Log in

Circulating microRNA-1a is a biomarker of Graves’ disease patients with atrial fibrillation

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

It has been increasingly suggested that specific microRNAs expression profiles in the circulation and atrial tissue are associated with the susceptibility to atrial fibrillation. Nonetheless, the role of circulating microRNAs in Graves’ disease patients with atrial fibrillation has not yet been well described. The objective of the study was to identify the role of circulating microRNAs as specific biomarkers for the diagnosis of Graves’ disease with atrial fibrillation.

Methods

The expression profiles of eight serum microRNAs, which are found to be critical in the pathogenesis of atrial fibrillation, were determined in patients with Graves’ disease with or without atrial fibrillation. MicroRNA expression analysis was performed by real-time PCR in normal control subjects (NC; n = 17), patients with Graves’ disease without atrial fibrillation (GD; n = 29), patients with Graves’ disease with atrial fibrillation (GD + AF; n = 14), and euthyroid patients with atrial fibrillation (AF; n = 22).

Results

Three of the eight serum microRNAs,i.e., miR-1a, miR-26a, and miR-133, had significantly different expression profiles among the four groups. Spearman’s correlation analysis showed that the relative expression level of miR-1a was positively correlated with free triiodothyronine (FT3) and free thyroxine (FT4), and negatively related to thyroid stimulating hormone. Spearman’s correlations analysis also revealed that the level of miR-1a was negatively correlated with a critical echocardiographic parameter (left atrial diameter), which was dramatically increased in GD + AF group compared to GD group. Furthermore, the receiver-operating characteristic curve analysis indicated that, among the eight microRNAs, miR-1a had the largest area under the receiver-operating characteristic curves not only for discriminating between individuals with and without Graves’ disease, but also for predicting the presence of atrial fibrillation in patients with Graves’ disease.

