Role of β 1-adrenoceptor autoantibodies in the pathogenesis of dilated cardiomyopathy

Immunobiology

Volumn 217, Issue 5, 2012, Pages 511-520

  Dandel, Michael ^a   Wallukat, Gerd ^a   Potapov, Evgenij ^a   Hetzer, Roland ^a  

^a DEUTSCHES HERZZENTRUM BERLIN   (Germany)

Author keywords

1 receptors; Autoantibodies; Dilated cardiomyopathy; Immunoadsorption; Pathogenesis

Indexed keywords

AUTOANTIBODY; BETA 1 ADRENERGIC RECEPTOR; BETA 1 ADRENERGIC RECEPTOR ANTIBODY; BETA 1 ADRENERGIC RECEPTOR BLOCKING AGENT; BISOPROLOL; CARVEDILOL; IMMUNOGLOBULIN; METOPROLOL; UNCLASSIFIED DRUG;

AUTOIMMUNITY; CONGESTIVE CARDIOMYOPATHY; DISEASE COURSE; HEART ASSIST DEVICE; HEART TRANSPLANTATION; HUMAN; IMMUNOADSORPTION; MEDICAL RESEARCH; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PREVALENCE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVIEW; TREATMENT OUTCOME;

ANIMALS; AUTOANTIBODIES; CARDIOMYOPATHY, DILATED; HUMANS; INFLAMMATION; RECEPTORS, ADRENERGIC, BETA-1;

EID: 84858798293     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2011.07.012     Document Type: Review

References (98)

