Telethonin deficiency is associated with maladaptation to biomechanical stress in the mammalian heart

Circulation Research

Volumn 109, Issue 7, 2011, Pages 758-769

  Knöll, Ralph ^a,c,k   Linke, Wolfgang A ^b   Zou, Peijian ^e   Miočic, Snježana ^d   Kostin, Sawa ^c   Buyandelger, Byambajav ^a   Ku, Ching Hsin ^k   Neef, Stefan ^a   Bug, Monika ^c   Schäfer, Katrin ^l   Knöll, Gudrun ^o   Felkin, Leanne E ^m   Wessels, Johannes ^a   Toischer, Karl ^c   Hagn, Franz ⁱ   Kessler, Horst ⁱ   Didié, Michael ^c   Quentin, Thomas ^c   Maier, Lars S ^a   Teucher, Nils ^a   Unsöld, Bernhard ^a   Schmidt, Albrecht ^a   Birks, Emma J ^m   Gunkel, Sylvia ^a   Lang, Patrick ^f   Granzier, Henk ^g   Zimmermann, Wolfram Hubertus ^c   Field, Loren J ^c   Faulkner, Georgine ^d   Dobbelstein, Matthias ^c   Barton, Paul J R ^m,n   Sattler, Michael ^h   Wilmanns, Matthias ^e   Chien, Kenneth R ^j   more..

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d UNIVERSITY OF PADOVA   (Italy)

^e DESY   (Germany)

^f UNIVERSITY OF MÜNSTER   (Germany)

^g UNIVERSITY OF ARIZONA   (United States)

^h INSTITUTE OF EPIDEMIOLOGY   (Germany)

ⁱ TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^j HARVARD STEM CELL INSTITUTE   (United States)

^k UNIVERSITY OF CALIFORNIA   (United States)

^l MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^m IMPERIAL COLLEGE LONDON   (United Kingdom)

ⁿ ROYAL BROMPTON AND HAREFIELD NHS FOUNDATION TRUST   (United Kingdom)

^o KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

more..

Author keywords

cardiomyopathy; genetics; heart failure; mechanosensation; mechanotransduction

Indexed keywords

ACTIN; ALPHA ACTININ; CONNECTIN; MESSENGER RNA; MUSCLE PROTEIN; PROTEIN P53; TELETHONIN; UNCLASSIFIED DRUG;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOMECHANICAL STRESS; CELL NUCLEUS; CONTROLLED STUDY; CROSS LINKING; GENE DELETION; GENE OVEREXPRESSION; HEART FAILURE; HEART MUSCLE FIBROSIS; HEART STRESS; HUMAN; HUMAN CELL; MAMMAL; MECHANICAL STRESS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; RAT; SARCOMERE; SIGNAL TRANSDUCTION; WILD TYPE; Z DISK;

EID: 80053046816     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.245787     Document Type: Article

References (55)