Conclusions

Our findings showed that the levels of serum miR-1a were significantly decreased in GD + AF group compared with GD group, suggesting that serum miR-1a might serve as a novel biomarker for diagnosis of atrial fibrillation in patients with Graves’ disease.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. M. den Hoed, M. Eijgelsheim, T. Esko, B.J. Brundel, D.S. Peal, D.M. Evans, I.M. Nolte, A.V. Segre, H. Holm, R.E. Handsaker, H.J. Westra, T. Johnson, A. Isaacs, J. Yang, A. Lundby, J.H. Zhao, Y.J. Kim, M.J. Go, P. Almgren, M. Bochud, G. Boucher, M.C. Cornelis, D. Gudbjartsson, D. Hadley, P. van der Harst, C. Hayward, M. den Heijer, W. Igl, A.U. Jackson, Z. Kutalik, J. Luan, J.P. Kemp, K. Kristiansson, C. Ladenvall, M. Lorentzon, M.E. Montasser, O.T. Njajou, P.F. O’Reilly, S. Padmanabhan, B. St Pourcain, T. Rankinen, P. Salo, T. Tanaka, N.J. Timpson, V. Vitart, L. Waite, W. Wheeler, W. Zhang, H.H. Draisma, M.F. Feitosa, K.F. Kerr, P.A. Lind, E. Mihailov, N.C. Onland-Moret, C. Song, M.N. Weedon, W. **e, L. Yengo, D. Absher, C.M. Albert, A. Alonso, D.E. Arking, P.I. de Bakker, B. Balkau, C. Barlassina, P. Benaglio, J.C. Bis, N. Bouatia-Naji, S. Brage, S.J. Chanock, P.S. Chines, M. Chung, D. Darbar, C. Dina, M. Dorr, P. Elliott, S.B. Felix, K. Fischer, C. Fuchsberger, E.J. de Geus, P. Goyette, V. Gudnason, T.B. Harris, A.L. Hartikainen, A.S. Havulinna, S.R. Heckbert, A.A. Hicks, A. Hofman, S. Holewijn, F. Hoogstra-Berends, J.J. Hottenga, M.K. Jensen, A. Johansson, J. Junttila, S. Kaab, B. Kanon, S. Ketkar, K.T. Khaw, J.W. Knowles, A.S. Kooner, J.A. Kors, M. Kumari, L. Milani, P. Laiho, E.G. Lakatta, C. Langenberg, M. Leusink, Y. Liu, R.N. Luben, K.L. Lunetta, S.N. Lynch, M.R. Markus, P. Marques-Vidal, I. Mateo Leach, W.L. McArdle, S.A. McCarroll, S.E. Medland, K.A. Miller, G.W. Montgomery, A.C. Morrison, M. Muller-Nurasyid, P. Navarro, M. Nelis, J.R. O’Connell, C.J. O’Donnell, K.K. Ong, A.B. Newman, A. Peters, O. Polasek, A. Pouta, P.P. Pramstaller, B.M. Psaty, D.C. Rao, S.M. Ring, E.J. Rossin, D. Rudan, S. Sanna, R.A. Scott, J.S. Sehmi, S. Sharp, J.T. Shin, A.B. Singleton, A.V. Smith, N. Soranzo, T.D. Spector, C. Stewart, H.M. Stringham, K.V. Tarasov, A.G. Uitterlinden, L. Vandenput, S.J. Hwang, J.B. Whitfield, C. Wijmenga, S.H. Wild, G. Willemsen, J.F. Wilson, J.C. Witteman, A. Wong, Q. Wong, Y. Jamshidi, P. Zitting, J.M. Boer, D.I. Boomsma, I.B. Borecki, C.M. van Duijn, U. Ekelund, N.G. Forouhi, P. Froguel, A. Hingorani, E. Ingelsson, M. Kivimaki, R.A. Kronmal, D. Kuh, L. Lind, N.G. Martin, B.A. Oostra, N.L. Pedersen, T. Quertermous, J.I. Rotter, Y.T. van der Schouw, W.M. Verschuren, M. Walker, D. Albanes, D.O. Arnar, T.L. Assimes, S. Bandinelli, M. Boehnke, R.A. de Boer, C. Bouchard, W.L. Caulfield, J.C. Chambers, G. Curhan, D. Cusi, J. Eriksson, L. Ferrucci, W.H. van Gilst, N. Glorioso, J. de Graaf, L. Groop, U. Gyllensten, W.C. Hsueh, F.B. Hu, H.V. Huikuri, D.J. Hunter, C. Iribarren, B. Isomaa, M.R. Jarvelin, A. Jula, M. Kahonen, L.A. Kiemeney, M.M. van der Klauw, J.S. Kooner, P. Kraft, L. Iacoviello, T. Lehtimaki, M.L. Lokki, B.D. Mitchell, G. Navis, M.S. Nieminen, C. Ohlsson, N.R. Poulter, L. Qi, O.T. Raitakari, E.B. Rimm, J.D. Rioux, F. Rizzi, I. Rudan, V. Salomaa, P.S. Sever, D.C. Shields, A.R. Shuldiner, J. Sinisalo, A.V. Stanton, R.P. Stolk, D.P. Strachan, J.C. Tardif, U. Thorsteinsdottir, J. Tuomilehto, D.J. van Veldhuisen, J. Virtamo, J. Viikari, P. Vollenweider, G. Waeber, E. Widen, Y.S. Cho, J.V. Olsen, P.M. Visscher, C. Willer, L. Franke, B.C. Global, C.A. Consortium, J. Erdmann, J.R. Thompson, P.G. Consortium, A. Pfeufer, Q.G. Consortium, N. Sotoodehnia, Q.-I. Consortium, C. Newton-Cheh, C.-A. Consortium, P.T. Ellinor, B.H. Stricker, A. Metspalu, M. Perola, J.S. Beckmann, G.D. Smith, K. Stefansson, N.J. Wareham, P.B. Munroe, O.C. Sibon, D.J. Milan, H. Snieder, N.J. Samani, R.J. Loos, Identification of heart rate-associated loci and their effects on cardiac conduction and rhythm disorders. Nat. Genet. 45(6), 621–631 (2013)

    Article  Google Scholar 

  2. C.T. Sawin, A. Geller, P.A. Wolf, A.J. Belanger, E. Baker, P. Bacharach, P.W. Wilson, E.J. Benjamin, R.B. D’Agostino, Low serum thyrotropin concentrations as a risk factor for atrial fibrillation in older persons. N. Engl. J. Med. 331(19), 1249–1252 (1994)

    Article  CAS  PubMed  Google Scholar 

  3. J. Heeringa, E.H. Hoogendoorn, W.M. van der Deure, A. Hofman, R.P. Peeters, W.C. Hop, M. den Heijer, T.J. Visser, J.C. Witteman, High-normal thyroid function and risk of atrial fibrillation: the Rotterdam study. Arch. Intern. Med. 168(20), 2219–2224 (2008)

