Hypercoagulability causes atrial fibrosis and promotes atrial fibrillation

European Heart Journal

Volumn 38, Issue 1, 2017, Pages 38-50

  Spronk, Henri M H ^a   De Jong, Anne Margreet ^b   Verheule, Sander ^a   De Boer, Hetty C ^c   Maass, Alexander H ^b   Lau, Dennis H ^a   Rienstra, Michiel ^b   Van Hunnik, Arne ^a   Kuiper, Marion ^a   Lumeij, Stijn ^a   Zeemering, Stef ^a   Linz, Dominik ^d   Kamphuisen, Pieter Willem ^b   Ten Cate, Hugo ^a   Crijns, Harry J ^e   Van Gelder, Isabelle C ^b   Van Zonneveld, Anton Jan ^c   Schotten, Ulrich ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d SAARLAND UNIVERSITY   (Germany)

^e MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Atrial fibrillation; Atrial fibrosis; Direct thrombin inhibitors; Hypercoagulability; Protease activated receptors; Stroke

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; DABIGATRAN; INTERLEUKIN 6; INTERSTITIAL COLLAGENASE; MONOCYTE CHEMOTACTIC PROTEIN 1; NADROPARIN; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA1; ANTITHROMBIN; FIBRINOLYTIC AGENT; INDAZOLE DERIVATIVE; N3-CYCLOPROPYL-7-((4-(1-METHYLETHYL)PHENYL)METHYL)-7H-PYRROLO(3, 2-F)QUINAZOLINE-1,3-DIAMINE; PEPTIDE HYDROLASE; PYRROLE DERIVATIVE; QUINAZOLINE DERIVATIVE; RWJ-56110; THROMBIN RECEPTOR; UREA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATRIAL FIBRILLATION; CELL PROLIFERATION; COLLAGEN SYNTHESIS; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTROCARDIOGRAM; FEMALE; GENE EXPRESSION; HYPERCOAGULABILITY; MYOFIBROBLAST; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; VASCULAR SMOOTH MUSCLE CELL; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; DRUG EFFECTS; FIBROBLAST; FIBROSIS; GOAT; HEART ATRIUM; PATHOLOGY; PATHOPHYSIOLOGY; THROMBOPHILIA; TRANSGENIC MOUSE;

ANALYSIS OF VARIANCE; ANIMALS; ANTITHROMBINS; ATRIAL FIBRILLATION; CELL PROLIFERATION; DABIGATRAN; FEMALE; FIBRINOLYTIC AGENTS; FIBROBLASTS; FIBROSIS; GOATS; HEART ATRIA; INDAZOLES; MICE, TRANSGENIC; NADROPARIN; PEPTIDE HYDROLASES; PYRROLES; QUINAZOLINES; RATS; RECEPTORS, THROMBIN; THROMBIN; THROMBOPHILIA; UREA;

EID: 85016061061     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehw119     Document Type: Article

References (40)

1. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinase-activated receptors. Pharmacol Rev 2001;53:245-282.
2. Borissoff JI, Spronk HM, ten Cate H. The hemostatic system as a modulator of ath-erosclerosis. N Engl J Med 2011;364:1746-1760.
3. Borensztajn K, Peppelenbosch MP, Spek CA. Factor Xa: at the crossroads between coagulation and signaling in physiology and disease. Trends Mol Med 2008;14: 429-440.
4. Antoniak S, Pawlinski R, Mackman N. Protease-activated receptors and myocardial infarction. IUBMB Life 2011;63:383-389.
5. Borissoff JI, Spronk HM, Heeneman S, ten Cate H. Is thrombin a key player in the 'coagulation-atherogenesis' maze? Cardiovasc Res 2009;82:392-403.
6. Steinberg SF. The cardiovascular actions of protease-activated receptors. Mol Phar-macol 2005;67:2-11.
7. Sabri A, Muske G, Zhang H, Pak E, Darrow A, Andrade-Gordon P, Steinberg SF. Signaling properties and functions of two distinct cardiomyocyte protease-activated receptors. Circ Res 2000;86:1054-1061.
8. Antoniak S, Rojas M, Spring D, Bullard TA, Verrier ED, Blaxall BC, Mackman N, Pawlinski R. Protease-activated receptor 2 deficiency reduces cardiac ischemia/reperfusion injury. Arterioscler Thromb Vasc Biol 2010;30:2136-2142.
9. Moshal KS, Tyagi N, Moss V, Henderson B, Steed M, Ovechkin A, Aru GM, Tyagi SC. Early induction of matrix metalloproteinase-9 transduces signaling in human heart end stage failure. J Cell Mol Med 2005;9:704-713.
10. Ide J, Aoki T, Ishivata S, Glusa E, Strukova SM. Proteinase-activated receptor agonists stimulate the increase in intracellular Ca2+ in cardiomyocytes and proliferation of cardiac fibroblasts from chick embryos. Bull Exp Biol Med 2007;144: 760-763.
11. Sabri A, Short J, Guo J, Steinberg SF. Protease-activated receptor-1-mediated DNA synthesis in cardiac fibroblast is via epidermal growth factor receptor transactiva-tion: distinct PAR-1 signaling pathways in cardiac fibroblasts and cardiomyocytes. Circ Res 2002;91:532-539.
12. Pawlinski R, Tencati M, Hampton CR, Shishido T, Bullard TA, Casey LM, Andrade-Gordon P, Kotzsch M, Spring D, Luther T, Abe J, Pohlman TH, Verrier ED, Blaxall BC, Mackman N. Protease-activated receptor-1 contributes to cardiac remodeling and hypertrophy. Circulation 2007;116:2298-2306.
13. Bogatkevich GS, Ludwicka-Bradley A, Silver RM. Dabigatran, a direct thrombin inhibitor, demonstrates antifibrotic effects on lung fibroblasts. Arthritis Rheum 2009; 60:3455-3464.
14. Cevikbas F, Seeliger S, Fastrich M, Hinte H, Metze D, Kempkes C, Homey B, Steinhoff M. Role of protease-activated receptors in human skin fibrosis and sclero-derma. Exp Dermatol 2011;20:69-71.
15. Fiorucci S, Antonelli E, Distrutti E, Severino B, Fiorentina R, Baldoni M, Caliendo G, Santagada V, Morelli A, Cirino G. PAR1 antagonism protects against experimental liver fibrosis. Role of proteinase receptors in stellate cell activation. Hepatology 2004;39:365-375.
16. Schotten U, Verheule S, Kirchhof P, Goette A. Pathophysiological mechanisms of atrial fibrillation: a translational appraisal. Physiol Rev 2011;91:265-325.
17. Voloshenyuk TG, Landesman ES, Khoutorova E, Hart AD, Gardner JD. Induction of cardiac fibroblast lysyl oxidase by TGF-beta1 requires PI3K/Akt, Smad3, and MAPK signaling. Cytokine 2011;55:90-97.
18. Takeda N, Manabe I, Uchino Y, Eguchi K, Matsumoto S, Nishimura S, Shindo T, Sano M, Otsu K, Snider P, Conway SJ, Nagai R. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest 2010;120:254-265.
19. Weiler-Guettler H, Christie PD, Beeler DL, Healy AM, Hancock WW, Rayburn H, Edelberg JM, Rosenberg RD. A targeted point mutation in thrombomodulin generates viable mice with a prethrombotic state. J Clin Invest 1998;101:1983-1991.
20. Borissoff JI, Otten JJ, Heeneman S, Leenders P, van Oerle R, Soehnlein O, Loubele ST, Hamulyak K, Hackeng TM, Daemen MJ, Degen JL, Weiler H, Esmon CT, van Ryn J, Biessen EA, Spronk HM, Ten Cate H. Genetic and pharmacological modifications of thrombin formation in apolipoprotein E-deficient mice determine atherosclerosis severity and atherothrombosis onset in a neutrophil-dependent manner. PLoS One 2013;8:e55784.
21. Allessie MA, de Groot NM, Houben RP, Schotten U, Boersma E, Smeets JL, Crijns HJ. Electropathological substrate of long-standing persistent atrial fibrillation in patients with structural heart disease: longitudinal dissociation. Circ Arrhythm Electrophysiol 2010;3:606-615.
