Abstract
Long noncoding RNAs (LncRNAs) have emerged as a diverse class of functional molecules that contribute to nearly every facet of mammalian cardiac development and disease. Recent examples show that lncRNAs can be important co-regulators of cardiac patterning and morphogenesis and modulators of the pathogenic signaling that drives heart disease. The flexibility and chemical nature of RNA allows lncRNAs to utilize diverse mechanisms, mediating their effects through their sequence, structure, and molecular interactions with DNA, protein, and other RNAs. In vivo, i.e., animal, studies of individual lncRNAs highlight their ability to balance conserved cardiac gene expression networks, serve as specific and early biomarkers, and indicate their promise as useful therapeutic targets to treat human heart disease. Here, we review recent functionally characterized lncRNAs in cardiac biology and pathology and provide a perspective on emerging approaches to decipher the role of lncRNAs in the heart.
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References
Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, Cox DB, Shmakov S, Makarova KS, Semenova E, Minakhin L, Severinov K, Regev A, Lander ES, Koonin EV, Zhang F (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science. https://doi.org/10.1126/science.aaf5573
Abudayyeh OO, Gootenberg JS, Essletzbichler P, Han S, Joung J, Belanto JJ, Verdine V, Cox DBT, Kellner MJ, Regev A, Lander ES, Voytas DF, Ting AY, Zhang F (2017) RNA targeting with CRISPR-Cas13. Nature 550:280–284
Akazawa H, Komuro I (2003) Roles of cardiac transcription factors in cardiac hypertrophy. Circ Res 92:1079–1088
Alexanian M, Ounzain S (2020) Long noncoding RNAs in cardiac development. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a037374
Alexanian M, Maric D, Jenkinson SP, Mina M, Friedman CE, Ting CC, Micheletti R, Plaisance I, Nemir M, Maison D, Kernen J, Pezzuto I, Villeneuve D, Burdet F, Ibberson M, Leib SL, Palpant NJ, Hernandez N, Ounzain S, Pedrazzini T (2017) A transcribed enhancer dictates mesendoderm specification in pluripotency. Nat Commun 8:1806
Anderson DM, Arredondo J, Hahn K, Valente G, Martin JF, Wilson-Rawls J, Rawls A (2006) Mohawk is a novel homeobox gene expressed in the developing mouse embryo. Dev Dyn 235:792–801
Anderson DM, Anderson KM, Chang CL, Makarewich CA, Nelson BR, McAnally JR, Kasaragod P, Shelton JM, Liou J, Bassel-Duby R, Olson EN (2015) A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 160:595–606
Anderson DM, Cannavino J, Li H, Anderson KM, Nelson BR, McAnally J, Bezprozvannaya S, Liu Y, Lin W, Liu N, Bassel-Duby R, Olson EN (2016a) Severe muscle wasting and denervation in mice lacking the RNA-binding protein ZFP106. Proc Natl Acad Sci USA 113:E4494-4503
Anderson DM, Makarewich CA, Anderson KM, Shelton JM, Bezprozvannaya S, Bassel-Duby R, Olson EN (2016) Widespread control of calcium signaling by a family of SERCA-inhibiting micropeptides. Sci Signal. https://doi.org/10.1126/scisignal.aaj1460
Anderson KM, Anderson DM, McAnally JR, Shelton JM, Bassel-Duby R, Olson EN (2016c) Transcription of the non-coding RNA upperhand controls Hand2 expression and heart development. Nature 539:433–436
Anderson DM, Anderson KM, Nelson BR, McAnally JR, Bezprozvannaya S, Shelton JM, Bassel-Duby R, Olson EN (2021) A myocardin-adjacent lncRNA balances SRF-dependent gene transcription in the heart. Genes Dev 35:835–840