    Article  PubMed  Google Scholar 

  4. M.D. Gammage, J.V. Parle, R.L. Holder, L.M. Roberts, F.D. Hobbs, S. Wilson, M.C. Sheppard, J.A. Franklyn, Association between serum free thyroxine concentration and atrial fibrillation. Arch. Intern. Med. 167(9), 928–934 (2007)

    Article  CAS  PubMed  Google Scholar 

  5. X. Luo, B. Yang, S. Nattel, MicroRNAs and atrial fibrillation: mechanisms and translational potential. Nat. Rev. Cardiol. 12(2), 80–90 (2015)

    Article  CAS  PubMed  Google Scholar 

  6. G. Santulli, G. Iaccarino, N. De Luca, B. Trimarco, G. Condorelli, Atrial fibrillation and microRNAs. Front. Physiol. 5, 15 (2014)

    Article  PubMed Central  PubMed  Google Scholar 

  7. R. Liu, X. Ma, L. Xu, D. Wang, X. Jiang, W. Zhu, B. Cui, G. Ning, D. Lin, S. Wang, Differential microRNA expression in peripheral blood mononuclear cells from Graves’ disease patients. J. Clin. Endocrinol. Metab. 97(6), E968–E972 (2012)

    Article  CAS  PubMed  Google Scholar 

  8. R.M. O’Connell, D.S. Rao, A.A. Chaudhuri, D. Baltimore, Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10(2), 111–122 (2010)

    Article  PubMed  Google Scholar 

  9. M. Hulsmans, P. Sinnaeve, B. Van der Schueren, C. Mathieu, S. Janssens, P. Holvoet, Decreased miR-181a expression in monocytes of obese patients is associated with the occurrence of metabolic syndrome and coronary artery disease. J. Clin. Endocrinol. Metab. 97(7), E1213–E1218 (2012)

    Article  CAS  PubMed  Google Scholar 

  10. D.P. Bartel, MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281–297 (2004)

    CAS  PubMed  Google Scholar 

  11. S. Fichtlscherer, S. De Rosa, H. Fox, T. Schwietz, A. Fischer, C. Liebetrau, M. Weber, C.W. Hamm, T. Roxe, M. Muller-Ardogan, A. Bonauer, A.M. Zeiher, S. Dimmeler, Circulating microRNAs in patients with coronary artery disease. Circ. Res. 107(5), 677–684 (2010)

    Article  CAS  PubMed  Google Scholar 

  12. M. Karakas, C. Schulte, S. Appelbaum, F. Ojeda, K.J. Lackner, T. Munzel, R.B. Schnabel, S. Blankenberg, T. Zeller Circulating microRNAs strongly predict cardiovascular death in patients with coronary artery disease-results from the large AtheroGene study. Eur. Heart. J. 38(7), 516–523 (2017)

  13. M.A. Cortez, C. Bueso-Ramos, J. Ferdin, G. Lopez-Berestein, A.K. Sood, G.A. Calin, MicroRNAs in body fluids--the mix of hormones and biomarkers. Nat. Rev. Clin. Oncol. 8(8), 467–477 (2011)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. P.S. Mitchell, R.K. Parkin, E.M. Kroh, B.R. Fritz, S.K. Wyman, E.L. Pogosova-Agadjanyan, A. Peterson, J. Noteboom, K.C. O’Briant, A. Allen, D.W. Lin, N. Urban, C.W. Drescher, B.S. Knudsen, D.L. Stirewalt, R. Gentleman, R.L. Vessella, P.S. Nelson, D.B. Martin, M. Tewari, Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U. S. A. 105(30), 10513–10518 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Y. Zhao, J.F. Ransom, A. Li, V. Vedantham, M. von Drehle, A.N. Muth, T. Tsuchihashi, M.T. McManus, R.J. Schwartz, D. Srivastava, Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 129(2), 303–317 (2007)

    Article  CAS  PubMed  Google Scholar 

  16. O. Adam, B. Lohfelm, T. Thum, S.K. Gupta, S.L. Puhl, H.J. Schafers, M. Bohm, U. Laufs, Role of miR-21 in the pathogenesis of atrial fibrosis. Basic. Res. Cardiol. 107(5), 278 (2012)

