T-cell receptors. Diabetes. 2008;57:1321-30.
57. Leiter EH, Coleman DL, Eppig JJ. Endocrine pancreatic cells of postnatal "diabetes" (db) mice in cell culture. In Vitro. 1979;15:507-21. (Pubitemid 10230808)
58. Coulaud J, Durant S, Homo-Delarche F. Glucose homeostasis in pre-diabetic NOD and lymphocyte-deficient NOD/SCID mice during gestation. Rev Diabet Stud. 2010;7:36-46.
59. Amrani A, Durant S, Throsby M, Coulaud J, Dardenne M, Homo-Delarche F. Glucose homeostasis in the nonobese diabetic mouse at the prediabetic stage. Endocrinology. 1998;139:1115-24. (Pubitemid 28510130)
60. Aaen K, Rygaard J, Josefsen K, Petersen H, Brogren CH, Horn T, et al. Dependence of antigen expression on functional state of beta-cells. Diabetes. 1990;39:697-701. (Pubitemid 20218968)
61. Buschard K. The functional state of the beta cells in the pathogenesis of insulin-dependent diabetes mellitus. Autoimmunity. 1991;10:65-9.
62. Greenbaum CJ, Prigeon RL, D'Alessio DA. Impaired beta-cell function, incretin effect, and glucagon suppression in patients with type 1 diabetes who have normal fasting glucose. Diabetes. 2002;51:951-7. (Pubitemid 34438336)
63. Unger RH, Aguilar-Parada E, Muller WA, Eisentraut AM. Studies of pancreatic alpha cell function in normal and diabetic subjects. J Clin Investig. 1970;49:837-48.
64. Dinneen S, Alzaid A, Turk D, Rizza R. Failure of glucagon suppression contributes to postprandial hyperglycaemia in IDDM. Diabetologia. 1995;38:337-43.
65. Hollander PH, Asplin CM, Kniaz D, Hansen JA, Palmer JP. Beta-cell dysfunction in nondiabetic HLA identical siblings of insulindependent diabetics. Diabetes. 1982;31:149-53. (Pubitemid 12223967)
66. Lopez-Bigas N, Audit B, Ouzounis C, Parra G, Guigo R. Are splicing mutations the most frequent cause of hereditary disease? FEBS Lett. 2005;579:1900-3. (Pubitemid 40404028)
67. Douglas AG, Wood MJ. RNA splicing: disease and therapy. Brief Funct Genomics. 2011;10:151-64.
68. Bauman J, Jearawiriyapaisarn N, Kole R. Therapeutic potential of splice-switching oligonucleotides. Oligonucleotides. 2009;19:1-13.
69. Mourich DV, Oda SK, Schnell FJ, Crumley SL, Hauck LL, Moentenich CA, et al. Alternative splice forms of CTLA-4 induced by antisense mediated splice-switching influences autoimmune diabetes susceptibility in NOD mice. Nucleic Acid Ther. 2014;24:114-26.
70. van Deutekom JC, Janson AA, Ginjaar IB, Frankhuizen WS, Aartsma-Rus A, Bremmer-Bout M, et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med. 2007;357:2677-86.
71. Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, Adkin C, et al. Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of- concept study. Lancet Neurol. 2009;8:918-28.
72. Luo YB, Mastaglia FL, Wilton SD. Normal and aberrant splicing of LMNA. J Med Genet. 2014;51:215-23.
73. Wan J, Bauman JA, Graziewicz MA, Sazani P, Kole R. Oligonucleotide therapeutics in cancer. Cancer Treat Res. 2013;158: 213-33.
74. Yilmaz-Elis S, Aartsma-Rus A, Vroon A, van Deutekom J, de Kimpe S, t Hoen PA, et al. Antisense oligonucleotide mediated exon skipping as a potential strategy for the treatment of a variety of inflammatory diseases such as rheumatoid arthritis. Ann Rheum Dis. 2012;71(Suppl 2):i75-7.
75. Hua Y, Krainer AR. Antisense-mediated exon inclusion. Methods Mol Biol. 2012;867:307-23.