Anderson KM, Poosala P, Lindley SR, Anderson DM (2019) Targeted Cleavage and Polyadenylation of RNA by CRISPR-Cas13. bioRxiv 531111; https://doi.org/10.1101/531111
Aznaourova M, Schmerer N, Schmeck B, Schulte LN (2020) Disease-causing mutations and rearrangements in long non-coding RNA gene loci. Front Genet 11:527484
Bennett M, Ulitsky I, Alloza I, Vandenbroeck K, Miscianinov V, Mahmoud AD, Ballantyne M, Rodor J, Baker AH (2021) Novel transcript discovery expands the repertoire of pathologically-associated, long non-coding RNAs in vascular smooth muscle cells. Int J Mol Sci. https://doi.org/10.3390/ijms22031484
Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927
Cai X, Zhang P, Wang S, Hong L, Yu S, Li B, Zeng H, Yang X, Shao L (2020) lncRNA FGD5 antisense RNA 1 upregulates RORA to suppress hypoxic injury of human cardiomyocyte cells by inhibiting oxidative stress and apoptosis via miR195. Mol Med Rep 22:4579–4588
Castello A, Fischer B, Frese CK, Horos R, Alleaume AM, Foehr S, Curk T, Krijgsveld J, Hentze MW (2016) Comprehensive identification of RNA-binding domains in human cells. Mol Cell 63:696–710
Chen B, Deng S, Ge T, Ye M, Yu J, Lin S, Ma W, Songyang Z (2020a) Live cell imaging and proteomic profiling of endogenous NEAT1 lncRNA by CRISPR/Cas9-mediated knock-in. Protein Cell 11:641–660
Chen H, Liu J, Wang B, Li Y (2020b) Protective effect of lncRNA CRNDE on myocardial cell apoptosis in heart failure by regulating HMGB1 cytoplasm translocation through PARP-1. Arch Pharm Res 43:1325–1334
Chen S, Wu Y, Qin X, Wen P, Liu J, Yang M (2021) Global gene expression analysis using RNA-seq reveals the new roles of Panax notoginseng Saponins in ischemic cardiomyocytes. J Ethnopharmacol 268:113639
Cheng X, Jiang H (2019) Long non-coding RNA HAND2-AS1 downregulation predicts poor survival of patients with end-stage dilated cardiomyopathy. J Int Med Res 47:3690–3698
Chu C, Quinn J, Chang HY (2012) Chromatin isolation by RNA purification (ChIRP). JoVE. https://doi.org/10.3791/3912
Correia M, Bernardes de Jesus B, Nobrega-Pereira S (2021) Novel insights linking lncRNAs and metabolism with implications for cardiac regeneration. Front Physiol 12:586927
Cox DBT, Gootenberg JS, Abudayyeh OO, Franklin B, Kellner MJ, Joung J, Zhang F (2017) RNA editing with CRISPR-Cas13. Science 358:1019–1027
Denzler R, Agarwal V, Stefano J, Bartel DP, Stoffel M (2014) Assessing the ceRNA hypothesis with quantitative measurements of miRNA and target abundance. Mol Cell 54:766–776
Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789
Dong X, Dong X, Gao F, Liu N, Liang T, Zhang F, Fu X, Pu L, Chen J (2021) Non-coding RNAs in cardiomyocyte proliferation and cardiac regeneration: Dissecting their therapeutic values. J Cell Mol Med 25:2315–2332
East-Seletsky A, O’Connell MR, Burstein D, Knott GJ, Doudna JA (2017) RNA targeting by functionally orthogonal type VI-A CRISPR-Cas enzymes. Molecular cell 66:373-383 e373
Fan J, Li H, Xie R, Zhang X, Nie X, Shi X, Zhan J, Yin Z, Zhao Y, Dai B, Yuan S, Wen Z, Chen C, Wang DW (2021) LncRNA ZNF593-AS alleviates contractile dysfunction in dilated cardiomyopathy. Circ Res. https://doi.org/10.1161/CIRCRESAHA.120.318437
Fang Y, Xu Y, Wang R, Hu L, Guo D, Xue F, Guo W, Zhang D, Hu J, Li Y, Zhang W, Zhang M (2020) Recent advances on the roles of LncRNAs in cardiovascular disease. J Cell Mol Med 24:12246–12257
Gao L, Liu Y, Guo S, Yao R, Wu L, Xiao L, Wang Z, Liu Y, Zhang Y (2017) Circulating long noncoding RNA HOTAIR is an essential mediator of acute myocardial infarction. Cell Physiol Biochem 44:1497–1508