1. Knöll R, Hoshijima M, Hoffman HM, Person V, Lorenzen-Schmidt I, Bang ML, Hayashi T, Shiga N, Yasukawa H, Schaper W, McKenna W, Yokoyama M, Schork NJ, Omens JH, McCulloch AD, Kimura A, Gregorio CC, Poller W, Schaper J, Schultheiss HP, Chien KR. The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell. 2002; 111:943-955 (Pubitemid 36044687)
2. Knöll R, Kostin S, Klede S, Savvatis K, Klinge L, Stehle I, Gunkel S, Kotter S, Babicz K, Sohns M, Miocic S, Didie M, Knoll G, Zimmermann WH, Thelen P, Bickeboller H, Maier LS, Schaper W, Schaper J, Kraft T, Tschope C, Linke WA, Chien KR. A common MLP (muscle LIM protein) variant is associated with cardiomyopathy. Circ Res. 2010;106:695-704
3. Knöll R, Postel R, Wang J, Kratzner R, Hennecke G, Vacaru AM, Vakeel P, Schubert C, Murthy K, Rana BK, Kube D, Knoll G, Schafer K, Hayashi T, Holm T, Kimura A, Schork N, Toliat MR, Nurnberg P, Schultheiss HP, Schaper W, Schaper J, Bos E, Den Hertog J, van Eeden FJ, Peters PJ, Hasenfuss G, Chien KR, Bakkers J. Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation. 2007;116:515-525 (Pubitemid 47450260)
4. Zou P, Pinotsis N, Lange S, Song YH, Popov A, Mavridis I, Mayans OM, Gautel M, Wilmanns M. Palindromic assembly of the giant muscle protein titin in the sarcomeric Z-disk. Nature. 2006;439:229-233 (Pubitemid 43083147)
5. Bertz M, Wilmanns M, Rief M. The titin-telethonin complex is a directed, superstable molecular bond in the muscle Z-disk. Proc Natl Acad Sci USA. 2009;106:13307-13310
6. Haworth RS, Cuello F, Herron TJ, Franzen G, Kentish JC, Gautel M, Avkiran M. Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ Res. 2004;95: 1091-1099 (Pubitemid 39557896)
7. Mayans O, van der Ven PF, Wilm M, Mues A, Young P, Furst DO, Wilmanns M, Gautel M. Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature. 1998;395:863-869 (Pubitemid 28503420)
8. Miller MK, Granzier H, Ehler E, Gregorio CC. The sensitive giant: the role of titin-based stretch sensing complexes in the heart. Trends Cell Biol. 2004;14:119-126 (Pubitemid 38293454)
9. Osio A, Tan L, Chen SN, Lombardi R, Nagueh SF, Shete S, Roberts R, Willerson JT, Marian AJ. Myozenin 2 is a novel gene for human hypertrophic cardiomyopathy. Circ Res. 2007;100:766-768 (Pubitemid 46555681)
10. Kontrogianni-Konstantopoulos A, Bloch RJ. The hydrophilic domain of small ankyrin-1 interacts with the two N-terminal immunoglobulin domains of titin. J Biol Chem. 2003;278:3985-3991 (Pubitemid 36801130)
11. Faulkner G, Pallavicini A, Comelli A, Salamon M, Bortoletto G, Ievolella C, Trevisan S, Kojic S, Dalla Vecchia F, Laveder P, Valle G, Lanfranchi G. FATZ, a filamin-, actinin-, and telethonin-binding protein of the Z-disc of skeletal muscle. J Biol Chem. 2000;275:41234-41242 (Pubitemid 32054956)
12. Frey N, Olson EN. Calsarcin-3, a novel skeletal muscle-specific member of the calsarcin family, interacts with multiple Z-disc proteins. J Biol Chem. 2002;277:13998-14004 (Pubitemid 34968008)
13. Furukawa T, Ono Y, Tsuchiya H, Katayama Y, Bang M, Labeit D, Labeit S, Inagaki N, Gregorio C. Specific interaction of the potassium channel beta-subunit minK with the sarcomeric protein T-cap suggests a T-tubulemyofibril linking system. J Mol Biol. 2001;313:775-784 (Pubitemid 33063426)
14. Kojic S, Medeot E, Guccione E, Krmac H, Zara I, Martinelli V, Valle G, Faulkner G. The Ankrd2 protein, a link between the sarcomere and the nucleus in skeletal muscle. J Mol Biol. 2004;339:313-325 (Pubitemid 38596951)
15. Tian LF, Li HY, Jin BF, Pan X, Man JH, Zhang PJ, Li WH, Liang B, Liu H, Zhao J, Gong WL, Zhou T, Zhang XM. MDM2 interacts with and downregulates a sarcomeric protein, TCAP. Biochem Biophys Res Commun. 2006;345:355-361
16. Witt SH, Granzier H, Witt CC, Labeit S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J Mol Biol. 2005;350: 713-722 (Pubitemid 40848669)
17. Mihatsch K, Nestler M, Saluz HP, Henke A, Munder T. Proapoptotic protein Siva binds to the muscle protein telethonin in cardiomyocytes during coxsackieviral infection. Cardiovasc Res. 2009;81:108-115
18. Ferreiro A, Mezmezian M, Olive M, Herlicoviez D, Fardeau M, Richard P, Romero NB. Telethonin-deficiency initially presenting as a congenital muscular dystrophy. Neuromuscul Disord. 2011;21:433-438
