Genome-wide identification of microRNAs regulating cholesterol and triglyceride homeostasis

Nature Medicine

Volumn 21, Issue 11, 2015, Pages 1290-1297

  Wagschal, Alexandre ^a,b   Najafi Shoushtari, S Hani ^a,b,h,k   Wang, Lifeng ^a,b   Goedeke, Leigh ^c   Sinha, Sumita ^a   Delemos, Andrew S ^a,h,l   Black, Josh C ^a   Ramírez, Cristina M ^c   Li, Yingxia ^d   Tewhey, Ryan ^e,f   Hatoum, Ida ^a   Shah, Naisha ^g   Lu, Yong ^g   Kristo, Fjoralba ^a   Psychogios, Nikolaos ^a   Vrbanac, Vladimir ^f   Lu, Yi Chien ^h   Hla, Timothy ^h   De Cabo, Rafael ⁱ   Tsang, John S ^g   Schadt, Eric ^j   Sabeti, Pardis C ^e,f   Kathiresan, Sekar ^a,e   Cohen, David E ^d   Whetstine, Johnathan ^a   Chung, Raymond T ^a   Fernández Hernando, Carlos ^c   Kaplan, Lee M ^a   Bernards, Andre ^a   Gerszten, Robert E ^a   Näär, Anders M ^a,b   more..

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f HARVARD UNIVERSITY   (United States)

^g NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^h WEILL CORNELL MEDICAL COLLEGE   (United States)

ⁱ NATIONAL INSTITUTE ON AGING   (United States)

^j MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^k QATAR FOUNDATION   (Qatar)

^l CAROLINAS MEDICAL CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; CHOLESTEROL; CHOLESTEROL ESTER TRANSFER PROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MICRORNA; MICRORNA 128; MICRORNA 130B; MICRORNA 148A; MICRORNA 301B; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ARTICLE; ATHEROSCLEROSIS; CARDIOMETABOLIC RISK; CHOLESTEROL BLOOD LEVEL; CHROMOSOME 11; CHROMOSOME 16; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC REGULATION; HOMEOSTASIS AND REGULATION; HUMAN; LIPID BLOOD LEVEL; LIPID DIET; LIPID HOMEOSTASIS; LIPID METABOLISM; META ANALYSIS; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; C57BL MOUSE; DYSLIPIDEMIA; GENETICS; HOMEOSTASIS; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; APOLIPOPROTEINS E; ATP BINDING CASSETTE TRANSPORTER 1; CHOLESTEROL; CHOLESTEROL, HDL; CHOLESTEROL, LDL; DIET, HIGH-FAT; DYSLIPIDEMIAS; GENOME-WIDE ASSOCIATION STUDY; HOMEOSTASIS; HUMANS; LIPOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, LDL; TRIGLYCERIDES;

EID: 84946218930     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3980     Document Type: Article

References (49)

