Detection and comparison of microRNA expression in the serum of Doberman Pinschers with dilated cardiomyopathy and healthy controls

BMC Veterinary Research

Volumn 9, Issue , 2013, Pages

  Steudemann, Carola ^a   Bauersachs, Stefan ^a   Weber, Karin ^a   Wess, Gerhard ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Dilated cardiomyopathy; Dobermann Pinscher; Dog; Microarray; miRNA; Serum

Indexed keywords

CANIS FAMILIARIS;

MICRORNA;

ANIMAL; ANIMAL DISEASE; ARTICLE; CASE CONTROL STUDY; CONGESTIVE CARDIOMYOPATHY; DOG; DOG DISEASE; ECHOCARDIOGRAPHY; ECHOGRAPHY; ELECTROCARDIOGRAPHY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; MALE; PARASITOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CARDIOMYOPATHY, DILATED; CASE-CONTROL STUDIES; DOG DISEASES; DOGS; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; FEMALE; GENE EXPRESSION PROFILING; MALE; MICRORNAS;

MLCS; MLOWN;

EID: 84872272007     PISSN: None     EISSN: 17466148     Source Type: Journal    
DOI: 10.1186/1746-6148-9-12     Document Type: Article

References (107)

1. O'Grady MR, O'Sullivan ML. Dilated cardiomyopathy: an update. Vet Clin North Am Small Anim Pract 2004, 34(5):1187-1207. 10.1016/j.cvsm.2004.05.009, 15325477.
2. Tidholm A, Haggstrom J, Borgarelli M, Tarducci A. Canine idiopathic dilated cardiomyopathy. Part I: aetiology, clinical characteristics, epidemiology and pathology. Vet J 2001, 162(2):92-107. 10.1053/tvjl.2001.0571, 11531394.
3. Vollmar AC. The prevalence of cardiomyopathy in the Irish wolfhound: a clinical study of 500 dogs. J Am Anim Hosp Assoc 2000, 36(2):125-132.
4. Calvert CA, Meurs KM. Cardiomyopathy in doberman pinschers. Kirk′s Current Veterinary Therapy XIV 2009, 800-803. St. Louis: Saunders Elsevier, Bonagura JD, Twedt DC, vol. XIV.
5. Calvert CA, Brown J. Influence of antiarrhythmia therapy on survival times of 19 clinically healthy doberman pinschers with dilated cardiomyopathy that experienced syncope, ventricular tachycardia, and sudden death (1985-1998). J Am Anim Hosp Assoc 2004, 40(1):24-28.
6. Calvert CA, Chapman WL, Toal RL. Congestive cardiomyopathy in doberman pinscher dogs. J Am Vet Med Assoc 1982, 181(6):598-602.
7. Mausberg TB, Wess G, Simak J, Keller L, Drogemuller M, Drogemuller C, Webster MT, Stephenson H, Dukes-McEwan J, Leeb T. A locus on chromosome 5 is associated with dilated cardiomyopathy in doberman pinschers. PLoS One 2011, 6(5):e20042. 10.1371/journal.pone.0020042, 3098859, 21625443.
8. Wess G, Schulze A, Butz V, Simak J, Killich M, Keller LJ, Maeurer J, Hartmann K. Prevalence of dilated cardiomyopathy in doberman pinschers in various age groups. J Vet Intern Med 2010, 24(3):533-538. 10.1111/j.1939-1676.2010.0479.x, 20202106.
9. Calvert CA, Pickus CW, Jacobs GJ, Brown J. Signalment, survival, and prognostic factors in doberman pinschers with end-stage cardiomyopathy. J Vet Intern Med 1997, 11(6):323-326. 10.1111/j.1939-1676.1997.tb00474.x, 9470155.
10. Calvert CA, Hall G, Jacobs G, Pickus C. Clinical and pathologic findings in doberman pinschers with occult cardiomyopathy that died suddenly or developed congestive heart failure: 54 cases (1984-1991). J Am Vet Med Assoc 1997, 210(4):505-511.
11. Petric AD, Stabej P, Zemva A. Dilated cardiomyopathy in doberman pinschers: survival, causes of death and a pedigree review in a related line. J Vet Cardiol 2002, 4(1):17-24. 10.1016/S1760-2734(06)70019-4, 19081342.
