Adaptations of cytoarchitecture in human dilated cardiomyopathy

Agarkova I, Perriard JC (2005) The M-band: an elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol 15:477–485 Agarkova I, Auerbach D, Ehler E, Perriard J-C (2000) A novel marker for vertebrate embryonic heart, the EH-myomesin isoform. J Biol Chem 275:10256–10264 Arber S, Hunter JJ, Ross JJ, Hongo M, Sansig G, Borg J, Perriard J-C, Chien KR, Caroni P (1997) MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88:393–403 Copeland O, Nowak KJ, Laing NG, Ravenscroft G, Messer AE, Bayliss CR, Marston SB (2010) Investigation of changes in skeletal muscle alpha-actin expression in normal and pathological human and mouse hearts. J Muscle Res Cell Motil 31:207–214 Dwyer J, Pluess M, Iskratsch T, Dos Remedios CG, Ehler E (2014) The formin FHOD1 in cardiomyocytes. Anat Rec (Hoboken) 297:1560–1570 Ehler E, Horowits R, Zuppinger C, Price RL, Perriard E, Leu M, Caroni P, Sussman M, Eppenberger HM, Perriard JC (2001) Alterations at the intercalated disk associated with the absence of muscle LIM protein. J Cell Biol 153:763–772. First detailed analysis of the dilated cardiomyopathy phenotype at the level of the cardiomyocyte using mouse models for this disease. Földes G, Mioulane M, Wright JS, Liu AQ, Novak P, Merkely B, Gorelik J, Schneider MD, Ali NN, Harding SE (2011) Modulation of human embryonic stem cell-derived cardiomyocyte growth: a testbed for studying human cardiac hypertrophy? J Mol Cell Cardiol 50:367–376 Forbes MS, Sperelakis N (1985) Intercalated discs of mammalian heart: a review of structure and function. Tissue Cell 17:605–648 Franke WW, Borrmann CM, Grund C, Pieperhoff S (2006) The area composita of adhering junctions connecting heart muscle cells of vertebrates. I. Molecular definition in intercalated disks of cardiomyocytes by immunoelectron microscopy of desmosomal proteins. Eur J Cell Biol 85:69–82. The first in a series of publications that showed that the traditional segregation of desmosomes and adherens junctions is not followed in cardiomyocytes at a molecular basis and that the term “area composita” to define this type of cell-cell contact would be more appropriate. Fürst DO, Osborn M, Nave R, Weber K (1988) The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J Cell Biol 106:1563–1572 Gerull B, Gramlich M, Atherton J, McNabb M, Trombitas K, Sasse-Klaassen S, Seidman JG, Seidman C, Granzier H, Labeit S, Frenneaux M, Thierfelder L (2002) Mutations of TTN, encoding the giant muscle filament titin, cause familial dilated cardiomyopathy. Nat Genet 30:201–204 Herman DS, Lam L, Taylor MR, Wang L, Teekakirikul P, Christodoulou D, Conner L, DePalma SR, McDonough B, Sparks E, Teodorescu DL, Cirino AL, Banner NR, Pennell DJ, Graw S, Merlo M, Di Lenarda A, Sinagra G, Bos JM, Ackerman MJ, Mitchell RN, Murry CE, Lakdawala NK, Ho CY, Barton PJ, Cook SA, Mestroni L, Seidman JG, Seidman CE (2012) Truncations of titin causing dilated cardiomyopathy. N Engl J Med 366:619–628 Hirschy A, Croquelois A, Perriard E, Schoenauer R, Agarkova I, Hoerstrup SP, Taketo MM, Pedrazzini T, Perriard JC, Ehler E (2010) Stabilised beta-catenin in postnatal ventricular myocardium leads to dilated cardiomyopathy and premature death. Basic Res Cardiol 105:597–608 Iskratsch T, Lange S, Dwyer J, Kho AL, dos Remedios C, Ehler E (2010) Formin follows function: a muscle specific isoform of FHOD3 is regulated by CK2 phosphorylation and promotes myofibril maintenance. J Cell Biol 191:1159–1172 Leu M, Ehler E, Perriard JC (2001) Characterisation of postnatal growth of the murine heart. Anat Embryol (Berl) 204:217–224 Lu S, Crawford GL, Dore J, Anderson SA, Despres D, Horowits R (2011) Cardiac-specific NRAP overexpression causes right ventricular dysfunction in mice. Exp Cell Res 317:1226–1237 MacLellan WR, Schneider MD (2000) Genetic dissection of cardiac