1. Alvarez F.L., Neu N., Rose N.R., Craig S.W., Beisel K.W. Heart-specific autoantibodies induced by coxackievirus B3: identification of heart autoantigens. Clin. Immunol. Immunopathol. 1987, 43:129-139.
2. Anderson J.L., Carlquist J.F., Hammond E.H. Deficient natural killer cell activity in patients with idiopathic dilated cardiomyopathy. Lancet 1982, 2:1124-1127.
3. Angers S., Salahpour A., Bouvier M. Dimerization: an emerging concept for G protein-coupled receptor ontogeny and function. Annu. Rev. Pharmacol. Toxicol. 2002, 42:409-435.
4. Baba A., Yoshikawa T., Ogawa S. Autoantibodies against sarcolemmal Na-K-ATPase: possible upstream targets of arrhythmias and sudden deaths in patients with dilated cadiomyopathy. J. Am. Coll. Cardiol. 2002, 40:1153-1159.
5. Baba A., Yoshikawa T., Fukuda Y., Sugiyama T., Shimada M., Akaishi M., Tsuchimoto K., Ogawa S., Fu M. Autoantibodies against M2-muscarinic acetylcholine receptors: new upstream targets in atrial fibrilation in patients with dilated cardiomyopathy. Eur. Heart J. 2004, 25:1108-1115.
6. Bristow M.R. β-Adrenergic receptor blockade in chronic heart failure. Circulation 2000, 101:558-569.
7. 1-adrenergic receptor. Clin. Exp. Immunol. 2006, 143(2):209-215.
8. Caforio A.L., Grazini M.M., Mann M.J., Keeling P.J., Bottazzo G.F., McKenna W.J., Schiaffino S. Identification of alpha- and beta-cardiac myosin heavy chain isoforms as major antigens in dilated cardiomyopathy. Circulation 1992, 85:1734-1742.
9. Caforio A.L., Mahon N.J., Tona F., McKenna W.J. Circulating cardiac autoantibodies in dilated cardiomyopathy and myocarditis: pathogenic and clinical significance. Eur. J. Heart Fail. 2002, 4:411-417.
10. Carlquist J.F., Menlove R.L., Murray M.B., O'Connell J.B., Anderson J.L. HLA class II (DR and DQ) antigen associations in idiopathic dilated cardiomyopathy. Validation study and meta-analysis of published HLA association studies. Circulation 1991, 83:515-522.
11. Christ T., Wettwer E., Dobrew D., Adolph E., Knaut M., Wallukat G., Ravens U. Autoantibodies against the beta-1 adrenoceptor prolong action potential duration and enhance contractility in isolated cardiomyocytes. J. Mol. Cell. Cardiol. 2001, 33:1515-1525.
12. Cooper L.T., Belohlavek M., Korinek J., Yoshifuku S., Sengupta P.P., Burgstaler E.A., Winters J.L. A pilot study to asses the use of protein A immunoadsorption for chronic dilated cardiomyopathy. J. Clin. Apheresis 2007, 22:210-214.
13. Cunningham M.W., Hall N.K., Krisher K.K., Spanier A.M. A study of antigroup A streptococcal monoclonal antibodies cross-reactive with myosin. J. Immunol. 1986, 136:293-298.
14. Dandel M., Weng Y., Siniawski H., Potapov E., Drews T., Lehmkuhl H.B., Knosalla C., Hetzer R. Prediction of cardiac stability after weaning from ventricular assist devices in patients with idiopathic dilated cardiomyopathy. Circulation 2008, 118(Suppl. 1):S94-S105.
15. Dandel M., Wallukat G., Englert A., Lehmkuhl H.B., Hetzer R. Are the therapeutic benefits of extracorporeal immunoglobulin adsorption in beta-1 adrenoceptor autoantibody positive patients with dilated cardiomyopathy indeed related to the removal of these antibodies?. Circulation 2010, 122(Suppl.):A10319.
16. Dandel M., Wallukat G., Englert A., Lehmkuhl H.B., Hetzer R. Efficacy of immunoadsorption as bridge-to-transplant therapy in patients with idiopathic dilated cardiomyopathy and evidence of Beta-1 adrenoceptor autoantibodies. J. Heart Lung Transplant. 2010, 29(2):163-164.
