Dystrophin and the Cardiomyocyte Membrane Cytoskeleton in the Healthy and Failing Heart
Tóm tắt
The cardiomyocyte membrane cytoskeleton consists of the costameric proteins that mediate force transduction from the cell to the extracellular matrix, and a sub-membrane network composed of dystrophin and associated proteins. Studies of the precise cellular distribution of dystrophin and of the consequences of genetic mutations leading to abnormal expression of the dystrophin molecule, as occurs in Duchenne and Becker's muscular dystrophies, highlight potential functional roles of this sub-membrane protein complex in cardiomyocytes. Detailed investigation of dystrophin distribution using the complementary cell imaging techniques of immunoconfocal microscopy and freeze-fracture cytochemistry at the electron-microscopical level show that, in contrast to rat cardiomyocytes, the dystrophin network in human cardiomyocytes is locally enriched at costameres. Thus located, the dystrophin network appears to have a mechanical role, involving stabilization of the peripheral plasma membrane during the repetitive distortion associated with cardiac contraction and, in the human myocyte, contributing to lateral force-transduction. Evidence from animal models of muscular dystrophy and from investigation of the interactions of the sub-membrane cytoskeleton with other membrane-associated proteins including ion channels, receptors and enzymes, further suggests a role for dystrophin in organization and regulation of membrane domains. The relative preservation of the membrane cytoskeleton in non-dystrophic dilated cardiomyopathy and in ischemic cardiomyopathy, conditions in which the myocyte contractile apparatus and internal desmin-based cytoskeleton are commonly disrupted, emphasizes the vital role of the membrane cytoskeleton in cell survival. Continued cardiomyocyte survival despite loss of contractile protein organization has implications in the potential for reversibility of left ventricular remodeling that can be achieved in the clinical setting.
Tài liệu tham khảo
Pardo JV, Siliciano JD, Craig SW. A vinculin-containing cortical lattice in skeletal muscle: Transverse lattice elements ('costameres') mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci USA 1983;80:1008-1012.
Pardo JV, Siliciano JD, Craig SW. Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibres. J Cell Biol 1983;97:1081-1088.
Craig SW, Pardo JV. Gamma actin, spectrin, and intermediate filament proteins colocalise with vinculin at costameres, myofibril to sarcolemmal attachment sites. Cell Motil Cytoskeleton 1983;3:449-462.
Belkin AM, Zhidkova NI, Koteliansky VE. Localisation of talin in skeletal and cardiac muscle. FEBS Lett 1986;200:32-36.
Belkin AM, Ornatsky OI, Glukhova MA, Koteliansky VE. Immunolocalisation of meta-vinculin in human smooth and cardiac muscle. J Cell Biol 1988;107:545-553.
Hynes RO. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 1992;69:11-25.
Borg TK, Johnson LD, Lill PH. Specific attachment of collagen to cardiac myocytes: In vivo and in vitro. Dev Biol 1983;97:417-423.
Terracio L, Gullberg D, Rubin K, Craig S, Borg TK. Expression of collagen adhesion proteins (COLL-CAM) and their association with the cytoskeleton in developing, normal and hypertrophied rat cardiac myocytes. Anat Rec 1989;223:62-71.
Danowski BA, Imanaki-Yoshida K, Sanger JM, Sanger JW. Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes. J Cell Biol 1992;118:1411-1420.
Lewis JM, Schwartz MA. Mapping in vivo associations of cytoplasmic proteins with integrin beta 1 cytoplasmic domain mutants. Mol Biol Cell 1995;69:151-160.
Ross RS, Pham C, Shai S-Y, Goldhaber JI, Fenczik C, Glombotski CC, Ginsberg MH, Loftus JC. β 1-integrins participate in the hypertrophic response of rat ventricular myocytes. Circ Res 1998;82:1160-1172.
Hoffman EP, Hudecki MS, Rosenberg PA, Pollina CM, Kunkel LM. Cell and fiber-type distribution of dystrophin. Neuron 1988;1:411-420.
Hoffman EP, Kunkel LM. Dystrophin abnormalities in Duchenne/Becker muscular dystrophy. Neuron 1989;2:1019-1029.
Ahn AH, Kunkel LM. The structural and functional diversity of dystrophin. Nature Genetics 1993;3:283-291.
Keeling PJ, Gang Y, Smith G, Seo H, Bent SE, Murday V, Caforio ALP, McKenna WJ. Familial dilated cardiomyopathy in the United Kingdom. BR Heart J 1995;73:417-421.
Maron BJ. Hypertrophic cardiomyopathy. N Engl J Med 1997;350:127-133.
