Myocardial transcriptome analysis of human arrhythmogenic right ventricular cardiomyopathy

Physiological Genomics

Volumn 44, Issue 1, 2012, Pages 99-109

  Gaertner, Anna ^a   Schwientek, Patrick ^b   Ellinghaus, Peter ^c   Summer, Holger ^c   Golz, Stefan ^c   Kassner, Astrid ^a   Schulz, Uwe ^a   Gummert, Jan ^a   Milting, Hendrik ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b BIELEFELD UNIVERSITY   (Germany)

^c BAYER PHARMA AG   (Germany)

Author keywords

Cardiomyopathy; Heart failure; Right ventricle; Transcriptome

Indexed keywords

TRANSCRIPTOME;

ADOLESCENT; ADULT; AGED; ARRHYTHMOGENESIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DOMINANT INHERITANCE; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC HETEROGENEITY; GENETIC TRANSCRIPTION; HEART FAILURE; HEART MUSCLE; HEART MUSCLE CELL; HEART RIGHT VENTRICLE DYSPLASIA; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STUDENT T TEST;

ADOLESCENT; ADULT; AGED; ARRHYTHMOGENIC RIGHT VENTRICULAR DYSPLASIA; CASE-CONTROL STUDIES; CLUSTER ANALYSIS; COHORT STUDIES; FEMALE; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDIES; HEART FAILURE; HUMANS; MALE; MICROARRAY ANALYSIS; MIDDLE AGED; MYOCARDIUM; TRANSCRIPTOME; YOUNG ADULT;

EID: 84856005009     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00094.2011     Document Type: Article

References (82)

