Skip to main content
Log in

Epigenetic control of natriuretic peptides: implications for health and disease

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The natriuretic peptides (NPs) family, including a class of hormones and their receptors, is largely known for its beneficial effects within the cardiovascular system to preserve regular functions and health. The concentration level of each component of the family is of crucial importance to guarantee a proper control of both systemic and local cardiovascular functions. A fine equilibrium between gene expression, protein secretion and clearance is needed to achieve the final optimal level of NPs. To this aim, the regulation of gene expression and translation plays a key role. In this regard, we know the existence of fine regulatory mechanisms, the so-called epigenetic mechanisms, which target many genes at either the promoter or the 3′UTR region to inhibit or activate their expression. The gene encoding ANP (NPPA) is regulated by histone modifications, DNA methylation, distinct microRNAs and a natural antisense transcript (NPPA-AS1) with consequent implications for both health and disease conditions. Notably, ANP modulates microRNAs on its own. Histone modifications of BNP gene (NPPB) are associated with several cardiomyopathies. The proBNP processing is regulated by miR30-GALNT1/2 axis. Among other components of the NPs family, CORIN, NPRA, NPRC and NEP may undergo epigenetic regulation. A better understanding of the epigenetic control of the NPs family will allow to gain more insights on the pathological basis of common cardiovascular diseases and to identify novel therapeutic targets. The present review article aims to discuss the major achievements obtained so far with studies on the epigenetic modulation of the NPs family.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Levin ER, Gardner DG, Samson WK (1998) Natriuretic peptides. N Engl J Med 339(5):321–328. https://doi.org/10.1056/NEJM199807303390507

    Article  CAS  PubMed  Google Scholar 

  2. Potter LR, Yoder AR, Flora DR, Antos LK, Dickey DM (2009) Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb Exp Pharmacol 191:341–366. https://doi.org/10.1007/978-3-540-68964-5_15

    Article  CAS  Google Scholar 

  3. Nakagawa Y, Nishikimi T, Kuwahara K (2019) Atrial and brain natriuretic peptides: hormones secreted from the heart. Peptides 111:18–25. https://doi.org/10.1016/j.peptides.2018.05.012

    Article  CAS  PubMed  Google Scholar 

  4. Rubattu S, Sciarretta S, Valenti V, Stanzione R, Volpe M (2008) Natriuretic peptides: an update on bioactivity, potential therapeutic use, and implication in cardiovascular diseases. Am J Hypertens 21(7):733–741. https://doi.org/10.1038/ajh.2008.174

    Article  CAS  PubMed  Google Scholar 

  5. Volpe M, Rubattu S, Burnett J Jr (2014) Natriuretic peptides in cardiovascular diseases: current use and perspectives. Eur Heart J 35(7):419–425. https://doi.org/10.1093/eurheartj/eht466

    Article  CAS  PubMed  Google Scholar 

  6. Tamura N, Ogawa Y, Chusho H, Nakamura K, Nakao K, Suda M, Kasahara M, Hashimoto R, Katsuura G, Mukoyama M, Itoh H, Saito Y, Tanaka I, Otani H, Katsuki M (2000) Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc Natl Acad Sci USA 97(8):4239–4244. https://doi.org/10.1073/pnas.070371497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Volpe M, Rubattu S (2019) Natriuretic Peptides. In: Dorobantu M, Mancia G, Grassi G, Voicu V (eds) Hypertension and heart failure: epidemiology, mechanisms and treatment. Springer International Publishing, Cham, pp 87–100. https://doi.org/10.1007/978-3-319-93320-7_6

    Chapter  Google Scholar 

  8. de Bold AJ, Bruneau BG, Kuroski de Bold ML (1996) Mechanical and neuroendocrine regulation of the endocrine heart. Cardiovasc Res 31(1):7–18

    Article  PubMed  Google Scholar 

  9. Egger G, Liang G, Aparicio A, Jones PA (2004) Epigenetics in human disease and prospects for epigenetic therapy. Nature 429(6990):457–463. https://doi.org/10.1038/nature02625