Poetter K, Jiang H, Hassanzadeh S, Master S, Chang A, Dalakas M, Rayment I, Fananapazir L, Epstein N. Mutations in either the essential or regulatory light chains of myosin are associated with a rare myopathy in human heart and skeletal muscle. Nature Genet 1996;13:63-69.
Kimura A, Harada H, Park JE, Nishi H, Satoh M, Takahashi M, Hiroi S, Sasaoka T, Ohbuchi M, Nakamura T. Mutations in the cardiac troponin-I gene associated with hypertrophic cardiomyopathy. Nat Genet 1997;16:379-382.
Beggs AH. Dystrophinopathy, the expanding phenotype: Dystrophin abnormalities in X-linked dilated cardiomyopathy. Circulation 1997;95:2344-2347.
Towbin JA, Hejtmancik JF, Brink P, Gelb B, Zhu XM, Chamberlain JS, McCabe ERB, Swift M. X-linked dilated cardiomyopathy. Molecular genetic evidence of linkage to the Duchenne muscular dystrophy (dystrophin) gene at the Xp21 locus. Circulation 1993;87:1854-1865.
Muntoni F, Wilson L, Marrosu MG, Cianchetti C, Mestroni L, Ganau A, Dubowitz V, Sewry C. A mutation in the dystrophin gene selectively affecting dystrophin expression in the heart. J Clin Invest 1995;96:693-699.
Ohlendieck K. Towards an understanding of the dystrophin-glycoprotein complex: Linkage between the extracellular matrix and the membrane cytoskeleton in muscle fibers. Eur J Cell Biol 1996;69:1-10.
Brown RH Jr. Dystrophin-associated proteins and the muscular dystrophies: A glossary. Brain Pathology 1996;6:19-24.
Severs NJ, Shotton DM, eds. Rapid Freezing, Freeze Fracture, and Deep Etching. New York: Wiley-Liss Inc., 1995:1-372.
Pinto da Silva P, Barbosa MLF, Aguas AP. A guide to fracture-label: Cytochemical labeling of freeze-fractured cells. In: Koehler JK ed. Advanced Techniques in Biological Electron Microscopy. Volume 3. Springer Verlag, 1986:201-227.
Severs NJ. Freeze-fracture cytochemistry: An explanatory survey of methods, In: Severs NJ, Shotton DM, eds. Rapid Freezing, Freeze Fracture, and Deep Etching. New York: Wiley-Liss Inc., 1995:173-208.
Stevenson S, Rothery S, Cullen MJ, Severs NJ. Dystrophin is not a specific component of the cardiac costamere. Circ Res 1997;80:269-280.
Kaprielian RR, Stevenson S, Rothery SM, Cullen MJ, Severs NJ. Distinct patterns of dystrophin organisation in myocyte sarcolemma and transverse tubules of normal and diseased human myocardium. Circulation 2000;101:2586-2594.
Zubrzycka-Gaarn EE, Bulman DE, Karpati G, Burghes AHM, Belfall B, Klamut HJ, Talbot J, Hodges RS, Ray PN, Worton RG. The Duchenne muscular dystrophy gene product is localised in sarcolemma of human skeletal muscle. Nature 1988;333:466-469.
Watkins SC, Hoffman EP, Slayter HS, Kunkel LM. Immunoelectron microscopic localisation of dystrophin in myofibres. Nature 1988;333:863-866.
Arahata K, Ishiura T, Tsukahara T, Suhara Y, Eguchi C, Ishihara T, Nonaka I, Ozawa E, Sugita H. Immunostaining of skeletal and cardiac muscle surface membrane with antibody against Duchenne muscular dystrophy peptide. Nature 1988;333:861-863.
Bonilla E, Samitt C, Miranda A, Hays A, Salviati G, Dimauro S, Kunkel LM, Hoffman E, Rowland I. Duchenne muscular dystrophy: Deficiency of dystrophin at muscle cell surface. Cell 1988;54:447-452.
Byers TJ, Kunkel LM, Watkins SC. The subcellular distribution of dystrophin in mouse skeletal, cardiac and smooth muscle. J Cell Biol 1991;115:411-421.
Porter GA, Dmytrenko GM, Winkelmann JC, Bloch RJ. Dystrophin colocalises with β spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J Cell Biol 1992;117:997-1005.
Masuda T, Fujimaki N, Ozawa E, Ishikawa H. Confocal laser microscopy of dystrophin localization in guinea pig skeletal muscle fibers. J Cell Biol 1992;119:543-548.
