MicroRNA regulation of cardiovascular development.

The transcriptional regulation of cardiovascular development requires precise spatiotemporal control of gene expression, and heterozygous mutations of transcription factors have frequently been implicated in human cardiovascular malformations. A novel mechanism involving posttranscriptional regulation by small, noncoding microRNAs (miRNAs) has emerged as a central regulator of many cardiogenic processes. We are beginning to understand the functions that miRNAs play during essential biological processes, such as cell proliferation, differentiation, apoptosis, stress response, and tumorigenesis. The identification of miRNAs expressed in specific cardiac and vascular cell types has led to the discovery of important regulatory roles for these small RNAs during cardiomyocyte differentiation, cell cycle, conduction, vessel formation, and during stages of cardiac hypertrophy in the adult. Here, we overview the recent findings on miRNA regulation in cardiovascular development and report the latest advances in understanding their function by unveiling their mRNA targets. Further analysis of miRNA function during cardiovascular development will allow us to determine the potential for novel miRNA-based therapeutic strategies.

[1]  D. Srivastava,et al.  MicroRNAs: Opening a New Vein in Angiogenesis Research , 2009, Science Signaling.

[2]  E. Olson,et al.  microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. , 2008, Genes & development.

[3]  D. Srivastava,et al.  microRNA-138 modulates cardiac patterning during embryonic development , 2008, Proceedings of the National Academy of Sciences.

[4]  Y. Pinto,et al.  Conditional Dicer Gene Deletion in the Postnatal Myocardium Provokes Spontaneous Cardiac Remodeling , 2008, Circulation.

[5]  Ru-Fang Yeh,et al.  miR-126 regulates angiogenic signaling and vascular integrity. , 2008, Developmental cell.

[6]  John McAnally,et al.  The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. , 2008, Developmental cell.

[7]  Ju Chen,et al.  A myocardial lineage derives from Tbx18 epicardial cells , 2008, Nature.

[8]  Guson Kang,et al.  Foxn4 directly regulates tbx2b expression and atrioventricular canal formation. , 2008, Genes & development.

[9]  R. Yeh,et al.  MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. , 2008, Cell stem cell.

[10]  Chaoqian Xu,et al.  The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2 , 2011, Nature Medicine.

[11]  E. Olson,et al.  An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133 , 2007, Proceedings of the National Academy of Sciences.

[12]  J. Männer,et al.  Epicardium-derived progenitor cells require β-catenin for coronary artery formation , 2007, Proceedings of the National Academy of Sciences.

[13]  Tsung-Cheng Chang,et al.  Human TOB, an Antiproliferative Transcription Factor, Is a Poly(A)-Binding Protein-Dependent Positive Regulator of Cytoplasmic mRNA Deadenylation , 2007, Molecular and Cellular Biology.

[14]  Chaoqian Xu,et al.  The muscle-specific microRNAs miR-1 and miR-133 produce opposing effects on apoptosis by targeting HSP60, HSP70 and caspase-9 in cardiomyocytes , 2007, Journal of Cell Science.

[15]  Jiening Xiao,et al.  Retracted: Transcriptional activation by stimulating protein 1 and post‐transcriptional repression by muscle‐specific microRNAs of IKs‐encoding genes and potential implications in regional heterogeneity of their expressions , 2007, Journal of cellular physiology.

[16]  Wei Yan,et al.  Tissue-dependent paired expression of miRNAs , 2007, Nucleic acids research.

[17]  D. Bartel,et al.  Intronic microRNA precursors that bypass Drosha processing , 2007, Nature.

[18]  L. Lim,et al.  A microRNA component of the p53 tumour suppressor network , 2007, Nature.

[19]  K. Chaudhuri,et al.  MicroRNA detection and target prediction: integration of computational and experimental approaches. , 2007, DNA and cell biology.

[20]  Anindya Dutta,et al.  The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. , 2007, Genes & development.

[21]  Xiaoxia Qi,et al.  Control of Stress-Dependent Cardiac Growth and Gene Expression by a MicroRNA , 2007, Science.

[22]  Michael T. McManus,et al.  Dysregulation of Cardiogenesis, Cardiac Conduction, and Cell Cycle in Mice Lacking miRNA-1-2 , 2007, Cell.

[23]  Yong Zhao,et al.  A developmental view of microRNA function. , 2007, Trends in biochemical sciences.

[24]  Thomas Thum,et al.  MicroRNAs in the Human Heart: A Clue to Fetal Gene Reprogramming in Heart Failure , 2007, Circulation.

[25]  D. Srivastava,et al.  The genetics of cardiac birth defects. , 2007, Seminars in cell & developmental biology.

[26]  B. Davidson,et al.  RNA polymerase III transcribes human microRNAs , 2006, Nature Structural &Molecular Biology.

[27]  A. Fischer,et al.  Developmental patterning of the cardiac atrioventricular canal by Notch and Hairy-related transcription factors , 2006, Development.

[28]  A. Hatzigeorgiou,et al.  A guide through present computational approaches for the identification of mammalian microRNA targets , 2006, Nature Methods.

[29]  D. Srivastava Making or Breaking the Heart: From Lineage Determination to Morphogenesis , 2006, Cell.

[30]  Takuya Yamazaki,et al.  Prognostic Significance of Quantitative Qrs Duration , 2022 .