12. Calvert CA, Jacobs G, Pickus CW, Smith DD. Results of ambulatory electrocardiography in overtly healthy doberman pinschers with echocardiographic abnormalities. J Am Vet Med Assoc 2000, 217(9):1328-1332. 10.2460/javma.2000.217.1328, 11061384.
13. Calvert CA, Jacobs GJ, Smith DD, Rathbun SL, Pickus CW. Association between results of ambulatory electrocardiography and development of cardiomyopathy during long-term follow-up of doberman pinschers. J Am Vet Med Assoc 2000, 216(1):34-39. 10.2460/javma.2000.216.34, 10638315.
14. Hazlett MJ, Maxie MG, Allen DG, Wilcock BP. A retrospective study of heart disease in doberman pinscher dogs. Can Vet J 1983, 24(7):205-210. 1790348, 17422276.
15. O'Grady MR, O'Sullivan ML, Minors SL, Horne R. Efficacy of benazepril hydrochloride to delay the progression of occult dilated cardiomyopathy in doberman pinschers. J Vet Intern Med 2009, 23(5):977-983. 10.1111/j.1939-1676.2009.0346.x, 19572914.
16. Oyama MA, Sisson DD, Solter PF. Prospective screening for occult cardiomyopathy in dogs by measurement of plasma atrial natriuretic peptide, B-type natriuretic peptide, and cardiac troponin-I concentrations. Am J Vet Res 2007, 68(1):42-47. 10.2460/ajvr.68.1.42, 17199417.
17. Oyama MA, Sisson DD. Cardiac troponin-I concentration in dogs with cardiac disease. J Vet Intern Med 2004, 18(6):831-839. 10.1111/j.1939-1676.2004.tb02629.x, 15638266.
18. Spratt DP, Mellanby RJ, Drury N, Archer J. Cardiac troponin I: evaluation I of a biomarker for the diagnosis of heart disease in the dog. J Small Anim Pract 2005, 46(3):139-145. 10.1111/j.1748-5827.2005.tb00304.x, 15789809.
19. O'Sullivan ML, O'Grady MR, Minors SL. Plasma big endothelin-1, atrial natriuretic peptide, aldosterone, and norepinephrine concentrations in normal doberman pinschers and doberman pinschers with dilated cardiomyopathy. J Vet Intern Med 2007, 21(1):92-99.
20. Wess G, Butz V, Mahling M, Hartmann K. Evaluation of N-terminal pro-B-type natriuretic peptide as a diagnostic marker of various stages of cardiomyopathy in doberman pinschers. Am J Vet Res 2011, 72(5):642-649. 10.2460/ajvr.72.5.642, 21529216.
21. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006, 6(4):259-269.
22. Zhang S, Chen L, Jung EJ, Calin GA. Targeting microRNAs with small molecules: from dream to reality. Clin Pharmacol Ther 2010, 87(6):754-758. 10.1038/clpt.2010.46, 20428111.
23. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009, 19(1):92-105. 2612969, 18955434.
24. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008, 105(30):10513-10518. 10.1073/pnas.0804549105, 2492472, 18663219.
25. Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, Li K, Yu B, Li Z, Wang R. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun 2010, 391(1):73-77. 10.1016/j.bbrc.2009.11.005, 19896465.
26. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 2008, 18(10):997-1006. 10.1038/cr.2008.282, 18766170.
27. Etheridge A, Lee I, Hood L, Galas D, Wang K. Extracellular microRNA: a new source of biomarkers. Mutat Res 2011, 717(1-2):85-90. 10.1016/j.mrfmmm.2011.03.004, 3199035, 21402084.
28. Wang K, Zhang S, Marzolf B, Troisch P, Brightman A, Hu Z, Hood LE, Galas DJ. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA 2009, 106(11):4402-4407. 10.1073/pnas.0813371106, 2657429, 19246379.
29. Tsujiura M, Ichikawa D, Komatsu S, Shiozaki A, Takeshita H, Kosuga T, Konishi H, Morimura R, Deguchi K, Fujiwara H. Circulating microRNAs in plasma of patients with gastric cancers. Br J Cancer 2010, 102(7):1174-1179. 10.1038/sj.bjc.6605608, 2853097, 20234369.
30. Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Newell J, Kerin MJ. Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann Surg 2010, 251(3):499-505. 10.1097/SLA.0b013e3181cc939f, 20134314.
31. 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(6):659-666. 10.1093/eurheartj/ehq013, 20159880.
32. Huang Z, Huang D, Ni S, Peng Z, Sheng W, Du X. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int J Cancer 2010, 127(1):118-126. 10.1002/ijc.25007, 19876917.
33. Lodes MJ, Caraballo M, Suciu D, Munro S, Kumar A, Anderson B. Detection of cancer with serum miRNAs on an oligonucleotide microarray. PLoS One 2009, 4(7):e6229. 10.1371/journal.pone.0006229, 2704963, 19597549.
34. Zhang Y, Jia Y, Zheng R, Guo Y, Wang Y, Guo H, Fei M, Sun S. Plasma microRNA-122 as a biomarker for viral-, alcohol-, and chemical-related hepatic diseases. Clin Chem 2010, 56(12):1830-1838. 10.1373/clinchem.2010.147850, 20930130.
35. Baskerville S, Bartel DP. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 2005, 11(3):241-247. 10.1261/rna.7240905, 1370713, 15701730.
36. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr Biol 2002, 12(9):735-739. 10.1016/S0960-9822(02)00809-6, 12007417.
37. Satoh M, Minami Y, Takahashi Y, Tabuchi T, Nakamura M. Expression of microRNA-208 is associated with adverse clinical outcomes in human dilated cardiomyopathy. J Card Fail 2010, 16(5):404-410. 10.1016/j.cardfail.2010.01.002, 20447577.
38. Ikeda S, Pu WT. Expression and function of MicroRNAs in heart disease. Curr Drug Targets 2010, 11(8):913-925. 10.2174/138945010791591304, 20415651.
39. Cai B, Pan Z, Lu Y. The roles of microRNAs in heart diseases: a novel important regulator. Curr Med Chem 2010, 17(5):407-411. 10.2174/092986710790226129, 20015039.
40. van Rooij E, Olson EN. MicroRNAs: powerful new regulators of heart disease and provocative therapeutic targets. J Clin Invest 2007, 117(9):2369-2376. 10.1172/JCI33099, 1952642, 17786230.
41. Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, Zhang Y, Xu C, Bai Y, Wang H. The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med 2007, 13(4):486-491. 10.1038/nm1569, 17401374.
42. Zhao Y, Ransom JF, Li A, Vedantham V, von Drehle M, Muth AN, Tsuchihashi T, McManus MT, Schwartz RJ, Srivastava D. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 2007, 129(2):303-317. 10.1016/j.cell.2007.03.030, 17397913.
43. 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(5824):575-579. 10.1126/science.1139089, 17379774.
44. van Rooij E, Sutherland LB, Liu N, Williams AH, McAnally J, Gerard RD, Richardson JA, Olson EN. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci USA 2006, 103(48):18255-18260. 10.1073/pnas.0608791103, 1838739, 17108080.
45. Chen JF, Murchison EP, Tang R, Callis TE, Tatsuguchi M, Deng Z, Rojas M, Hammond SM, Schneider MD, Selzman CH. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci USA 2008, 105(6):2111-2116. 10.1073/pnas.0710228105, 2542870, 18256189.
46. Rao PK, Toyama Y, Chiang HR, Gupta S, Bauer M, Medvid R, Reinhardt F, Liao R, Krieger M, Jaenisch R. Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ Res 2009, 105(6):585-594. 10.1161/CIRCRESAHA.109.200451, 2828903, 19679836.
47. Liu N, Bezprozvannaya S, Williams AH, Qi X, Richardson JA, Bassel-Duby R, Olson EN. microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev 2008, 22(23):3242-3254. 10.1101/gad.1738708, 2600761, 19015276.
48. Ikeda S, Kong SW, Lu J, Bisping E, Zhang H, Allen PD, Golub TR, Pieske B, Pu WT. Altered microRNA expression in human heart disease. Physiol Genomics 2007, 31(3):367-373. 10.1152/physiolgenomics.00144.2007, 17712037.
