Circulating MicroRNAs: Novel biomarkers and extracellular communicators in cardiovascular disease?

Circulation Research

Volumn 110, Issue 3, 2012, Pages 483-495

  Creemers, Esther E ^a   Tijsen, Anke J ^a   Pinto, Yigal M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

biomarkers; cell derived microparticles; exosomes; paracrine communication; plasma microRNAs; review

Indexed keywords

APOLIPOPROTEIN A1; ARGONAUTE 2 PROTEIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CERAMIDE; CHEMOKINE RECEPTOR CXCR4; HIGH DENSITY LIPOPROTEIN; INTERLEUKIN 6; MICRORNA; MICRORNA 1; MICRORNA 133; MICRORNA 499; NUCLEOPHOSMIN; PHOSPHOLIPASE A2; RIBONUCLEASE; UNCLASSIFIED DRUG;

ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CELL COMMUNICATION; CELL SECRETION; CORONARY ARTERY DISEASE; DOWN REGULATION; ENDOTHELIUM CELL; ESSENTIAL HYPERTENSION; EXOSOME; EXTRACELLULAR SPACE; FIBROBLAST; GEL PERMEATION CHROMATOGRAPHY; HEART FAILURE; HEART INFARCTION; HUMAN; HYPERCHOLESTEROLEMIA; IMMUNOPRECIPITATION; LIPID VESICLE; MASS SPECTROMETRY; MEMBRANE MICROPARTICLE; MOLECULAR WEIGHT; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PLASMA; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PURIFICATION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; RNA INTERFERENCE; RNA SEQUENCE; RNA STABILITY; SEX DIFFERENCE; SMOOTH MUSCLE FIBER; WESTERN BLOTTING;

ANIMALS; BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; CELL COMMUNICATION; EXTRACELLULAR MATRIX; HUMANS; MICRORNAS; MODELS, ANIMAL;

EID: 84856695673     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.247452     Document Type: Review

References (70)

