Metabolic regulation in progression to autoimmune diabetes

PLoS Computational Biology

Volumn 7, Issue 10, 2011, Pages

  Sysi Aho, Marko ^a   Ermolov, Andrey ^b   Gopalacharyulu, Peddinti V ^a   Tripathi, Abhishek ^c,j   Seppänen Laakso, Tuulikki ^a   Maukonen, Johanna ^a   Mattila, Ismo ^a   Ruohonen, Suvi T ^d   Vähätalo, Laura ^d   Yetukuri, Laxman ^a   Härkönen, Taina ^c   Lindfors, Erno ^a   Nikkilä, Janne ^e   Ilonen, Jorma ^d,f   Simell, Olli ^d   Saarela, Maria ^a   Knip, Mikael ^c,g,h   Kaski, Samuel ^b,c   Savontaus, Eriika ^d,i   Orešič, Matej ^a,c  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b AALTO UNIVERSITY   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

^e FINNISH RED CROSS BLOOD SERVICE   (Finland)

^f UNIVERSITY OF EASTERN FINLAND   (Finland)

^g TAMPERE UNIVERSITY HOSPITAL   (Finland)

^h FOLKHÄLSAN RESEARCH CENTER   (Finland)

ⁱ TURKU UNIVERSITY HOSPITAL   (Finland)

^j XEROX RESEARCH CENTRE EUROPE   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; MAMMALS; PHYSIOLOGY;

AUTOIMMUNE DIABETES; GLUCOSE-STIMULATED INSULIN SECRETIONS; HUMAN STUDY; LIPIDOMICS; METABOLIC CHANGES; METABOLIC REGULATIONS; METABOLIC STATE; METABOLOMICS; MURINE MODEL; TYPE 1 DIABETES;

METABOLISM;

ADIPONECTIN; GLUCOSE; INSULIN; LEPTIN; LYSOPHOSPHATIDYLCHOLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CLOSTRIDIUM; CLOSTRIDIUM LEPTUM; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE MARKER; DOWN REGULATION; FEMALE; GLUCOSE BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INSULIN RESISTANCE; LIPID ANALYSIS; LIPIDOMICS; MALE; METABOLIC REGULATION; METABOLOMICS; MICROBIAL DIVERSITY; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PROTEIN BLOOD LEVEL; PROTEIN LOCALIZATION; RISK FACTOR; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CLUSTER ANALYSIS; DISEASE COURSE; HUMAN; LIVER; METABOLISM; METABOLOME; NONOBESE DIABETIC MOUSE; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

CLOSTRIDIUM LEPTUM; MURINAE; MUS;

ADIPONECTIN; ANIMALS; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; FEMALE; HUMANS; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; LEPTIN; LIVER; LYSOPHOSPHATIDYLCHOLINES; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MICE; MICE, INBRED NOD; MODELS, BIOLOGICAL; RISK FACTORS;

EID: 80055090409     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002257     Document Type: Article

References (75)