George MR, Duan Q, Nagle A, Kathiriya IS, Huang Y, Rao K, Haldar SM, Bruneau BG (2019) Minimal in vivo requirements for developmentally regulated cardiac long intergenic non-coding RNAs. Development. https://doi.org/10.1242/dev.185314
Gong C, Maquat LE (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3’ UTRs via Alu elements. Nature 470:284–288
Gong C, Maquat LE (2015) Affinity purification of long noncoding RNA-protein complexes from formaldehyde cross-linked mammalian cells. Methods Mol Biol 1206:81–86
Grote P, Wittler L, Hendrix D, Koch F, Wahrisch S, Beisaw A, Macura K, Blass G, Kellis M, Werber M, Herrmann BG (2013) The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell 24:206–214
Ha H, Song J, Wang S, Kapusta A, Feschotte C, Chen KC, Xing J (2014) A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements. BMC Genomics 15:545
Han P, Li W, Lin CH, Yang J, Shang C, Nuernberg ST, Jin KK, Xu W, Lin CY, Lin CJ, Xiong Y, Chien H, Zhou B, Ashley E, Bernstein D, Chen PS, Chen HV, Quertermous T, Chang CP (2014) A long noncoding RNA protects the heart from pathological hypertrophy. Nature 514:102–106
Han X, Luo S, Peng G, Lu JY, Cui G, Liu L, Yan P, Yin Y, Liu W, Wang R, Zhang J, Ai S, Chang Z, Na J, He A, Jing N, Shen X (2018) Mouse knockout models reveal largely dispensable but context-dependent functions of lncRNAs during development. J Mol Cell Biol 10:175–178
He J, Ma X (2021) Interaction between LncRNA and UPF1 in tumors. Front Genet 12:624905
Hentze MW, Castello A, Schwarzl T, Preiss T (2018) A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol 19:327–341
Hezroni H, Koppstein D, Schwartz MG, Avrutin A, Bartel DP, Ulitsky I (2015) Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species. Cell Rep 11:1110–1122
Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA (2009) Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci USA 106:9362–9367
Hori Y, Tanimoto Y, Takahashi S, Furukawa T, Koshiba-Takeuchi K, Takeuchi JK (2018) Important cardiac transcription factor genes are accompanied by bidirectional long non-coding RNAs. BMC Genomics 19:967
Huang L, Ding Y, Yang L, Jiang X, Xia Z, You Z (2021) The effect of LncRNA SNHG16 on vascular smooth muscle cells in CHD by targeting miRNA-218-5p. Exp Mol Pathol 118:104595
Ishii N, Ozaki K, Sato H, Mizuno H, Susumu S, Takahashi A, Miyamoto Y, Ikegawa S, Kamatani N, Hori M, Satoshi S, Nakamura Y, Tanaka T (2006) Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J Hum Genet 51:1087–1099
Jusic A, Devaux Y, Action EU-CC (2020) Mitochondrial noncoding RNA-regulatory network in cardiovascular disease. Basic Res Cardiol 115:23
Kang X, Zhao Y, Van Arsdell G, Nelson SF, Touma M (2020) Ppp1r1b-lncRNA inhibits PRC2 at myogenic regulatory genes to promote cardiac and skeletal muscle development in mouse and human. RNA 26:481–491
Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, Rinn JL (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA 106:11667–11672
Klattenhoff CA, Scheuermann JC, Surface LE, Bradley RK, Fields PA, Steinhauser ML, Ding H, Butty VL, Torrey L, Haas S, Abo R, Tabebordbar M, Lee RT, Burge CB, Boyer LA (2013) Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 152:570–583
Konermann S, Lotfy P, Brideau NJ, Oki J, Shokhirev MN, Hsu PD (2018) Transcriptome engineering with RNA-targeting type VI-D CRISPR effectors. Cell 173:665-676 e614