    Article  CAS  PubMed  Google Scholar 

  10. Bird A (2007) Perceptions of epigenetics. Nature 447(7143):396–398. https://doi.org/10.1038/nature05913

    Article  CAS  PubMed  Google Scholar 

  11. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl):245–254. https://doi.org/10.1038/ng1089

    Article  CAS  PubMed  Google Scholar 

  12. Ordovas JM, Smith CE (2010) Epigenetics and cardiovascular disease. Nat Rev Cardiol 7(9):510–519. https://doi.org/10.1038/nrcardio.2010.104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Teperino R, Schoonjans K, Auwerx J (2010) Histone methyl transferases and demethylases; can they link metabolism and transcription? Cell Metab 12(4):321–327. https://doi.org/10.1016/j.cmet.2010.09.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Lachner M, Jenuwein T (2002) The many faces of histone lysine methylation. Curr Opin Cell Biol 14(3):286–298. https://doi.org/10.1016/s0955-0674(02)00335-6

    Article  CAS  PubMed  Google Scholar 

  15. Udali S, Guarini P, Moruzzi S, Choi SW, Friso S (2013) Cardiovascular epigenetics: from DNA methylation to microRNAs. Mol Aspects Med 34(4):883–901. https://doi.org/10.1016/j.mam.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  16. Sergeeva IA, Hooijkaas IB, Ruijter JM, van der Made I, de Groot NE, van de Werken HJ, Creemers EE, Christoffels VM (2016) Identification of a regulatory domain controlling the Nppa-Nppb gene cluster during heart development and stress. Development 143(12):2135–2146. https://doi.org/10.1242/dev.132019

    Article  CAS  PubMed  Google Scholar 

  17. Hohl M, Wagner M, Reil JC, Muller SA, Tauchnitz M, Zimmer AM, Lehmann LH, Thiel G, Bohm M, Backs J, Maack C (2013) HDAC4 controls histone methylation in response to elevated cardiac load. J Clin Invest 123(3):1359–1370. https://doi.org/10.1172/JCI61084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Man J, Barnett P, Christoffels VM (2018) Structure and function of the Nppa-Nppb cluster locus during heart development and disease. Cell Mol Life Sci 75(8):1435–1444. https://doi.org/10.1007/s00018-017-2737-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Papait R, Cattaneo P, Kunderfranco P, Greco C, Carullo P, Guffanti A, Vigano V, Stirparo GG, Latronico MV, Hasenfuss G, Chen J, Condorelli G (2013) Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy. Proc Natl Acad Sci USA 110(50):20164–20169. https://doi.org/10.1073/pnas.1315155110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mahmoud SA, Poizat C (2013) Epigenetics and chromatin remodeling in adult cardiomyopathy. J Pathol 231(2):147–157. https://doi.org/10.1002/path.4234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Rosales W, Lizcano F (2018) The histone demethylase JMJD2A modulates the induction of hypertrophy markers in iPSC-derived cardiomyocytes. Front Genet 9:14. https://doi.org/10.3389/fgene.2018.00014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Takaya T, Kawamura T, Morimoto T, Ono K, Kita T, Shimatsu A, Hasegawa K (2008) Identification of p300-targeted acetylated residues in GATA4 during hypertrophic responses in cardiac myocytes. J Biol Chem 283(15):9828–9835. https://doi.org/10.1074/jbc.M707391200

    Article  CAS  PubMed  Google Scholar 

  23. Miyamoto S, Kawamura T, Morimoto T, Ono K, Wada H, Kawase Y, Matsumori A, Nishio R, Kita T, Hasegawa K (2006) Histone acetyltransferase activity of p300 is required for the promotion of left ventricular remodeling after myocardial infarction in adult mice in vivo. Circulation 113(5):679–690. https://doi.org/10.1161/CIRCULATIONAHA.105.585182

    Article  CAS  PubMed  Google Scholar 

  24. Mathiyalagan P, Chang L, Du XJ, El-Osta A (2010) Cardiac ventricular chambers are epigenetically distinguishable. Cell Cycle 9(3):612–617. https://doi.org/10.4161/cc.9.3.10612

