Deep RNA sequencing reveals novel cardiac transcriptomic signatures for physiological and pathological hypertrophy

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Song, Hong Ki ^a   Hong, Seong Eui ^a   Kim, Taeyong ^a   Kim, Do Han ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CHEMOKINE; COLLAGEN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HUB; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXM1 PROTEIN, MOUSE; ISOPROTEIN; ONCOPROTEIN; POLO LIKE KINASE 1; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

ABLIM2 GENE; ACTA1 GENE; ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CXXC5 GENE; DNA BINDING MOTIF; DOWN REGULATION; EGFL7 GENE; ENAH GENE; EXON; FHL1 GENE; FOXM1 GENE; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HEART; HEART VENTRICLE HYPERTROPHY; HIGH THROUGHPUT SEQUENCING; MALE; MAPK14 GENE; MOUSE; MYH7 GENE; NDRG2 GENE; NONHUMAN; NPPA GENE; NPPB GENE; PATHOGENESIS; PLK1 GENE; PLN GENE; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RCAN1 GENE; RNA SEQUENCE; SOX17 GENE; SYNPO GENE; TMPO GENE; TRANSCRIPTOMICS; TTLL1 GENE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CARDIOMEGALY; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETICS; HEART FAILURE; HEART MUSCLE; HYPERTROPHY; PATHOLOGY; PROTEIN MICROARRAY; SEQUENCE ANALYSIS;

ALTERNATIVE SPLICING; ANIMALS; CARDIOMEGALY; CELL CYCLE PROTEINS; DISEASE MODELS, ANIMAL; EXONS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; HEART FAILURE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HYPERTROPHY; MALE; MICE; MICE, INBRED C57BL; MYOCARDIUM; PROTEIN ARRAY ANALYSIS; PROTEIN ISOFORMS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; SEQUENCE ANALYSIS, RNA;

EID: 84859879034     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035552     Document Type: Article

References (64)

