Dysregulation of lipid and amino acid metabolism precedes islet autoimmunity in children who later progress to type 1 diabetes

Journal of Experimental Medicine

Volumn 205, Issue 13, 2008, Pages 2975-2984

  Orešič, Matej ^a   Simell, Satu ^b   Sysi Aho, Marko ^a   Näntö Salonen, Kirsti ^b   Seppänen Laakso, Tuulikki ^a   Parikka, Vilhelmiina ^b   Katajamaa, Mikko ^a   Hekkala, Anne ^c   Mattila, Ismo ^a   Keskinen, Päivi ^d   Yetukuri, Laxman ^a   Reinikainen, Arja ^e   Lähde, Jyrki ^d   Suortti, Tapani ^a   Hakalax, Jari ^b   Simell, Tuula ^b   Hyöty, Heikki ^d,f   Veijola, Riitta ^c   Ilonen, Jorma ^b,g   Lahesmaa, Riitta ^e   Knip, Mikael ^d,h   Simell, Olli ^b   more..

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF OULU   (Finland)

^d TAMPERE UNIVERSITY HOSPITAL   (Finland)

^e TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^f TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^g UNIVERSITY OF EASTERN FINLAND   (Finland)

^h UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOISOCAPROIC ACID; AMINO ACID; ANTIOXIDANT; AUTOANTIBODY; ETHER PHOSPHOLIPID; GLUTAMATE DECARBOXYLASE; INSULIN; LIPID; PHOSPHATIDYLCHOLINE; SUCCINIC ACID; TRIACYLGLYCEROL;

AMINO ACID BLOOD LEVEL; AMINO ACID METABOLISM; ARTICLE; AUTOIMMUNITY; CHILD; CONTROLLED STUDY; FEMALE; FOLLOW UP; GENETIC RISK; HLA SYSTEM; HUMAN; IMMUNOPATHOGENESIS; INSULIN DEPENDENT DIABETES MELLITUS; LIPID METABOLISM; MAJOR CLINICAL STUDY; MALE; METABOLIC DISORDER; METABOLOME; PRIORITY JOURNAL; PROSPECTIVE STUDY; SEROCONVERSION; ADOLESCENT; BLOOD; DISEASE COURSE; FINLAND; IMMUNOLOGY; INFANT; METABOLISM; METABOLOMICS; PANCREAS ISLET; PATHOPHYSIOLOGY; PRESCHOOL CHILD;

ADOLESCENT; AMINO ACIDS; AUTOANTIBODIES; AUTOIMMUNITY; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; FEMALE; FINLAND; HUMANS; INFANT; ISLETS OF LANGERHANS; LIPID METABOLISM; MALE; METABOLIC DISEASES; METABOLOMICS;

EID: 59649105735     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20081800     Document Type: Article

References (43)