    Article  PubMed  Google Scholar 

  17. Z. Girmatsion, P. Biliczki, A. Bonauer, G. Wimmer-Greinecker, M. Scherer, A. Moritz, A. Bukowska, A. Goette, S. Nattel, S.H. Hohnloser, J.R. Ehrlich, Changes in microRNA-1 expression and IK1 up-regulation in human atrial fibrillation. Heart. Rhythm. 6(12), 1802–1809 (2009)

    Article  PubMed  Google Scholar 

  18. X. Luo, Z. Pan, H. Shan, J. **ao, X. Sun, N. Wang, H. Lin, L. **ao, A. Maguy, X.Y. Qi, Y. Li, X. Gao, D. Dong, Y. Zhang, Y. Bai, J. Ai, L. Sun, H. Lu, X.Y. Luo, Z. Wang, Y. Lu, B. Yang, S. Nattel, MicroRNA-26 governs profibrillatory inward-rectifier potassium current changes in atrial fibrillation. J. Clin. Invest. 123(5), 1939–1951 (2013)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. K. Dawson, R. Wakili, B. Ordog, S. Clauss, Y. Chen, Y. Iwasaki, N. Voigt, X.Y. Qi, M.F. Sinner, D. Dobrev, S. Kaab, S. Nattel, MicroRNA29: a mechanistic contributor and potential biomarker in atrial fibrillation. Circulation. 127(14), 1466–1475 (2013). 1475e1461-1428

    Article  CAS  PubMed  Google Scholar 

  20. R.F. Duisters, A.J. Tijsen, B. Schroen, J.J. Leenders, V. Lentink, I. van der Made, V. Herias, R.E. van Leeuwen, M.W. Schellings, P. Barenbrug, J.G. Maessen, S. Heymans, Y.M. Pinto, E.E. Creemers, miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ. Res. 104(2), 170–178 (2009). 176p following 178

    Article  CAS  PubMed  Google Scholar 

  21. N. Cooley, M.J. Cowley, R.C. Lin, S. Marasco, C. Wong, D.M. Kaye, A.M. Dart, E.A. Woodcock, Influence of atrial fibrillation on microRNA expression profiles in left and right atria from patients with valvular heart disease. Physiol. Genomics. 44(3), 211–219 (2012)

    Article  CAS  PubMed  Google Scholar 

  22. Y. Lu, Y. Zhang, N. Wang, Z. Pan, X. Gao, F. Zhang, Y. Zhang, H. Shan, X. Luo, Y. Bai, L. Sun, W. Song, C. Xu, Z. Wang, B. Yang, MicroRNA-328 contributes to adverse electrical remodeling in atrial fibrillation. Circulation. 122(23), 2378–2387 (2010)

    Article  CAS  PubMed  Google Scholar 

  23. T.Y. Ling, X.L. Wang, Q. Chai, T.W. Lau, C.M. Koestler, S.J. Park, R.C. Daly, K.L. Greason, J. Jen, L.Q. Wu, W.F. Shen, W.K. Shen, Y.M. Cha, H.C. Lee, Regulation of the SK3 channel by microRNA-499--potential role in atrial fibrillation. Heart. Rhythm. 10(7), 1001–1009 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  24. C. Bernecker, L. Lenz, M.S. Ostapczuk, S. Schinner, H. Willenberg, M. Ehlers, S. Vordenbaumen, J. Feldkamp, M. Schott, MicroRNAs miR-146a1, miR-155_2, and miR-200a1 are regulated in autoimmune thyroid diseases. Thyroid. 22(12), 1294–1295 (2012)

    Article  CAS  PubMed  Google Scholar 

  25. European Heart Rhythm, A., European Association for Cardio-Thoracic, S., A.J. Camm, P. Kirchhof, G.Y. Lip, U. Schotten, I. Savelieva, S. Ernst, I.C. Van Gelder, N. Al-Attar, G. Hindricks, B. Prendergast, H. Heidbuchel, O. Alfieri, A. Angelini, D. Atar, P. Colonna, R. De Caterina, J. De Sutter, A. Goette, B. Gorenek, M. Heldal, S.H. Hohloser, P. Kolh, J.Y. Le Heuzey, P. Ponikowski, F.H. Rutten, Guidelines for the management of atrial fibrillation: the Task Force for the Management of Atrial Fibrillation of the European Society of Cardiology (ESC). Eur. Heart. J. 31(19), 2369–2429 (2010)

