Massive analysis of cDNA Ends (MACE) and miRNA expression profiling identifies proatherogenic pathways in chronic kidney disease

Epigenetics

Volumn 9, Issue 1, 2014, Pages 161-172

  Zawada, Adam M ^a   Rogacev, Kyrill S ^a   Müller, Sören ^b,c   Rotter, Björn ^b   Winter, Peter ^b   Fliser, Danilo ^a   Heine, Gunnar H ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b GENXPRO GMBH   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Atherosclerosis; Cardiovascular disease; Epigenetics; Hemodialysis; Kidney disease; MACE; miRNA; Next generation sequencing

Indexed keywords

COMPLEMENTARY DNA; DUAL SPECIFICITY PHOSPHATASE 6; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 1A; INTERLEUKIN 1BETA; KRUPPEL LIKE FACTOR 4; KRUPPEL LIKE FACTOR 6; MICRORNA; MICRORNA 146B; MICRORNA 155; MICRORNA 21; MICRORNA 26B; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; MYELOID DIFFERENTIATION FACTOR 88; P21 ACTIVATED KINASE 1; PROTEIN FOS; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; TRANSCRIPTION FACTOR JUND; TRISTETRAPROLIN; UNCLASSIFIED DRUG;

ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; HEMODIALYSIS; HUMAN; INFLAMMATION; MALE; MASSIVE ANALYSIS OF CDNA ENDS; MRNA EXPRESSION ASSAY; NUCLEIC ACID ANALYSIS; UPREGULATION; GENETICS; METABOLISM; MIDDLE AGED; RENAL INSUFFICIENCY, CHRONIC; RENAL REPLACEMENT THERAPY; SIGNAL TRANSDUCTION;

ATHEROSCLEROSIS; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE ONTOLOGY; HUMANS; MALE; MICRORNAS; MIDDLE AGED; RENAL DIALYSIS; RENAL INSUFFICIENCY, CHRONIC; SIGNAL TRANSDUCTION;

EID: 84891932458     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.26931     Document Type: Article

References (51)