17. Dörfel W.V., Felix S.B., Wallukat G., Brehme S., Bestvater K., Hofmann T., Kleber F.X., Baumann G., Reinke P. Short term hemodynamic effects of immunoadsorption in dilated cardiomyopathy. Circulation 1997, 95:1994-1997.
18. Dörfel W.V., Wallukat G., Dörfel Y., Felix S.B., Baumann G. Immunoadsorption in dilated cardiomyopathy, a 3 year follow-up. Int. J. Cardiol. 2004, 97(3):529-534.
19. Felix S.B., Staudt A., Dörffel W.V., Stangl V., Merkel K., Pohl M., Döcke W.D., Morgera S., Neumayer H.H., Wernecke K.D., Wallukat G., Stangl K., Baumann G. Hemodynamic effects of immunoadsorption and subsequent immunoglobulin substitution in dilated cardiomyopathy: three month results from a randomized study. J. Am. Coll. Cardiol. 2000, 35(6):1590-1598.
20. Felix S.B., Staudt A., Landsberger M., Grosse Y., Stangl V., Spielhagen T., Wallukat G., Wernecke K.D., Baumann G., Stangl K. Removal of cardiodepressant antibodies in dilated cardiomyopathy by immunoadsorbtion. J. Am. Coll. Cardiol. 2002, 39(4):646-652.
21. Felix S., Staudt A. Immunoadsorption as treatment option in dilated cardiomyopathy. Autoimmunity 2008, 41(6):484-489.
22. Fowles R.E., Bieker C.P., Stinson E.B. Defective in vitro suppressor cell function in idiopathic congestive cardiomyopathy. Circulation 1979, 59:483-491.
23. Freedman N.J., Lefkowitz R.J. Anti-beta(1)-adrenergic receptor antibodies and heart failure: causation, not just correlation. J. Clin. Invest. 2004, 113:1379-1382.
24. 1-adrenergic receptor: involvement of G protein-coupled receptor kinase and cAMP dependent protein kinase. J. Biol. Chem. 1995, 270:17953-17961.
25. Fu L.X., Magnusson Y., Bergh C.H., Liljeqvist J.A., Waagstein F., Hjalmarson A., Hoebeke J. Location of functional autoimmune epitope on muscarinic acetylcholine receptor-2 in patients with idiopathic dilated cardiomyopathy. J. Clin. Invest. 1993, 91(5):1964-1968.
26. 1-adrenergic receptors induces early after-depolarization and decreases in K-channel density in rabbits. J. Am. Coll. Cardiol. 2004, 43:1090-1100.
27. Gavin J.E., Hemric M.E., Kosanke S.D., Factor S.M., Quinn A., Cunningham M.W. Induction of myocarditis and valvulitis in Lewis rats by different epitopes of cardiac myosin and its implications in rheumatic carditis. Am. J. Pathol. 2002, 160:297-306.
28. Gerli R., Rambotti P., Spinozzi F., Bertotto A., Chiodini V., Solinas P., Gernini I., Davis S. Immunologic studies of peripheral blood from patients with idiopathic dilated cardiomyopathy. Am. Heart J. 1986, 112:350-355.
29. Groser S., Andrassy M., Buss S.J., Leuschner F., Volz C.H., Ottl R., Zittrich S., Blaudeck N., Hardt S.E., Pfitzer G., Rose N.R., Katus H.A., Kaya Z. Cardiac troponin I but not cardiac troponin T induces severe autoimmune inflammation in the myocardium. Circulation 2006, 114:1693-1702.
30. Goodwin J.F. Mechanisms in cardiomyopathies. J. Mol. Cell. Cardiol. 1985, 17(Suppl. 2):5-9.
31. Herda L.R., Trimpert C., Nauke U., Landsberger M., Hummel A., Beug D., Kieback A., Dörr M., Empen K., Knebel F., Ewert R., Angelow A., Hoffmann W., Felix S.B., Staudt A. Effects of immunoadsorption and subsequent immunoglobulin G substitution on cardiopulmonary exercise capacity in patients with dilated cardiomyopathy. Am. Heart J. 2010, 159(5):809-816.
32. Hoebecke J. Structural basis of autoimmunity against G protein coupled membrane receptors. Int. J. Cardiol. 1996, 54:103-111.
33. Horwich T.B., Patel J., MacLellan W.R., Fonarow G.C. Cardiac troponin I is associated with impaired hemodynamics, progressive left ventricular dysfunction and increased mortality rates in advanced heart failure. Circulation 2003, 108:833-838.