1. Ambros V. The functions of animal microRNAs. Nature. 2004;431: 350-355. (Pubitemid 39265675)
2. Van Rooij E, Marshall WS, Olson EN. Toward microRNA-based therapeutics for heart disease: the sense in antisense. Circ Res. 2008;103: 919-928.
3. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513-10518.
4. Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, Pulford K, Banham AH, Pezzella F, Boultwood J, Wainscoat JS, Hatton CS, Harris AL. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol. 2008;141:672-675. (Pubitemid 351667616)
5. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, Li Q, Li X, Wang W, Wang J, Jiang X, Xiang Y, Xu C, Zheng P, Zhang J, Li R, Zhang H, Shang X, Gong T, Ning G, Zen K, Zhang CY. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18:997-1006.
6. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Koppel T, Jahantigh MN, Lutgens E, Wang S, Olson EN, Schober A, Weber C. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal. 2009;2:ra81.
7. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9: 654-659. (Pubitemid 47214727)
8. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, 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.
9. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13:423-433.
10. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, Sun Q, Wang K, Ba Y, Wang Q, Wang D, Yang J, Liu P, Xu T, Yan Q, Zhang J, Zen K, Zhang CY. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133-144.
11. Wang GK, Zhu JQ, Zhang JT, Li Q, Li Y, He J, Qin YW, Jing Q. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J. 2010;31:659-666.
12. Tijsen AJ, Creemers EE, Moerland PD, de Windt LJ, van der Wal AC, Kok WE, Pinto YM. MiR423-5p as a circulating biomarker for heart failure. Circ Res. 2010;106:1035-1039.
13. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, Weber M, Hamm CW, Roxe T, Muller-Ardogan M, Bonauer A, Zeiher AM, Dimmeler S. Circulating microRNAs in patients with coronary artery disease. Circ Res. 2010;107:677-684.
14. Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, Mayr A, Weger S, Oberhollenzer F, Bonora E, Shah A, Willeit J, Mayr M. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res. 2010;107:810-817.
15. Li S, Zhu J, Zhang W, Chen Y, Zhang K, Popescu LM, Ma X, Bond Lau W, Rong R, Yu X, Wang B, Li Y, Xiao C, Zhang M, Wang S, Yu L, Chen AF, Yang X, Cai J. Signature microRNA expression profile of essential hypertension and its novel link to human cytomegalovirus infection. Circulation. 2011;124:175-184.
16. Kamm RC, Smith AG. Nucleic acid concentrations in normal human plasma. Clin Chem. 1972;18:519-522.
17. El-Hefnawy T, Raja S, Kelly L, Bigbee WL, Kirkwood JM, Luketich JD, Godfrey TE. Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics. Clin Chem. 2004;50: 564-573. (Pubitemid 38297307)
18. 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.
19. Pigati L, Yaddanapudi SC, Iyengar R, Kim DJ, Hearn SA, Danforth D, Hastings ML, Duelli DM. Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS One. 2010;5: e13515.
20. Chen TS, Lai RC, Lee MM, Choo AB, Lee CN, Lim SK. Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs. Nucleic Acids Res. 2010;38:215-224.
21. Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 2010;38:7248-7259.
22. Borer RA, Lehner CF, Eppenberger HM, Nigg EA. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 1989;56:379-390.
23. Maggi LB Jr, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, Pandolfi PP, Weber JD. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the mammalian ribosome. Mol Cell Biol. 2008;28:7050-7065.
24. Nawa Y, Kawahara K, Tancharoen S, Meng X, Sameshima H, Ito T, Masuda Y, Imaizumi H, Hashiguchi T, Maruyama I. Nucleophosmin may act as an alarmin: implications for severe sepsis. J Leukoc Biol. 2009;86: 645-653.
25. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39: 7223-7233.
26. Janas T, Yarus M. Specific RNA binding to ordered phospholipid bilayers. Nucleic Acids Res. 2006;34:2128-2136. (Pubitemid 44314210)
27. Kim SI, Shin D, Choi TH, Lee JC, Cheon GJ, Kim KY, Park M, Kim M. Systemic and specific delivery of small interfering RNAs to the liver mediated by apolipoprotein A-I. Mol Ther. 2007;15:1145-1152. (Pubitemid 46813617)
28. Muralidharan-Chari V, Clancy JW, Sedgwick A, D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci. 2010;123(part 10):1603-1611.
29. Koppler B, Cohen C, Schlondorff D, Mack M. Differential mechanisms of microparticle transfer to B cells and monocytes: anti-inflammatory properties of microparticles. Eur J Immunol. 2006;36:648-660.
30. Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, Cihak J, Plachy J, Stangassinger M, Erfle V, Schlondorff D. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med. 2000;6:769-775. (Pubitemid 30469425)
31. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10: 1470-1476.
32. Morel O, Toti F, Hugel B, Freyssinet JM. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol. 2004;11:156-164. (Pubitemid 38952003)
33. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006;20:847-856.
34. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, Rajewsky N, Bender TP, Rajewsky K. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell. 2007;131:146-159. (Pubitemid 47498525)
35. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB, Farber DB. Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One. 2009;4:e4722.
36. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Wurdinger T, Middeldorp JM. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA. 2010;107:6328-6333.
37. Etheridge A, Lee I, Hood L, Galas D, Wang K. Extracellular microRNA: a new source of biomarkers. Mutat Res. 2011;717:85-90.
38. Corsten MF, Dennert R, Jochems S, Kuznetsova T, Devaux Y, Hofstra L, Wagner DR, Staessen JA, Heymans S, Schroen B. Circulating microRNA-208b and microRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet. 2010;3:499-506.