1. Herzog CA, Asinger RW, Berger AK, Charytan DM, Díez J, Hart RG, Eckardt KU, Kasiske BL, McCullough PA, Passman RS, et al. Cardiovascular disease in chronic kidney disease. A clinical update from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int 201180:572-586 PMID:21750584 http://dx.doi.org/10.1038/ki.2011.223.
2. Dwivedi RS, Herman JG, McCaffrey TA, Raj DS. Beyond genetics: epigenetic code in chronic kidney disease. Kidney Int 201179:23-32 PMID:20881938 http://dx.doi.org/10.1038/ ki.2010.335.
3. Stenvinkel P, Ekström TJ. Epigenetics--a helpful tool to better understand processes in clinical nephrology? Nephrol Dial Transplant 200823:1493-1496 PMID:18308770 http://dx.doi.org/10.1093/ndt/ gfn056.
4. Zawada AM, Rogacev KS, Heine GH. Clinical relevance of epigenetic dysregulation in chronic kidney disease-associated cardiovascular disease. Nephrol Dial Transplant 201328:1663-1671 PMID:23512108 http://dx.doi.org/10.1093/ndt/gft042.
5. Zawada AM, Rogacev KS, Hummel B, Grün OS, Friedrich A, Rotter B, Winter P, Geisel J, Fliser D, Heine GH. SuperTAG methylation-specific digital karyotyping reveals uremia-induced epigenetic dysregulation of atherosclerosis-related genes. Circ Cardiovasc Genet 20125:611-620 PMID:23074332 http://dx.doi.org/10.1161/CIRCGENETICS.112.963207.
6. Liu G, Abraham E. MicroRNAs in immune response and macrophage polarization. Arterioscler Thromb Vasc Biol 201333:170-177 PMID:23325473 http:// dx.doi.org/10.1161/ATVBAHA.112.300068.
7. Nazari-Jahantigh M, Wei Y, Schober A. The role of microRNAs in arterial remodelling. Thromb Haemost 2012107:611-618 PMID:22371089 http:// dx.doi.org/10.1160/TH11-12-0826.
8. Nazari-Jahantigh M, Wei Y, Noels H, Akhtar S, Zhou Z, Koenen RR, Heyll K, Gremse F, Kiessling F, Grommes J, et al. MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J Clin Invest 2012122:4190-4202 PMID:23041630 http://dx.doi.org/10.1172/JCI61716.
9. Small EM, Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature 2011469:336-342 PMID:21248840 http://dx.doi.org/10.1038/nature09783.
10. Wei Y, Nazari-Jahantigh M, Neth P, Weber C, Schober A. MicroRNA-126,-145, and-155: a therapeutic triad in atherosclerosis? Arterioscler Thromb Vasc Biol 201333:449-454 PMID:23324496 http://dx.doi.org/10.1161/ATVBAHA.112.300279.
11. Creemers EE, Tijsen AJ, Pinto YM. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res 2012110:483-95 PMID:22302755 http://dx.doi.org/10.1161/CIRCRESAHA.111.247452.
12. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, Weber M, Hamm CW, Röxe T, Müller-Ardogan M, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010107:677-684 PMID:20595655 http://dx.doi.org/10.1161/CIRCRESAHA.109.215566.
13. 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 2010394:792-797 PMID:20230787 http://dx.doi.org/10.1016/j.bbrc.2010.03.075.
14. 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) 2010119:335-343 PMID:20528768 http://dx.doi.org/10.1042/CS20100043.
15. van Empel VP, De Windt LJ, da Costa Martins PA. Circulating miRNAs: reflecting or affecting cardiovascular disease? Curr Hypertens Rep 201214:498-509 PMID:22996205 http://dx.doi.org/10.1007/s11906-012-0310-7.
16. Lovren F, Pan Y, Quan A, Singh KK, Shukla PC, Gupta N, Steer BM, Ingram AJ, Gupta M, Al-Omran M, et al. MicroRNA-145 targeted therapy reduces atherosclerosis. Circulation 2012126(Suppl 1):S81-S90 PMID:22965997 http://dx.doi.org/10.1161/ CIRCULATIONAHA.111.084186.
17. van Rooij E, Purcell AL, Levin AA. Developing microRNA therapeutics. Circ Res 2012110:496-507 PMID:22302756 http://dx.doi.org/10.1161/CIRCRESAHA.111.247916.
18. Wei Y, Nazari-Jahantigh M, Chan L, Zhu M, Heyll K, Corbalán-Campos J, Hartmann P, Thiemann A, Weber C, Schober A. The microRNA-342-5p fosters inflammatory macrophage activation through an Akt1-and microRNA-155-dependent pathway during atherosclerosis. Circulation 2013127:1609-1619 PMID:23513069 http://dx.doi.org/10.1161/CIRCULATIONAHA.112.000736.