    Article  Google Scholar 

  26. N. Hakimzadeh, A.Y. Nossent, A.M. van der Laan, S.H. Schirmer, M.W. de Ronde, S.J. Pinto-Sietsma, N. van Royen, P.H. Quax, I.E. Hoefer, J.J. Piek, Circulating MicroRNAs Characterizing Patients with Insufficient Coronary Collateral Artery Function. PLoS ONE 10(9), e0137035 (2015)

    Article  PubMed Central  PubMed  Google Scholar 

  27. N.S. Lai, D.G. Wu, X.G. Fang, Y.C. Lin, S.S. Chen, Z.B. Li, S.S. Xu, Serum microRNA-210 as a potential noninvasive biomarker for the diagnosis and prognosis of glioma. Br. J. Cancer. 112(7), 1241–1246 (2015)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. M. **ang, Y. Zeng, R. Yang, H. Xu, Z. Chen, J. Zhong, H. **e, Y. Xu, X. Zeng, U6 is not a suitable endogenous control for the quantification of circulating microRNAs. Biochem. Biophys. Res. Commun. 454(1), 210–214 (2014)

    Article  CAS  PubMed  Google Scholar 

  29. X. Zhang, S. Shao, H. Geng, Y. Yu, C. Wang, Z. Liu, C. Yu, X. Jiang, Y. Deng, L. Gao, J. Zhao, Expression profiles of six circulating microRNAs critical to atherosclerosis in patients with subclinical hypothyroidism: a clinical study. J. Clin. Endocrinol. Metab. 99(5), E766–E774 (2014)

    Article  CAS  PubMed  Google Scholar 

  30. H. Wang, W. Peng, X. Ouyang, W. Li, Y. Dai, Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Transl. Res. 160(3), 198–206 (2012)

    Article  CAS  PubMed  Google Scholar 

  31. Y. Shao, H. Ren, C. Lv, X. Ma, C. Wu, Q. Wang, Changes of serum Mir-217 and the correlation with the severity in type 2 diabetes patients with different stages of diabetic kidney disease. Endocrine 55(1), 130–138 (2017)

    Article  CAS  PubMed  Google Scholar 

  32. L. Jiang, J. Huang, Y. Chen, Y. Yang, R. Li, Y. Li, X. Chen, D. Yang, Identification of several circulating microRNAs from a genome-wide circulating microRNA expression profile as potential biomarkers for impaired glucose metabolism in polycystic ovarian syndrome. Endocrine 53(1), 280–290 (2016)

    Article  CAS  PubMed  Google Scholar 

  33. M. Pelloni, G. Coltrinari, D. Paoli, F. Pallotti, F. Lombardo, A. Lenzi, L. Gandini Differential expression of miRNAs in the seminal plasma and serum of testicular cancer patients. Endocrine (2016). [Epub ahead of print]. doi:10.1007/s12020-016-1150-z

    Article  PubMed  Google Scholar 

  34. L. Shen, F. Huang, L. Ye, W. Zhu, X. Zhang, S. Wang, W. Wang, G. Ning, Circulating microRNA predicts insensitivity to glucocorticoid therapy in Graves’ ophthalmopathy. Endocrine 49(2), 445–456 (2015)

    Article  CAS  PubMed  Google Scholar 

  35. D.D. McManus, K. Tanriverdi, H. Lin, N. Esa, M. Kinno, D. Mandapati, S. Tam, O.N. Okike, P.T. Ellinor, J.F. Keaney Jr., J.K. Donahue, E.J. Benjamin, J.E. Freedman, Plasma microRNAs are associated with atrial fibrillation and change after catheter ablation (the miRhythm study). Heart. Rhythm. 12(1), 3–10 (2015)

    Article  PubMed  Google Scholar 

  36. Z. Liu, C. Zhou, Y. Liu, S. Wang, P. Ye, X. Miao, J. **a, The expression levels of plasma micoRNAs in atrial fibrillation patients. PLoS ONE 7(9), e44906 (2012)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Y. Goren, E. Meiri, C. Hogan, H. Mitchell, D. Lebanony, N. Salman, J.E. Schliamser, O. Amir, Relation of reduced expression of MiR-150 in platelets to atrial fibrillation in patients with chronic systolic heart failure. Am. J. Cardiol. 113(6), 976–981 (2014)