19. Moreira ES, Wiltshire TJ, Faulkner G, Nilforoushan A, Vainzof M, Suzuki OT, Valle G, Reeves R, Zatz M, Passos-Bueno MR, Jenne DE. Limb-girdle muscular dystrophy type 2G is caused by mutations in the gene encoding the sarcomeric protein telethonin. Nat Genet. 2000;24: 163-166 (Pubitemid 30094717)
20. Olive M, Shatunov A, Gonzalez L, Carmona O, Moreno D, Quereda LG, Martinez-Matos JA, Goldfarb LG, Ferrer I. Transcription-terminating mutation in telethonin causing autosomal recessive muscular dystrophy type 2G in a European patient. Neuromuscul Disord. 2008;18:929-933
21. Bos JM, Poley RN, Ny M, Tester DJ, Xu X, Vatta M, Towbin JA, Gersh BJ, Ommen SR, Ackerman MJ. Genotype-phenotype relationships involving hypertrophic cardiomyopathy-associated mutations in titin, muscle LIM protein, and telethonin. Mol Genet Metab. 2006;88:78-85
22. Hayashi T, Arimura T, Itoh-Satoh M, Ueda K, Hohda S, Inagaki N, Takahashi M, Hori H, Yasunami M, Koga Y, Nakamura H, Matsuzaki M, Choi BY, Bae SW, Park JE, Knöll R, Hoshijima M, Chien KR, Kimura A. TCAP mutations in hypertrophic cardiomyopathy and dilated cardiomyopathy. J Am Coll Cardiol. 2004;44:2192-2201 (Pubitemid 39576040)
23. Mazzone A, Strege PR, Tester DJ, Bernard CE, Faulkner G, Degiorgio R, Makielski JC, Stanghellini V, Gibbons SJ, Ackerman MJ, Farrugia G. A mutation in telethonin alters Nav1.5 function. J Biol Chem. 2008;283: 16537-16544
24. Marziliano N, Pilotto A, Grasso M, Pasotti M, Arbustini E. Deletion of Glu at codon 13 of the TCAP gene encoding the titin-cap-telethonin is a rare polymorphism in a large Italian population. Mol Genet Metab. 2006;89:286-287 (Pubitemid 44442984)
25. Perrot A, Posch MG, Osterziel KJ. Deletion of Glu at codon 13 in the TCAP gene encoding the Z-disc protein titin-cap/telethonin is a rare non-synonymous polymorphism. Mol Genet Metab. 2006;88:199-200
26. Opitz CA, Kulke M, Leake MC, Neagoe C, Hinssen H, Hajjar RJ, Linke WA. Damped elastic recoil of the titin spring in myofibrils of human myocardium. Proc Natl Acad Sci USA. 2003;100:12688-12693 (Pubitemid 37339960)
27. Zou P, Gautel M, Geerlof A, Wilmanns M, Koch MH, Svergun DI. Solution scattering suggests cross-linking function of telethonin in the complex with titin. J Biol Chem. 2003;278:2636-2644 (Pubitemid 36801343)
28. Sanger JW, Wang J, Holloway B, Du A, Sanger JM. Myofibrillogenesis in skeletal muscle cells in zebrafish. Cell Motil Cytoskeleton. 2009;66: 556-566
29. Wang J, Shaner N, Mittal B, Zhou Q, Chen J, Sanger JM, Sanger JW. Dynamics of Z-band based proteins in developing skeletal muscle cells. Cell Motil Cytoskeleton. 2005;61:34-48. (Pubitemid 40604949)
30. Sadikot T, Hammond CR, Ferrari MB. Distinct roles for telethonin N-versus C-terminus in sarcomere assembly and maintenance. Dev Dyn. 2010;239:1124-1135
31. Zhang R, Yang J, Zhu J, Xu X. Depletion of zebrafish Tcap leads to muscular dystrophy via disrupting sarcomere-membrane interaction, not sarcomere assembly. Hum Mol Genet. 2009;18:4130-4140
32. Markert CD, Meaney MP, Voelker KA, Grange RW, Dalley HW, Cann JK, Ahmed M, Bishwokarma B, Walker SJ, Yu SX, Brown M, Lawlor MW, Beggs AH, Childers MK. Functional muscle analysis of the Tcap knockout mouse. Hum Mol Genet. 2010;19:2268-2283
33. Crow MT, Long X, Guglielmi MB, Asai T, Lakatta EG. The role of the tumor suppressor gene p53 in cardiomyocyte apoptosis. Heart Failure Reviews. 1998;3:45-61 (Pubitemid 28483162)
34. Crow MT. Revisiting p53 and its effectors in ischemic heart injury. CardiovascRes. 2006;70:401-403 (Pubitemid 44255554)
35. George I, Bish LT, Kamalakkannan G, Petrilli CM, Oz MC, Naka Y, Sweeney HL, Maybaum S. Myostatin activation in patients with advanced heart failure and after mechanical unloading. Eur J Heart Fail. 2010;12:444-453
36. Heineke J, Auger-Messier M, Xu J, Sargent M, York A, Welle S, Molkentin JD. Genetic deletion of myostatin from the heart prevents skeletal muscle atrophy in heart failure. Circulation. 2010;121:419-425
37. Reisz-Porszasz S, Bhasin S, Artaza JN, Shen R, Sinha-Hikim I, Hogue A, Fielder TJ, Gonzalez-Cadavid NF. Lower skeletal muscle mass in male transgenic mice with muscle-specific overexpression of myostatin. Am J Physiol Endocrinol Metab. 2003;285:E876-E888 (Pubitemid 37176437)