19. Rotllan N, Ramírez CM, Aryal B, Esau CC, Fernández-Hernando C. Therapeutic silencing of microRNA-33 inhibits the progression of atherosclerosis in Ldlr-/-mice--brief report. Arterioscler Thromb Vasc Biol 201333:1973-1977 PMID:23702658 http://dx.doi.org/10.1161/ATVBAHA.113.301732.
20. Janssen HL, Reesink HW, Lawitz EJ, Zeuzem S, Rodriguez-Torres M, Patel K, van der Meer AJ, Patick AK, Chen A, Zhou Y, et al. Treatment of HCV infection by targeting microRNA. N Engl J Med 2013368:1685-1694 PMID:23534542 http://dx.doi.org/10.1056/NEJMoa1209026.
21. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 19909:811-818 PMID:2218183 http://dx.doi.org/10.1002/sim.4780090710.
22. Goettsch C, Hutcheson JD, Aikawa E. MicroRNA in cardiovascular calcification: focus on targets and extracellular vesicle delivery mechanisms. Circ Res 2013112:1073-1084 PMID:23538277 http://dx.doi.org/10.1161/CIRCRESAHA.113.300937.
23. Fernández-Hernando C, Ramírez CM, Goedeke L, Suárez Y. MicroRNAs in metabolic disease. Arterioscler Thromb Vasc Biol 201333:178-185 PMID:23325474 http://dx.doi.org/10.1161/ATVBAHA.112.300144.
24. Asmann YW, Klee EW, Thompson EA, Perez EA, Middha S, Oberg AL, Therneau TM, Smith DI, Poland GA, Wieben ED, et al. 3′tag digital gene expression profiling of human brain and universal reference RNA using Illumina Genome Analyzer. BMC Genomics 200910:531 PMID:19917133 http://dx.doi.org/10.1186/1471-2164-10-531.
25. Lenz TL, Eizaguirre C, Rotter B, Kalbe M, Milinski M. Exploring local immunological adaptation of two stickleback ecotypes by experimental infection and transcriptome-wide digital gene expression analysis. Mol Ecol 201322:774-786 PMID:22971109 http://dx.doi.org/10.1111/j.1365-294X.2012.05756.x
26. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999340:115-126 PMID:9887164 http://dx.doi.org/10.1056/NEJM199901143400207.
27. Ismail N, Wang Y, Dakhlallah D, Moldovan L, Agarwal K, Batte K, Shah P, Wisler J, Eubank TD, Tridandapani S, et al. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 2013121:984-995 PMID:23144169 http://dx.doi.org/10.1182/blood-2011-08-374793.
28. Mayr M, Zampetaki A, Willeit P, Willeit J, Kiechl S. MicroRNAs within the continuum of postgenomics biomarker discovery. Arterioscler Thromb Vasc Biol 201333:206-214 PMID:23325478 http://dx.doi.org/10.1161/ATVBAHA.112.300141.
29. Zhuang G, Meng C, Guo X, Cheruku PS, Shi L, Xu H, Li H, Wang G, Evans AR, Safe S, et al. A novel regulator of macrophage activation: miR-223 in obesity-associated adipose tissue inflammation. Circulation 2012125:2892-2903 PMID:22580331 http://dx.doi.org/10.1161/CIRCULATIONAHA.111.087817.
30. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 201010:111-122 PMID:20098459 http://dx.doi.org/10.1038/nri2708.
31. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 2007104:1604-1609 PMID:17242365;http://dx.doi.org/10.1073/pnas.0610731104.
32. Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O'Leary JJ, Ruan Q, Johnson DS, Chen Y, O'Neill LA. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol 201011:141-7 PMID:19946272 http://dx.doi.org/10.1038/ni.1828.
33. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006103:12481-12486 PMID:16885212 http://dx.doi.org/10.1073/pnas.0605298103.
34. Raitoharju E, Lyytikäinen LP, Levula M, Oksala N, Mennander A, Tarkka M, Klopp N, Illig T, Kähönen M, Karhunen PJ, et al. miR-21, miR-210, miR-34a, and miR-146a/b are up-regulated in human atherosclerotic plaques in the Tampere Vascular Study. Atherosclerosis 2011219:211-217 PMID:21820659 http://dx.doi.org/10.1016/j.atherosclerosis.2011.07.020.
35. Bidzhekov K, Gan L, Denecke B, Rostalsky A, Hristov M, Koeppel TA, Zernecke A, Weber C. microRNA expression signatures and parallels between monocyte subsets and atherosclerotic plaque in humans. Thromb Haemost 2012107:619-625 PMID:22370758 http://dx.doi.org/10.1160/TH11-09-0607.