1. Arai A, Spencer JA, Olson EN. STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription. J Biol Chem 277: 24453-24459, 2002.
2. Aukrust P, Ueland T, Muller F, Andreassen AK, Nordoy I, Aas H, Kjekshus J, Simonsen S, Froland SS, Gullestad L. Elevated circulating levels of C-C chemokines in patients with congestive heart failure. Circulation 97: 1136-1143, 1998.
3. Awad MM, Calkins H, Judge DP. Mechanisms of disease: molecular genetics of arrhythmogenic right ventricular dysplasia/cardiomyopathy. Nat Clin Pract Cardiovasc Med 5: 258-267, 2008.
4. Barandon L, Dufourcq P, Costet P, Moreau C, Allieres C, Daret D, Dos Santos P, Daniel Lamaziere JM, Couffinhal T, Duplaa C. Involvement of FrzA/sFRP-1 and the Wnt/frizzled pathway in ischemic preconditioning. Circ Res 96: 1299-1306, 2005.
5. Basso C, Czarnowska E, Della Barbera M, Bauce B, Beffagna G, Wlodarska EK, Pilichou K, Ramondo A, Lorenzon A, Wozniek O, Corrado D, Daliento L, Danieli GA, Valente M, Nava A, Thiene G, Rampazzo A. Ultrastructural evidence of intercalated disc remodelling in arrhythmogenic right ventricular cardiomyopathy: an electron microscopy investigation on endomyocardial biopsies. Eur Heart J 27: 1847-1854, 2006.
6. Basso C, Thiene G, Corrado D, Angelini A, Nava A, Valente M. Arrhythmogenic right ventricular cardiomyopathy. Dysplasia, dystrophy, or myocarditis? Circulation 94: 983-991, 1996.
7. Beffagna G, Occhi G, Nava A, Vitiello L, Ditadi A, Basso C, Bauce B, Carraro G, Thiene G, Towbin JA, Danieli GA, Rampazzo A. Regulatory mutations in transforming growth factor-beta3 gene cause arrhythmogenic right ventricular cardiomyopathy type 1. Cardiovasc Res 65: 366-373, 2005.
8. Bengtsson L, Otto H. LUMA interacts with emerin and influences its distribution at the inner nuclear membrane. J Cell Sci 121: 536-548, 2008.
9. Bosman FT, Stamenkovic I. Functional structure and composition of the extracellular matrix. J Pathol 200: 423-428, 2003.
10. Burkett EL, Hershberger RE. Clinical and genetic issues in familial dilated cardiomyopathy. J Am Coll Cardiol 45: 969-981, 2005.
11. Camm AJ, Lüscher TF, Serruys PW. The ESC Textbook of Cardiovascular Medicine (2nd ed.). Oxford: European Society of Cardiology, 2009.
12. Chen H, Li B, Workman JL. A histone-binding protein, nucleoplasmin, stimulates transcription factor binding to nucleosomes and factor-induced nucleosome disassembly. EMBO J 13: 380-390, 1994.
13. Christensen AH, Andersen CB, Tybjaerg-Hansen A, Haunso S, Svendsen JH. Mutation analysis and evaluation of the cardiac localizationof TMEM43 in arrhythmogenic right ventricular cardiomyopathy. Clin Genet 80: 256-264, 2011.
14. Dalal D, Nasir K, Bomma C, Prakasa K, Tandri H, Piccini J, Roguin A, Tichnell C, James C, Russell SD, Judge DP, Abraham T, Spevak PJ, Bluemke DA, Calkins H. Arrhythmogenic right ventricular dysplasia: a United States experience. Circulation 112: 3823-3832, 2005.
15. Damas JK, Gullestad L, Ueland T, Solum NO, Simonsen S, Froland SS, Aukrust P. CXC-chemokines, a new group of cytokines in congestive heart failure-possible role of platelets and monocytes. Cardiovasc Res 45: 428-436, 2000.
16. Dec GW, Fuster V. Idiopathic dilated cardiomyopathy. N Engl J Med 331: 1564-1575, 1994.
17. Dennis S, Aikawa M, Szeto W, d'Amore PA, Papkoff J. A secreted frizzled related protein, FrzA, selectively associates with Wnt-1 protein and regulates wnt-1 signaling. J Cell Sci 112: 3815-3820, 1999.
18. Duplaa C, Jaspard B, Moreau C, D'Amore PA. Identification and cloning of a secreted protein related to the cysteine-rich domain of frizzled. Evidence for a role in endothelial cell growth control. Circ Res 84: 1433-1445, 1999.