38. Rodgers BD, Interlichia JP, Garikipati DK, Mamidi R, Chandra M, Nelson OL, Murry CE, Santana LF. Myostatin represses physiological hypertrophy of the heart and excitation-contraction coupling. J Physiol. 2009;587:4873-4886
39. Bish LT, Morine KJ, Sleeper MM, Sweeney HL. Myostatin is upregulated following stress in an Erk-dependent manner and negatively regulates cardiomyocyte growth in culture and in a mouse model. PLoS One. 2010;5:e10230
40. Sharma M, Kambadur R, Matthews KG, Somers WG, Devlin GP, Conaglen JV, Fowke PJ, Bass JJ. Myostatin, a transforming growth factor-beta superfamily member, is expressed in heart muscle and is upregulated in cardiomyocytes after infarct. J Cell Physiol. 1999;180:1-9 (Pubitemid 29249707)
41. Wang BW, Chang H, Kuan P, Shyu KG. Angiotensin II activates myostatin expression in cultured rat neonatal cardiomyocytes via p38 MAP kinase and myocyte enhance factor 2 pathway. J Endocrinol. 2008;197:85-93 (Pubitemid 351566928)
42. Morissette MR, Stricker JC, Rosenberg MA, Buranasombati C, Levitan EB, Mittleman MA, Rosenzweig A. Effects of myostatin deletion in aging mice. Aging Cell. 2009;8:573-583
43. Nicholas G, Thomas M, Langley B, Somers W, Patel K, Kemp CF, Sharma M, Kambadur R. Titin-cap associates with, and regulates secretion of, Myostatin. J Cell Physiol. 2002;193:120-131 (Pubitemid 34969135)
44. Yi X, Bekeredjian R, DeFilippis NJ, Siddiquee Z, Fernandez E, Shohet RV. Transcriptional analysis of doxorubicin-induced cardiotoxicity. Am J Physiol Heart Circ Physiol. 2006;290:H1098-H1102
45. Hagn F, Klein C, Demmer O, Marchenko N, Vaseva A, Moll UM, Kessler H. BclxL changes conformation upon binding to wild-type but not mutant p53 DNA binding domain. J Biol Chem. 2010;285:3439-3450
46. Muller L, Schaupp A, Walerych D, Wegele H, Buchner J. Hsp90 regulates the activity of wild type p53 under physiological and elevated temperatures. J Biol Chem. 2004;279:48846-48854 (Pubitemid 39625765)
47. Tidow H, Veprintsev DB, Freund SM, Fersht AR. Effects of oncogenic mutations and DNA response elements on the binding of p53 to p53-binding protein 2 (53BP2). J Biol Chem. 2006;281:32526-32533 (Pubitemid 46036807)
48. Nithipongvanitch R, Ittarat W, Cole MP, Tangpong J, Clair DK, Oberley TD. Mitochondrial and nuclear p53 localization in cardiomyocytes: redox modulation by doxorubicin (Adriamycin)? Antioxid Redox Signal. 2007; 9:1001-1008 (Pubitemid 46919601)
49. Pikkarainen S, Kennedy RA, Marshall AK, Tham el L, Lay K, Kriz TA, Handa BS, Clerk A, Sugden PH. Regulation of expression of the rat orthologue of mouse double minute 2 (MDM2) by H(2)O(2)-induced oxidative stress in neonatal rat cardiac myocytes. J Biol Chem. 2009;284: 27195-27210
50. Gregorio CC, Trombitas K, Centner T, Kolmerer B, Stier G, Kunke K, Suzuki K, Obermayr F, Herrmann B, Granzier H, Sorimachi H, Labeit S. The NH2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity. J Cell Biol. 1998;143:1013-1027 (Pubitemid 28547400)
51. Nakajima H, Nakajima HO, Tsai SC, Field LJ. Expression of mutant p193 and p53 permits cardiomyocyte cell cycle reentry after myocardial infarction in transgenic mice. Circ Res. 2004;94:1606-1614 (Pubitemid 38856968)
52. Zhu W, Soonpaa MH, Chen H, Shen W, Payne RM, Liechty EA, Caldwell RL, Shou W, Field LJ. Acute doxorubicin cardiotoxicity is associated with p53-induced inhibition of the mammalian target of rapamycin pathway. Circulation. 2009;119:99-106
53. Frey N, Barrientos T, Shelton JM, Frank D, Rutten H, Gehring D, Kuhn C, Lutz M, Rothermel B, Bassel-Duby R, Richardson JA, Katus HA, Hill JA, Olson EN. Mice lacking calsarcin-1 are sensitized to calcineurin signaling and show accelerated cardiomyopathy in response to pathological biomechanical stress. Nat Med. 2004;10:1336-1343 (Pubitemid 40022715)
54. Markert CD, Ning J, Staley JT, Heinzke L, Childers CK, Ferreira JA, Brown M, Stoker A, Okamura C, Childers MK. TCAP knockdown by RNA interference inhibits myoblast differentiation in cultured skeletal muscle cells. Neuromuscul Disord. 2008;18:413-422
55. Bos JM, Ackerman MJ. Z-disc genes in hypertrophic cardiomyopathy: stretching the cardiomyopathies? J Am Coll Cardiol. 2010;55:1136-1138