Functional Screening Identifies MicroRNA Regulators of Corin Activity and Atrial Natriuretic Peptide Biogenesis

REFERENCES

• Flynn TG, de Bold ML, de Bold AJ. 1983. The amino acid sequence of an atrial peptide with potent diuretic and natriuretic properties. Biochem Biophys Res Commun 117:859–865. https://doi.org/10.1016/0006-291X(83)91675-3.
   PubMed Web of Science ®Google Scholar
• Napier MA, Vandlen RL, Albers-Schönberg G, Nutt RF, Brady S, Lyle T, Winquist R, Faison EP, Heinel LA, Blaine EH. 1984. Specific membrane receptors for atrial natriuretic factor in renal and vascular tissues. Proc Natl Acad Sci U S A 81:5946–5950. https://doi.org/10.1073/pnas.81.19.5946.
   PubMed Web of Science ®Google Scholar
• McMurray JJV, Packer M, Desai AS, Gong J, Lefkowitz MP, Rizkala AR, Rouleau JL, Shi VC, Solomon SD, Swedberg K, Zile MR. 2014. Angiotensin-neprilysin inhibition versus enalapril in heart failure. N Engl J Med 371:993–1004. https://doi.org/10.1056/NEJMoa1409077.
   PubMed Web of Science ®Google Scholar
• Wu F, Yan W, Pan J, Morser J, Wu Q. 2002. Processing of pro-atrial natriuretic peptide by corin in cardiac myocytes. J Biol Chem 277:16900–16905. https://doi.org/10.1074/jbc.M201503200.
   PubMed Web of Science ®Google Scholar
• Chan JCY, Knudson O, Wu F, Morser J, Dole WP, Wu Q. 2005. Hypertension in mice lacking the proatrial natriuretic peptide convertase corin. Proc Natl Acad Sci U S A 102:785–790. https://doi.org/10.1073/pnas.0407234102.
   PubMed Web of Science ®Google Scholar
• Wang W, Shen J, Cui Y, Jiang J, Chen S, Peng J, Wu Q. 2012. Impaired sodium excretion and salt-sensitive hypertension in corin-deficient mice. Kidney Int 82:26–33. https://doi.org/10.1038/ki.2012.41.
   PubMed Web of Science ®Google Scholar
• Dries DL, Victor RG, Rame JE, Cooper RS, Wu X, Zhu X, Leonard D, Ho SI, Wu Q, Post W, Drazner MH. 2005. Corin gene minor allele defined by 2 missense mutations is common in blacks and associated with high blood pressure and hypertension. Circulation 112:2403–2410. https://doi.org/10.1161/CIRCULATIONAHA.105.568881.
   PubMed Web of Science ®Google Scholar
• Rame JE, Drazner MH, Post W, Peshock R, Lima J, Cooper RS, Dries DL. 2007. Corin I555(P568) allele is associated with enhanced cardiac hypertrophic response to increased systemic afterload. Hypertension 49:857–864. https://doi.org/10.1161/01.HYP.0000258566.95867.9e.
   PubMed Web of Science ®Google Scholar
• Rame JE, Tam SW, McNamara D, Worcel M, Sabolinski ML, Wu AH, Dries DL. 2009. Dysfunctional corin I555(P568) allele is associated with impaired brain natriuretic peptide processing and adverse outcomes in blacks with systolic heart failure: results from the Genetic Risk Assessment in Heart Failure substudy. Circ Heart Fail 2:541–548. https://doi.org/10.1161/CIRCHEARTFAILURE.109.866822.
   PubMed Web of Science ®Google Scholar
• Wang W, Liao X, Fukuda K, Knappe S, Wu F, Dries DL, Qin J, Wu Q. 2008. Corin variant associated with hypertension and cardiac hypertrophy exhibits impaired zymogen activation and natriuretic peptide processing activity. Circ Res 103:502–508. https://doi.org/10.1161/CIRCRESAHA.108.177352.
   PubMed Web of Science ®Google Scholar
• Langenickel TH, Pagel I, Buttgereit J, Tenner K, Lindner M, Dietz R, Willenbrock R, Bader M. 2004. Rat corin gene: molecular cloning and reduced expression in experimental heart failure. Am J Physiol Heart Circ Physiol 287:H1516–H1521. https://doi.org/10.1152/ajpheart.00947.2003.
   PubMed Web of Science ®Google Scholar
• Ichiki T, Boerrigter G, Huntley BK, Sangaralingham SJ, McKie PM, Harty GJ, Harders GE, Burnett JC. 2013. Differential expression of the pro-natriuretic peptide convertases corin and furin in experimental heart failure and atrial fibrosis. Am J Physiol Regul Integr Comp Physiol 304:R102–R109. https://doi.org/10.1152/ajpregu.00233.2012.
