Blood microRNA profile associates with the levels of serum lipids and metabolites associated with glucose metabolism and insulin resistance and pinpoints pathways underlying metabolic syndrome. The cardiovascular risk in Young Finns Study.

Molecular and Cellular Endocrinology

Volumn 391, Issue 1-2, 2014, Pages 41-49

  Raitoharju, Emma ^a   Seppälä, Ilkka ^a   Oksala, Niku ^a,b   Lyytikäinen, Leo Pekka ^a   Raitakari, Olli ^c,d   Viikari, Jorma ^c   Ala Korpela, Mika ^e,f,g,h   Soininen, Pasi ^e,f   Kangas, Antti J ^e,f   Waldenberger, Melanie ⁱ   Klopp, Norman ^i,j   Illig, Thomas ^i,j   Leiviskä, Jaana ^k   Loo, Britt Marie ^k   Hutri Kähönen, Nina ^l   Kähönen, Mika ^b   Laaksonen, Reijo ^a   Lehtimäki, Terho ^a  

^a PIRKANMAA HOSPITAL DISTRICT   (Finland)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

^e UNIVERSITY OF OULU   (Finland)

^f UNIVERSITY OF EASTERN FINLAND   (Finland)

^g OULU UNIVERSITY HOSPITAL   (Finland)

^h UNIVERSITY OF BRISTOL   (United Kingdom)

ⁱ INSTITUTE OF EPIDEMIOLOGY   (Germany)

^j HANNOVER MEDICAL SCHOOL   (Germany)

^k NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^l TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

more..

Author keywords

Diabetes; Metabolic syndrome; MicroRNA; MRNA expression; NMR metabolomics

Indexed keywords

CHOLESTEROL; FATTY ACID; GLUCOSE; GLYCEROL; GLYCOSYLATED HEMOGLOBIN; MICRORNA; MICRORNA 1207 5P; MICRORNA 1237 3P; MICRORNA 1288 3P; MICRORNA 129 1 3P; MICRORNA 129 2 3P; MICRORNA 144 5P; MICRORNA 331 3P; MICRORNA 484; MICRORNA 625 3P; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; UNCLASSIFIED DRUG; GLUCOSE BLOOD LEVEL; INSULIN;

ADULT; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE EXPRESSION; GLUCOSE METABOLISM; HUMAN; LIPID BLOOD LEVEL; LIPID METABOLISM; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; METABOLOMICS; MOLECULAR PATHOLOGY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; SEX DIFFERENCE; SIGNAL TRANSDUCTION; BLOOD; CARDIOVASCULAR DISEASES; CLINICAL TRIAL; COMPLICATION; FINLAND; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETICS; GLUCOSE BLOOD LEVEL; INSULIN RESISTANCE; METABOLISM; MIDDLE AGED; MULTICENTER STUDY; PROSPECTIVE STUDY; RISK;

ADULT; BLOOD GLUCOSE; CARDIOVASCULAR DISEASES; CHOLESTEROL; FATTY ACIDS, NONESTERIFIED; FEMALE; FINLAND; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; GLYCEROL; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; INSULIN; INSULIN RESISTANCE; MALE; METABOLIC SYNDROME X; MICRORNAS; MIDDLE AGED; PROSPECTIVE STUDIES; RISK; SIGNAL TRANSDUCTION;

EID: 84899817221     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.04.013     Document Type: Article

References (50)