19. Ellinor PT, MacRae CA, Thierfelder L. Arrhythmogenic right ventricular cardiomyopathy. Heart Fail Clin 6: 161-177, 2010.
20. Elliott P, Andersson B, Arbustini E, Bilinska Z, Cecchi F, Charron P, Dubourg O, Kuhl U, Maisch B, McKenna WJ, Monserrat L, Pankuweit S, Rapezzi C, Seferovic P, Tavazzi L, Keren A. Classification of the cardiomyopathies: a position statement from the European Society Of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 29: 270-276, 2008.
21. Elliott P, O'Mahony C, Syrris P, Evans A, Rivera Sorensen C, Sheppard MN, Carr-White G, Pantazis A, McKenna WJ. Prevalence of desmosomal protein gene mutations in patients with dilated cardiomyopathy. Circ Cardiovasc Genet 3: 314-322, 2010.
22. Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol 17: 375-412, 1963.
23. Garcia-Gras E, Lombardi R, Giocondo MJ, Willerson JT, Schneider MD, Khoury DS, Marian AJ. Suppression of canonical Wnt/beta-catenin signaling by nuclear plakoglobin recapitulates phenotype of arrhythmogenic right ventricular cardiomyopathy. J Clin Invest 116: 2012-2021, 2006.
24. Ge Y, Dudoit S, Speed TP. Resampling-based multiple testing for microarray data analysis. Sociedad de Estadística e Investigación Operativa Test 12: 1-77, 2003.
25. Gerull B, Heuser A, Wichter T, Paul M, Basson CT, McDermott DA, Lerman BB, Markowitz SM, Ellinor PT, MacRae CA, Peters S, Grossmann KS, Drenckhahn J, Michely B, Sasse-Klaassen S, Birchmeier W, Dietz R, Breithardt G, Schulze-Bahr E, Thierfelder L. Mutations in the desmosomal protein plakophilin-2 are common in arrhythmogenic right ventricular cardiomyopathy. Nat Genet 36: 1162-1164, 2004.
26. Hamid MS, Norman M, Quraishi A, Firoozi S, Thaman R, Gimeno JR, Sachdev B, Rowland E, Elliott PM, McKenna WJ. Prospective evaluation of relatives for familial arrhythmogenic right ventricular cardiomyopathy/ dysplasia reveals a need to broaden diagnostic criteria. J Am Coll Cardiol 40: 1445-1450, 2002.
27. Hayes NV, Scott C, Heerkens E, Ohanian V, Maggs AM, Pinder JC, Kordeli E, Baines AJ. Identification of a novel C-terminal variant of beta II spectrin: two isoforms of beta II spectrin have distinct intracellular locations and activities. J Cell Sci 113: 2023-2034, 2000.
28. Heuser A, Plovie ER, Ellinor PT, Grossmann KS, Shin JT, Wichter T, Basson CT, Lerman BB, Sasse-Klaassen S, Thierfelder L, MacRae CA, Gerull B. Mutant desmocollin-2 causes arrhythmogenic right ventricular cardiomyopathy. Am J Hum Genet 79: 1081-1088, 2006.
29. Hossain GS, van Thienen JV, Werstuck GH, Zhou J, Sood SK, Dickhout JG, de Koning AB, Tang D, Wu D, Falk E, Poddar R, Jacobsen DW, Zhang K, Kaufman RJ, Austin RC. TDAG51 is induced by homocysteine, promotes detachment-mediated programmed cell death, and contributes to the development of atherosclerosis in hyperhomocysteinemia. J Biol Chem 278: 30317-30327, 2003.
30. Ito T, Ikehara T, Nakagawa T, Kraus WL, Muramatsu M. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes Dev 14: 1899-1907, 2000.
31. Jones SE, Jomary C. Secreted Frizzled-related proteins: searching for relationships and patterns. Bioessays 24: 811-820, 2002.
32. Ju H, Dixon IM. Extracellular matrix and cardiovascular diseases. Can J Cardiol 12: 1259-1267, 1996.
33. Kawase H, Okuwaki M, Miyaji M, Ohba R, Handa H, Ishimi Y, Fujii-Nakata T, Kikuchi A, Nagata K. NAP-I is a functional homologue of TAF-I that is required for replication and transcription of the adenovirus genome in a chromatin-like structure. Genes Cells 1: 1045-1056, 1996.
