Targeted inhibition of ANKRD1 disrupts sarcomeric ERK-GATA4 signal transduction and abrogates phenylephrine-induced cardiomyocyte hypertrophy

Cardiovascular Research

Volumn 106, Issue 2, 2015, Pages 261-271

  Zhong, Lin ^a   Chiusa, Manuel ^a   Cadar, Adrian G ^a   Lin, Angel ^a   Samaras, Susan ^a   Davidson, Jeffrey M ^a,b   Lim, Chee C ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

CARP; GATA4; Hypertrophy; Sarcomere; Titin

Indexed keywords

ANKYRIN REPEAT DOMAIN 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHENYLEPHRINE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR GATA 4; UNCLASSIFIED DRUG; ANKRD1 PROTEIN, MOUSE; GATA4 PROTEIN, MOUSE; MUSCLE PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; BINDING AFFINITY; CELL GROWTH; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION; GENE SILENCING; HEART FUNCTION; HEART HEMODYNAMICS; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SARCOMERE; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; CARDIOMEGALY; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; CARDIOMEGALY; CELLS, CULTURED; GATA4 TRANSCRIPTION FACTOR; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; NUCLEAR PROTEINS; PHENYLEPHRINE; PHOSPHORYLATION; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84929091111     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv108     Document Type: Article

References (40)