   PubMed Web of Science ®Google Scholar
• Chen S, Sen S, Young D, Wang W, Moravec CS, Wu Q. 2010. Protease corin expression and activity in failing hearts. Am J Physiol Heart Circ Physiol 299:H1687–H1692. https://doi.org/10.1152/ajpheart.00399.2010.
   PubMed Web of Science ®Google Scholar
• Pan J, Hinzmann B, Yan W, Wu F, Morser J, Wu Q. 2002. Genomic structures of the human and murine corin genes and functional GATA elements in their promoters. J Biol Chem 277:38390–38398. https://doi.org/10.1074/jbc.M205686200.
   PubMed Web of Science ®Google Scholar
• Lee R, Xu B, Rame JE, Felkin LE, Barton P, Dries DL. 2014. Regulated inositol-requiring protein 1-dependent decay as a mechanism of corin RNA and protein deficiency in advanced human systolic heart failure. J Am Heart Assoc 3:e001104. https://doi.org/10.1161/JAHA.114.001104.
   Google Scholar
• Miller BH, Wahlestedt C. 2010. MicroRNA dysregulation in psychiatric disease. Brain Res 1338:89–99. https://doi.org/10.1016/j.brainres.2010.03.035.
   PubMed Web of Science ®Google Scholar
• Small EM, Olson EN. 2011. Pervasive roles of microRNAs in cardiovascular biology. Nature 469:336–342. https://doi.org/10.1038/nature09783.
   PubMed Web of Science ®Google Scholar
• Lu LF, Liston A. 2009. MicroRNA in the immune system, microRNA as an immune system. Immunology 127:291–298. https://doi.org/10.1111/j.1365-2567.2009.03092.x.
   PubMed Web of Science ®Google Scholar
• Croce CM. 2009. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 10:704–714. https://doi.org/10.1038/nrg2634.
   PubMed Web of Science ®Google Scholar
• Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215–233. https://doi.org/10.1016/j.cell.2009.01.002.
   PubMed Web of Science ®Google Scholar
• van Rooij E, Olson EN. 2012. MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov 11:860–872. https://doi.org/10.1038/nrd3864.
   PubMed Web of Science ®Google Scholar
• Arora P, Wu C, Khan AM, Bloch DB, Davis-Dusenbery BN, Ghorbani A, Spagnolli E, Martinez A, Ryan A, Tainish LT, Kim S, Rong J, Huan T, Freedman JE, Levy D, Miller KK, Hata A, del Monte F, Vandenwijngaert S, Swinnen M, Janssens S, Holmes TM, Buys ES, Bloch KD, Newton-Cheh C, Wang TJ. 2013. Atrial natriuretic peptide is negatively regulated by microRNA-425. J Clin Invest 123:3378–3382. https://doi.org/10.1172/JCI67383.
   PubMed Web of Science ®Google Scholar
• Wu C, Arora P, Agha O, Hurst LA, Allen K, Nathan DI, Hu D, Jiramongkolchai P, Smith JG, Melander O, Trenson S, Janssens SP, Domian I, Wang TJ, Bloch KD, Buys ES, Bloch DB, Newton-Cheh C. 2016. Novel microRNA regulators of atrial natriuretic peptide production. Mol Cell Biol 36:1977–1987. https://doi.org/10.1128/MCB.01114-15.
   PubMed Web of Science ®Google Scholar
• Endo K, Weng H, Naito Y, Sasaoka T, Takahashi A, Fukushima Y, Iwai N. 2013. Classification of various muscular tissues using miRNA profiling. Biomed Res 34:289–299. https://doi.org/10.2220/biomedres.34.289.
   PubMed Web of Science ®Google Scholar
• Ludwig N, Leidinger P, Becker K, Backes C, Fehlmann T, Pallasch C, Rheinheimer S, Meder B, Stähler C, Meese E, Keller A. 2016. Distribution of miRNA expression across human tissues. Nucleic Acids Res 44:3865–3877. https://doi.org/10.1093/nar/gkw116.
   PubMed Web of Science ®Google Scholar
• Wystub K, Besser J, Bachmann A, Boettger T, Braun T. 2013. miR-1/133a clusters cooperatively specify the cardiomyogenic lineage by adjustment of myocardin levels during embryonic heart development. PLoS Genet 9:e1003793. https://doi.org/10.1371/journal.pgen.1003793.
   Google Scholar
• Diniz GP, Lino CA, Moreno CR, Senger N, Barreto-Chaves M. 2017. MicroRNA-1 overexpression blunts cardiomyocyte hypertrophy elicited by thyroid hormone. J Cell Physiol 232:3360–3368. https://doi.org/10.1002/jcp.25781.
   PubMed Web of Science ®Google Scholar
• Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, Zhang Y, Xu C, Bai Y, Wang H, Chen G, Wang Z. 2007. The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med 13:486–491. https://doi.org/10.1038/nm1569.