    Article  CAS  PubMed  Google Scholar 

  38. T. Liu, S. Zhong, F. Rao, Y. Xue, Z. Qi, S. Wu, Catheter ablation restores decreased plasma miR-409-3p and miR-432 in atrial fibrillation patients. Europace. 18(1), 92–99 (2016)

    Article  PubMed  Google Scholar 

  39. S. Fazio, E.A. Palmieri, G. Lombardi, B. Biondi, Effects of thyroid hormone on the cardiovascular system. Recent. Prog. Horm. Res. 59, 31–50 (2004)

    Article  CAS  PubMed  Google Scholar 

  40. W.H. Dillmann, Biochemical basis of thyroid hormone action in the heart. Am. J. Med. 88(6), 626–630 (1990)

    Article  CAS  PubMed  Google Scholar 

  41. M. Lagos-Quintana, R. Rauhut, A. Yalcin, J. Meyer, W. Lendeckel, T. Tuschl, Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12(9), 735–739 (2002)

    Article  CAS  PubMed  Google Scholar 

  42. P.K. Rao, Y. Toyama, H.R. Chiang, S. Gupta, M. Bauer, R. Medvid, F. Reinhardt, R. Liao, M. Krieger, R. Jaenisch, H.F. Lodish, R. Blelloch, Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ. Res. 105(6), 585–594 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. D. Terentyev, A.E. Belevych, R. Terentyeva, M.M. Martin, G.E. Malana, D.E. Kuhn, M. Abdellatif, D.S. Feldman, T.S. Elton, S. Gyorke, miR-1 overexpression enhances Ca(2+) release and promotes cardiac arrhythmogenesis by targeting PP2A regulatory subunit B56alpha and causing CaMKII-dependent hyperphosphorylation of RyR2. Circ. Res. 104(4), 514–521 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Y. Lu, S. Hou, D. Huang, X. Luo, J. Zhang, J. Chen, W. Xu, Expression profile analysis of circulating microRNAs and their effects on ion channels in Chinese atrial fibrillation patients. Int. J. Clin. Exp. Med. 8(1), 845–853 (2015)

    CAS  PubMed Central  PubMed  Google Scholar 

  45. B. Yang, H. Lin, J. **ao, Y. Lu, X. Luo, B. Li, Y. Zhang, C. Xu, Y. Bai, H. Wang, G. Chen, Z. Wang, The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat. Med. 13(4), 486–491 (2007)

    Article  CAS  PubMed  Google Scholar 

  46. X. Jia, S. Zheng, X. **e, Y. Zhang, W. Wang, Z. Wang, Y. Zhang, J. Wang, M. Gao, Y. Hou, MicroRNA-1 accelerates the shortening of atrial effective refractory period by regulating KCNE1 and KCNB2 expression: an atrial tachypacing rabbit model. PLoS ONE 8(12), e85639 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  47. F. Stillitano, G. Lonardo, G. Giunti, M. Del Lungo, R. Coppini, V. Spinelli, L. Sartiani, C. Poggesi, A. Mugelli, E. Cerbai, Chronic atrial fibrillation alters the functional properties of If in the human atrium. J. Cardiovasc. Electrophysiol. 24(12), 1391–1400 (2013)

    Article  PubMed  Google Scholar 

  48. H.D. Yu, S. **a, C.Q. Zha, S.B. Deng, J.L. Du, Q. She, Spironolactone Regulates HCN Protein Expression Through Micro-RNA-1 in Rats With Myocardial Infarction. J. Cardiovasc. Pharmacol. 65(6), 587–592 (2015)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Y.D. Li, Y.F. Hong, Y. Yusufuaji, B.P. Tang, X.H. Zhou, G.J. Xu, J.X. Li, L. Sun, J.H. Zhang, Q. **n, J. **ong, Y.T. Ji, Y. Zhang, Altered expression of hyperpolarization-activated cyclic nucleotide-gated channels and microRNA-1 and -133 in patients with age-associated atrial fibrillation. Mol. Med. Rep. 12(3), 3243–3248 (2015)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (81400834), Young Talents Training Project of Tongji University (2013KJ092), and a grant of People’s Hospital of Shanghai Putuo District (RYK15-08).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ying Xue.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of ethic committees of our hospital and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, F., Zhang, Sj., Yao, X. et al. Circulating microRNA-1a is a biomarker of Graves’ disease patients with atrial fibrillation. Endocrine 57, 125–137 (2017). https://doi.org/10.1007/s12020-017-1331-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-017-1331-4

Keywords

Navigation