1. Hill JA, Olson EN. Cardiac plasticity. N Engl J Med 2008;358:1370-1380.
2. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 2006;7:589-600.
3. Jeyaseelan R, Poizat C, Baker RK, Abdishoo S, Isterabadi LB, Lyons GE, Kedes L. A novel cardiac-restricted target for doxorubicin. CARP, a nuclear modulator of gene expres-sionincardiacprogenitorcells and cardiomyocytes.JBiol Chem1997;272:22800-22808.
4. Kemp TJ, Sadusky TJ, Saltisi F, Carey N, Moss J, Yang SY, Sassoon DA, Goldspink G, Coulton GR. Identification of Ankrd2, a novel skeletal muscle gene coding for a stretch-responsive ankyrin-repeat protein. Genomics 2000;66:229-241.
5. Miller MK, Bang ML, Witt CC, Labeit D, Trombitas C, Watanabe K, Granzier H, McElhinny AS, Gregorio CC, Labeit S. The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules. J Mol Biol 2003;333:951-964.
6. Zou Y, Evans S, Chen J, Kuo HC, Harvey RP, Chien KR. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development 1997; 124:793-804.
7. Bang ML, Mudry RE, McElhinny AS, Trombitas K, Geach AJ, Yamasaki R, Sorimachi H, Granzier H, Gregorio CC, Labeit S. Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J Cell Biol 2001; 153:413-427.
8. Aihara Y, Kurabayashi M, Saito Y, Ohyama Y, Tanaka T, Takeda S, Tomaru K, Sekiguchi K, Arai M, Nakamura T, Nagai R. Cardiac ankyrin repeat protein isanovel markerofcardiac hypertrophy: role of M-CAT element within the promoter. Hypertension 2000;36: 48-53.
9. Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S, Witt CC, Becker K, Labeit S, Granzier HL. Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 2004;110:155-162.
10. Zolk O, Marx M, Jackel E, El-Armouche A, Eschenhagen T. Beta-adrenergic stimulation induces cardiac ankyrin repeat protein expression: involvement of protein kinase A and calmodulin-dependent kinase. Cardiovasc Res 2003;59:563-572.
11. Arimura T, Bos JM, Sato A, Kubo T, Okamoto H, Nishi H, Harada H, Koga Y, Moulik M, Doi YL, Towbin JA, Ackerman MJ, Kimura A. Cardiac ankyrin repeat protein gene (ANKRD1) mutations in hypertrophic cardiomyopathy. J Am Coll Cardiol 2009;54: 334-342.
12. Duboscq-Bidot L, Charron P, Ruppert V, Fauchier L, Richter A, Tavazzi L, Arbustini E, Wichter T, Maisch B, Komajda M, Isnard R, Villard E. Mutationsin the ANKRD1 gene encoding CARP are responsible for human dilated cardiomyopathy. Eur Heart J 2009;30: 2128-2136.
13. Moulik M, Vatta M, Witt SH, Arola AM, Murphy RT, McKenna WJ, Boriek AM, Oka K, Labeit S, Bowles NE, Arimura T, Kimura A, Towbin JA. ANKRD1, the gene encoding cardiac ankyrin repeat protein, is a novel dilated cardiomyopathy gene. J Am Coll Cardiol 2009;54:325-333.
14. Kuo CT, Morrisey EE, Anandappa R, Sigrist K, Lu MM, Parmacek MS, Soudais C, Leiden JM. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev 1997;11:1048-1060.
15. Oka T, Maillet M, Watt AJ, Schwartz RJ, Aronow BJ, Duncan SA, Molkentin JD. Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ Res 2006;98:837-845.
16. van Berlo JH, Elrod JW, Aronow BJ, Pu WT, Molkentin JD. Serine 105 phosphorylation of transcription factor GATA4 is necessary for stress-induced cardiac hypertrophy in vivo. Proc Natl Acad Sci USA 2011;108:12331-12336.
17. Chen B, Zhong L, Roush SF, Pentassuglia L, Peng X, Samaras S, Davidson JM, Sawyer DB, Lim CC. Disruptionofa GATA4/Ankrd1 signaling axis incardiomyocytes leads to sarco-mere disarray: implications for anthracycline cardiomyopathy. PLoS One 2012;7:e35743.
18. Samaras SE, Almodovar-Garcia K, Wu N, Yu F, Davidson JM. Global deletion of Ankrd1 results in a wound-healing phenotype associated with dermal fibroblast dysfunction. American J of Pathol 2015;185:96-109.
19. Lim CC, Zuppinger C, Guo X, Kuster GM, Helmes M, Eppenberger HM, Suter TM, Liao R, Sawyer DB. Anthracyclines induce calpain-dependent titin proteolysis and necrosis in cardiomyocytes. J Biol Chem 2004;279:8290-8299.
20. Molkentin JD, Kalvakolanu DV, Markham BE. Transcription factor GATA-4 regulates cardiac muscle-specific expression of the alpha-myosin heavy-chain gene. Mol Cell Biol 1994;14:4947-4957.
21. Kojic S, Nestorovic A, Rakicevic L, Belgrano A, Stankovic M, Divac A, Faulkner G. Anovel role for cardiac ankyrin repeat protein Ankrd1/CARPas a co-activator of the p53 tumor suppressor protein. Arch Biochem Biophys 2010;502:60-67.
22. Almodovar-Garcia K, Kwon M, Samaras SE, Davidson JM. ANKRD1 acts as a transcrip-tional repressor of MMP13 via the AP-1 site. Mol Cell Biol 2014;34:1500-1511.
23. Laure L, Suel L, Roudaut C, Bourg N, Ouali A, Bartoli M, Richard I, Daniele N. Cardiac ankyrin repeat protein is a marker of skeletal muscle pathological remodelling. FEBS J 2009;276:669-684.
24. Liang Q, Wiese RJ, Bueno OF, Dai YS, Markham BE, Molkentin JD. The transcription factor GATA4 is activated by extracellular signal-regulated kinase 1-and 2-mediated phosphorylation of serine 105 in cardiomyocytes. Mol Cell Biol 2001;21:7460-7469.
25. Charron F, Tsimiklis G, Arcand M, Robitaille L, Liang Q, Molkentin JD, Meloche S, Nemer M. Tissue-specific GATA factors are transcriptional effectors of the small GTPase Rho A. Genes Dev 2001;15:2702-2719.
26. Purcell NH, Darwis D, Bueno OF, Muller JM, Schule R, Molkentin JD. Extracellular signal-regulatedkinase2interacts with andisnegatively regulatedbythe LIM-only proteinFHL2 in cardiomyocytes. Mol Cell Biol 2004;24:1081-1095.
27. Sheikh F, Raskin A, Chu PH, Lange S, Domenighetti AA, Zheng M, Liang X, Zhang T, Yajima T, Gu Y, Dalton ND, Mahata SK, Dorn GW II, Brown JH, Peterson KL, Omens JH, McCulloch AD, Chen J. AnFHL1-containing complex within the cardiomyo-cyte sarcomere mediates hypertrophic biomechanical stress responses in mice. J Clin Invest 2008;118:3870-3880.
28. Granzier HL, Labeit S. The giant protein titin: a major player in myocardial mechanics, signaling, and disease. Circ Res 2004;94:284-295.
29. Linke WA, Hamdani N. Gigantic business: titin properties and function through thick and thin. Circ Res 2014;114:1052-1068.
30. Frank D, Kuhn C, Katus HA, Frey N. The sarcomeric Z-disc: anodal point in signalling and disease. J Mol Med (Berl) 2006;84:446-468.
31. Hojayev B, Rothermel BA, Gillette TG, Hill JA. FHL2 binds calcineurin and represses pathological cardiac growth. Mol Cell Biol 2012;32:4025-4034.
32. Zhou P, He A, Pu WT. Regulationof GATA4 transcriptional activityincardiovascular development and disease. Curr Top Dev Biol 2012;100:143-169.
33. Bang ML, Gu Y, Dalton ND, Peterson KL, Chien KR, Chen J. The muscle ankyrin repeat proteins CARP, Ankrd2, and DARP are not essential for normal cardiac development and function at basal conditions and in response to pressure overload. PLoS One 2014;9:e93638.
34. Chu PH, Bardwell WM, Gu Y, Ross J Jr, Chen J. FHL2 (SLIM3) is not essential for cardiac development and function. Mol Cell Biol 2000;20:7460-7462.
35. Kong Y, Shelton JM, Rothermel B, Li X, Richardson JA, Bassel-Duby R, Williams RS. Cardiac-specific LIM protein FHL2 modifies the hypertrophic response to beta-adrenergic stimulation. Circulation 2001;103:2731-2738.
36. Song Y, Xu J, Li Y, Jia C, Ma X, Zhang L, Xie X, Zhang Y, Gao X, Zhang Y, Zhu D. Cardiac ankyrin repeat protein attenuates cardiac hypertrophy by inhibition of ERK1/2 and TGF-beta signaling pathways. PLoS One 2012;7:e50436.
37. Lange S, Auerbach D, McLoughlin P, Perriard E, Schafer BW, Perriard JC, Ehler E. Subcel-lular targeting of metabolic enzymes to titin in heart muscle may be mediated by DRAL/FHL-2. J Cell Sci 2002;115:4925-4936.
38. Pyle WG, Solaro RJ. At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circ Res 2004;94:296-305.
39. Lun AS, Chen J, Lange S. Probing muscle ankyrin-repeat protein (MARP) structure and function. Anat Rec (Hoboken) 2014;297:1615-1629.
40. Crocini C, Arimura T, Reischmann S, Eder A, Braren I, Hansen A, Eschenhagen T, Kimura A, Carrier L. ImpactofANKRD1 mutations associated with hypertrophic cardio-myopathy on contraction parameters of engineered heart tissue. Basic Res Cardiol 2013; 108:349.