1. Achenbach P, Bonifacio E, Koczwara K, Ziegler A-G, (2005) Natural history of type 1 diabetes. Diabetes 54: S25-31.
2. Oresic M, Simell S, Sysi-Aho M, Näntö-Salonen K, Seppänen-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.
3. Gale EAM, (2002) The rise of childhood type 1 diabetes in the 20th century. Diabetes 51: 3353-3361.
4. Harjutsalo V, Sjöberg L, Tuomilehto J, (2008) Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet 371: 1777-1782.
5. Patterson CC, Dahlquist GG, Gyürüs E, Green A, Soltész G, (2009) Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet 373: 2027-2033.
6. Oresic M, Vidal-Puig A, Hänninen V, (2006) Metabolomic approaches to phenotype characterization and applications to complex diseases. Expert Rev Mol Diagn 6: 575-585.
7. Hagopian WA, Lernmark A, Rewers MJ, Simell OG, She J-X, et al. (2006) TEDDY- the environmental determinants of diabetes in the young: an observational clinical trial. Ann NY Acad Sci 1079: 320-326.
8. Kupila A, Muona P, Simell T, Arvilommi P, Savolainen H, et al. (2001) Feasibility of genetic and immunological prediction of type 1 diabetes in a population-based birth cohort. Diabetologia 44: 290-297.
9. Anderson MS, Bluestone JA, (2005) The NOD mouse: a model of immune dysregulation. Annu Rev Immunol 23: 447-485.
10. Atkinson MA, Leiter EH, (1999) The NOD mouse model of type 1 diabetes: as good as it gets? Nature 5: 601-604.
11. Chervonsky AV, (2010) Influence of microbial environment on autoimmunity. Nat Immunol 11: 28-35.
12. Singh B, Rabinovitch A, (1993) Influence of microbial agents on the development and prevention of autoimmune diabetes. Autoimmunity 15: 209-213.
13. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, et al. (2008) Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455: 1109-1113.
14. Nygren H, Seppanen-Laakso T, Castillo S, Hyotylainen T, Oresic M, (2011) Liquid Chromatography-Mass Spectrometry (LC-MS)-Based Lipidomics for Studies of Body Fluids and Tissues. Methods Mol Biol 708: 247-257.
15. Storey JD, (2002) A direct approach to false discovery rates. J R Stat Soc B 64: 479-498.
16. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445.
17. Floyd JCJ, Fajans SS, Knopf RF, Conn JW, (1963) Evidence that insulin release is the mechanism for experimentally induced leucine hypoglycemia in man. J Clin Invest 42: 1714-1719.
18. Nikkilä J, Sysi-Aho M, Ermolov A, Seppänen-Laakso T, Simell O, et al. (2008) Gender dependent progression of systemic metabolic states in early childhood. Mol Syst Biol 4: e197.
19. Tripathi A, Klami A, Oresic M, Kaski S, (2010) Matching samples of multiple views. Data Min Knowl Discov doi:10.1007/s10618-10010-10205-10617.
20. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Nat Acad Sci U S A 102: 15545-15550.
21. Keymeulen B, Vandemeulebroucke E, Ziegler AG, Mathieu C, Kaufman L, et al. (2005) Insulin needs after CD3-Antibody therapy in new-onset type 1 diabetes. N Engl J Med 352: 2598-2608.
22. Eizirik DL, Moore F, Flamez D, Ortis F, (2008) Use of systems biology approach to understand pancreatic {beta}-cell death in type 1 diabetes. Biochem Soc Trans 36: 321-327.
23. Zhernakova A, Alizadeh BZ, Eerligh P, Hanifi-Moghaddam P, Schloot NC, et al. (2006) Genetic variants of RANTES are associated with serum RANTES level and protection for type 1 diabetes. Genes Immun 7: 544-549.
24. Ortis F, Naamane N, Flamez D, Ladriere L, Moore F, et al. (2010) Cytokines interleukin-1b and tumor necrosis factor-a regulate different transcriptional and alternative splicing networks in primary b-cells. Diabetes 59: 358-374.
25. Calzascia T, Pellegrini M, Lin A, Garza KM, Elford AR, et al. (2008) CD4 T cells, lymphopenia, and IL-7 in a multistep pathway to autoimmunity. Proc Natl Acad Sci USA 105: 2999-3004.
26. Welthagen W, Shellie RA, Spranger J, Ristow M, Zimmermann R, et al. (2005) Comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry (GC-GC-TOF) for high resolution metabolomics: biomarker discovery on spleen tissue extracts of obese NZO compared to lean C57BL/6 mice. Metabolomics 1: 65-73.