36. Zampetaki A, Willeit P, Tilling L, Drozdov I, Prokopi M, Renard JM, Mayr A, Weger S, Schett G, Shah A, et al. Prospective study on circulating MicroRNAs and risk of myocardial infarction. J Am Coll Cardiol 201260:290-299 PMID:22813605 http://dx.doi.org/10.1016/j.jacc.2012.03.056.
37. Donners MM, Wolfs IM, Stöger LJ, van der Vorst EP, Pöttgens CC, Heymans S, Schroen B, Gijbels MJ, de Winther MP. Hematopoietic miR155 deficiency enhances atherosclerosis and decreases plaque stability in hyperlipidemic mice. PLoS One 20127:e35877 PMID:22558252 http://dx.doi.org/10.1371/journal.pone.0035877.
38. Heine GH, Ulrich C, Seibert E, Seiler S, Marell J, Reichart B, Krause M, Schlitt A, Köhler H, Girndt M. CD14(++)CD16+ monocytes but not total monocyte numbers predict cardiovascular events in dialysis patients. Kidney Int 200873:622-629PMID:18160960 http://dx.doi.org/10.1038/sj.ki.5002744.
39. Rogacev KS, Seiler S, Zawada AM, Reichart B, Herath E, Roth D, Ulrich C, Fliser D, Heine GH. CD14++CD16+ monocytes and cardiovascular outcome in patients with chronic kidney disease. Eur Heart J 201132:84-92 PMID:20943670 http://dx.doi.org/10.1093/eurheartj/ehq371.
40. Heine GH, Ortiz A, Massy ZA, Lindholm B, Wiecek A, Martínez-Castelao A, Covic A, Goldsmith D, Süleymanlar G, London GM, et al.European Renal and Cardiovascular Medicine (EURECA-m) working group of the European Renal Association-European Dialysis and Transplant Association (ERA-EDTA). Monocyte subpopulations and cardiovascular risk in chronic kidney disease. Nat Rev Nephrol 20128:362-369 PMID:22410492 http://dx.doi.org/10.1038/nrneph.2012.41.
41. Rogacev KS, Cremers B, Zawada AM, Seiler S, Binder N, Ege P, Große-Dunker G, Heisel I, Hornof F, Jeken J, et al. CD14++CD16+ monocytes independently predict cardiovascular events: a cohort study of 951 patients referred for elective coronary angiography. J Am Coll Cardiol 201260:1512-1520 PMID:22999728 http://dx.doi.org/10.1016/j.jacc.2012.07.019.
42. Zawada AM, Rogacev KS, Schirmer SH, Sester M, Böhm M, Fliser D, Heine GH. Monocyte heterogeneity in human cardiovascular disease. Immunobiology 2012217:1273-1284 PMID:22898391 http://dx.doi.org/10.1016/j.imbio.2012.07.001.
43. Zawada AM, Rogacev KS, Rotter B, Winter P, Marell RR, Fliser D, Heine GH. SuperSAGE evidence for CD14++CD16+ monocytes as a third monocyte subset. Blood 2011118:e50-e61 PMID:21803849 http://dx.doi.org/10.1182/blood-2011-01-326827.
44. Neal CS, Michael MZ, Pimlott LK, Yong TY, Li JY, Gleadle JM. Circulating microRNA expression is reduced in chronic kidney disease. Nephrol Dial Transplant 201126:3794-3802 PMID:21891774 http://dx.doi.org/10.1093/ndt/gfr485.
45. Lorenzen JM, Kielstein JT, Hafer C, Gupta SK, Kümpers P, Faulhaber-Walter R, Haller H, Fliser D, Thum T. Circulating miR-210 predicts survival in critically ill patients with acute kidney injury. Clin J Am Soc Nephrol 20116:1540-1546 PMID:21700819 http://dx.doi.org/10.2215/CJN.00430111.
46. Khella HW, Bakhet M, Lichner Z, Romaschin AD, Jewett MA, Yousef GM. MicroRNAs in kidney disease: an emerging understanding. Am J Kidney Dis 201361:798-808 PMID:23219107 http://dx.doi.org/10.1053/j.ajkd.2012.09.018.
47. Hafner M, Landgraf P, Ludwig J, Rice A, Ojo T, Lin C, Holoch D, Lim C, Tuschl T. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 200844:3-12 PMID:18158127 http://dx.doi.org/10.1016/j.ymeth.2007.09.009.
48. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 201011:R106 PMID:20979621 http://dx.doi.org/10.1186/gb-2010-11-10-r106.
49. Müller S, Rycak L, Winter P, Kahl G, Koch I, Rotter B. omiRas: a Web server for differential expression analysis of miRNAs derived from small RNA-Seq data. Bioinformatics 201329:2651-2652 PMID:23946503 http://dx.doi.org/10.1093/bioinformatics/btt457.
50. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 200925:1754-1760 PMID:19451168 http://dx.doi.org/10.1093/bioinformatics/btp324.
51. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 201026:136-138 PMID:19855105 http://dx.doi.org/10.1093/bioinformatics/btp612