[31]  Harvey F Lodish,et al.  Myogenic factors that regulate expression of muscle-specific microRNAs. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  N. Rajewsky microRNA target predictions in animals , 2006, Nature Genetics.

[33]  Jian-Fu Chen,et al.  The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation , 2006, Nature Genetics.

[34]  Byoung-Tak Zhang,et al.  miTarget: microRNA target gene prediction using a support vector machine , 2006, BMC Bioinformatics.

[35]  Zhe Han,et al.  MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  R. Russell,et al.  Animal MicroRNAs Confer Robustness to Gene Expression and Have a Significant Impact on 3′UTR Evolution , 2005, Cell.

[37]  R. Shiekhattar,et al.  Human RISC Couples MicroRNA Biogenesis and Posttranscriptional Gene Silencing , 2005, Cell.

[38]  M. Buckingham,et al.  Building the mammalian heart from two sources of myocardial cells , 2005, Nature Reviews Genetics.

[39]  Phillip D Zamore,et al.  microPrimer: the biogenesis and function of microRNA , 2005, Development.

[40]  B. Bruneau,et al.  The Homeodomain Transcription Factor Irx5 Establishes the Mouse Cardiac Ventricular Repolarization Gradient , 2005, Cell.

[41]  V. Ambros,et al.  Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. , 2005, Genes & development.

[42]  Oliver H. Tam,et al.  Characterization of Dicer-deficient murine embryonic stem cells. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Yong Zhao,et al.  Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis , 2005, Nature.

[44]  Gregory J. Hannon,et al.  MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies , 2005, Nature Cell Biology.

[45]  Anton J. Enright,et al.  Materials and Methods Figs. S1 to S4 Tables S1 to S5 References and Notes Micrornas Regulate Brain Morphogenesis in Zebrafish , 2022 .

[46]  Shridar Ganesan,et al.  Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. , 2005, Genes & development.

[47]  R. Russell,et al.  Principles of MicroRNA–Target Recognition , 2005, PLoS biology.

[48]  C. Burge,et al.  Conserved Seed Pairing, Often Flanked by Adenosines, Indicates that Thousands of Human Genes are MicroRNA Targets , 2005, Cell.

[49]  Robert B. Russell,et al.  Principles of MicroRNATarget Recognition , 2005 .

[50]  T. Tuschl,et al.  The Human DiGeorge Syndrome Critical Region Gene 8 and Its D. melanogaster Homolog Are Required for miRNA Biogenesis , 2004, Current Biology.

[51]  B. Cullen,et al.  Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. , 2004, RNA.

[52]  V. Ambros The functions of animal microRNAs , 2004, Nature.

[53]  John G Doench,et al.  Specificity of microRNA target selection in translational repression. , 2004, Genes & development.

[54]  K. Czaplinski,et al.  Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. , 2004, RNA.

[55]  B. Cullen,et al.  Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. , 2004, Nucleic acids research.

[56]  T. Du,et al.  Asymmetry in the Assembly of the RNAi Enzyme Complex , 2003, Cell.

[57]  S. Jayasena,et al.  Functional siRNAs and miRNAs Exhibit Strand Bias , 2003, Cell.

[58]  Edwin Cuppen,et al.  The microRNA-producing enzyme Dicer1 is essential for zebrafish development , 2003, Nature Genetics.

[59]  S. Elledge,et al.  Dicer is essential for mouse development , 2003, Nature Genetics.

[60]  J. Miano,et al.  Serum response factor: toggling between disparate programs of gene expression. , 2003, Journal of molecular and cellular cardiology.

[61]  Cheol‐Hee Kim,et al.  Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. , 2003, Developmental cell.

[62]  J. Hoffman,et al.  The incidence of congenital heart disease. , 2002, Journal of the American College of Cardiology.

[63]  R. Schwartz,et al.  Embryonic expression of an Nkx2‐5/Cre gene using ROSA26 reporter mice , 2001, Genesis.

[64]  D. Srivastava,et al.  The combinatorial activities of Nkx2.5 and dHAND are essential for cardiac ventricle formation. , 2001, Developmental biology.

[65]  V. Ambros,et al.  An Extensive Class of Small RNAs in Caenorhabditis elegans , 2001, Science.

[66]  D. Corrado,et al.  Dispersion of Ventricular Depolarization-Repolarization: A Noninvasive Marker for Risk Stratification in Arrhythmogenic Right Ventricular Cardiomyopathy , 2001, Circulation.

[67]  B. Reinhart,et al.  Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA , 2000, Nature.

[68]  B. Reinhart,et al.  The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans , 2000, Nature.

[69]  S. Artavanis-Tsakonas,et al.  Notch Signaling : Cell Fate Control and Signal Integration in Development , 1999 .

[70]  D. Srivastava,et al.  The bHLH factors, dHAND and eHAND, specify pulmonary and systemic cardiac ventricles independent of left-right sidedness. , 1998, Developmental biology.

[71]  D. Srivastava,et al.  Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND , 1997, Nature Genetics.

[72]  Erratum: Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND , 1997, Nature Genetics.

[73]  M. Kirby,et al.  Neural crest and cardiovascular patterning. , 1995, Circulation research.

[74]  G. Lyons,et al.  Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. , 1994, Development.

[75]  G. Ruvkun,et al.  Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans , 1993, Cell.

[76]  V. Ambros,et al.  The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 , 1993, Cell.