34. Kittleson MM, Minhas KM, Irizarry RA, Ye SQ, Edness G, Breton E, Conte JV, Tomaselli G, Garcia JG, Hare JM. Gene expression analysis of ischemic and nonischemic cardiomyopathy: shared and distinct genes in the development of heart failure. Physiol Genomics 21: 299-307, 2005.
35. Klauke B, Kossmann S, Gaertner A, Brand K, Stork I, Brodehl A, Dieding M, Walhorn V, Anselmetti D, Gerdes D, Bohms B, Schulz U, Zu Knyphausen E, Vorgerd M, Gummert J, Milting H. De novo desmin-mutation N116S is associated with arrhythmogenic right ventricular cardiomyopathy. Hum Mol Genet 19: 4595-4607, 2010.
36. 2 ATPase expression. Circulation 113: 2724-2732, 2006.
37. Kuner R, Barth AS, Ruschhaupt M, Buness A, Zwermann L, Kreuzer E, Steinbeck G, Poustka A, Sultmann H, Nabauer M. Genomic analysis reveals poor separation of human cardiomyopathies of ischemic and nonischemic etiologies. Physiol Genomics 34: 88-94, 2008.
38. Kuwahara K, Barrientos T, Pipes GC, Li S, Olson EN. Muscle-specific signaling mechanism that links actin dynamics to serum response factor. Mol Cell Biol 25: 3173-3181, 2005.
39. Kuwahara K, Teg Pipes GC, McAnally J, Richardson JA, Hill JA, Bassel-Duby R, Olson EN. Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity. J Clin Invest 117: 1324-1334, 2007.
40. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ. Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18: 1440-1463, 2005.
41. MacRae CA, Birchmeier W, Thierfelder L. Arrhythmogenic right ventricular cardiomyopathy: moving toward mechanism. J Clin Invest 116: 1825-1828, 2006.
42. Marcus FI, Fontaine GH, Guiraudon G, Frank R, Laurenceau JL, Malergue C, Grosgogeat Y. Right ventricular dysplasia: a report of 24 adult cases. Circulation 65: 384-398, 1982.
43. Matkovich SJ, Zhang Y, Van Booven DJ, Dorn GW II. Deep mRNA sequencing for in vivo functional analysis of cardiac transcriptional regulators: application to Galphaq. Circ Res 106: 1459-1467, 2010.
44. McKoy G, Protonotarios N, Crosby A, Tsatsopoulou A, Anastasakis A, Coonar A, Norman M, Baboonian C, Jeffery S, McKenna WJ. Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet 355: 2119-2124, 2000.
45. Merner ND, Hodgkinson KA, Haywood AF, Connors S, French VM, Drenckhahn JD, Kupprion C, Ramadanova K, Thierfelder L, McKenna W, Gallagher B, Morris-Larkin L, Bassett AS, Parfrey PS, Young TL. Arrhythmogenic right ventricular cardiomyopathy type 5 is a fully penetrant, lethal arrhythmic disorder caused by a missense mutation in the TMEM43 gene. Am J Hum Genet 82: 809-821, 2008.
46. Mestroni L, Maisch B, McKenna WJ, Schwartz K, Charron P, Rocco C, Tesson F, Richter A, Wilke A, Komajda M. Guidelines for the study of familial dilated cardiomyopathies. Collaborative Research Group of the European Human and Capital Mobility Project on Familial Dilated Cardiomyopathy. Eur Heart J 20: 93-102, 1999.
47. Mestroni L, Rocco C, Gregori D, Sinagra G, Di Lenarda A, Miocic S, Vatta M, Pinamonti B, Muntoni F, Caforio AL, McKenna WJ, Falaschi A, Giacca M, Camerini. Familial dilated cardiomyopathy: evidence for genetic and phenotypic heterogeneity. Heart Muscle Disease Study Group. J Am Coll Cardiol 34: 181-190, 1999.
48. Mewis C, Spyridopoulos J, Riessen R. Kardiologie compact (2nd ed.). Stuttgart: Thieme Verlag, 2006.
49. Nava A, Bauce B, Basso C, Muriago M, Rampazzo A, Villanova C, Daliento L, Buja G, Corrado D, Danieli GA, Thiene G. Clinical profileand long-term follow-up of 37 families with arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol 36: 2226-2233, 2000.