27. Newsholme P, Brennan L, Bender K, (2006) Amino acid metabolism, {beta}-cell function, and diabetes. Diabetes 55: S39-47.
28. Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu PV, Yetukuri L, et al. (2010) The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 51: 1101-1112.
29. Maukonen J, Mättö J, Satokari R, Söderlund H, Mattila-Sandholm T, et al. (2006) PCR DGGE and RT-PCR DGGE show diversity and short-term temporal stability in the Clostridium coccoides-Eubacterium rectale group in the human intestinal microbiota. FEMS Microbiol Ecol 58: 517-528.
30. Maukonen J, Matto J, Suihko M-L, Saarela M, (2008) Intra-individual diversity and similarity of salivary and faecal microbiota. J Med Microbiol 57: 1560-1568.
31. Satokari RM, Vaughan EE, Akkermans AD, Saarela M, de Vos WM, (2001) Bifidobacterial diversity in human feces detected by genus-specific PCR and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67: 504-513.
32. Fourlanos S, Narendran P, Byrnes GB, Colman PG, Harrison LC, (2004) Insulin resistance is a risk factor for progression to Type 1 diabetes. Diabetologia 47: 1661-1667.
33. Xu P, Cuthbertson D, Greenbaum C, Palmer JP, Krischer JP, (2007) Role of insulin resistance in predicting progression to type 1 diabetes. Diabetes Care 30: 2314-2320.
34. Chaparro RJ, Konigshofer Y, Beilhack GF, Shizuru JA, McDevitt HO, et al. (2006) Nonobese diabetic mice express aspects of both type 1 and type 2 diabetes. Proc Natl Acad Sci USA 103: 12475-12480.
35. Rapoport M, Jaramillo A, Zipris D, Lazarus A, Serreze D, et al. (1993) Interleukin 4 reverses T cell proliferative unresponsiveness and prevents the onset of diabetes in nonobese diabetic mice. J Exp Med 178: 87-99.
36. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B, (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12: 913-922.
37. Ostman J, Lönnberg G, Arnqvist HJ, Blohme G, Bolinder J, et al. (2008) Gender differences and temporal variation in the incidence of type 1 diabetes: results of 8012 cases in the nationwide Diabetes Incidence Study in Sweden 1983-2002. J Intern Med 263: 386-394.
38. Powell JD, Delgoffe GM, (2010) The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity 33: 301-311.
39. Fox CJ, Hammerman PS, Thompson CB, (2005) Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol 5: 844-852.
40. Seufert J, Kieffer TJ, Leech CA, Holz GG, Moritz W, et al. (1999) Leptin suppression of insulin secretion and gene expression in human pancreatic islets: implications for the development of adipogenic diabetes mellitus. J Clin Endocrinol Metab 84: 670-676.
41. Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, et al. (2006) Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest 116: 1784-1792.
42. Truyen I, De Grijse J, Van Schravendijk C, De Smet D, Decochez K, et al. (2007) Adiponectin levels do not predict clinical onset of type 1 diabetes in antibody-positive relatives. Diabetologia 50: 2143-2146.
43. Matarese G, Leiter EH, Cava AL, (2007) Leptin in autoimmunity: many questions, some answers. Tissue Antigens 70: 87-95.
44. De Rosa V, Procaccini C, Calì G, Pirozzi G, Fontana S, et al. (2007) A key role of leptin in the control of regulatory T cell proliferation. Immunity 26: 241-255.
45. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, et al. (1998) Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394: 897-901.
46. Ozata M, Ozdemir IC, Licinio J, (1999) Human leptin deficiency caused by a missense mutation: multiple endocrine defects, decreased sympathetic tone, and immune system dysfunction indicate new targets for leptin action, greater central than peripheral resistance to the effects of leptin, and spontaneous correction of leptin-mediated defects. J Clin Endocrinol Metab 84: 3686-3695.
47. Matarese G, Sanna V, Lechler RI, Sarvetnick N, Fontana S, et al. (2002) Leptin accelerates autoimmune diabetes in female NOD mice. Diabetes 51: 1356-1361.
48. Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S, et al. (2009) Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab 9: 35-51.