   PubMed Web of Science ®Google Scholar
• Terentyev D, Belevych AE, Terentyeva R, Martin MM, Malana GE, Kuhn DE, Abdellatif M, Feldman DS, Elton TS, Györke S. 2009. MiR-1 overexpression enhances ca2+ release and promotes cardiac arrhythmogenesis by targeting pp2a regulatory subunit b56α and causing camkii-dependent hyperphosphorylation of RyR2. Circ Res 104:514–521. https://doi.org/10.1161/CIRCRESAHA.108.181651.
   PubMed Web of Science ®Google Scholar
• Qian L, Wythe JD, Liu J, Cartry J, Vogler G, Mohapatra B, Otway RT, Huang Y, King IN, Maillet M, Zheng Y, Crawley T, Taghli-Lamallem O, Semsarian C, Dunwoodie S, Winlaw D, Harvey RP, Fatkin D, Towbin JA, Molkentin JD, Srivastava D, Ocorr K, Bruneau BG, Bodmer R. 2011. Tinman/Nkx2-5 acts via miR-1 and upstream of Cdc42 to regulate heart function across species. J Cell Biol 193:1181–1196. https://doi.org/10.1083/jcb.201006114.
   PubMed Web of Science ®Google Scholar
• Wang F, Song G, Liu M, Li X, Tang H. 2011. miRNA-1 targets fibronectin1 and suppresses the migration and invasion of the HEp2 laryngeal squamous carcinoma cell line. FEBS Lett Federation of European Biochemical Societies 585:3263–3269. https://doi.org/10.1016/j.febslet.2011.08.052.
   PubMed Web of Science ®Google Scholar
• Carvajal A, Garrido JJ, Bautista R, Zaldívar-López S, Claros MG, Herrera-Uribe J, Aguilar C, Luque C. 2018. Regulatory role of microRNA in mesenteric lymph nodes after Salmonella Typhimurium infection. Vet Res 49:9. https://doi.org/10.1186/s13567-018-0506-1.
   PubMed Web of Science ®Google Scholar
• Lin CY, Lee HC, Fu CY, Ding YY, Chen JS, Lee MH, Huang WJ, Tsai HJ. 2013. MiR-1 and miR-206 target different genes to have opposing roles during angiogenesis in zebrafish embryos. Nat Commun 4:2829. https://doi.org/10.1038/ncomms3829.
   PubMed Web of Science ®Google Scholar
• Wang L, Yuan Y, Li J, Ren H, Cai Q, Chen X, Liang H, Shan H, Fu ZD, Gao X, Lv Y, Yang B, Zhang Y. 2015. MicroRNA-1 aggravates cardiac oxidative stress by post-transcriptional modification of the antioxidant network. Cell Stress Chaperones 20:411–420. https://doi.org/10.1007/s12192-014-0565-9.
   PubMed Web of Science ®Google Scholar
• Agarwal V, Bell GW, Nam J-W, Bartel DP. 2015. Predicting effective microRNA target sites in mammalian mRNAs. Elife 4:1–38. https://doi.org/10.7554/eLife.05005.
   Web of Science ®Google Scholar
• Zhao Y, Shen X, Tang T, Wu CI. 2017. Weak regulation of many targets is cumulatively powerful—an evolutionary perspective on microRNA functionality. Mol Biol Evol 34:3041–3046. https://doi.org/10.1093/molbev/msx260.
   PubMed Web of Science ®Google Scholar
• Stark A, Brennecke J, Russell RB, Cohen SM. 2003. Identification of Drosophila microRNA targets. PLoS Biol 1:e60. https://doi.org/10.1371/journal.pbio.0000060.
   PubMed Web of Science ®Google Scholar
• Grün D, Wang Y-L, Langenberger D, Gunsalus K, Rajewsky N. 2005. microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comp Biol 1:e13. https://doi.org/10.1371/journal.pcbi.0010013.
   PubMed Web of Science ®Google Scholar
• Lall S, Grün D, Krek A, Chen K, Wang YL, Dewey CN, Sood P, Colombo T, Bray N, MacMenamin P, Kao HL, Gunsalus KC, Pachter L, Piano F, Rajewsky N. 2006. A genome-wide map of conserved microRNA targets in C. elegans. Curr Biol 16:460–471. https://doi.org/10.1016/j.cub.2006.01.050.
   PubMed Web of Science ®Google Scholar
• Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20. https://doi.org/10.1016/j.cell.2004.12.035.
   PubMed Web of Science ®Google Scholar
• Lim JY, Park SJ, Hwang HY, Park EJ, Nam JH, Kim J, Park SI. 2005. TGF-β1 induces cardiac hypertrophic responses via PKC-dependent ATF-2 activation. J Mol Cell Cardiol 39:627–636. https://doi.org/10.1016/j.yjmcc.2005.06.016.