Straub V, Bittner RE, Leger JJ, Voit T. Direct visualization of the dystrophin network on skeletal muscle fiber membrane. J Cell Biol 1992;119:1183-1191.
Minetti C, Beltrame F, Marcenaro G, Bonilla E. Dystrophin at the plasma membrane of human fibres shows a costameric localisation. Neuromusc Disord 1992;2:99-109.
Klietsch R, Ervasti JM, Arnold W, Campbell KP, Jorgensen AO. Dystrophin-glycoprotein complex and laminin colocalize to the sarcolemma and transverse tubules of cardiac muscle. Circ Res 1993;72:349-360.
Frank JS, Mottino G, Chen F, Peri V, Holland P, Tuana BS. Subcellular distribution of dystrophin in isolated adult and neonatal cardiac myocytes. Am J Physiol Cell Physiol 1994;267:C1707-C1716.
Meng HP, Leddy JJ, Frank J, Holland P, Tuana BS. The association of cardiac dystrophin with myofibrils/Z-disc regions in cardiac muscle suggests a novel role in the contractile apparatus. J Biol Chem 1996;271:12364-12371.
Kostin S, Scholz D, Shimada T, Maeno Y, Mollnau H, Hein S, Schaper J. The internal and external protein scaffold of the T-tubular system in cardiomyocytes. Cell Tissue Res 1998;294:449-460.
Stevenson S, Rothery S, Cullen MJ, Severs NJ. Spatial relationship of the C-terminal domains of dystrophin and β-dystroglycan in cardiac muscle support a direct molecular interaction at the plasma membrane interface. Circ Res 1998;82:82-93.
Cullen MJ, Walsh J, Nicholson LV, Harris JB. Ultrastructural localisation of dystrophin in human muscle by using gold immunolabelling. Proc R Soc Lond B 1990;240:197-210.
Engel AG, Yamamoto M, Fischbeck KH. Dystrophinopathies In: Engel AG, Franzini-Armstrong C, eds. Myology: Basic and Clinical, Vol 2, Section 1, 1994;Chap 41:1133-1187.
Mokri B, Engel AG. Duchenne dystrophy: Electron microscopic findings pointing to a basic or early abnormality in the plasma membrane of the muscle fiber. Neurology 1975;25:1111-1120.
Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 1993;90:3710-3714.
Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ. The molecular basis of muscular dystrophy on the mdx mouse: A point mutation. Science 1989;244:1578-1580.
Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Slakdy JT, Kelly AM. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 1991;352:536-539.
Sigurdsen WJ, Sachs F. Sarcolemmal mechanical properties in mouse myoblasts and muscle fibers. Biopys J 1994;66:A171.
Pasternak C, Wong S, Elson EL. Mechanical function of dystrophin in muscle cells. J Cell Biol 1995;128:355-361.
Dupont-Versteegden EE. McCarter RJ, Katz MS. Voluntary exercise decreases progression of muscular dystrophy in diaphragm of mdx mice. J Appl Physiol 1994;77:1736-1741.
Love DR, Byth BC, Tinsley JM, Blake DJ, Davies KE. Dystrophin and dystrophin-related proteins: A review of protein and RNA studies. Neuromusc Disord 1993;3:5-21.
Muñoz P, Rosemblatt M, Testar X, Palacin M, Zorzano A. Isolation and characterization of distinct domains of sarcolemma and T-tubules from rat skeletal muscle. Biochem J 1995;307:273-280.
Franco A, Lansman JB. Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 1990;344:670-673.
Fong P, Turner PR, Denetclaw WF, Steinhardt RA. Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 1990;250:673-676.
Hopf FW, Turner PR, Denetclaw WF, Reddy P, Steinhardt RA. A critical evaluation of resting intracellular free calcium regulation in dystrophic mdx muscle. Am J Physiol 1996;271:C1325-C1339.
Carlson CG, Officer T. Single channel evidence for a cytoskeletal defect involving acetylcholine receptors and calcium influx in cultured dystrophic (mdx) myotubes. Muscle Nerve 1996;19:1116-1126.
Brenman JE, Chao DS, Xia H, Aldape X, Bredt DS. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 1995;82:743-752.
Chang WJ, Iannaccone ST, Lau KS, Masters BSS, Mccabe TJ, Mcmillan K, Padre RC, Spencer MJ, Tidball JG, Stull JT. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA 1996;93:9142-9147.
Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP. Expression of caveolin-3 in skeletal cardiac and smooth muscle cells: Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophinassociated glycoproteins. J Biol Chem 1996;271:15150-15165.
Towbin JA. The role of cytoskeletal proteins in cardiomyopathies. Curr Op in Cell Biol 1998;10:131-139.