34. Iaccario G., Tomhave E.D., Lefkowitz R.J., Koch W.J. Reciprocal in vivo regulation of myocardial G protein-coupled receptor kinase expression by β-adrenergic receptor stimulation and blockade. Circulation 1998, 98:1783-1789.
35. Ikeda U., Kasai H., Izawa A., Koyama J., Yazaki Y., Takahashi M., Higuchi M., Koh C.S., Yamamoto K. Immunoadsorbtion therapy for patients with dilated cardiomyopathy and heart failure. Curr. Cardiol. Rev. 2008, 4:219-222.
36. 1-adrenergic receptors predict ventricular tachycardia and sudden death in patients with idiopathic dilated cardiomyopathy. J. Am. Coll. Cardiol. 2001, 37:418-424.
37. Jahns R., Boivin V., Siegmund C., Inselmann G., Lohse M.J., Boege F. Autoantibodies activating human beta adrenergic receptors are associated with reduced cardiac function in chronic heart failure. Circulation 1999, 99:649-654.
38. 1-adrenoceptor activity by domain specific antibodies and heart failure-associated autoantibodies. J. Am. Coll. Cardiol. 2000, 36:1280-1287.
39. Jahns R., Boivin V., Hein L., Triebel S., Angermann C.E., Ertl G., Lohse M.J. Direct evidence for beta-1 adrenergic receptor directed autoimmune attack as a cause of idiopathic dilated cardiomyopathy. J. Clin. Invest. 2004, 113:1419-1429.
40. Jane-wit D., Altuntas C.Z., Johnson J.M., Yong S., Wickley P.J., Clark P., Wang Q., Popović Z.B., Penn M.S., Damron D.S., Perez D.M., Tuohy V.K. β1-adrenergic receptor autoantibodies mediate dilated cardiomyopathy by agonistic induced apoptosis. Circulation 2007, 116:399-410.
41. Kawai C., Takatsu T. Clinical experimental studies on cardiomyopathy. N. Engl. J. Med. 1975, 293:592-597.
42. Knebel F., Böhm M., Staudt A., Borges A.C., Tepper M., Jochmann N., Wernicke K.D., Felix S., Baumann G. Reduction of morbidity by immunoadsorption therapy in patients with dilated cardiomyopathy. Int. J. Cardiol. 2004, 97(3):517-520.
43. Konstadoulakis M.M., Krombouzou H., Tsiamis H., Trikas A., Toutouzas P. Clinical significance of antibodies against tropomyosin, actin and myosin in patients with dilated cardiomyopathy. J. Clin. Lab. Immunol. 1993, 40:61-67.
44. Kuethe F., Sigusch H.H., Hilbig K., Tresselt C., Glück B., Egerer R., Figulla H.R. Detection of viral genome in the myocardium: lack of prognostic and functional relevance. Am. Heart J. 2007, 153:850-858.
45. Kühl U., Noutsias M., Seeberg B., Schultheiss H.P. Immunological evidence of a chronic intramyocardial inflammatory process in dilated cardiomyopathy. Heart 1996, 75:295-300.
46. Kühl U., Pauschinger M., Seeberg B., Lassner D., Noutsias M., Poller W., Schultheiss H.P. Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation 2005, 112:1965-1970.
47. Kühl U., Pauschinger M., Schwimmbeck P.L., Seeberg B., Lober C., Noutsias M., Poller W., Schultheiss H.P. Interferon-beta treatment eliminates cardiotropic viruses and improves left ventricular function in patients with myocardial persistence of viral genomes and left ventricular dysfunction. Circulation 2003, 107:2793-2798.
48. Lappé J.M., Pelfrey C.M., Tang W.W.H. Recent insights into the role of autoimmunity in idiopathic dilated cardiomyopathy. J. Card. Fail. 2008, 14(6):521-530.
49. Lauer B., Schannwell M., Kuhl U., Strauer B.E., Schultheiss H.P. Anitimyosin autoantibodies are associated with deterioration of systolic and diastolic left ventricular function in patients with chronic myocarditis. J. Am. Coll. Cardiol. 2000, 35:11-18.
50. 1-adrenoceptor antibodies in dilated cardiomyopathy and Chagas' disease. Autoimmunity 2008, 41(6):429-433.