49. Sucharov C, Bristow MR, Port JD. miRNA expression in the failing human heart: functional correlates. J Mol Cell Cardiol 2008, 45(2):185-192. 10.1016/j.yjmcc.2008.04.014, 2561965, 18582896.
50. Satoh M, Minami Y, Takahashi Y, Tabuchi T, Nakamura M. A cellular MicroRNA, let-7i, is a novel biomarker for clinical outcome in patients with dilated cardiomyopathy. J Card Fail 2011, 17(11):923-929. 10.1016/j.cardfail.2011.07.012, 22041329.
51. Zhou B, Rao L, Peng Y, Wang Y, Chen Y, Song Y, Zhang L. Common genetic polymorphisms in pre-microRNAs were associated with increased risk of dilated cardiomyopathy. Clin Chim Acta 2010, 32(1):60-65.
52. Voellenkle C, van Rooij J, Cappuzzello C, Greco S, Arcelli D, Di Vito L, Melillo G, Rigolini R, Costa E, Crea F. MicroRNA signatures in peripheral blood mononuclear cells of chronic heart failure patients. Physiol Genomics 2010, 42(3):420-426. 10.1152/physiolgenomics.00211.2009, 20484156.
53. 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(6):1035-1039. 10.1161/CIRCRESAHA.110.218297, 20185794.
54. Zampetaki A, Willeit P, Tilling L, Drozdov I, Prokopi M, Renard JM, Mayr A, Weger S, Schett G, Shah A. Prospective study on circulating MicroRNAs and risk of myocardial infarction. J Am Coll Cardiol 2012, 60(4):290-299. 10.1016/j.jacc.2012.03.056, 22813605.
55. Van Empel VP, De Windt LJ, Martins PA. Circulating miRNAs: reflecting or affecting cardiovascular disease. Curr Hypertens Rep 2012, 14(6):498-509. 10.1007/s11906-012-0310-7, 22996205.
56. Elton TS, Khan M, Terentyev D. MicroRNAs in cardiovascular disease. F1000 Med Rep 2011, 3:10. 3096884, 21654926.
57. 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(11):1944-1949. 10.1373/clinchem.2009.125310, 19696117.
58. Dorn GW. MicroRNAs in cardiac disease. Transl Res 2011, 157(4):226-235. 10.1016/j.trsl.2010.12.013, 3070425, 21420033.
59. 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(3):e18388. 10.1371/journal.pone.0018388, 3068182, 21479190.
60. Zhou D, Li S, Wen J, Gong X, Xu L, Luo Y. Genome-wide computational analyses of microRNAs and their targets from Canis familiaris. Comput Biol Chem 2008, 32(1):60-65.
61. Boggs RM, Moody JA, Long CR, Tsai KL, Murphy KE. Identification, amplification and characterization of miR-17-92 from canine tissue. Gene 2007, 404(1-2):25-30.
62. Gioia G, Mortarino M, Gelain ME, Albonico F, Ciusani E, Forno I, Marconato L, Martini V, Comazzi S. Immunophenotype-related microRNA expression in canine chronic lymphocytic leukemia. Vet Immunol Immunopathol 2011, 142(3-4):228-235.
63. Boggs RM, Wright ZM, Stickney MJ, Porter WW, Murphy KE. MicroRNA expression in canine mammary cancer. Mamm Genome 2008, 19(7-8):561-569.
64. Mortarino M, Gioia G, Gelain ME, Albonico F, Roccabianca P, Ferri E, Comazzi S. Identification of suitable endogenous controls and differentially expressed microRNAs in canine fresh-frozen and FFPE lymphoma samples. Leuk Res 2010, 34(8):1070-1077. 10.1016/j.leukres.2009.10.023, 19945163.
65. Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, Doevendans PA, Mummery CL, Borlak J, Haverich A. MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation 2007, 116(3):258-267. 10.1161/CIRCULATIONAHA.107.687947, 17606841.
66. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008, 456(7224):980-984. 10.1038/nature07511, 19043405.
67. 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(2):87-95.
68. Kroh EM, Parkin RK, Mitchell PS, Tewari M. Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 2010, 50(4):298-301. 10.1016/j.ymeth.2010.01.032, 20146939.