Sakamoto A, Ono K, Abe M, Jasmin G, Eki T, Murakami Y, Masaki T, Toyo-Oka T, Hanaoka F. Both hypertrophic and dilated cardiomyopathies are caused by mutation of the same gene, delta-sarcoglycan, in hamster: An animal model of disrupted dystrophin-associated glycoprotein complex. Proc Natl Acad Sci 1997;94:13873-13878.
Lu S, Hoey A. Changes in function of cardiac receptors mediating the effects of the autonomic nervous system in the muscular dystrophy (mdx) mouse. J Mol Cell Cardiol 2000; 32:143-152.
Alloatti G, Gallo MP, Penna C, Levi RC. Properties of cardiac cells from dystrophic mouse. J Mol Cell Cardiol 1995;27:1775-1779.
Schaper J, Froede R, Hein St, Buck A, Hashizume H, Speiser B, Friedl A, Bleese N. Impairment of the myocardial ultrastructure and changes of the cytoskeleton in dilated cardiomyopathy. Circulation 1991;83:504-514.
Ganote CE, Armstrong S. Ischemia and the myocyte cytoskeleton: review and speculation. Cardiovasc Res 1993;27:1387-1403.
Severs NJ, Dupont E, Kaprielian RR, Yeh H-I, Rothery S. Gap junctions and connexins in the cardiovascular system. In: Yacoub MH, Carpentier A, Pepper J, Fabiani J-N, eds. Annual of Cardiac Surgery, 9th edition. London: Current Science, 1996:31-44.
Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y. Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 1996;134:1255-1270.
Cameron CHS, Mirakhur M, Allen IV. Desmin myopathy with cardiomyopathy. Acta Neuropathol 1995;89:560-566.
Maeda M, Holder E, Lowes B, Valent S, Blies RB. Dilated cardiomyopathy with deficiency of the cytoskeletal protein metavinculin. Circulation 1997;95:17-20.
Bowles KR, Gajarski R, Porter P, Goytia V, Bachinski L, Roberts R, Pignatelli R, Towbin JA. Gene mapping of familial autosomal dominant dilated cardiomyopathy to chromosome 10q21-23. J Clin Invest 1996;98:1355-1360.
Kaprielian RR, Poole-Wilson PA, Severs NJ. Different mechanisms of ventricular dilatation in idiopathic dilated cardiomyopathy and ischemic heart failure: A study of myocyte dimensions. JACC 1998;31 (suppl A):374A.
Beltrami CA, Finato N, Rocco, Feruglio GA, Puricelli C, Cigola E, Quaini F, Sonnenblick EH, Olivetti G, Anversa P. Structural basis of end-stage failure in ischemic cardiomyopathy in humans. Circulation 1994;89:151-163.
Beltrami CA, Finato N, Rocco M, Feruglio GA, Puricelli C, Cigola E, Sonnenblick EH, Olivetti G, Anversa P. The cellular basis of dilated cardiomyopathy in humans. J Mol Cell Cardiol 1995;27:291-305.
Pfeffer MA, Braunwald E, Moye LA, Basta L, Brown EJ, Cuddy TE, Davis BR, Geltman EM, Goldman S, Flaker GC, Klein H, Lamas GA, Packer M, Rouleau JL, Rutherford J, Wertheimer JH, Hawkins CM. Effect of captopril on mortality and morbidity in patients with left ventricular dysfunction after myocardial infarction-results of the Survival and Ventricular Enlargement Trial. N Engl J Med 1992;327:669-677.
Merit Study Group. Effect of metoprolol in chronic heart failure: Metoprolol CR/XL. Randomized intervention trial in congestive heart failure. Lancet 1999;99:2396-2401.
Rahimtoola SH The hibernating myocardium. Am Heart J 1989;117:211-221.
Levin HR, Oz MC, Chen JM, Packer M, Burkhoff D. Reversal of chronic ventricular dilatation in patients with end-stage dilated cardiomyopathy by prolonged mechanical unloading. Circulation 1995;91:2717-2720.
Muller J, Wallukat G, Weng Y-G, Dandel M, Spiegelsberger S, Semrau S, Brandes K, Theodoridis V, Loebe M, Meyer R, Hetzer R. Weaning from mechanical support in patients with idiopathic dilated cardiomyopathy. Circulation 1997;96:542-549.
Gerdes AM, Kellerman SE, Moore JA, Muffly KE, Clark LC, Reaves PY, Malec KB, Mckeown PP, Schocken DD. Structural remodelling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation 1992;86:426-430.