39. Ji X, Takahashi R, Hiura Y, Hirokawa G, Fukushima Y, Iwai N. Plasma miR-208 as a biomarker of myocardial injury. Clin Chem. 2009;55: 1944-1949.
40. D'Alessandra Y, Devanna P, Limana F, Straino S, Di Carlo A, Brambilla PG, Rubino M, Carena MC, Spazzafumo L, De Simone M, Micheli B, Biglioli P, Achilli F, Martelli F, Maggiolini S, Marenzi G, Pompilio G, Capogrossi MC. Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur Heart J. 2010;31:2765-2773.
41. Bostjancic E, Zidar N, Stajer D, Glavac D. MicroRNAs miR-1, miR-133a, miR-133b and miR-208 are dysregulated in human myocardial infarction. Cardiology. 2010;115:163-169.
42. Kuwabara Y, Ono K, Horie T, Nishi H, Nagao K, Kinoshita M, Watanabe S, Baba O, Kojima Y, Shizuta S, Imai M, Tamura T, Kita T, Kimura T. Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate the existence of myocardial damage. Circ Cardiovasc Genet. 2011;4:446-454.
43. Adachi T, Nakanishi M, Otsuka Y, Nishimura K, Hirokawa G, Goto Y, Nonogi H, Iwai N. Plasma microRNA 499 as a biomarker of acute myocardial infarction. Clin Chem. 2010;56:1183-1185.
44. Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, Li K, Yu B, Li Z, Wang R, Wang L, Li Q, Wang N, Shan H, Li Z, Yang B. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun. 2010;391:73-77.
45. Cheng Y, Tan N, Yang J, Liu X, Cao X, He P, Dong X, Qin S, Zhang C. A translational study of circulating cell-free microRNA-1 in acute myocardial infarction. Clin Sci (Lond). 2010;119:87-95.
46. Van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007;316:575-579. (Pubitemid 46683138)
47. Van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, Kelm RJ Jr, Olson EN. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell. 2009;17: 662-673.
48. Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006;38: 228-233. (Pubitemid 43177239)
49. Mizuno H, Nakamura A, Aoki Y, Ito N, Kishi S, Yamamoto K, Sekiguchi M, Takeda S, Hashido K. Identification of muscle-specific microRNAs in serum of muscular dystrophy animal models: promising novel blood-based markers for muscular dystrophy. PLoS One. 2011;6:e18388.
50. Wu AH, Feng YJ. Biochemical differences between cTnT and cTnI and their significance for diagnosis of acute coronary syndromes. Eur Heart J. 1998;19(suppl N):N25-N29. (Pubitemid 28524046)
51. Hu Z, Chen X, Zhao Y, Tian T, Jin G, Shu Y, Chen Y, Xu L, Zen K, Zhang C, Shen H. Serum microRNA signatures identified in a genome-wide serum microRNA expression profiling predict survival of non-small-cell lung cancer. J Clin Oncol. 2010;28:1721-1726.
52. Ng EK, Chong WW, Jin H, Lam EK, Shin VY, Yu J, Poon TC, Ng SS, Sung JJ. Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut. 2009;58:1375-1381.
53. Fukushima Y, Nakanishi M, Nonogi H, Goto Y, Iwai N. Assessment of plasma miRNAs in congestive heart failure. Circ J. 2011;75:336-340.
54. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature. 2011;473:317-325.
55. Lobbes MB, Kooi ME, Lutgens E, Ruiters AW, Lima Passos V, Braat SH, Rousch M, Ten Cate H, van Engelshoven JM, Daemen MJ, Heeneman S. Leukocyte counts, myeloperoxidase, and pregnancyassociated plasma protein a as biomarkers for cardiovascular disease: towards a multi-biomarker approach. Int J Vasc Med. 2010;2010:726207.
56. Boulanger CM, Amabile N, Tedgui A. Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension. 2006;48:180-186. (Pubitemid 44309805)
57. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res. 2004;95:343-353. (Pubitemid 39100452)
58. Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest. 2003;111:1805-1812. (Pubitemid 38057722)
59. Taurino C, Miller WH, McBride MW, McClure JD, Khanin R, Moreno MU, Dymott JA, Delles C, Dominiczak AF. Gene expression profiling in whole blood of patients with coronary artery disease. Clin Sci (Lond). 2010;119:335-343.
60. Nathan DM. Long-term complications of diabetes mellitus. N Engl J Med. 1993;328:1676-1685. (Pubitemid 23157351)
61. Bonora E, Kiechl S, Willeit J, Oberhollenzer F, Egger G, Meigs JB, Bonadonna RC, Muggeo M. Population-based incidence rates and risk factors for type 2 diabetes in white individuals: the Bruneck study. Diabetes. 2004;53:1782-1789. (Pubitemid 38857036)
62. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15: 261-271.
63. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY, Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008;15:272-284.
64. Cheng J, Ke Q, Jin Z, Wang H, Kocher O, Morgan JP, Zhang J, Crumpacker CS. Cytomegalovirus infection causes an increase of arterial blood pressure. PLoS Pathog. 2009;5:e1000427.
65. Lee LW, Zhang S, Etheridge A, Ma L, Martin D, Galas D, Wang K. Complexity of the microRNA repertoire revealed by next-generation sequencing. RNA. 2010;16:2170-2180.
66. Fernandez-Valverde SL, Taft RJ, Mattick JS. Dynamic isomiR regulation in Drosophila development. RNA. 2010;16:1881-1888.
67. Ebhardt HA, Tsang HH, Dai DC, Liu Y, Bostan B, Fahlman RP. Metaanalysis of small RNA-sequencing errors reveals ubiquitous posttranscriptional RNA modifications. Nucleic Acids Res. 2009;37: 2461-2470.
68. Borel C, Antonarakis SE. Functional genetic variation of human miRNAs and phenotypic consequences. Mamm Genome. 2008;19:503-509.
69. Liu R, Zhang C, Hu Z, Li G, Wang C, Yang C, Huang D, Chen X, Zhang H, Zhuang R, Deng T, Liu H, Yin J, Wang S, Zen K, Ba Y, Zhang CY. A five-microRNA signature identified from genome-wide serum microRNA expression profiling serves as a fingerprint for gastric cancer diagnosis. Eur J Cancer. 2011;47:784-791.
70. Hoekstra M, van der Lans CA, Halvorsen B, Gullestad L, Kuiper J, Aukrust P, van Berkel TJ, Biessen EA. The peripheral blood mononuclear cell microRNA signature of coronary artery disease. Biochem Biophys Res Commun. 2010;394:792-797.