1. Adiels M., Olofsson S.O., Taskinen M.R., Boren J. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1225-1236.
2. Alberti K.G., Zimmet P., Shaw J., IDF Epidemiology Task Force Consensus Group The metabolic syndrome - a new worldwide definition. Lancet 2005, 366:1059-1062.
3. Andersson D.P., Lofgren P., Thorell A., Arner P., Hoffstedt J. Visceral fat cell lipolysis and cardiovascular risk factors in obesity. Horm. Metab. Res. 2011, 43:809-815.
4. Arroyo J.D., Chevillet J.R., Kroh E.M., Ruf I.K., Pritchard C.C., Gibson D.F., Mitchell P.S., Bennett C.F., Pogosova-Agadjanyan E.L., Stirewalt D.L., Tait J.F., Tewari M. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA 2011, 108:5003-5008.
5. Cho S., Jang I., Jun Y., Yoon S., Ko M., Kwon Y., Choi I., Chang H., Ryu D., Lee B., Kim V.N., Kim W., Lee S. MiRGator v3.0: a microRNA portal for deep sequencing, expression profiling and mRNA targeting. Nucleic Acids Res. 2013, 41. D252-7.
6. Civelek M., Hagopian R., Pan C., Che N., Yang W.P., Kayne P.S., Saleem N.K., Cederberg H., Kuusisto J., Gargalovic P.S., Kirchgessner T.G., Laakso M., Lusis A.J. Genetic regulation of human adipose microRNA expression and its consequences for metabolic traits. Hum. Mol. Genet. 2013, 22:3023-3037.
7. Dolmans G.H., Werker P.M., Hennies H.C., Furniss D., Festen E.A., Franke L., Becker K., van der Vlies P., Wolffenbuttel B.H., Tinschert S., Toliat M.R., Nothnagel M., Franke A., Klopp N., Wichmann H.E., Nurnberg P., Giele H., Ophoff R.A., Wijmenga C., Dutch Dupuytren Study Group, German Dupuytren Study Group, LifeLines Cohort Study, BSSH-GODD Consortium Wnt signaling and Dupuytren's disease. N. Engl. J. Med. 2011, 365:307-317.
8. Eckel R.H., Alberti K.G., Grundy S.M., Zimmet P.Z. The metabolic syndrome. Lancet 2010, 375:181-183.
9. Erol A. Systemic DNA damage response and metabolic syndrome as a premalignant state. Curr. Mol. Med. 2010, 10:321-334.
10. Guay C., Regazzi R. Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat. Rev. Endocrinol. 2013, 9:513-521.
11. Huang da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
12. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
13. Inouye M., Kettunen J., Soininen P., Silander K., Ripatti S., Kumpula L.S., Hämäläinen E., Jousilahti P., Kangas A.J., Männisto S., Savolainen M.J., Jula A., Leiviskä J., Palotie A., Salomaa V., Perola M., Ala-Korpela M., Peltonen L. Metabonomic, transcriptomic, and genomic variation of a population cohort. Mol. Syst. Biol. 2010, 6:441.
14. Jansson P.A., Larsson A., Smith U., Lonnroth P. Glycerol production in subcutaneous adipose tissue in lean and obese humans. J. Clin. Invest. 1992, 89:1610-1617.
15. Karolina D.S., Armugam A., Tavintharan S., Wong M.T., Lim S.C., Sum C.F., Jeyaseelan K. MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus. PLoS ONE 2011, 6:e22839.
16. Karolina D.S., Tavintharan S., Armugam A., Sepramaniam S., Pek S.L., Wong M.T., Lim S.C., Sum C.F., Jeyaseelan K. Circulating miRNA profiles in patients with metabolic syndrome. J. Clin. Endocrinol. Metab. 2012, 97. E2271-6.
17. Kettunen J., Tukiainen T., Sarin A.P., Ortega-Alonso A., Tikkanen E., Lyytikäinen L.P., Kangas A.J., Soininen P., Würtz P., Silander K., Dick D.M., Rose R.J., Savolainen M.J., Viikari J., Kähönen M., Lehtimäki T., Pietiläinen K.H., Inouye M., McCarthy M.I., Jula A., Eriksson J., Raitakari O.T., Salomaa V., Kaprio J., Järvelin M.R., Peltonen L., Perola M., Freimer N.B., Ala-Korpela M., Palotie A., Ripatti S. Genome-wide association study identifies multiple loci influencing human serum metabolite levels. Nat. Genet. 2012, 44:269-276.