Kumarswamy R, Bauters C, Volkmann I, Maury F, Fetisch J, Holzmann A, Lemesle G, de Groote P, Pinet F, Thum T (2014) Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ Res 114:1569–1575
Kurian L, Aguirre A, Sancho-Martinez I, Benner C, Hishida T, Nguyen TB, Reddy P, Nivet E, Krause MN, Nelles DA, Esteban CR, Campistol JM, Yeo GW, Belmonte JCI (2015) Identification of novel long noncoding RNAs underlying vertebrate cardiovascular development. Circulation 131:1278–1290
Kurreck J (2003) Antisense technologies. Improvement through novel chemical modifications. Eur J Biochem 270:1628–1644
La Greca A, Scarafia MA, Hernandez Canas MC, Perez N, Castaneda S, Colli C, Mobbs AM, Santin Velazque NL, Neiman G, Garate X, Aban C, Waisman A, Moro LN, Sevlever G, Luzzani C, Miriuka SG (2020) PIWI-interacting RNAs are differentially expressed during cardiac differentiation of human pluripotent stem cells. PloS one 15:e0232715
Latif S, Masino A, Garry DJ (2006) Transcriptional pathways direct cardiac development and regeneration. Trends Cardiovasc Med 16:234–240
Lee JH, Gao C, Peng G, Greer C, Ren S, Wang Y, Xiao X (2011) Analysis of transcriptome complexity through RNA sequencing in normal and failing murine hearts. Circ Res 109:1332–1341
Li B, Hu Y, Li X, Jin G, Chen X, Chen G, Chen Y, Huang S, Liao W, Liao Y, Teng Z, Bin J (2018) Sirt1 antisense long noncoding RNA promotes cardiomyocyte proliferation by enhancing the stability of Sirt1. J Am Heart Assoc 7:e009700
Liu N, Olson EN (2010) MicroRNA regulatory networks in cardiovascular development. Dev Cell 18:510–525
Liu S, Zhu J, Jiang T, Zhong Y, Tie Y, Wu Y, Zheng X, Jin Y, Fu H (2015) Identification of lncRNA MEG3 binding protein using MS2-Tagged RNA affinity purification and mass spectrometry. Appl Biochem Biotechnol 176:1834–1845
Liu S, Yang G, Huang Y, Zhang C, Jin H (2021) Predictive value of LncRNA on coronary restenosis after percutaneous coronary intervention in patients with coronary heart disease: A protocol for systematic review and meta-analysis. Medicine (Baltimore) 100:e24114
Lucas BA, Lavi E, Shiue L, Cho H, Katzman S, Miyoshi K, Siomi MC, Carmel L, Ares M Jr, Maquat LE (2018) Evidence for convergent evolution of SINE-directed Staufen-mediated mRNA decay. Proc Natl Acad Sci USA 115:968–973
Luo B, He Z, Huang S, Wang J, Han D, Xue H, Liu P, Zeng X, Lu D (2020) Long non-coding RNA 554 promotes cardiac fibrosis via TGF-beta1 pathway in mice following myocardial infarction. Front Pharmacol 11:585680
Luo S, Zhang M, Wu H, Ding X, Li D, Dong X, Hu X, Su S, Shang W, Wu J, Xiao H, Yang W, Zhang Q, Zhang J, Lu Y, Pan Z (2021) SAIL: a new conserved anti-fibrotic lncRNA in the heart. Basic Res Cardiol 116:15
Makarewich CA, Munir AZ, Schiattarella GG, Bezprozvannaya S, Raguimova ON, Cho EE, Vidal AH, Robia SL, Bassel-Duby R, Olson EN (2018) The DWORF micropeptide enhances contractility and prevents heart failure in a mouse model of dilated cardiomyopathy. Elife. https://doi.org/10.7554/eLife.38319
Matkovich SJ, Edwards JR, Grossenheider TC, de Guzman SC, Dorn GW 2nd (2014) Epigenetic coordination of embryonic heart transcription by dynamically regulated long noncoding RNAs. Proc Natl Acad Sci USA 111:12264–12269
Mester-Tonczar J, Hasimbegovic E, Spannbauer A, Traxler D, Kastner N, Zlabinger K, Einzinger P, Pavo N, Goliasch G, Gyongyosi M (2020) Circular RNAs in cardiac regeneration: cardiac cell proliferation, differentiation, survival, and reprogramming. Front Physiol 11:580465
Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, Zeller U, Baker JC, Grutzner F, Kaessmann H (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505:635–640
Nelson BR, Makarewich CA, Anderson DM, Winders BR, Troupes CD, Wu F, Reese AL, McAnally JR, Chen X, Kavalali ET, Cannon SC, Houser SR, Bassel-Duby R, Olson EN (2016) A peptide encoded by a transcript annotated as long noncoding RNA enhances SERCA activity in muscle. Science 351:271–275
Niu L, Lou F, Sun Y, Sun L, Cai X, Liu Z, Zhou H, Wang H, Wang Z, Bai J, Yin Q, Zhang J, Chen L, Peng D, Xu Z, Gao Y, Tang S, Fan L, Wang H (2020) A micropeptide encoded by lncRNA MIR155HG suppresses autoimmune inflammation via modulating antigen presentation. Sci Adv. https://doi.org/10.1126/sciadv.aaz2059
O’Connell MR (2019) Molecular mechanisms of RNA targeting by cas13-containing Type VI CRISPR-cas systems. J Mol Biol 431:66–87
Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, Yamanaka I, Kiyosawa H, Yagi K, Tomaru Y, Hasegawa Y, Nogami A, Schonbach C, Gojobori T, Baldarelli R, Hill DP, Bult C, Hume DA, Quackenbush J, Schriml LM, Kanapin A, Matsuda H, Batalov S, Beisel KW, Blake JA, Bradt D, Brusic V, Chothia C, Corbani LE, Cousins S, Dalla E, Dragani TA, Fletcher CF, Forrest A, Frazer KS, Gaasterland T, Gariboldi M, Gissi C, Godzik A, Gough J, Grimmond S, Gustincich S, Hirokawa N, Jackson IJ, Jarvis ED, Kanai A, Kawaji H, Kawasawa Y, Kedzierski RM, King BL, Konagaya A, Kurochkin IV, Lee Y, Lenhard B, Lyons PA, Maglott DR, Maltais L, Marchionni L, McKenzie L, Miki H, Nagashima T, Numata K, Okido T, Pavan WJ, Pertea G, Pesole G, Petrovsky N, Pillai R, Pontius JU, Qi D, Ramachandran S, Ravasi T, Reed JC, Reed DJ, Reid J, Ring BZ, Ringwald M, Sandelin A, Schneider C, Semple CA, Setou M, Shimada K, Sultana R, Takenaka Y, Taylor MS, Teasdale RD, Tomita M, Verardo R, Wagner L, Wahlestedt C, Wang Y, Watanabe Y, Wells C, Wilming LG, Wynshaw-Boris A, Yanagisawa M, Yang I, Yang L, Yuan Z, Zavolan M, Zhu Y, Zimmer A, Carninci P, Hayatsu N, Hirozane-Kishikawa T, Konno H, Nakamura M, Sakazume N, Sato K, Shiraki T, Waki K, Kawai J, Aizawa K, Arakawa T, Fukuda S, Hara A, Hashizume W, Imotani K, Ishii Y, Itoh M, Kagawa I, Miyazaki A, Sakai K, Sasaki D, Shibata K, Shinagawa A, Yasunishi A, Yoshino M, Waterston R, Lander ES, Rogers J, Birney E, Hayashizaki Y, Consortium F, I RGERGP, Team II (2002) Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420:563–573
Ounzain S, Micheletti R, Arnan C, Plaisance I, Cecchi D, Schroen B, Reverter F, Alexanian M, Gonzales C, Ng SY, Bussotti G, Pezzuto I, Notredame C, Heymans S, Guigo R, Johnson R, Pedrazzini T (2015) CARMEN, a human super enhancer-associated long noncoding RNA controlling cardiac specification, differentiation and homeostasis. J Mol Cell Cardiol 89:98–112
Padula SL, Velayutham N, Yutzey KE (2021) Transcriptional regulation of postnatal cardiomyocyte maturation and regeneration. Int J Mol Sci. https://doi.org/10.3390/ijms22063288
Paradis AN, Gay MS, Zhang L (2014) Binucleation of cardiomyocytes: the transition from a proliferative to a terminally differentiated state. Drug Discov Today 19:602–609
Patterson M, Barske L, Van Handel B, Rau CD, Gan P, Sharma A, Parikh S, Denholtz M, Huang Y, Yamaguchi Y, Shen H, Allayee H, Crump JG, Force TI, Lien CL, Makita T, Lusis AJ, Kumar SR, Sucov HM (2017) Frequency of mononuclear diploid cardiomyocytes underlies natural variation in heart regeneration. Nat Genet 49:1346–1353