69. Cannarozzi G, Schneider A, Gonnet G. A phylogenomic study of human, dog, and mouse. PLoS Comput Biol 2007, 3(1):e2. 10.1371/journal.pcbi.0030002, 1761043, 17206860.
70. Lunter G. Dog as an outgroup to human and mouse. PLoS Comput Biol 2007, 3(4):e74. 10.1371/journal.pcbi.0030074, 1857806, 17465673.
71. Zhao Y, Sheng Z, Huang J. A systematic analysis of heart transcriptome highlights divergent cardiovascular disease pathways between animal models and humans. Mol Biosyst 2012, 8(2):504-510. 10.1039/c1mb05415e, 22159153.
72. Chen XM, Splinter PL, O'Hara SP, LaRusso NF. A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. J Biol Chem 2007, 282(39):28929-28938. 10.1074/jbc.M702633200, 2194650, 17660297.
73. Satoh M, Nakamura M, Akatsu T, Shimoda Y, Segawa I, Hiramori K. Toll-like receptor 4 is expressed with enteroviral replication in myocardium from patients with dilated cardiomyopathy. Lab Invest 2004, 84(2):173-181. 10.1038/labinvest.3700031, 14688801.
74. Frankel LB, Wen J, Lees M, Hoyer-Hansen M, Farkas T, Krogh A, Jaattela M, Lund AH. microRNA-101 is a potent inhibitor of autophagy. EMBO J 2011, 30(22):4628-4641. 10.1038/emboj.2011.331, 3243595, 21915098.
75. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y, Zhuang SM. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 2009, 69(3):1135-1142. 10.1158/0008-5472.CAN-08-2886, 19155302.
76. Krichevsky AM, Gabriely G. miR-21: a small multi-faceted RNA. J Cell Mol Med 2009, 13(1):39-53.
77. Selcuklu SD, Donoghue MT, Spillane C. miR-21 as a key regulator of oncogenic processes. Biochem Soc Trans 2009, 37(Pt 4):918-925.
78. Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, Dean DB, Zhang C. MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 2007, 100(11):1579-1588. 10.1161/CIRCRESAHA.106.141986, 17478730.
79. Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 2007, 100(8):1164-1173. 10.1161/01.RES.0000265065.26744.17, 17379831.
80. Cheng Y, Ji R, Yue J, Yang J, Liu X, Chen H, Dean DB, Zhang C. MicroRNAs are aberrantly expressed in hypertrophic heart: do they play a role in cardiac hypertrophy?. Am J Pathol 2007, 170(6):1831-1840. 10.2353/ajpath.2007.061170, 1899438, 17525252.
81. Roy S, Khanna S, Hussain SR, Biswas S, Azad A, Rink C, Gnyawali S, Shilo S, Nuovo GJ, Sen CK. MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res 2009, 82(1):21-29. 10.1093/cvr/cvp015, 2652741, 19147652.
82. Tatsuguchi M, Seok HY, Callis TE, Thomson JM, Chen JF, Newman M, Rojas M, Hammond SM, Wang DZ. Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy. J Mol Cell Cardiol 2007, 42(6):1137-1141. 10.1016/j.yjmcc.2007.04.004, 1934409, 17498736.
83. Sayed D, Hong C, Chen IY, Lypowy J, Abdellatif M. MicroRNAs play an essential role in the development of cardiac hypertrophy. Circ Res 2007, 100(3):416-424. 10.1161/01.RES.0000257913.42552.23, 17234972.
84. Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, Wang D, Krall TJ, Delphin ES, Zhang C. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem 2009, 284(43):29514-29525. 10.1074/jbc.M109.027896, 2785585, 19706597.
85. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA 2008, 105(35):13027-13032. 10.1073/pnas.0805038105, 2529064, 18723672.
86. Everett RM, McGann J, Wimberly HC, Althoff J. Dilated cardiomyopathy of Doberman pinschers: retrospective histomorphologic evaluation of heart from 32 cases. Vet Pathol 1999, 36(3):221-227. 10.1354/vp.36-3-221, 10332830.