growth control pathways. Annu Rev Physiol 62:289–319 Makarenko I, Opitz CA, Leake MC, Neagoe C, Kulke M, Gwathmey JK, del Monte F, Hajjar RJ, Linke WA (2004) Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circ Res 95:708–716 Manasek FJ (1968) Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol 125:329–365 Marston S, Copeland O, Jacques A, Livesey K, Tsang V, McKenna WJ, Jalilzadeh S, Carballo S, Redwood C, Watkins H (2009) Evidence from human myectomy samples that MYBPC3 mutations cause hypertrophic cardiomyopathy through haploinsufficiency. Circ Res 105:219–222 Meysen S, Marger L, Hewett KW, Jarry-Guichard T, Agarkova I, Chauvin JP, Perriard JC, Izumo S, Gourdie RG, Mangoni ME, Nargeot J, Gros D, Miquerol L (2007) Nkx2.5 cell-autonomous gene function is required for the postnatal formation of the peripheral ventricular conduction system. Dev Biol 303:740–753 Obermann WM, Gautel M, Steiner F, van der Ven PF, Weber K, Fürst DO (1996) The structure of the sarcomeric M band: localization of defined domains of myomesin, M-protein, and the 250-kD carboxy-terminal region of titin by immunoelectron microscopy. J Cell Biol 134:1441–1453 Perriard JC, Hirschy A, Ehler E (2003) Dilated cardiomyopathy: a disease of the intercalated disc? Trends Cardiovasc Med 13:30–38 Schoenauer R, Bertoncini P, Machaidze G, Aebi U, Perriard JC, Hegner M, Agarkova I (2005) Myomesin is a molecular spring with adaptable elasticity. J Mol Biol 349:367–379 Schoenauer R, Emmert MY, Felley A, Ehler E, Brokopp C, Weber B, Nemir M, Faggian GG, Pedrazzini T, Falk V, Hoerstrup SP, Agarkova I (2011) EH-myomesin splice isoform is a novel marker for dilated cardiomyopathy. Basic Res Cardiol 106:233–247 Seidman JG, Seidman C (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104:557–567 Severs NJ, Bruce AF, Dupont E, Rothery S (2008) Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 80:9–19 Sussman MA, Welch S, Cambon N, Klevitsky R, Hewett TE, Price R, Witt SA, Kimball TR (1998) Myofibril degeneration caused by tropomodulin overexpression leads to dilated cardiomyopathy in juvenile mice. J Clin Invest 101:51–61 Tripathi S, Schultz I, Becker E, Montag J, Borchert B, Francino A, Navarro-Lopez F, Perrot A, Ozcelik C, Osterziel KJ, McKenna WJ, Brenner B, Kraft T (2011) Unequal allelic expression of wild-type and mutated beta-myosin in familial hypertrophic cardiomyopathy. Basic Res Cardiol 106:1041–1055 van Dijk SJ, Dooijes D, dos Remedios C, Michels M, Lamers JM, Winegrad S, Schlossarek S, Carrier L, ten Cate FJ, Stienen GJ, van der Velden J (2009) Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy: haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation 119:1473–1483 Vignier N, Schlossarek S, Fraysse B, Mearini G, Kramer E, Pointu H, Mougenot N, Guiard J, Reimer R, Hohenberg H, Schwartz K, Vernet M, Eschenhagen T, Carrier L (2009) Nonsense-mediated mRNA decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein C mutant levels in cardiomyopathic mice. Circ Res 105:239–248 Vite A, Radice GL (2014) N-cadherin/catenin complex as a master regulator of intercalated disc function. Cell Commun Adhes 21:169–179 Wilson AJ, Schoenauer R, Ehler E, Agarkova I, Bennett PM (2014) Cardiomyocyte growth and sarcomerogenesis at the intercalated disc. Cell Mol Life Sci 71:165–181. This manuscript focuses on the transitional junction, a kind of Z-disc light, which appears to be crucial in cardiomyocyte growth in the adult heart, by allowing the insertion of new sarcomeres and whose function appears to be compromised in dilated cardiomyopathy. Yoshida M, Sho E, Nanjo H, Takahashi M, Kobayashi M, Kawamura K, Honma M, Komatsu M, Sugita A, Yamauchi M, Hosoi T, Ito Y, Masuda H (2010) Weaving hypothesis of cardiomyocyte sarcomeres: discovery of periodic broadening and narrowing of intercalated disk during volume-load change. Am J Pathol 176:660–678