1. Hunter JJ, Chien KR, (1999) Signaling pathways for cardiac hypertrophy and failure. N Engl J Med 341: 1276-1283.
2. Catalucci D, Latronico MV, Ellingsen O, Condorelli G, (2008) Physiological myocardial hypertrophy: how and why? Front Biosci 13: 312-324.
3. Ueno S, Ohki R, Hashimoto T, Takizawa T, Takeuchi K, et al. (2003) DNA microarray analysis of in vivo progression mechanism of heart failure. Biochem Biophys Res Commun 307: 771-777.
4. Zhao M, Chow A, Powers J, Fajardo G, Bernstein D, (2004) Microarray analysis of gene expression after transverse aortic constriction in mice. Physiol Genomics 19: 93-105.
5. Iemitsu M, Maeda S, Miyauchi T, Matsuda M, Tanaka H, (2005) Gene expression profiling of exercise-induced cardiac hypertrophy in rats. Acta Physiol Scand 185: 259-270.
6. Galindo CL, Skinner MA, Errami M, Olson LD, Watson DA, et al. (2009) Transcriptional profile of isoproterenol-induced cardiomyopathy and comparison to exercise-induced cardiac hypertrophy and human cardiac failure. BMC Physiol 9: 23.
7. Eklund AC, Turner LR, Chen P, Jensen RV, deFeo G, et al. (2006) Replacing cRNA targets with cDNA reduces microarray cross-hybridization. Nat Biotechnol 24: 1071-1073.
8. Okoniewski MJ, Miller CJ, (2006) Hybridization interactions between probesets in short oligo microarrays lead to spurious correlations. BMC Bioinformatics 7: 276.
9. Casneuf T, Van de Peer Y, Huber W, (2007) In situ analysis of cross-hybridisation on microarrays and the inference of expression correlation. BMC Bioinformatics 8: 461.
10. Chien KR, Knowlton KU, Zhu H, Chien S, (1991) Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. Faseb J 5: 3037-3046.
11. Komuro I, Yazaki Y, (1993) Control of cardiac gene expression by mechanical stress. Annu Rev Physiol 55: 55-75.
12. McMullen JR, Shioi T, Zhang L, Tarnavski O, Sherwood MC, et al. (2003) Phosphoinositide 3-kinase(p110alpha) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy. Proc Natl Acad Sci U S A 100: 12355-12360.
13. van den Bosch BJ, Lindsey PJ, van den Burg CM, van der Vlies SA, Lips DJ, et al. (2006) Early and transient gene expression changes in pressure overload-induced cardiac hypertrophy in mice. Genomics 88: 480-488.
14. Cha H, Kim JM, Oh JG, Jeong MH, Park CS, et al. (2008) PICOT is a critical regulator of cardiac hypertrophy and cardiomyocyte contractility. J Mol Cell Cardiol 45: 796-803.
15. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
16. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y, (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509-1517.
17. Matkovich SJ, Zhang Y, Van Booven DJ, Dorn GW II, (2010) Deep mRNA sequencing for in vivo functional analysis of cardiac transcriptional regulators: application to Galphaq. Circ Res 106: 1459-1467.
18. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-208.
19. Bolte C, Zhang Y, Wang IC, Kalin TV, Molkentin JD, et al. (2011) Expression of Foxm1 transcription factor in cardiomyocytes is required for myocardial development. PLoS One 6: e22217.
20. Wontakal SN, Guo X, Will B, Shi M, Raha D, et al. (2011) A large gene network in immature erythroid cells is controlled by the myeloid and B cell transcriptional regulator PU.1. PLoS Genet 7: e1001392.
21. Bossone SA, Asselin C, Patel AJ, Marcu KB, (1992) MAZ, a zinc finger protein, binds to c-MYC and C2 gene sequences regulating transcriptional initiation and termination. Proc Natl Acad Sci U S A 89: 7452-7456.
22. DesJardins E, Hay N, (1993) Repeated CT elements bound by zinc finger proteins control the absolute and relative activities of the two principal human c-myc promoters. Mol Cell Biol 13: 5710-5724.
23. Himeda CL, Ranish JA, Hauschka SD, (2008) Quantitative proteomic identification of MAZ as a transcriptional regulator of muscle-specific genes in skeletal and cardiac myocytes. Mol Cell Biol 28: 6521-6535.
24. Johnson JM, Castle J, Garrett-Engele P, Kan Z, Loerch PM, et al. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302: 2141-2144.
25. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ, (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415.
26. Ladd AN, Charlet N, Cooper TA, (2001) The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol Cell Biol 21: 1285-1296.
27. Han J, Ding JH, Byeon CW, Kim JH, Hertel KJ, et al. (2011) SR proteins induce alternative exon skipping through their activities on the flanking constitutive exons. Mol Cell Biol 31: 793-802.
28. Yamazaki T, Walchli S, Fujita T, Ryser S, Hoshijima M, et al. (2010) Splice variants of enigma homolog, differentially expressed during heart development, promote or prevent hypertrophy. Cardiovasc Res 86: 374-382.
29. Reyes AA, Small SJ, Akeson R, (1991) At least 27 alternatively spliced forms of the neural cell adhesion molecule mRNA are expressed during rat heart development. Mol Cell Biol 11: 1654-1661.
30. Ikebe C, Ohashi K, Mizuno K, (1998) Identification of testis-specific (Limk2t) and brain-specific (Limk2c) isoforms of mouse LIM-kinase 2 gene transcripts. Biochem Biophys Res Commun 246: 307-312.
31. Henderson DM, Conner SD, (2007) A novel AAK1 splice variant functions at multiple steps of the endocytic pathway. Mol Biol Cell 18: 2698-2706.
32. Kogo H, Aiba T, Fujimoto T, (2004) Cell type-specific occurrence of caveolin-1alpha and-1beta in the lung caused by expression of distinct mRNAs. J Biol Chem 279: 25574-81.
33. Yan C, Zhao AZ, Bentley JK, Beavo JA, (1996) The calmodulin-dependent phosphodiesterase gene PDE1C encodes several functionally different splice variants in a tissue-specific manner. J Biol Chem 271: 25699-25706.
34. Hayashi Y, Ohmori S, Ito T, Seo H, (1997) A splicing variant of Steroid Receptor Coactivator-1 (SRC-1E): the major isoform of SRC-1 to mediate thyroid hormone action. Biochem Biophys Res Commun 236: 83-87.