18. Koch L. Paediatrics: circulating microRNAs-predictors of obesity?. Nat. Rev. Endocrinol. 2013, 9:565.
19. Kosaka N., Iguchi H., Yoshioka Y., Takeshita F., Matsuki Y., Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J. Biol. Chem. 2010, 285:17442-17452.
20. Kristiansson K., Perola M., Tikkanen E., Kettunen J., Surakka I., Havulinna A.S., Stancakova A., Barnes C., Widen E., Kajantie E., Eriksson J.G., Viikari J., Kähönen M., Lehtimäki T., Raitakari O.T., Hartikainen A.L., Ruokonen A., Pouta A., Jula A., Kangas A.J., Soininen P., Ala-Korpela M., Männisto S., Jousilahti P., Bonnycastle L.L., Järvelin M.R., Kuusisto J., Collins F.S., Laakso M., Hurles M.E., Palotie A., Peltonen L., Ripatti S., Salomaa V. Genome-wide screen for metabolic syndrome susceptibility Loci reveals strong lipid gene contribution but no evidence for common genetic basis for clustering of metabolic syndrome traits. Circ. Cardiovasc. Genet. 2012, 5:242-249.
21. Kujala U.M., Mäkinen V.P., Heinonen I., Soininen P., Kangas A.J., Leskinen T.H., Rahkila P., Würtz P., Kovanen V., Cheng S., Sipila S., Hirvensalo M., Telama R., Tammelin T., Savolainen M.J., Pouta A., O'Reilly P.F., Mäntyselkä P., Viikari J., Kähönen M., Lehtimäki T., Elliott P., Vanhala M.J., Raitakari O.T., Järvelin M.R., Kaprio J., Kainulainen H., Ala-Korpela M. Long-term leisure-time physical activity and serum metabolome. Circulation 2013, 127:340-348.
22. Latronico M.V., Catalucci D., Condorelli G. MicroRNA and cardiac pathologies. Physiol. Genomics 2008, 34:239-242.
23. Liang T., Liu C., Ye Z. Deep sequencing of small RNA repertoires in mice reveals metabolic disorders-associated hepatic miRNAs. PLoS ONE 2013, 8:e80774.
24. Lu J., Xie G., Jia W., Jia W. Insulin resistance and the metabolism of branched-chain amino acids. Front. Med. 2013, 7:53-59.
25. Lujambio A., Lowe S.W. The microcosmos of cancer. Nature 2012, 482:347-355.
26. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstrale M., Laurila E., Houstis N., Daly M.J., Patterson N., Mesirov J.P., Golub T.R., Tamayo P., Spiegelman B., Lander E.S., Hirschhorn J.N., Altshuler D., Groop L.C. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003, 34:267-273.
27. Mosakhani N., Guled M., Lahti L., Borze I., Forsman M., Pääkkonen V., Ryhänen J., Knuutila S. Unique microRNA profile in Dupuytren's contracture supports deregulation of beta-catenin pathway. Mod. Pathol. 2010, 23:1544-1552.
28. Moustakas A., Pardali K., Gaal A., Heldin C.H. Mechanisms of TGF-beta signaling in regulation of cell growth and differentiation. Immunol. Lett. 2002, 82:85-91.
29. Nigro J., Osman N., Dart A.M., Little P.J. Insulin resistance and atherosclerosis. Endocr. Rev. 2006, 27:242-259.
30. Pasini E., Flati V., Paiardi S., Rizzoni D., Porteri E., Aquilani R., Assanelli D., Corsetti G., Speca S., Rezzani R., De Ciuceis C., Agabiti-Rosei E. Intracellular molecular effects of insulin resistance in patients with metabolic syndrome. Cardiovasc. Diabetol. 2010, 9. 46-2840-9-46.
31. Pescador N., Perez-Barba M., Ibarra J.M., Corbaton A., Martinez-Larrad M.T., Serrano-Rios M. Serum circulating microRNA profiling for identification of potential type 2 diabetes and obesity biomarkers. PLoS ONE 2013, 8:e77251.