49. Eizirik DL, Colli ML, Ortis F, (2009) The role of inflammation in insulitis and {beta}-cell loss in type 1 diabetes. Nat Rev Endocrinol 5: 219-226.
50. Hypponen E, Virtanen S, Kenward M, Knip M, Akerblom H, (2000) Obesity, increased linear growth, and risk of type 1 diabetes in children. Diabetes Care 23: 1755-1760.
51. Mrena S, Virtanen SM, Laippala P, Kulmala P, Hannila ML, et al. (2006) Models for predicting type 1 diabetes in siblings of affected children. Diabetes Care 29: 662-667.
52. Kimm SYS, Obarzanek E, (2002) Childhood obesity: a new pandemic of the new millennium. Pediatrics 110: 1003-1007.
53. 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.
54. Allison SD, Martiny JBH, (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105: 11512-11519.
55. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, et al. (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105: 16731-16736.
56. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, et al. (2010) Induction of colonic regulatory T cells by indigenous Clostridium species. Science doi:10.1126/science.1198469.
57. Sakaguchi S, Sakaguchi N, Shimizu J, Yamazaki S, Sakihama T, et al. (2001) Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 182: 18-32.
58. Freiesleben De Blasio B, Bak P, Pociot F, Karlsen A, Nerup J, (1999) Onset of type 1 diabetes: a dynamical instability. Diabetes 48: 1677-1685.
59. Nevo U, Golding I, Neumann AU, Schwartz M, Akselrod S, (2004) Autoimmunity as an immune defense against degenerative processes: a primary mathematical model illustrating the bright side of autoimmunity. J Theor Biol 227: 583-592.
60. Szot GL, Koudria P, Bluestone JA, (2007) Murine pancreatic islet isolation. J Vis Exp pp. 255.
61. Ronkainen MS, Hämäläinen A-M, Koskela P, Åkerblom HK, Knip M, (2001) Pregnancy induces nonimmunoglobulin insulin-binding activity in both maternal and cord blood serum. Clin Exp Immunol 124: 190-196.
62. Katajamaa M, Miettinen J, Oresic M, (2006) MZmine: toolbox for processing and visualization of mass spectrometry based molecular profile data. Bioinformatics 22: 634-636.
63. Katajamaa M, Oresic M, (2005) Processing methods for differential analysis of LC/MS profile data. BMC Bioinformatics 6: 179.
64. Yetukuri L, Katajamaa M, Medina-Gomez G, Seppanen-Laakso T, Vidal-Puig A, et al. (2007) Bioinformatics strategies for lipidomics analysis: characterization of obesity related hepatic steatosis. BMC Syst Biol 1: e12.
65. Laaksonen R, Katajamaa M, Päivä H, Sysi-Aho M, Saarinen L, et al. (2006) A systems biology strategy reveals biological pathways and plasma biomarker candidates for potentially toxic statin induced changes in muscle. PLoS ONE 1: e97.
66. Castillo S, Mattila I, Miettinen J, Orešič M, Hyötyläinen T, (2011) Data analysis tool for comprehensive two-dimensional gas chromatography-time of flight mass spectrometry. Anal Chem 83: 3058-3067.
67. Dunning MJ, Smith ML, Ritchie ME, Tavare S, (2007) beadarray: R classes and methods for Illumina bead-based data. Bioinformatics 23: 2183-2184.
68. Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S, (2005) Bioinformatics and computational biology solutions using R and Bioconductor New York, NY Springer Science+Business Media, Inc.
69. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
70. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3 doi:10.2202/1544-6115.1027.
71. Ashburner M, Ball C, Blake J, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. Nat Genet 25: 25-29.
72. Salomonis N, Hanspers K, Zambon A, Vranizan K, Lawlor S, et al. (2007) GenMAPP 2: new features and resources for pathway analysis. BMC Bioinformatics 8: 217.
73. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, et al. (2008) KEGG for linking genomes to life and the environment. Nucl Acids Res 36: D480-484.
74. Jain AK, Murty MN, Flynn PJ, (1999) Data clustering: a review. ACM Computing Surveys 31: 264-323.
75. Sharma S, (1995) Applied multivariate techniques New York, NY John Wiley & Sons, Inc.