    Article  CAS  PubMed  Google Scholar 

  25. Meder B, Haas J, Sedaghat-Hamedani F, Kayvanpour E, Frese K, Lai A, Nietsch R, Scheiner C, Mester S, Bordalo DM, Amr A, Dietrich C, Pils D, Siede D, Hund H, Bauer A, Holzer DB, Ruhparwar A, Mueller-Hennessen M, Weichenhan D, Plass C, Weis T, Backs J, Wuerstle M, Keller A, Katus HA, Posch AE (2017) Epigenome-wide association study identifies cardiac gene patterning and a novel class of biomarkers for heart failure. Circulation 136(16):1528–1544. https://doi.org/10.1161/CIRCULATIONAHA.117.027355

    Article  CAS  PubMed  Google Scholar 

  26. Ito E, Miyagawa S, Fukushima S, Yoshikawa Y, Saito S, Saito T, Harada A, Takeda M, Kashiyama N, Nakamura Y, Shiozaki M, Toda K, Sawa Y (2017) Histone modification is correlated with reverse left ventricular remodeling in nonischemic dilated cardiomyopathy. Ann Thorac Surg 104(5):1531–1539. https://doi.org/10.1016/j.athoracsur.2017.04.046

    Article  PubMed  Google Scholar 

  27. Kee HJ, Kook H (2009) Kruppel-like factor 4 mediates histone deacetylase inhibitor-induced prevention of cardiac hypertrophy. J Mol Cell Cardiol 47(6):770–780. https://doi.org/10.1016/j.yjmcc.2009.08.022

    Article  CAS  PubMed  Google Scholar 

  28. Ooi JY, Tuano NK, Rafehi H, Gao XM, Ziemann M, Du XJ, El-Osta A (2015) HDAC inhibition attenuates cardiac hypertrophy by acetylation and deacetylation of target genes. Epigenetics 10(5):418–430. https://doi.org/10.1080/15592294.2015.1024406

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kao YH, Liou JP, Chung CC, Lien GS, Kuo CC, Chen SA, Chen YJ (2013) Histone deacetylase inhibition improved cardiac functions with direct antifibrotic activity in heart failure. Int J Cardiol 168(4):4178–4183. https://doi.org/10.1016/j.ijcard.2013.07.111

    Article  PubMed  Google Scholar 

  30. Lee E, Song MJ, Lee HA, Kang SH, Kim M, Yang EK, Lee do Y, Ro S, Cho JM, Kim I (2016) Histone deacetylase inhibitor, CG200745, attenuates cardiac hypertrophy and fibrosis in DOCA-induced hypertensive rats. Korean J Physiol Pharmacol 20(5):477–485. https://doi.org/10.4196/kjpp.2016.20.5.477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Malek V, Sharma N, Gaikwad AB (2019) Histone acetylation regulates natriuretic peptides and neprilysin gene expressions in diabetic cardiomyopathy and nephropathy. Curr Mol Pharmacol 12(1):61–71. https://doi.org/10.2174/1874467212666181122092300

    Article  CAS  PubMed  Google Scholar 

  32. Tabibiazar R, Wagner RA, Liao A, Quertermous T (2003) Transcriptional profiling of the heart reveals chamber-specific gene expression patterns. Circ Res 93(12):1193–1201. https://doi.org/10.1161/01.RES.0000103171.42654.DD

    Article  CAS  PubMed  Google Scholar 

  33. Glahn A, Rhein M, Frieling H, Schuster R, El Aissami A, Bleich S, Hillemacher T, Muschler M (2017) Smoking and promoter-specific deoxyribonucleic acid methylation of the atrial natriuretic peptide gene: methylation of smokers and non-smokers differs significantly during withdrawal. Eur Addict Res 23(6):306–311. https://doi.org/10.1159/000486279

    Article  PubMed  Google Scholar 

  34. Glahn A, Riera Knorrenschild R, Rhein M, Haschemi Nassab M, Groschl M, Heberlein A, Muschler M, Frieling H, Bleich S, Hillemacher T (2014) Alcohol-induced changes in methylation status of individual CpG sites, and serum levels of vasopressin and atrial natriuretic peptide in alcohol-dependent patients during detoxification treatment. Eur Addict Res 20(3):143–150. https://doi.org/10.1159/000357473