50. Norgett EE, Hatsell SJ, Carvajal-Huerta L, Cabezas JC, Common J, Purkis PE, Whittock N, Leigh IM, Stevens HP, Kelsell DP. Recessive mutation in desmoplakin disrupts desmoplakin-intermediate filament interactions and causes dilated cardiomyopathy, woolly hair and keratoderma. Hum Mol Genet 9: 2761-2766, 2000.
51. Norman M, Simpson M, Mogensen J, Shaw A, Hughes S, Syrris P, Sen-Chowdhry S, Rowland E, Crosby A, McKenna WJ. Novel mutation in desmoplakin causes arrhythmogenic left ventricular cardiomyopathy. Circulation 112: 636-642, 2005.
52. Odland GF. The fine structure of the interrelationship of cells in the human epidermis. J Biophys Biochem Cytol 4: 529-538, 1958.
53. Pap M, Cooper GM. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J Biol Chem 273: 19929-19932, 1998.
54. Pennica D, Shaw KJ, Swanson TA, Moore MW, Shelton DL, Zioncheck KA, Rosenthal A, Taga T, Paoni NF, Wood Cardiotrophin-1 WI. Biological activities and binding to the leukemia inhibitory factor receptor/gp130 signaling complex. J Biol Chem 270: 10915-10922, 1995.
55. Pilichou K, Remme CA, Basso C, Campian ME, Rizzo S, Barnett P, Scicluna BP, Bauce B, van den Hoff MJ, de Bakker JM, Tan HL, Valente M, Nava A, Wilde AA, Moorman AF, Thiene G, Bezzina CR. Myocyte necrosis underlies progressive myocardial dystrophy in mouse dsg2-related arrhythmogenic right ventricular cardiomyopathy. J Exp Med 206: 1787-1802, 2009.
56. Radicke S, Cotella D, Graf EM, Banse U, Jost N, Varro A, Tseng GN, Ravens U, Wettwer E. Functional modulation of the transient outward current Ito by KCNE beta-subunits and regional distribution in human non-failing and failing hearts. Cardiovasc Res 71: 695-703, 2006.
57. Railson JE, Liao Z, Brar BK, Buddle JC, Pennica D, Stephanou A, Latchman DS. Cardiotrophin-1 and urocortin cause protection by the same pathway and hypertrophy via distinct pathways in cardiac myocytes. Cytokine 17: 243-253, 2002.
58. Rayns DG, Simpson FO, Ledingham JM. Ultrastructure of desmosomes in mammalian intercalated disc; appearances after lanthanum treatment. J Cell Biol 42: 322-326, 1969.
59. Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. Transcriptional regulation of adipogenesis. Genes Dev 14: 1293-1307, 2000.
60. Saegusa J, Akakura N, Wu CY, Hoogland C, Ma Z, Lam KS, Liu FT, Takada YK, Takada Y. Pro-inflammatory secretory phospholipase A2 type IIA binds to integrins alphavbeta3 and alpha4beta1 and induces proliferation of monocytic cells in an integrin-dependent manner. J Biol Chem 283: 26107-26115, 2008.
61. Schafer S, Ellinghaus P, Janssen W, Kramer F, Lustig K, Milting H, Kast R, Klein M. Chronic inhibition of phosphodiesterase 5 does not prevent pressure overload induced right ventricular remodelling. Cardiovasc Res, 2009.
62. Sen-Chowdhry S, McKenna WJ. Reconciling the protean manifestations of arrhythmogenic cardiomyopathy. Circ Arrhythm Electrophysiol 3: 566-570, 2010.
63. Sen-Chowdhry S, Morgan RD, Chambers JC, McKenna WJ. Arrhythmogenic cardiomyopathy: etiology, diagnosis, treatment. Annu Rev Med 61: 233-253, 2010.
64. Sen-Chowdhry S, Syrris P, McKenna WJ. Genetics of right ventricular cardiomyopathy. J Cardiovasc Electrophysiol 16: 927-935, 2005.
65. Sen-Chowdhry S, Syrris P, Prasad SK, Hughes SE, Merrifield R, Ward D, Pennell DJ, McKenna WJ. Left-dominant arrhythmogenic cardiomyopathy: an under-recognized clinical entity. J Am Coll Cardiol 52: 2175-2187, 2008.
66. Sen-Chowdhry S, Syrris P, Ward D, Asimaki A, Sevdalis E, McKenna WJ. Clinical and genetic characterization of families with arrhythmogenic right ventricular dysplasia/cardiomyopathy provides novel insights into patterns of disease expression. Circulation 115: 1710-1720, 2007.