   PubMed Web of Science ®Google Scholar
• Van Tuyn J, Knaän-Shanzer S, Van De Watering MJM, De Graaf M, Van Der Laarse A, Schalij MJ, Van Der Wall EE, De Vries AAF, Atsma DE. 2005. Activation of cardiac and smooth muscle-specific genes in primary human cells after forced expression of human myocardin. Cardiovasc Res 67:245–255. https://doi.org/10.1016/j.cardiores.2005.04.013.
   PubMed Web of Science ®Google Scholar
• Stennard FA, Costa MW, Elliott DA, Rankin S, Haast SJP, Lai D, McDonald LPA, Niederreither K, Dolle P, Bruneau BG, Zorn AM, Harvey RP. 2003. Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart. Dev Biol 262:206–224. https://doi.org/10.1016/s0012-1606(03)00385-3.
   PubMed Web of Science ®Google Scholar
• Ogawa E, Saito Y, Kuwahara K, Harada M, Miyamoto Y, Hamanaka I, Kajiyama N, Takahashi N, Izumi T, Kawakami R, Kishimoto I, Naruse Y, Mori N, Nakao K. 2002. Fibronectin signaling stimulates BNP gene transcription by inhibiting neuron-restrictive silencer element-dependent repression. Cardiovasc Res 53:451–459. https://doi.org/10.1016/s0008-6363(01)00492-8.
   PubMed Web of Science ®Google Scholar
• Piccini I, Rao J, Seebohm G, Greber B. 2015. Human pluripotent stem cell-derived cardiomyocytes: genome-wide expression profiling of long-term in vitro maturation in comparison to human heart tissue. Genomics Data 4:69. https://doi.org/10.1016/j.gdata.2015.03.008.
   PubMedGoogle Scholar
• Barbuti A, Robinson RB. 2015. Stem cell-derived nodal-like cardiomyocytes as a novel pharmacologic tool: insights from sinoatrial node development and function. Pharmacol Rev 67:368. https://doi.org/10.1124/pr.114.009597.
   PubMed Web of Science ®Google Scholar
• Karakikes I, Chaanine AH, Kang S, Mukete BN, Jeong D, Zhang S, Hajjar RJ, Lebeche D. 2013. Therapeutic cardiac-targeted delivery of miR-1 reverses pressure overload-induced cardiac hypertrophy and attenuates pathological remodeling. J Am Heart Assoc 2:e000078. https://doi.org/10.1161/JAHA.113.000078.
   PubMed Web of Science ®Google Scholar
• Ikeda S, He A, Kong SW, Lu J, Bejar R, Bodyak N, Lee K-H, Ma Q, Kang PM, Golub TR, Pu WT. 2009. MicroRNA-1 negatively regulates expression of the hypertrophy-associated calmodulin and Mef2a genes. Mol Cell Biol 29:2193–2204. https://doi.org/10.1128/MCB.01222-08.
   PubMed Web of Science ®Google Scholar
• Belevych AE, Sansom SE, Terentyeva R, Ho HT, Nishijima Y, Martin MM, Jindal HK, Rochira JA, Kunitomo Y, Abdellatif M, Carnes CA, Elton TS, Györke S, Terentyev D. 2011. MicroRNA-1 and -133 increase arrhythmogenesis in heart failure by dissociating phosphatase activity from RyR2 complex. PLoS One 6:e28324. https://doi.org/10.1371/journal.pone.0028324.
   Google Scholar
• Rupaimoole R, Slack FJ. 2017. MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 16:203–222. https://doi.org/10.1038/nrd.2016.246.
   PubMed Web of Science ®Google Scholar
• Heidersbach A, Saxby C, Carver-Moore K, Huang Y, Ang YS, de Jong PJ, Ivey KN, Srivastava D. 2013. MicroRNA-1 regulates sarcomere formation and suppresses smooth muscle gene expression in the mammalian heart. Elife 2:e01323. https://doi.org/10.7554/eLife.01323.
   Google Scholar
• Minami T, Kuwahara K, Nakagawa Y, Takaoka M, Kinoshita H, Nekao K, Kuwabara Y, Yamada Y, Yamada C, Shibata J, Usami S, Yasuno S, Nishikimi T, Ueshima K, Sata M, Nakano H, Seno T, Kawahito Y, Sobue K, Kimura A, Nagai R, Nakao K. 2012. Reciprocal expression of MRTF-A and myocardin is crucial for pathological vascular remodelling in mice. EMBO J 31:4428–4440. https://doi.org/10.1038/emboj.2012.296.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x.
   Google Scholar
• Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264. https://doi.org/10.1093/biostatistics/4.2.249.
   PubMed Web of Science ®Google Scholar