    Article  PubMed  Google Scholar 

  35. Glahn A, Rhein M, Heberlein A, Muschler M, Kornhuber J, Frieling H, Bleich S, Hillemacher T (2016) The epigenetic regulation of GATA4-dependent brain natriuretic peptide expression during alcohol withdrawal. Neuropsychobiology 74(3):131–138. https://doi.org/10.1159/000456011

    Article  CAS  PubMed  Google Scholar 

  36. Hillemacher T, Kahl KG, Heberlein A, Muschler MA, Eberlein C, Frieling H, Bleich S (2010) Appetite- and volume-regulating neuropeptides: role in treating alcohol dependence. Curr Opin Investig Drugs 11(10):1097–1106

    CAS  PubMed  Google Scholar 

  37. Frieling H, Bleich S, Otten J, Romer KD, Kornhuber J, de Zwaan M, Jacoby GE, Wilhelm J, Hillemacher T (2008) Epigenetic downregulation of atrial natriuretic peptide but not vasopressin mRNA expression in females with eating disorders is related to impulsivity. Neuropsychopharmacology 33(11):2605–2609. https://doi.org/10.1038/sj.npp.1301662

    Article  CAS  PubMed  Google Scholar 

  38. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233. https://doi.org/10.1016/j.cell.2009.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wojciechowska A, Braniewska A, Kozar-Kaminska K (2017) MicroRNA in cardiovascular biology and disease. Adv Clin Exp Med 26(5):865–874. https://doi.org/10.17219/acem/62915

    Article  PubMed  Google Scholar 

  40. Arora P, Wu C, Khan AM, Bloch DB, Davis-Dusenbery BN, Ghorbani A, Spagnolli E, Martinez A, Ryan A, Tainsh 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(8):3378–3382. https://doi.org/10.1172/JCI67383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Arora P, Wu C, Hamid T, Arora G, Agha O, Allen K, Tainsh RET, Hu D, Ryan RA, Domian IJ, Buys ES, Bloch DB, Prabhu SD, Bloch KD, Newton-Cheh C, Wang TJ (2016) Acute metabolic influences on the natriuretic peptide system in humans. J Am Coll Cardiol 67(7):804–812. https://doi.org/10.1016/j.jacc.2015.11.049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. 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(14):1977–1987. https://doi.org/10.1128/MCB.01114-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Patel N, Russell GK, Musunuru K, Gutierrez OM, Halade G, Kain V, Lv W, Prabhu SD, Margulies KB, Cappola TP, Arora G, Wang TJ, Arora P (2019) Race, natriuretic peptides, and high-carbohydrate challenge: a clinical trial. Circ Res 125(11):957–968. https://doi.org/10.1161/CIRCRESAHA.119.315026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Cannone V, Cabassi A, Volpi R, Burnett JC Jr (2019) Atrial natriuretic peptide: a molecular target of novel therapeutic approaches to cardio-metabolic disease. Int J Mol Sci. https://doi.org/10.3390/ijms20133265