35. Zhang M, Kimura A, Saltiel AR, (2003) Cloning and characterization of Cbl-associated protein splicing isoforms. Mol Med 9: 18-25.
36. Brown SE, Campbell RD, Sanderson CM, (2001) Novel NG36/G9a gene products encoded within the human and mouse MHC class III regions. Mamm Genome 12: 916-924.
37. Rezniczek GA, Abrahamsberg C, Fuchs P, Spazierer D, Wiche G, (2003) Plectin 5′-transcript diversity: short alternative sequences determine stability of gene products, initiation of translation and subcellular localization of isoforms. Hum Mol Genet 12: 3181-3194.
38. Lee S, Seo CH, Lim B, Yang JO, Oh J, et al. (2011) Accurate quantification of transcriptome from RNA-Seq data by effective length normalization. Nucleic Acids Res 39: e9.
39. Soncin F, Mattot V, Lionneton F, Spruyt N, Lepretre F, et al. (2003) VE-statin, an endothelial repressor of smooth muscle cell migration. Embo J 22: 5700-5711.
40. Berger R, Theodor L, Shoham J, Gokkel E, Brok-Simoni F, et al. (1996) The characterization and localization of the mouse thymopoietin/lamina-associated polypeptide 2 gene and its alternatively spliced products. Genome Res 6: 361-370.
41. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
42. Lee JH, Gao C, Peng G, Greer C, Ren S, et al. (2011) Analysis of transcriptome complexity through RNA sequencing in normal and failing murine hearts. Circ Res 109: 1332-1341.
43. Chan DW, Yu SY, Chiu PM, Yao KM, Liu VW, et al. (2008) Over-expression of FOXM1 transcription factor is associated with cervical cancer progression and pathogenesis. J Pathol 215: 245-252.
44. Ramakrishna S, Kim IM, Petrovic V, Malin D, Wang IC, et al. (2007) Myocardium defects and ventricular hypoplasia in mice homozygous null for the Forkhead Box M1 transcription factor. Dev Dyn 236: 1000-1013.
45. Fu Z, Malureanu L, Huang J, Wang W, Li H, et al. (2008) Plk1-dependent phosphorylation of FoxM1 regulates a transcriptional programme required for mitotic progression. Nat Cell Biol 10: 1076-82.
46. Brown S, McGrath MJ, Ooms LM, Gurung R, Maimone MM, et al. (1999) Characterization of two isoforms of the skeletal muscle LIM protein 1, SLIM1. Localization of SLIM1 at focal adhesions and the isoform slimmer in the nucleus of myoblasts and cytoplasm of myotubes suggests distinct roles in the cytoskeleton and in nuclear-cytoplasmic communication. J Biol Chem 274: 27083-27091.
47. Fryknäs M, Wickenberg-Bolin U, Göransson H, Gustafsson MG, Foukakis T, et al. (2006) Molecular markers for discrimination of benign and malignant follicular thyroid tumors. Tumour Biol 27: 211-220.
48. McGrath MJ, Mitchell CA, Coghill ID, Robinson PA, Brown S, (2003) Skeletal muscle LIM protein 1 (SLIM1/FHL1) induces alpha 5 beta 1-integrin-dependent myocyte elongation. Am J Physiol Cell Physiol 285: C1513-1526.
49. Davies KJ, Ermak G, Rothermel BA, Pritchard M, Heitman J, et al. (2007) Renaming the DSCR1/Adapt78 gene family as RCAN: regulators of calcineurin. FASEB J 21: 3023-3028.
50. U M, Shen L, Oshida T, Miyauchi J, Yamada M, et al. (2004) Identification of novel direct transcriptional targets of glucocorticoid receptor. Leukemia 18: 1850-1856.
51. Yang J, Rothermel B, Vega RB, Frey N, McKinsey TA, et al. (2000) Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ Res 87: E61-68.
52. Boulkroun S, Fay M, Zennaro MC, Escoubet B, Jaisser F, et al. (2002) Characterization of rat NDRG2 (N-Myc downstream regulated gene 2), a novel early mineralocorticoid-specific induced gene. J Biol Chem 277: 31506-31515.
53. Asanuma K, Kim K, Oh J, Giardino L, Chabanis S, et al. (2005) Synaptopodin regulates the actin-bundling activity of alpha-actinin in an isoform-specific manner. J Clin Invest 115: 1188-1198.
54. Trichet V, Ruault M, Roizes G, De Sario A, (2000) Characterization of the human tubulin tyrosine ligase-like 1 gene (TTLL1) mapping to 22q13.1. Gene 257: 109-117.
55. Park JY, Li W, Zheng D, Zhai P, Zhao Y, et al. (2011) Comparative analysis of mRNA isoform expression in cardiac hypertrophy and development reveals multiple post-transcriptional regulatory modules. PLoS One 6: e22391.
56. Beisvag V, Kemi OJ, Arbo I, Loennechen JP, Wisløff U, et al. (2009) Pathological and physiological hypertrophies are regulated by distinct gene programs. Eur J Cardiovasc Prev Rehabil 16: 690-697.
57. Ahuja P, Sdek P, MacLellan WR, (2007) Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 87: 521-544.
58. Damilano F, Franco I, Perrino C, Schaefer K, Azzolino O, et al. (2010) Distinct effects of leukocyte and cardiac phosphoinositide 3-kinase gamma activity in pressure overload-induced cardiac failure. Circulation 123: 391-399.
59. Arndt-Marić R, Nägele H, Schewe G, Kromminga A, (2010) Are autoantibodies against the beta1-adrenergic receptor markers for dilated cardiomyopathy? Clin Lab 56: 519-526.
60. Hong CS, Kwon SJ, Cho MC, Kwak YG, Ha KC, et al. (2008) Overexpression of junctate induces cardiac hypertrophy and arrhythmia via altered calcium handling. J Mol Cell Cardiol 44: 672-682.
61. Vencio RZ, Brentani H, Patrao DF, Pereira CA, (2004) Bayesian model accounting for within-class biological variability in Serial Analysis of Gene Expression (SAGE). BMC Bioinformatics 5: 119.
62. Dreszer TR, Karolchik D, Zweig AS, Hinrichs AS, Raney BJ, et al. (2012) The UCSC Genome Browser database: extensions and updates. Nucleic Acids Res 40: D918-23.
63. Tanaka E, Bailey T, Grant CE, Noble WS, Keich U, (2011) Improved similarity scores for comparing motifs. Bioinformatics 27: 1603-1609.
64. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS, (2007) Quantifying similarity between motifs. Genome Biol 8: R24.