87. Tidholm A, Jonsson L. Histologic characterization of canine dilated cardiomyopathy. Vet Pathol 2005, 42(1):1-8. 10.1354/vp.42-1-1, 15657266.
88. Orenes-Pinero E, Montoro-Garcia S, Patel JV, Valdes M, Marin F, Lip GY. Role of microRNAs in cardiac remodelling: New insights and future perspectives. Int J Cardiol 2012, pii: S0167-5273(12)01241-7. http://dx.doi.org/10.1016/j.ijcard.2012.09.120. [Epub ahead of print].
89. Liu F, Yin L, Zhang L, Liu W, Liu J, Wang Y, Yu B. Trimetazidine improves right ventricular function by increasing miR-21 expression. Int J Mol Med 2012, 30(4):849-855.
90. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, Burchfield J, Fox H, Doebele C, Ohtani K. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 2009, 324(5935):1710-1713. 10.1126/science.1174381, 19460962.
91. Zhang X, Wang X, Zhu H, Zhu C, Wang Y, Pu WT, Jegga AG, Fan GC. Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death. J Mol Cell Cardiol 2010, 49(5):841-850. 10.1016/j.yjmcc.2010.08.007, 2949485, 20708014.
92. Jeong MH, Lee JS, Kim DH, Park WJ, Yang DK. Identification of novel microRNAs negatively regulating cardiac hypertrophy. Biochem Biophys Res Commun 2012,
93. 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(20):7248-7259. 10.1093/nar/gkq601, 2978372, 20615901.
94. Creemers EE, Tijsen AJ, Pinto YM. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease?. Circ Res 2012, 110(3):483-495. 10.1161/CIRCRESAHA.111.247452, 22302755.
95. 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(4):423-433. 10.1038/ncb2210, 3074610, 21423178.
96. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011, 108(12):5003-5008. 10.1073/pnas.1019055108, 3064324, 21383194.
97. 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(6):654-659. 10.1038/ncb1596, 17486113.
98. Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, Muramatsu K, Fukuda Y, Ogura S, Yamaguchi K. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One 2010, 5(10):e13247. 10.1371/journal.pone.0013247, 2951912, 20949044.
99. Lee YS, Pressman S, Andress AP, Kim K, White JL, Cassidy JJ, Li X, Lubell K, Lim Do H, Cho IS. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 2009, 11(9):1150-1156. 10.1038/ncb1930, 2737091, 19684574.
100. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010, 39(1):133-144. 10.1016/j.molcel.2010.06.010, 20603081.
101. Summerfield NJ, Boswood A, O'Grady MR, Gordon SG, Dukes-McEwan J, Oyama MA, Smith S, Patteson M, French AT, Culshaw GJ. Efficacy of pimobendan in the prevention of congestive heart failure or sudden death in doberman pinschers with preclinical dilated cardiomyopathy (the PROTECT study). J Vet Intern Med 2012, 26(6):1337-1349. 10.1111/j.1939-1676.2012.01026.x, 3546380, 23078651.
102. Wess G, Maurer J, Simak J, Hartmann K. Use of Simpson's method of disc to detect early echocardiographic changes in doberman pinschers with dilated cardiomyopathy. J Vet Intern Med 2010, 24(5):1069-1076. 10.1111/j.1939-1676.2010.0575.x, 20707842.
103. Griffiths-Jones S. The microRNA registry. Nucleic Acids Res 2004, 32(Database issue):D109-D111. 308757, 14681370.
104. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 2002, 18(Suppl 1):S96-S104. 10.1093/bioinformatics/18.suppl_1.S96, 12169536.
105. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 2003, 31(4):265-273. 10.1016/S1046-2023(03)00155-5, 14597310.
106. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45. 10.1093/nar/29.9.e45, 55695, 11328886.
107. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30(9):e36. 10.1093/nar/30.9.e36, 113859, 11972351.