51. Li Y., Heuser J.S., Cunningham L.C., Kosanke S.D., Cunningham M.W. Mimicry and antibody-mediated cell signaling in autoimmune myocarditis. J. Immunol. 2006, 177:8234-8240.
52. Limas C.J., Goldenberg I.F., Limas C. Autoantibodies against beta-1-adrenoceptors in human idiopathic dilated cardiomyopathy. Circ. Res. 1989, 64:97-103.
53. Limas C.J., Goldenberg I.F., Limas C. Soluble interleukin-2 receptor levels in patients with dilated cardiomyopathy: correlation with disease severity and cardiac antibodies. Circulation 1995, 91:631-634.
54. Limas C.J., Iakovis P., Anyfantakis A., Kroupis C., Cokkinos D.V. Familial clustering of autoimmune diseases in patients with dilated cardiomyopathy. Am. J. Cardiol. 2004, 93:1189-1191.
55. Maekawa Y., Ouzounian M., Opavsky M.A., Liu P.P. Connecting the missing link between dilated cardiomyopathy and viral myocarditis: virus, cytoskeleton, and innate immunity. Circulation 2007, 115:5-8.
56. Magnusson Y., Wallukat G., Waagstein F., Hjalmarson A., Hoebeke J. Autoimmunity in idiopathic dilated cardiomyopathy: characterization of antibodies against the beta-1-adrenoceptor with positive chronotropic effect. Circulation 1994, 89:2760-2767.
57. Maron B.J., Towbin J.A., Thieme G., Antzelevitch C., Corrado D., Arnett D., Moss A.J., Seidman C.E., Young J.B. Contemporary definitions and classification of cardiomyopathies: an American Heart Association Scientific Statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Group; Council on Epidemiology and Prevention. Circulation 2006, 113:1807-1816.
58. Matsui S., Fu M.L., Katsuda S., Hayase M., Yamaguchi N., Teraoka K., Kurihara T., Takekoshi N., Murakami E., Hoebeke J., Hjalmarson A. Peptides derived from cardiovascular G-protein-coupled receptors induce morphological cardiomyopathic changes in immunized rabbits. J. Mol. Cell. Cardiol. 1997, 29:641-655.
59. Matsui S., Persson M., Fu H.-M., Hayase M., Katsuda S., Teraoka K., Kurihara T., Fu M.L. Protective effect of bisoprolol on beta-1 adrenoceptor peptide-induced autoimmune myocardial damage in rabbits. Herz 2000, 3:267-270.
60. Matsui S., Fu M.L., Hayase M., Katsuda S., Yamaguchi N., Teraoka K., Kurihara T., Murano H., Takekoshi N. Transfer of immune components from rabbit autoimmune cardiomyopathy into severe combined immunodeficiency (SCID) mice induces cardiomyopathic changes. Autoimmunity 2006, 39(2):121-128.
61. McKenna C.J., Codd M.B., McCann H.A., Sugrue D.D. Idiopathic dilated cardiomyopathy: familial prevalence and HLA distribution. Heart 1997, 77:549-552.
62. Mestroni L., Gilbert E.M., Bohmeyer T.J., Bristow M.R. Dilated cardiomyopathies. Hurst's The Heart 2004, vol. 2:1889-1908. McGraw-Hill Companies Inc, New York, London, Toronto, Part 11 (Chapter 76). 11th ed.
63. Michels V.V., Moll P.P., Miller F.A., Tajik A.J., Chu J.S., Driscoll D.J., Burnett J.C., Rodeheffer R.J., Chesebro J.H., Tazelaar H.D. The frequency of familial dilated cardiomyopathy in a series of patients with dilated cardiomyopathy. N. Engl. J. Med. 1992, 326:77-82.
64. 1-adrenoceptor. J. Autoimmun. 1999, 13:179-186.
65. Mobini R., Staudt A., Felix S.B., Baumann G., Wallukat G., Deinum J., Svensson H., Hjalmarson A., Fu M. Hemodynamic improvement and removal of auto-antibodies against beta-1-adrenergic receptor by immunoadsorption therapy in dilated cardiomyopathy. J. Autoimmun. 2003, 20:345-350.
66. Müller J., Wallukat G., Weng Y., Dandel M., Spiegelsberger S., Semrau S., Brandes K., Theodoridis V., Loebe M., Meyer R., Hetzer R. Weaning from mechanical cardiac support in patients with idiopathic dilated cardiomyopathy. Circulation 1997, 96:542-549.