1. Gale, E.A.M. 2002. The rise of childhood type 1 diabetes in the 20th century. Diabetes. 51:3353-3361.
2. Knip, M., R. Veijola, S.M. Virtanen, H. Hyöty, O. Vaarala, and H.K. Åkerblom. 2005. Environmental triggers and determinants of type 1 diabetes. Diabetes. 54:S125-S136.
3. Tuomilehto, J., M. Karvonen, J. Pitkäniemi, E. Virtala, K. Kohtamäki, L. Toivanen, and E. Tuomilehto-Wolf. 1999. Record-high incidence of type 1 (insulin-dependent) diabetes mellitus in Finnish children. Diabetologia. 42:655-660.
4. Harjutsalo, V., L. Sjo ̈berg, and J. Tuomilehto. 2008. Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet. 371:1777-1782.
5. Achenbach, P., E. Bonifacio, K. Koczwara, and A.-G. Ziegler. 2005. Natural history of type 1 diabetes. Diabetes. 54:S25-S31.
6. Kupila, A., P. Muona, T. Simell, P. Arvilommi, H. Savolainen, A.-M. Hämäläinen, S. Korhonen, T. Kimpimäki, M. Sjåroos, J. Ilonen, et al. 2001. Feasibility of genetic and immunological prediction of type 1 diabetes in a population-based birth cohort. Diabetologia. 44:290-297.
7. Orešič, M., A. Vidal-Puig, and V. Hänninen. 2006. Metabolomic approaches to phenotype characterization and applications to complex diseases. Expert Rev. Mol. Diagn. 6:575-585.
8. Nikkilä, J., M. Sysi-Aho, A. Ermolov, T. Seppänen-Laakso, O. Simell, S. Kaski, and M. Orešič. 2008. Gender dependent progression of systemic metabolic states in early childhood. Mol. Syst. Biol. 4:197.
9. Lenz, E.M., J. Bright, I.D. Wilson, A. Hughes, J. Morrisson, H. Lindberg, and A. Lockton. 2004. Metabonomics, dietary influences and cultural differences: a 1H NMR-based study of urine samples obtained from healthy British and Swedish subjects. J. Pharm. Biomed. Anal. 36:841-849.
10. Bäckhed, F., H. Ding, T. Wang, L.V. Hooper, G.Y. Koh, A. Nagy, C.F. Semenkovich, and J.I. Gordon. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA. 101:15718-15723.
11. Gluckman, P.D., M.A. Hanson, C. Cooper, and K.L. Thornburg. 2008. Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359:61-73.
12. Simell, O., H. Niinikoski, T. Ronnemaa, H. Lapinleimu, T. Routi, H. Lagström, P. Salo, E. Jokinen, and J. Viikari. 2000. Special Turku Coronary Risk Factor Intervention Project for Babies (STRIP). Am. J. Clin. Nutr. 72:1316S-1331S.
13. Watson, A.D. 2006. Thematic review series: systems biology approaches to metabolic and cardiovascular disorders. Lipidomics: a global approach to lipid analysis in biological systems. J. Lipid Res. 47:2101-2111.
14. Orešič, M., V.A. Hänninen, and A. Vidal-Puig. 2008. Lipidomics: a new window to biomedical frontiers. Trends Biotechnol. 26:647-652.
15. Laaksonen, R., M. Katajamaa, H. Päivä, M. Sysi-Aho, L. Saarinen, P. Junni, D. Lütjohann, J. Smet, R.V. Coster, T. Seppänen-Laakso, 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.
16. Welthagen, W., R.A. Shellie, J. Spranger, M. Ristow, R. Zimmermann, and O. Fiehn. 2005. Comprehensive two-dimensional gas chroma- tography 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.
17. Niculescu, M.D., C.N. Craciunescu, and S.H. Zeisel. 2006. Dietary cho- line deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. FASEB J. 20:43-49.
18. Yao, Z.M., and D. Vance. 1988. The active synthesis of phosphatidyl- choline is required for very low density lipoprotein secretion from rat hepatocytes. J. Biol. Chem. 263:2998-3004.
19. Dumas, M.-E., R.H. Barton, A. Toye, O. Cloarec, C. Blancher, A. Rothwell, J. Fearnside, R. Tatoud, V. Blanc, J.C. Lindon, et al. 2006. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc. Natl. Acad. Sci. USA. 103:12511-12516.
20. Macy, J.M., L.G. Ljungdahl, and G. Gottschalk. 1978. Pathway of suc- cinate and propionate formation in Bacteroides fragilis. J. Bacteriol. 134:84-91.
21. Gill, S.R., M. Pop, R.T. DeBoy, P.B. Eckburg, P.J. Turnbaugh, B.S. Samuel, J.I. Gordon, D.A. Relman, C.M. Fraser-Liggett, and K.E. Nelson. 2006. Metagenomic analysis of the human distal gut microbi- ome. Science. 312:1355-1359.
22. Wen, L., R.E. Ley, P.Y. Volchkov, P.B. Stranges, L. Avanesyan, A.C. Stonebraker, C. Hu, F.S. Wong, G.L. Szot, J.A. Bluestone, et al. 2008. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 455:1109-1113.
23. Zoeller, R.A., T.J. Grazia, P. LaCamera, J . Park, D.P. Gaposchkin, and H.W. Farber. 2002. Increasing plasmalogen levels protects human endothelial cells during hypoxia. Am. J. Physiol. Heart Circ. Physiol. 283:H671-H679.