32. Raitakari O.T., Juonala M., Rönnemaa T., Keltikangas-Järvinen L., Räsänen L., Pietikäinen M., Hutri-Kähönen N., Taittonen L., Jokinen E., Marniemi J., Jula A., Telama R., Kähönen M., Lehtimäki T., Akerblom H.K., Viikari J.S. Cohort profile: the cardiovascular risk in Young Finns Study. Int. J. Epidemiol. 2008, 37:1220-1226.
33. Raitoharju E., Oksala N., Lehtimäki T. MicroRNAs in the Atheroclerotic Plaque. Clin. Chem. 2013.
34. Rayner K.J., Esau C.C., Hussain F.N., McDaniel A.L., Marshall S.M., van Gils J.M., Ray T.D., Sheedy F.J., Goedeke L., Liu X., Khatsenko O.G., Kaimal V., Lees C.J., Fernandez-Hernando C., Fisher E.A., Temel R.E., Moore K.J. Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 2011, 478:404-407.
35. Rottiers V., Naar A.M. MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol. 2012, 13:239-250.
36. Silvestri P., Di Russo C., Rigattieri S., Fedele S., Todaro D., Ferraiuolo G., Altamura G., Loschiavo P. MicroRNAs and ischemic heart disease: towards a better comprehension of pathogenesis, new diagnostic tools and new therapeutic targets. Recent Pat. Cardiovasc. Drug Discovery 2009, 4:109-118.
37. Soininen P., Kangas A.J., Würtz P., Tukiainen T., Tynkkynen T., Laatikainen R., Järvelin M.R., Kähönen M., Lehtimäki T., Viikari J., Raitakari O.T., Savolainen M.J., Ala-Korpela M. High-throughput serum NMR metabonomics for cost-effective holistic studies on systemic metabolism. Analyst 2009, 134:1781-1785.
38. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
39. Tang X., Muniappan L., Tang G., Ozcan S. Identification of glucose-regulated miRNAs from pancreatic beta cells reveals a role for miR-30d in insulin transcription. RNA 2009, 15:287-293.
40. Tangen S.E., Tsinajinnie D., Nunez M., Shaibi G.Q., Mandarino L.J., Coletta D.K. Whole blood gene expression profiles in insulin resistant Latinos with the metabolic syndrome. PLoS ONE 2013, 8:e84002.
41. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
42. Vickers K.C., Remaley A.T. MicroRNAs in atherosclerosis and lipoprotein metabolism. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17:150-155.
43. Vickers K.C., Palmisano B.T., Shoucri B.M., Shamburek R.D., Remaley A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 2011, 13:423-433.
44. Wang K., Zhang S., Weber J., Baxter D., Galas D.J. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 2010, 38:7248-7259.
45. Wang K., Long B., Jiao J.Q., Wang J.X., Liu J.P., Li Q., Li P.F. MiR-484 regulates mitochondrial network through targeting Fis1. Nat. Commun. 2012, 3:781.
46. Wang Y.T., Tsai P.C., Liao Y.C., Hsu C.Y., Juo S.H. Circulating microRNAs have a sex-specific association with metabolic syndrome. J. Biomed. Sci. 2013, 20. 72-0127-20-72.
47. Würtz P., Mäkinen V.P., Soininen P., Kangas A.J., Tukiainen T., Kettunen J., Savolainen M.J., Tammelin T., Viikari J.S., Rönnemaa T., Kähönen M., Lehtimäki T., Ripatti S., Raitakari O.T., Järvelin M.R., Ala-Korpela M. Metabolic signatures of insulin resistance in 7,098 young adults. Diabetes 2012, 61:1372-1380.
48. Würtz P., Tiainen M., Mäkinen V.P., Kangas A.J., Soininen P., Saltevo J., Keinänen-Kiukaanniemi S., Mäntyselkä P., Lehtimäki T., Laakso M., Jula A., Kahonen M., Vanhala M., Ala-Korpela M. Circulating metabolite predictors of glycemia in middle-aged men and women. Diabetes Care 2012, 35:1749-1756.
49. Ye Q., Zhao X., Xu K., Li Q., Cheng J., Gao Y., Du J., Shi H., Zhou L. Polymorphisms in lipid metabolism related miRNA binding sites and risk of metabolic syndrome. Gene 2013, 528:132-138.
50. Yoon Y., Galloway C.A., Jhun B.S., Yu T. Mitochondrial dynamics in diabetes. Antioxid. Redox Signal. 2011, 14:439-457.