67. Sheng Z, Knowlton K, Chen J, Hoshijima M, Brown JH, Chien KR. Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase-dependent pathway. Divergence from downstream CT-1 signals for myocardial cell hypertrophy. J Biol Chem 272: 5783-5791, 1997.
68. Shikama N, Chan HM, Krstic-Demonacos M, Smith L, Lee CW, Cairns W, La Thangue NB. Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators. Mol Cell Biol 20: 8933-8943, 2000.
69. Sjostrand FS, Andersson E. Electron microscopy of the intercalated discs of cardiac muscle tissue. Experientia 10: 369-370, 1954.
70. Syrris P, Ward D, Asimaki A, Evans A, Sen-Chowdhry S, Hughes SE, McKenna WJ. Desmoglein-2 mutations in arrhythmogenic right ventricular cardiomyopathy: a genotype-phenotype characterization of familial disease. Eur Heart J 28: 581-588, 2007.
71. Syrris P, Ward D, Evans A, Asimaki A, Gandjbakhch E, Sen-Chowdhry S, McKenna WJ. Arrhythmogenic right ventricular dysplasia/ cardiomyopathy associated with mutations in the desmosomal gene desmocollin-2. Am J Hum Genet 79: 978-984, 2006.
72. Tan FL, Moravec CS, Li J, Apperson-Hansen C, McCarthy PM, Young JB, Bond M. The gene expression fingerprint of human heart failure. Proc Natl Acad Sci USA 99: 11387-11392, 2002.
73. Taylor M, Graw S, Sinagra G, Barnes C, Slavov D, Brun F, Pinamonti B, Salcedo EE, Sauer W, Pyxaras S, Anderson B, Simon B, Bogomolovas J, Labeit S, Granzier H, Mestroni L. Genetic variation in titin in arrhythmogenic right ventricular cardiomyopathy-overlap syndromes. Circulation, 2011.
74. Thiene G, Nava A, Corrado D, Rossi L, Pennelli N. Right ventricular cardiomyopathy and sudden death in young people. N Engl J Med 318: 129-133, 1988.
75. Thomsen MB, Wang C, Ozgen N, Wang HG, Rosen MR, Pitt GS. Accessory subunit KChIP2 modulates the cardiac L-type calcium current. Circ Res 104: 1382-1389, 2009.
76. Tiso N, Stephan DA, Nava A, Bagattin A, Devaney JM, Stanchi F, Larderet G, Brahmbhatt B, Brown K, Bauce B, Muriago M, Basso C, Thiene G, Danieli GA, Rampazzo A. Identification of mutations in the cardiac ryanodine receptor gene in families affected with arrhythmogenic right ventricular cardiomyopathy type 2 (ARVD2). Hum Mol Genet 10: 189-194, 2001.
77. Van Breemen VL. Intercalated discs in heart muscle studied with the electron microscope. Anat Rec 117: 49-63, 1953.
78. Waardenberg AJ, Bernardo BC, Ng DC, Shepherd PR, Cemerlang N, Sbroggiò M, Wells CA, Dalrymple BP, Brancaccio M, Lin RC, Mc-Mullen JR. Phosphoinositide 3-kinase [PI3K(P110alpha)] directly regulates key components of the Z-disc and cardiac structure. J Biol Chem 286: 30837-30846, 2011.
79. Watanabe TK, Fujiwara T, Nakamura Y, Hirai Y, Maekawa H, Takahashi E. Cloning, expression pattern and mapping to Xq of NAP1L3, a gene encoding a peptide homologous to human and yeast nucleosome assembly proteins. Cytogenet Cell Genet 74: 281-285, 1996.
80. Wei YJ, Cui CJ, Huang YX, Zhang XL, Zhang H, Hu SS. Upregulated expression of cardiac ankyrin repeat protein in human failing hearts due to arrhythmogenic right ventricular cardiomyopathy. Eur J Heart Fail 11: 559-566, 2009.
81. Yang J, Moravec CS, Sussman MA, DiPaola NR, Fu D, Hawthorn L, Mitchell CA, Young JB, Francis GS, McCarthy PM, Bond M. Decreased SLIM1 expression and increased gelsolin expression in failing human hearts measured by high-density oligonucleotide arrays. Circulation 102: 3046-3052, 2000.
82. Zolk O, Frohme M, Maurer A, Kluxen FW, Hentsch B, Zubakov D, Hoheisel JD, Zucker IH, Pepe S, Eschenhagen T. Cardiac ankyrin repeat protein, a negative regulator of cardiac gene expression, is augmented in human heart failure. Biochem Biophys Res Commun 293: 1377-1382, 2002.