Prummel KD, Nieuwenhuize S, Mosimann C (2020) The lateral plate mesoderm. Development. https://doi.org/10.1242/dev.175059
Quiat D, Olson EN (2013) MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment. J Clin Investig 123:11–18
Rajan KS, Velmurugan G, Pandi G, Ramasamy S (2014) miRNA and piRNA mediated Akt pathway in heart: antisense expands to survive. Int J Biochem Cell Biol 55:153–156
Ritter N, Ali T, Kopitchinski N, Schuster P, Beisaw A, Hendrix DA, Schulz MH, Muller-McNicoll M, Dimmeler S, Grote P (2019) The lncRNA locus handsdown regulates cardiac gene programs and is essential for early mouse development. Dev Cell 50:644-657 e648
Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell 146:353–358
Santos F, Correia M, Nobrega-Pereira S, Bernardes de Jesus B (2020) Age-Related Pathways in Cardiac Regeneration: A Role for lncRNAs? Front Physiol 11:583191
Sauvageau M, Goff LA, Lodato S, Bonev B, Groff AF, Gerhardinger C, Sanchez-Gomez DB, Hacisuleyman E, Li E, Spence M, Liapis SC, Mallard W, Morse M, Swerdel MR, D’Ecclessis MF, Moore JC, Lai V, Gong G, Yancopoulos GD, Frendewey D, Kellis M, Hart RP, Valenzuela DM, Arlotta P, Rinn JL (2013) Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife 2:e01749
Shrivastava A, Haase T, Zeller T, Schulte C (2020) Biomarkers for heart failure prognosis: proteins, genetic scores and non-coding RNAs. Front Cardiovasc Med 7:601364
Singh S, Nguyen HC, Ehsan M, Michels DCR, Singh P, Qadura M, Singh KK (2021) Pravastatin-induced changes in expression of long non-coding and coding RNAs in endothelial cells. Physiol Rep 9:e14661
Small EM, Olson EN (2011) Pervasive roles of microRNAs in cardiovascular biology. Nature 469:336–342
Song J, Kim YK (2020) Discovery and functional prediction of long non-coding RNAs common to ischemic stroke and myocardial infarction. J Lipid Atheroscler 9:449–459
Spiroski AM, Sanders R, Meloni M, McCracken IR, Thomson A, Brittan M, Gray GA, Baker AH (2021) The influence of the LINC00961/SPAAR locus loss on murine development, myocardial dynamics, and cardiac response to myocardial infarction. Int J Mol Sci. https://doi.org/10.3390/ijms22020969
Ulitsky I (2018) Interactions between short and long noncoding RNAs. FEBS Lett 592:2874–2883
Vance KW (2017) Mapping long noncoding RNA chromatin occupancy using capture hybridization analysis of RNA targets (CHART). Methods Mol Biol 1468:39–50
Vella S, Gallo A, Lo Nigro A, Galvagno D, Raffa GM, Pilato M, Conaldi PG (2016) PIWI-interacting RNA (piRNA) signatures in human cardiac progenitor cells. Int J Biochem Cell Biol 76:1–11
Viereck J, Kumarswamy R, Foinquinos A, Xiao K, Avramopoulos P, Kunz M, Dittrich M, Maetzig T, Zimmer K, Remke J, Just A, Fendrich J, Scherf K, Bolesani E, Schambach A, Weidemann F, Zweigerdt R, de Windt LJ, Engelhardt S, Dandekar T, Batkai S, Thum T (2016) Long noncoding RNA Chast promotes cardiac remodeling. Sci Transl Med 8:326ra322
Wamstad JA, Alexander JM, Truty RM, Shrikumar A, Li F, Eilertson KE, Ding H, Wylie JN, Pico AR, Capra JA, Erwin G, Kattman SJ, Keller GM, Srivastava D, Levine SS, Pollard KS, Holloway AK, Boyer LA, Bruneau BG (2012) Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 151:206–220
Wang L, Zhang J (2020) Exosomal lncRNA AK139128 derived from hypoxic cardiomyocytes promotes apoptosis and inhibits cell proliferation in cardiac fibroblasts. Int J Nanomedicine 15:3363–3376
Wang J, Gong C, Maquat LE (2013) Control of myogenesis by rodent SINE-containing lncRNAs. Genes Dev 27:793–804