24. Lenzen, S., J. Drinkgern, and M. Tiedge. 1996. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic. Biol. Med. 20:463-466.
25. Mehta, D. 2005. Lysophosphatidylcholine: an enigmatic lysolipid. Am. J. Physiol. Lung Cell. Mol. Physiol. 289:L174-L175.
26. Kabarowski, J .H.S., Y. Xu, and O.N. Witte. 2002. Lysophospha- tidylcholine as a ligand for immunoregulation. Biochem. Pharmacol. 64:161-167.
27. Floyd, J.C.J., S.S. Fajans, R.F. Knopf, and J.W. Conn. 1963. Evidence that insulin release is the mechanism for experimentally induced leucine hypoglycemia in man. J. Clin. Invest. 42:1714-1719.
28. Marliss, E.B., A.F. Nakhooda, P. Poussier, and A.A. Sima. 1982. The diabetic syndrome of the ' BB' Wistar rat: possible relevance to type 1 (insulin-dependent) diabetes in man. Diabetologia. 22:225-232.
29. Nevo, U., I. Golding, A.U. Neumann, M. Schwartz, and S. Akselrod. 2004. Autoimmunity as an immune defense against degenerative processes: a primary mathematical model illustrating the bright side of auto- immunity. J. Theor. Biol. 227:583-592.
30. Hauben, E., M.G. Roncarolo, U. Nevo, and M. Schwartz. 2005. Beneficial autoimmunity in type 1 diabetes mellitus. Trends Immunol. 26:248-253.
31. Kimpimaki, T., P. Kulmala, K. Savola, A. Kupila, S. Korhonen, T. Simell, J . I lonen, O. Simell, and M. Knip. 2002. Natural history of (beta)-cell autoimmunity in young children with increased genetic susceptibility to type 1 diabetes recruited from the general population. J. Clin. Endocrinol. Metab. 87:4572-4579.
32. Näntö-Salonen, K., A. Kupila, S. Simell, H. Siljander, T. Salonsaari, A. Hekkala, S. Korhonen, R. Erkkola, J.I. Sipilä, L. Haavisto, et al. 2008. Nasal insulin to prevent type 1 diabetes in children with HLA genotypes and autoantibodies conferring increased risk of disease: a double-blind, randomised controlled trial. Lancet. 372:1746-1755.
33. Gaposchkin, D.P., and R.A. Zoeller. 1999. Plasmalogen status influences docosahexaenoic acid levels in a macrophage cell line: insights using ether lipid-deficient variants. J. Lipid Res. 40:495-503.
34. Stene, L.C., and G. J oner, and the Norwegian Childhood Diabetes Study Group. 2003. Use of cod liver oil during the first year of life is associated with lower risk of childhood-onset type 1 diabetes: a large, population-based, case-control study. Am. J. Clin. Nutr. 78:1128-134.
35. Norris, J.M., X. Yin, M.M. Lamb, K. Barriga, J. Seifert, M. Hoffman, H.D. Orton, A.E. Baron, M. Clare-Salzler, H.P. Chase, et al. 2007. Omega-3 polyunsaturated fatty acid intake and islet au-toimmunity in children at increased risk for type 1 diabetes. JAMA. 298:1420-1428.
36. Achenbach, P., K. Koczwara, A. Knopff, H. Naserke, A.-G. Ziegler, and E. Bonifacio. 2004. Mature high-affinity immune responses to (pro)insulin anticipate the autoimmune cascade that leads to type 1 diabetes. J. Clin. Invest. 114:589-597.
37. Baschal, E.E., T.A. Aly, S.R. Babu, M.S. Fernando, L. Yu, D. Miao, K.J. Barriga, J.M. Norris, J.A. Noble, H.A. Erlich, et al. 2007. HLA- DPB1*0402 protects against type 1A diabetic autoimmunity in the highest risk DR3-DQB1*0201/DR4-DQB1*302 DAISY population. Diabetes. 56:2405-2409.
38. Carmichael, S.K., S.B. Johnson, A. Baughcum, K. North, D. Hopkins, M.G. Dukes, J.X. She, and D.A. Schatz. 2003. Prospective assessment in newborns of diabetes autoimmunity (PANDA): maternal understanding of infant diabetes risk. Genet. Med. 5:77-83.
39. Hagopian, W.A., A. Lernmark, M.J. Rewers, O.G. Simell, J.-X. She, A.G. Ziegler, J.P. Krischer, and B. Akolkar. 2006. TEDDY - the environmental determinants of diabetes in the young: an observational clinical trial. Ann. N. Y. Acad. Sci. 1079:320-326.
40. . Kupila, A., P. Keskinen, T. Simell , S. Erkkilä, P. Arvilommi , S. Korhonen, T. Kimpimaki , M. Sjöroos , M. Ronkainen, J. Ilonen, et al , 2002, Genetic risk determines the emergence of diabetes-associated autoantibodies in young children. Diabetes. 51:646-651,
41. Katajamaa, M., and M. Orešič. 2005. Processing methods for differential analysis of LC/MS profile data. BMC Bioinformatics. 6:179-190.
42. Katajamaa, M., J. Miettinen, and M. Orešič. 2006. MZmine: toolbox for processing and visualization of mass spectrometry based molecular profile data. Bioinformatics. 22:634-636.
43. Storey, J.D. 2002. A direct approach to false discovery rates. Journal of the Royal Statistical Society Series B. 64:479-498.