67. Müller J., Wallukat G., Dandel M., Bieda H., Brandes K., Spiegelsberger S., Nissen E., Kunze R., Hetzer R. Immunoglobulin adsorption in patients with idiopathic dilated cardiomyopathy. Circulation 2000, 101(4):385-391.
68. Noutsias M., Pauschinger M., Schultheiss H., Kh U. Phenotype characterization in dilated cardiomyopathy - diagnostic significance of T lymphocytes and macrophages in inflammatory cardiomyopathy. Med. Sci. Monit. 2002, 8:CR478-CR487.
69. Okazaki T., Tanaka Y., Nishio R., Mitsuiye T., Mizoguchi A., Wang J., Ishida M., Hiai H., Matsumori A., Minato N., Honjo T. Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat. Med. 2003, 9:1477-1483.
70. Okuno T., Takahashi K., Balachandra K., Shiraki K., Yamanishi K., Takahashi M., Baba K. Sero-epidemiology of human herpes virus 6 infection in normal children and adults. J. Clin. Microbiol. 1989, 27:651-653.
71. Omerovic E., Bollano E., Andersson B., Kujacic V., Schulze W., Hjalmarson A., Waagstein F., Fu M. Induction of cardiomyopathy in severe combined immuno-deficiency mice by transfer of lymphocytes from patients with idiopathic dilated cardiomyopathy. Autoimmunity 2000, 32:271-280.
72. Pitcher J.A., Freedman N.J., Lefkowitz R.J. G protein-coupled receptor kinase. Annu. Rev. Biochem. 1998, 67:553-592.
73. 1-adrenergic receptor expression in neonatal rat cardiomyocytes. Circulation 1998, 98:2470-2476.
74. Sampietro T., Neglia D., Bionda A., Dal Pino B., Bigazzi F., Puntoni M., Startari U., Morales A., Minichilli F., Bianchi F., L'Abbate A. Inflammatory markers and serum lipids in idiopathic dilated cardiomyopathy. Am. J. Cardiol. 2005, 96:1718-1720.
75. Schimke I., Müller J., Priem F., Kruse I., Schön B., Stein J., Kunze R., Wallukat G., Hetzer R. Decreased oxidative stress in patients with idiopathic dilated cardiomyopathy: one year after immunoglobulin adsorption. J. Am. Coll. Cardiol. 2001, 38:178-183.
76. Schulze K., Becker B.F., Schauer R., Schultheiss H.P. Antibodies to ADP-ATP carrier - an autoantigen in myocarditis and dilated cardiomyopathy-impair cardiac function. Circulation 1990, 81:959-969.
77. Schulze W., Kunze R., Wallukat G. Pathophysiological role of autoantibodies against G-protein-coupled receptors in the cardiovascular system. Exp. Clin. Cardiol. 2005, 10:170-178.
78. Shmilowich H., Danon A., Binah O., Roth A., Chen G., Wexler D., Keren G., George J. Autoantibodies to cardiac troponin I in patients with idiopathic dilated and ischemic cardiomyopathy. Int. J. Cardiol. 2007, 117:198-203.
79. Staudt A., Schaper F., Stangl V., Plagemann A., Böhm M., Merkel K., Wallukat G., Wernecke K.D., Stangl K., Baumann G., Felix S.B. Immunohistological changes in dilated cardiomyopathy induced by immunoadsorption therapy and subsequent immunoglobulin substitution. Circulation 2001, 103:2681-2686.
80. Staudt A., Mobini R., Fu M., Grosse Y., Stangl V., Stangl K., Thiele A., Baumann G., Felix S.B. Beta (1)-adrenoceptor antibodies induce positive inotropic response in isolated cardiomyocytes. Eur. J. Pharmacol. 2001, 423:115-119.
81. Staudt A., Böhm M., Knebel F., Grosse Y., Bischoff C., Hummel A., Dahm J.B., Borges A., Jochmann N., Wernecke K.D., Wallukat G., Baumann G., Felix S.B. Potential role of antibodies belonging to the immunoglobulin G-3 subclass in cardiac dysfunction among patients with dilated cardiomyopathy. Circulation 2002, 106:2448-2453.