Wang K, Liu F, Zhou LY, Long B, Yuan SM, Wang Y, Liu CY, Sun T, Zhang XJ, Li PF (2014) The long noncoding RNA CHRF regulates cardiac hypertrophy by targeting miR-489. Circ Res 114:1377–1388
Wang Z, Zhang XJ, Ji YX, Zhang P, Deng KQ, Gong J, Ren S, Wang X, Chen I, Wang H, Gao C, Yokota T, Ang YS, Li S, Cass A, Vondriska TM, Li G, Deb A, Srivastava D, Yang HT, Xiao X, Li H, Wang Y (2016) The long noncoding RNA Chaer defines an epigenetic checkpoint in cardiac hypertrophy. Nat Med 22:1131–1139
Washietl S, Kellis M, Garber M (2014) Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res 24:616–628
White JK, Gerdin AK, Karp NA, Ryder E, Buljan M, Bussell JN, Salisbury J, Clare S, Ingham NJ, Podrini C, Houghton R, Estabel J, Bottomley JR, Melvin DG, Sunter D, Adams NC, Sanger Institute Mouse Genetics P, Tannahill D, Logan DW, Macarthur DG, Flint J, Mahajan VB, Tsang SH, Smyth I, Watt FM, Skarnes WC, Dougan G, Adams DJ, Ramirez-Solis R, Bradley A, Steel KP (2013) Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 154:452–464
Xu H, Zhang X, Yu K, Zhang G, Shi Y, Jiang Y (2020) Analysis on the expression and prognostic value of LncRNA FAF in patients with coronary heart disease. Biomed Res Int 2020:9471329
Ye M, Zhang J, Wei M, Liu B, Dong K (2020) Emerging role of long noncoding RNA-encoded micropeptides in cancer. Cancer Cell Int 20:506
Zhang F, Lupski JR (2015) Non-coding genetic variants in human disease. Hum Mol Genet 24:R102-110
Zhang Y, Du W, Yang B (2019) Long non-coding RNAs as new regulators of cardiac electrophysiology and arrhythmias: Molecular mechanisms, therapeutic implications and challenges. Pharmacol Ther 203:107389
Zhang F, Fu X, Kataoka M, Liu N, Wang Y, Gao F, Liang T, Dong X, Pei J, Hu X, Zhu W, Yu H, Cowan DB, Hu X, Huang ZP, Wang J, Wang DZ, Chen J (2021a) Long noncoding RNA Cfast regulates cardiac fibrosis. Mol Ther Nucleic Acids 23:377–392
Zhang Y, Zhang X, Cai B, Li Y, Jiang Y, Fu X, Zhao Y, Gao H, Yang Y, Yang J, Li S, Wu H, Jin X, Xue G, Yang J, Ma W, Han Q, Tian T, Li Y, Yang B, Lu Y, Pan Z (2021b) The long noncoding RNA lncCIRBIL disrupts the nuclear translocation of Bclaf1 alleviating cardiac ischemia-reperfusion injury. Nat Commun 12:522
Zhao J, Hyman L, Moore C (1999) Formation of mRNA 3’ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63:405–445
Zhao C, Li G, Li J (2020) Non-coding RNAs and cardiac aging. Adv Exp Med Biol 1229:247–258
Zhao P, Wang Y, Zhang L, Zhang J, Liu N, Wang H (2021) Mechanism of long noncoding RNA metastasisassociated lung adenocarcinoma transcript 1 in lipid metabolism and inflammation in heart failure. Int J Mol Med. https://doi.org/10.3892/ijmm.2020.4838
Zhao Z, Liu G, Zhang H, Ruan P, Ge J, Liu Q (2021b) BIRC5, GAJ5, and lncRNA NPHP3-AS1 are correlated with the development of atrial fibrillation-valvular heart disease. Int Heart J 62:153–161
Zhu L, Li N, Sun L, Zheng D, Shao G (2021) Non-coding RNAs: The key detectors and regulators in cardiovascular disease. Genomics 113:1233–1246
Acknowledgements
This work was supported by a Grant from the National Institutes of Health (1R01HL151583-01 to D.M.A).
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Anderson, K.M., Anderson, D.M. LncRNAs at the heart of development and disease. Mamm Genome 33, 354–365 (2022). https://doi.org/10.1007/s00335-021-09937-6
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DOI: https://doi.org/10.1007/s00335-021-09937-6