    Article  PubMed  PubMed Central  Google Scholar 

  45. Newton-Cheh C, Larson MG, Vasan RS, Levy D, Bloch KD, Surti A, Guiducci C, Kathiresan S, Benjamin EJ, Struck J, Morgenthaler NG, Bergmann A, Blankenberg S, Kee F, Nilsson P, Yin X, Peltonen L, Vartiainen E, Salomaa V, Hirschhorn JN, Melander O, Wang TJ (2009) Association of common variants in NPPA and NPPB with circulating natriuretic peptides and blood pressure. Nat Genet 41(3):348–353. https://doi.org/10.1038/ng.328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Cannone V, Boerrigter G, Cataliotti A, Costello-Boerrigter LC, Olson TM, McKie PM, Heublein DM, Lahr BD, Bailey KR, Averna M, Redfield MM, Rodeheffer RJ, Burnett JC Jr (2011) A genetic variant of the atrial natriuretic peptide gene is associated with cardiometabolic protection in the general community. J Am Coll Cardiol 58(6):629–636. https://doi.org/10.1016/j.jacc.2011.05.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Cannone V, Cefalu AB, Noto D, Scott CG, Bailey KR, Cavera G, Pagano M, Sapienza M, Averna MR, Burnett JC Jr (2013) The atrial natriuretic peptide genetic variant rs5068 is associated with a favorable cardiometabolic phenotype in a Mediterranean population. Diabetes Care 36(9):2850–2856. https://doi.org/10.2337/dc12-2337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Jujic A, Nilsson PM, Engstrom G, Hedblad B, Melander O, Magnusson M (2014) Atrial natriuretic peptide and type 2 diabetes development–biomarker and genotype association study. PLoS ONE 9(2):e89201. https://doi.org/10.1371/journal.pone.0089201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Cannone V, Scott CG, Decker PA, Larson NB, Palmas W, Taylor KD, Wang TJ, Gupta DK, Bielinski SJ, Burnett JC Jr (2017) A favorable cardiometabolic profile is associated with the G allele of the genetic variant rs5068 in African Americans: the Multi-Ethnic Study of Atherosclerosis (MESA). PLoS ONE 12(12):e0189858. https://doi.org/10.1371/journal.pone.0189858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Rubattu S, Volpe M (2019) Natriuretic peptides in the cardiovascular system: multifaceted roles in physiology, pathology and therapeutics. Int J Mol Sci. https://doi.org/10.3390/ijms20163991

    Article  PubMed  PubMed Central  Google Scholar 

  51. Vandenwijngaert S, Ledsky CD, Agha O, Wu C, Hu D, Bagchi A, Domian IJ, Buys ES, Newton-Cheh C, Bloch DB (2018) MicroRNA-425 and microRNA-155 cooperatively regulate atrial natriuretic peptide expression and cGMP production. PLoS ONE 13(4):e0196697. https://doi.org/10.1371/journal.pone.0196697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Gangwar RS, Rajagopalan S, Natarajan R, Deiuliis JA (2018) Noncoding RNAs in cardiovascular disease: pathological relevance and emerging role as biomarkers and therapeutics. Am J Hypertens 31(2):150–165. https://doi.org/10.1093/ajh/hpx197

    Article  CAS  PubMed  Google Scholar 

  53. Elton TS, Selemon H, Elton SM, Parinandi NL (2013) Regulation of the MIR155 host gene in physiological and pathological processes. Gene 532(1):1–12. https://doi.org/10.1016/j.gene.2012.12.009

    Article  CAS  PubMed  Google Scholar 

  54. Zhang L, Liu C, Huang C, Xu X, Teng J (2020) miR-155 knockdown protects against cerebral ischemia and reperfusion injury by targeting MafB. Biomed Res Int 2020:6458204. https://doi.org/10.1155/2020/6458204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Xi J, Li QQ, Li BQ, Li N (2020) miR155 inhibition represents a potential valuable regulator in mitigating myocardial hypoxia/reoxygenation injury through targeting BAG5 and MAPK/JNK signaling. Mol Med Rep 21(3):1011–1020. https://doi.org/10.3892/mmr.2020.10924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kotlo KU, Hesabi B, Danziger RS (2011) Implication of microRNAs in atrial natriuretic peptide and nitric oxide signaling in vascular smooth muscle cells. Am J Physiol Cell Physiol 301(4):C929–C937. https://doi.org/10.1152/ajpcell.00088.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Song J, Hu B, Qu H, Bi C, Huang X, Zhang M (2012) Mechanical stretch modulates microRNA 21 expression, participating in proliferation and apoptosis in cultured human aortic smooth muscle cells. PLoS ONE 7(10):e47657. https://doi.org/10.1371/journal.pone.0047657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kang H, Davis-Dusenbery BN, Nguyen PH, Lal A, Lieberman J, Van Aelst L, Lagna G, Hata A (2012) Bone morphogenetic protein 4 promotes vascular smooth muscle contractility by activating microRNA-21 (miR-21), which down-regulates expression of family of dedicator of cytokinesis (DOCK) proteins. J Biol Chem 287(6):3976–3986. https://doi.org/10.1074/jbc.M111.303156