82. Staudt Y., Mobini R., Fu M., Felix S.B., Kühn J.P., Staudt A. Beta-1-adrenoceptor autoantibodies induce apoptosis in adult isolated cardiomyocytes. Eur. J. Pharmacol. 2003, 466:1-6.
83. Staudt A., Dörr M., Staud Y., Böhm M., Probst M., Empen K., Plötz S., Maschke H.E., Hummel A., Baumann G., Felix S.B. Role of immunoglobulin G3 subclass in dilated cardiomyopathy: results from protein A immunoadsorption. Am. Heart J. 2005, 150:729-736.
84. Staudt A., Hummel A., Ruppert J., Dörr M., Trimpert C., Birkenmeier K., Krieg T., Staudt Y., Felix S.B. Immunoadsorption in dilated cardiomyopathy: 6 months results from a randomized study. Am. Heart J. 2006, 152(712):e1-e16.
85. Staudt A., Herda R., Trimpert C., Lubenow L., Landsberger M., Dörr M., Hummel A., Eckerle L.G., Beug D., Müller C., Hoffmann W., Weitmann K., Klingel K., Kandolf R., Kroemer H.K., Greinacher A., Felix S.B. Fcγ-receptor IIa polymorphism and the role of immunoadsorption in cardiac dysfunction in patients with dilated cardiomyopathy. Clin. Pharmacol. Ther. 2010, 87(4):452-458.
86. Störk S., Boivin V., Horf R., Hein L., Lohse M.J., Angermann C.E., Jahns R. Stimulating autoantibodies directed against beta-1 adrenergic receptor predict increased mortality in idiopathic cardiomyopathy. Am. Heart J. 2006, 152:697-704.
87. Taylor D.O., Stehlik J., Edwards L.B., Aurora P., Christie J.D., Dobbels F., Kirk R., Kucheryavaya A.Y., Rahmel A.O., Hertz M.I. Registry of the International Society for Heart and Lung Transplantation: twenty-sixth Official Adult Heart Transplant Report-2009. J. Heart Lung Transplant. 2009, 28(10):1007-1022.
88. 1-adrenergic receptor autoantibodies are potent stimulators of the ERK1/2 pathway in cardiac cells. Cardiovasc. Res. 2007, 76:51-60.
89. Wallukat G., Wollenberger A. Effects of serum gamma globulin fraction of patients with allergic asthma and dilated cardiomyopathy on chronotropic β-adrenergic function in cultured rat heart myocytes. Biomed. Biochim. Acta 1987, 78:634-639.
90. Wallukat G., Wollenberger A., Morwinski R., Pitschner H.F. Anti-β1-adrenoceptor antibodies with chronotropic activity from serum of patients with dilated cardiomyopathy: mapping of epitopes in the first and second extracellular loops. J. Mol. Cell. Cardiol. 1995, 27(1):397-406.
91. Wallukat G., Reinke P., Dörffel W.V., Luther H.P., Bestvater K., Felix S.B., Baumann G. Removal of autoantibodies in dilated cardiomyopathy by immunoadsorption. Int. J. Cardiol. 1996, 54:91-95.
92. Wallukat G., Müller J., Podlowski S., Nissen E., Morwinski R., Hetzer R. Agonist like beta-adrenergic antibodies in heart failure. Am. J. Cardiol. 1999, 83:75H-79H.
93. Wallukat G., Nissen E., Morwinski R., Müller J. Autoantibodies against the beta- and muscarinic receptors in cardiomyopathy. Herz 2000, 3:261-266.
94. Wallukat G., Müller J., Hetzer R. Specific removal of beta-1-adrenergic autoantibodies from patients with dilated cardiomyopathy. N. Engl. J. Med. 2002, 347:1806.
95. Woolf A.D., Campion G.V., Chishick A., Wise S., Cohen B.J., Klouda P.T., Caul O., Dieppe P.A. Clinical manifestations of human parvovirus B19 in adults. Arch. Intern. Med. 1989, 149:1153-1156.
96. Yoshikawa T., Baba A., Nagatomo Y. Autoimmune mechanisms underlying dilated cardiomyopathy. Circ. J. 2009, 73:602-607.
97. Zannad F., Briancon S., Juilliere Y., Mertes P.M., Villemot J.P., Alla F., Virion J.M. Incidence, clinical and etiologic features and outcomes of advanced chronic heart failure: the EPICAL study. J. Am. Coll. Cardiol. 1999, 33:734-742.
98. 2+/calmodulin kinase II. J. Clin. Invest. 2003, 11:617-625.