1. Cornier, M. A. et al. The metabolic syndrome. Endocr. Rev. 29, 777-822 (2008).
2. Go, A. S. et al. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 127, e6-e245 (2013).
3. Quiat, D. & Olson, E. N. MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment. J. Clin. Invest. 123, 11-18 (2013).
4. Rottiers, V. & Naar, A. M. MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol. 13, 239-250 (2012).
5. Najafi-Shoushtari, S. H. et al. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328, 1566-1569 (2010).
6. Rayner, K. J. et al. Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J. Clin. Invest. 121, 2921-2931 (2011).
7. Marquart, T. J., Allen, R. M., Ory, D. S. & Baldan, A. miR-33 links SREBP-2 induction to repression of sterol transporters. Proc. Natl. Acad. Sci. USA 107, 12228-12232 (2010).
8. Horie, T. et al. MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo. Proc. Natl. Acad. Sci. USA 107, 17321-17326 (2010).
9. Rayner, K. J. et al. Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 478, 404-407 (2011).
10. Goedeke, L., Aranda, J. F. & Fernandez-Hernando, C. microRNA regulation of lipoprotein metabolism. Curr. Opin. Lipidol. 25, 282-288 (2014).
11. Willer, C. J. et al. Discovery and refinement of loci associated with lipid levels. Nat. Genet. 45, 1274-1283 (2013).
12. Merino, D. M., Ma, D. W. & Mutch, D. M. Genetic variation in lipid desaturases and its impact on the development of human disease. Lipids Health Dis. 9, 63 (2010).
13. Charles, M. A. & Kane, J. P. New molecular insights into CETP structure and function: a review. J. Lipid Res. 53, 1451-1458 (2012).
14. Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (2005).
15. Dennis, G. Jr. et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3 (2003).
16. Ishibashi, S. et al. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92, 883-893 (1993).
17. Brown, M. S. & Goldstein, J. L. How LDL receptors influence cholesterol and atherosclerosis. Sci. Am. 251, 58-66 (1984).
18. Tall, A. R., Yvan-Charvet, L., Terasaka, N., Pagler, T. & Wang, N. HDL, ABC transporters, and cholesterol efflux: implications for the treatment of atherosclerosis. Cell Metab. 7, 365-375 (2008).
19. Navab, M., Reddy, S. T., Van Lenten, B. J. & Fogelman, A. M. HDL and cardiovascular disease: atherogenic and atheroprotective mechanisms. Nat. Rev. Cardiol. 8, 222-232 (2011).
20. Duffy, D. & Rader, D. J. Update on strategies to increase HDL quantity and function. Nat. Rev. Cardiol. 6, 455-463 (2009).
21. Sparks, J. D., Sparks, C. E. & Adeli, K. Selective hepatic insulin resistance, VLDL overproduction, and hypertriglyceridemia. Arterioscler. Thromb. Vasc. Biol. 32, 2104-2112 (2012).
22. Stein, S. & Matter, C. M. Protective roles of SIRT1 in atherosclerosis. Cell Cycle 10, 640-647 (2011).
23. Yoon, Y. S., Seo, W. Y., Lee, M. W., Kim, S. T. & Koo, S. H. Salt-inducible kinase regulates hepatic lipogenesis by controlling SREBP-1c phosphorylation. J. Biol. Chem. 284, 10446-10452 (2009).
24. Hardie, D. G. Organismal carbohydrate and lipid homeostasis. Cold Spring Harb. Perspect. Biol. 4 (2012).
25. Bonnefont, J. P. et al. Carnitine palmitoyltransferases 1 and 2: biochemical, molecular and medical aspects. Mol. Aspects Med. 25, 495-520 (2004).
26. Goldstein, J. L., DeBose-Boyd, R. A. & Brown, M. S. Protein sensors for membrane sterols. Cell 124, 35-46 (2006).
27. Goldstein, J. L. & Brown, M. S. The LDL receptor. Arterioscler. Thromb. Vasc. Biol. 29, 431-438 (2009).
28. Soutar, A. K. & Naoumova, R. P. Mechanisms of disease: genetic causes of familial hypercholesterolemia. Nat. Clin. Pract. Cardiovasc. Med. 4, 214-225 (2007).
29. Lu, Y. C. et al. ELAVL1 modulates transcriptome-wide miRNA binding in murine macrophages. Cell Rep. 9, 2330-2343 (2014).
30. Zhang, S. H., Reddick, R. L., Piedrahita, J. A. & Maeda, N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258, 468-471 (1992).
31. Nakashima, Y., Plump, A. S., Raines, E. W., Breslow, J. L. & Ross, R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler. Thromb. 14, 133-140 (1994).
32. Teslovich, T. M. et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466, 707-713 (2010).
33. Hatoum, I. J. et al. Melanocortin-4 receptor signaling is required for weight loss after gastric bypass surgery. J. Clin. Endocrinol. Metab. 97, E1023-E1031 (2012).
34. Greenawalt, D. M. et al. A survey of the genetics of stomach, liver, and adipose gene expression from a morbidly obese cohort. Genome Res. 21, 1008-1016 (2011).
35. Hatoum, I. J. et al. Weight loss after gastric bypass is associated with a variant at 15q26. 1. Am. J. Hum. Genet. 92, 827-834 (2013).
36. Raymond, C. K., Roberts, B. S., Garrett-Engele, P., Lim, L. P. & Johnson, J. M. Simple, quantitative primer-extension PCR assay for direct monitoring of microRNAs and short-interfering RNAs. RNA 11, 1737-1744 (2005).
37. Bates, D. et al. Fitting linear mixed-effects models using lme4. arXiv, http://arxiv. org/abs/1406. 5823 (2014).
38. Liu, E. Y., Li, M., Wang, W. & Li, Y. MaCH-admix: genotype imputation for admixed populations. Genet. Epidemiol. 37, 25-37 (2013).
39. Price, A. L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904-909 (2006).
40. Shabalin, A. A. Matrix eQTL: ultra fast eQTL analysis via large matrix operations. Bioinformatics 28, 1353-1358 (2012).
41. Weischenfeldt, J. & Porse, B. Bone marrow-derived macrophages (BMM): isolation and applications. CSH Protoc 2008 doi:10. 1101/pdb. prot5080 (2010).
42. Hafner, M. et al. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 44, 3-12 (2008).
43. Hafner, M. et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129-141 (2010).
44. Corcoran, D. L. et al. PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data. Genome Biol. 12, R79 (2011).
45. Mattison, J. A. et al. Resveratrol prevents high fat/sucrose diet-induced central arterial wall inflammation and stiffening in nonhuman primates. Cell Metab. 20, 183-190 (2014).
46. Rayner, K. J. et al. MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328, 1570-1573 (2010).
47. Lillie, R. D. & Fulmer, H. M. Histopathologic Technique and Practical Histochemistry. (McGraw-Hill, 1976).
48. Ljungberg, O. & Tibblin, S. Peroperative fat staining of frozen sections in primary hyperparathyroidism. Am. J. Pathol. 95, 633-641 (1979).
49. Galabova, G. et al. Peptide-based anti-PCSK9 vaccines-an approach for long-term LDLc management. PLoS ONE 9, e114469 (2014).