    Article  CAS  PubMed  Google Scholar 

  59. Rubattu S, Marchitti S, Bianchi F, Di Castro S, Stanzione R, Cotugno M, Bozzao C, Sciarretta S, Volpe M (2014) The C2238/alphaANP variant is a negative modulator of both viability and function of coronary artery smooth muscle cells. PLoS ONE 9(11):e113108. https://doi.org/10.1371/journal.pone.0113108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Stanzione R, Sciarretta S, Marchitti S, Bianchi F, Di Castro S, Scarpino S, Cotugno M, Frati G, Volpe M, Rubattu S (2015) C2238/alphaANP modulates apolipoprotein E through Egr-1/miR199a in vascular smooth muscle cells in vitro. Cell Death Dis 6:e2033. https://doi.org/10.1038/cddis.2015.370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Khorkova O, Myers AJ, Hsiao J, Wahlestedt C (2014) Natural antisense transcripts. Hum Mol Genet 23(R1):R54–R63. https://doi.org/10.1093/hmg/ddu207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Celik S, Sadegh MK, Morley M, Roselli C, Ellinor PT, Cappola T, Smith JG, Gidlof O (2019) Antisense regulation of atrial natriuretic peptide expression. JCI Insight. https://doi.org/10.1172/jci.insight.130978

    Article  PubMed  PubMed Central  Google Scholar 

  63. Tsutamoto T, Wada A, Maeda K, Hisanaga T, Maeda Y, Fukai D, Ohnishi M, Sugimoto Y, Kinoshita M (1997) Attenuation of compensation of endogenous cardiac natriuretic peptide system in chronic heart failure: prognostic role of plasma brain natriuretic peptide concentration in patients with chronic symptomatic left ventricular dysfunction. Circulation 96(2):509–516. https://doi.org/10.1161/01.cir.96.2.509

    Article  CAS  PubMed  Google Scholar 

  64. Menon SG, Mills RM, Schellenberger U, Saqhir S, Protter AA (2009) Clinical implications of defective B-type natriuretic peptide. Clin Cardiol 32(12):E36–E41. https://doi.org/10.1002/clc.20480

    Article  PubMed  PubMed Central  Google Scholar 

  65. Semenov AG, Postnikov AB, Tamm NN, Seferian KR, Karpova NS, Bloshchitsyna MN, Koshkina EV, Krasnoselsky MI, Serebryanaya DV, Katrukha AG (2009) Processing of pro-brain natriuretic peptide is suppressed by O-glycosylation in the region close to the cleavage site. Clin Chem 55(3):489–498. https://doi.org/10.1373/clinchem.2008.113373

    Article  CAS  PubMed  Google Scholar 

  66. Nakagawa Y, Nishikimi T, Kuwahara K, Fujishima A, Oka S, Tsutamoto T, Kinoshita H, Nakao K, Cho K, Inazumi H, Okamoto H, Nishida M, Kato T, Fukushima H, Yamashita JK, Wijnen WJ, Creemers EE, Kangawa K, Minamino N, Nakao K, Kimura T (2017) MiR30-GALNT1/2 axis-mediated glycosylation contributes to the increased secretion of inactive human prohormone for brain natriuretic peptide (proBNP) from failing hearts. J Am Heart Assoc. https://doi.org/10.1161/jaha.116.003601

    Article  PubMed  PubMed Central  Google Scholar 

  67. Celik S, Karbalaei-Sadegh M, Radegran G, Smith JG, Gidlof O (2019) Functional screening identifies microRNA regulators of corin activity and atrial natriuretic peptide biogenesis. Mol Cell Biol. https://doi.org/10.1128/mcb.00271-19

    Article  PubMed  PubMed Central  Google Scholar 

  68. Chen YL, Li TJ, Hao Y, Wu BG, Li H, Geng N, Sun ZQ, Zheng LQ, Sun YX (2018) Association of rs2271037 and rs3749585 polymorphisms in CORIN with susceptibility to hypertension in a Chinese Han population: a case-control study. Gene 651:79–85. https://doi.org/10.1016/j.gene.2018.01.080