22. Verheule S, Tuyls E, Gharaviri A, Hulsmans S, van Hunnik A, Kuiper M, Serroyen J, Zeemering S, Kuijpers NH, Schotten U. Loss of continuity in the thin epicardial layer because of endomysial fibrosis increases the complexity of atrial fibrillatory conduction. Circ Arrhythm Electrophysiol 2013;6:202-211.
23. Eckstein J, Zeemering S, Linz D, Maesen B, Verheule S, van Hunnik A, Crijns H, Allessie MA, Schotten U. Transmural conduction is the predominant mechanism of breakthrough during atrial fibrillation: evidence from simultaneous endo-epicar-dial high-density activation mapping. Circ Arrhythm Electrophysiol 2013;6:334-341.
24. Zeemering S, Maesen B, Nijs J, Lau DH, Granier M, Verheule S, Schotten U. Auto-mated quantification of atrial fibrillation complexity by probabilistic electrogram analysis and fibrillation wave reconstruction. Conf Proc IEEE Eng Med Biol Soc 2012;2012:6357-6360.
25. Loeffen R, Kleinegris MC, Loubele ST, Pluijmen PH, Fens D, van Oerle R, ten Cate H, Spronk HM. Preanalytic variables of thrombin generation: towards a standard procedure and validation of the method. J Thromb Haemost 2012;10: 2544-2554.
26. Khairoun M, van der Pol P, de Vries DK, Lievers E, Schlagwein N, de Boer HC, Bajema IM, Rotmans JI, van Zonneveld AJ, Rabelink TJ, van Kooten C, Reinders ME. Renal ischemia-reperfusion induces a dysbalance of angiopoietins, ac-companied by proliferation of pericytes and fibrosis. Am J Physiol Renal Physiol 2013; 305:F901-F910.
27. Verheule S, Tuyls E, van Hunnik A, Kuiper M, Schotten U, Allessie M. Fibrillatory conduction in the atrial free walls of goats in persistent and permanent atrial fibrillation. Circ Arrhythm Electrophysiol 2010;3:590-599.
28. Nural-Guvener HF, Zakharova L, Nimlos J, Popovic S, Mastroeni D, Gaballa MA. HDAC class I inhibitor, Mocetinostat, reverses cardiac fibrosis in heart failure and diminishes CD90+ cardiac myofibroblast activation. Fibrogenesis Tissue Repair 2014;7:10.
29. Hewitson TD, Martic M, Kelynack KJ, Pagel CN, Mackie EJ, Becker GJ. Thrombin is a pro-fibrotic factor for rat renal fibroblasts in vitro. Nephron Exp Nephrol 2005;101: e42-e49.
30. Bogatkevich GS, Tourkina E, Silver RM, Ludwicka-Bradley A. Thrombin differentiates normal lung fibroblasts to a myofibroblast phenotype via the proteolytically activated receptor-1 and a protein kinase C-dependent pathway. J Biol Chem 2001;276:45184-45192.
31. Sonin DL, Wakatsuki T, Routhu KV, Harmann LM, Petersen M, Meyer J, Strande JL. Protease-Activated Receptor 1 Inhibition by SCH79797 Attenuates Left Ventricular Remodeling and Profibrotic Activities of Cardiac Fibroblasts. J Cardiovasc Phar-macol Ther 2013;18:460-475.
32. Snead AN, Insel PA. Defining the cellular repertoire of GPCRs identifies a profibro-tic role for the most highly expressed receptor, protease-activated receptor 1, in cardiac fibroblasts. FASEB J 2012;26:4540-4547.
33. Howell DC, Johns RH, Lasky JA, Shan B, Scotton CJ, Laurent GJ, Chambers RC. Absence of proteinase-activated receptor-1 signaling affords protection from bleomycin-induced lung inflammation and fibrosis. Am J Pathol 2005;166: 1353-1365.
34. Strande JL, Hsu A, Su J, Fu X, Gross GJ, Baker JE. SCH 79797, a selective PAR1 antagonist, limits myocardial ischemia/reperfusion injury in rat hearts. Basic Res Cardiol 2007;102:350-358.
35. Mann KG, Nesheim ME, Church WR, Haley P, Krishnaswamy S. Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 1990;76:1-16.
36. Mann KG, Butenas S, Brummel K. The dynamics of thrombin formation. Arterioscler Thromb Vasc Biol 2003;23:17-25.
37. Bae JS, Yang L, Rezaie AR. Factor X/Xa elicits protective signaling responses in endothelial cells directly via PAR-2 and indirectly via endothelial protein C receptor-dependent recruitment of PAR-1. J Biol Chem 2010;285:34803-34812.
38. Bukowska A, Zacharias I, Weinert S, Skopp K, Hartmann C, Huth C, Goette A. Coagulation factor Xa induces an inflammatory signalling by activation of protease-activated receptors in human atrial tissue. Eur J Pharmacol. 2013;718: 114-123.
39. Porter KE, Turner NA. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther 2009;123:255-278.
40. Rohr S. Cardiac fibroblasts in cell culture systems: myofibroblasts all along? J Cardiovasc Pharmacol 2011;57:389-399.