    Article  CAS  PubMed  Google Scholar 

  69. Kumar P, Tripathi S, Pandey KN (2014) Histone deacetylase inhibitors modulate the transcriptional regulation of guanylyl cyclase/natriuretic peptide receptor-a gene: interactive roles of modified histones, histone acetyltransferase, p300, AND Sp1. J Biol Chem 289(10):6991–7002. https://doi.org/10.1074/jbc.M113.511444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kumar P, Periyasamy R, Das S, Neerukonda S, Mani I, Pandey KN (2014) All-trans retinoic acid and sodium butyrate enhance natriuretic peptide receptor a gene transcription: role of histone modification. Mol Pharmacol 85(6):946–957. https://doi.org/10.1124/mol.114.092221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Rubattu S, Sciarretta S, Morriello A, Calvieri C, Battistoni A, Volpe M (2010) NPR-C: a component of the natriuretic peptide family with implications in human diseases. J Mol Med (Berl) 88(9):889–897. https://doi.org/10.1007/s00109-010-0641-2

    Article  CAS  Google Scholar 

  72. Rubattu S, Forte M, Marchitti S, Volpe M (2019) Molecular implications of natriuretic peptides in the protection from hypertension and target organ damage development. Int J Mol Sci. https://doi.org/10.3390/ijms20040798

    Article  PubMed  PubMed Central  Google Scholar 

  73. Santhekadur PK, Kumar DP, Seneshaw M, Mirshahi F, Sanyal AJ (2017) The multifaceted role of natriuretic peptides in metabolic syndrome. Biomed Pharmacother 92:826–835. https://doi.org/10.1016/j.biopha.2017.05.136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Wong LL, Wee AS, Lim JY, Ng JY, Chong JP, Liew OW, Lilyanna S, Martinez EC, Ackers-Johnson MA, Vardy LA, Armugam A, Jeyaseelan K, Ng TP, Lam CS, Foo RS, Richards AM, Chen YT (2015) Natriuretic peptide receptor 3 (NPR3) is regulated by microRNA-100. J Mol Cell Cardiol 82:13–21. https://doi.org/10.1016/j.yjmcc.2015.02.019

    Article  CAS  PubMed  Google Scholar 

  75. Wang J, Tong KS, Wong LL, Liew OW, Raghuram D, Richards AM, Chen YT (2018) MicroRNA-143 modulates the expression of Natriuretic Peptide Receptor 3 in cardiac cells. Sci Rep 8(1):7055. https://doi.org/10.1038/s41598-018-25489-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Chu T, Shu Y, Qu Y, Gao S, Zhang L (2018) miR-26b inhibits total neurite outgrowth, promotes cells apoptosis and downregulates neprilysin in Alzheimer’s disease. Int J Clin Exp Pathol 11(7):3383–3390

    PubMed  PubMed Central  Google Scholar 

  77. Yasojima K, McGeer EG, McGeer PL (2001) Relationship between beta amyloid peptide generating molecules and neprilysin in Alzheimer disease and normal brain. Brain Res 919(1):115–121. https://doi.org/10.1016/s0006-8993(01)03008-6

    Article  CAS  PubMed  Google Scholar 

  78. Lin CY, Perche F, Ikegami M, Uchida S, Kataoka K, Itaka K (2016) Messenger RNA-based therapeutics for brain diseases: an animal study for augmenting clearance of beta-amyloid by intracerebral administration of neprilysin mRNA loaded in polyplex nanomicelles. J Control Release 235:268–275. https://doi.org/10.1016/j.jconrel.2016.06.001

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by a Grant from the Italian Ministry of Health.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Speranza Rubattu.

Ethics declarations

Conflicts of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rubattu, S., Stanzione, R., Cotugno, M. et al. Epigenetic control of natriuretic peptides: implications for health and disease. Cell. Mol. Life Sci. 77, 5121–5130 (2020). https://doi.org/10.1007/s00018-020-03573-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-020-03573-0

Keywords

Navigation