Eye muscle sparing by the muscular dystrophies: Lessons to be learned?
2000; Wiley; Volume: 48; Issue: 3‐4 Linguagem: Inglês
10.1002/(sici)1097-0029(20000201/15)48
ISSN1097-0029
AutoresFrancisco H. Andrade, John D. Porter, Henry J. Kaminski,
Tópico(s)Laser Applications in Dentistry and Medicine
ResumoMicroscopy Research and TechniqueVolume 48, Issue 3-4 p. 192-203 Topical PaperFree Access Eye muscle sparing by the muscular dystrophies: Lessons to be learned? Francisco H. Andrade, Corresponding Author Francisco H. Andrade [email protected] Departments of Neurology, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106Department of Neurology, Case Western Reserve University and University Hospitals of Cleveland, 11100 Euclid Ave., Cleveland, OH 44106.Search for more papers by this authorJohn D. Porter, John D. Porter Departments of Neurology, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106Search for more papers by this authorHenry J. Kaminski, Henry J. Kaminski Departments of Neurology, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106 Department of Neurosciences, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106Search for more papers by this author Francisco H. Andrade, Corresponding Author Francisco H. Andrade [email protected] Departments of Neurology, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106Department of Neurology, Case Western Reserve University and University Hospitals of Cleveland, 11100 Euclid Ave., Cleveland, OH 44106.Search for more papers by this authorJohn D. Porter, John D. Porter Departments of Neurology, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106Search for more papers by this authorHenry J. Kaminski, Henry J. Kaminski Departments of Neurology, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106 Department of Neurosciences, Case Western Reserve University, University Hospitals of Cleveland, and Department of Veterans Affairs Medical Center, Cleveland, Ohio 44106Search for more papers by this author First published: 01 February 2000 https://doi.org/10.1002/(SICI)1097-0029(20000201/15)48:3/4 3.0.CO;2-JCitations: 42AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract The devastating consequences of the various muscular dystrophies are even more obvious when a muscle or muscle group is spared. The study of the exceptional cell or tissue responses may prove to be of considerable value in the analysis of disease mechanisms. The small muscles responsible for eye movements, the extraocular muscles, have functional and morphological characteristics that set them aside from other skeletal muscles. Notably, these muscles are clinically unaffected in Duchenne/Becker, limb-girdle, and congenital muscular dystrophies, pathologies due to a broken mechanical or signaling linkage between the cytoskeleton and the extracellular matrix. Uncovering the strategies used by the extraocular muscles to “naturally” protect themselves in these diseases should contribute to knowledge of both pathogenesis and treatment. We propose that careful investigation of the cellular determinants of extraocular muscle-specific properties may provide insights into how these muscles avoid or adapt to the cascade of events leading to myofiber degeneration in the muscular dystrophies. Microsc. Res. Tech. 48:192–203, 2000. © 2000 Wiley-Liss, Inc. REFERENCES Andrade FH, Krebs CR, Bonner PH, Porter JD. 1998. Extraocular muscle is spared in merosin-deficient congenital muscular dystrophy. Muscle Nerve Suppl. 7: S106 (Abstr). Google Scholar Asmussen G, Gaunitz U. 1981. Mechanical properties of the isolated inferior oblique muscle of the rabbit. Pflügers Arch 392: 183–190. 10.1007/BF00581270 CASPubMedWeb of Science®Google Scholar Asmussen G, Beckers-Bleukx G, Maréchal G. 1994. The force-velocity relation of the rabbit inferior oblique muscle; influence of temperature. Pflügers Arch 426: 542–547. 10.1007/BF00378532 CASPubMedWeb of Science®Google Scholar Bahn RS, Heufelder AE. 1993. Pathogenesis of Graves' ophthalmopathy. N Engl J Med 91: 1411–1419. Google Scholar Bertorini TE, Palmieri GM, Griffin J, Chesney C, Pifer D, Verling L, Airozo D, Fox IH. 1985. Chronic allopurinol and adenine therapy in Duchenne muscular dystrophy: effects on muscle function, nucleotide degradation, and muscle ATP and ADP content. Neurology 35: 61–65. 10.1212/WNL.35.1.61 CASPubMedWeb of Science®Google Scholar Blake DJ, Tinsley JM, Davies KE. 1996. Utrophin: a structural and functional comparison to dystrophin. Brain Pathol 6: 37–47. 10.1111/j.1750-3639.1996.tb00781.x CASPubMedWeb of Science®Google Scholar Briggs MH, Jacoby J, Davidowitz J, Schachat FH. 1988. Expression of a novel combination of fast and slow troponin T isoforms in rabbit extraocular muscles. J Muscle Res Cell Motil 9: 241–247. 10.1007/BF01773894 CASPubMedWeb of Science®Google Scholar Brueckner JK, Porter JD. 1998. Visual system maldevelopment disrupts extraocular muscle-specific myosin expresion. J Appl Physiol 85: 584–592. 10.1152/jappl.1998.85.2.584 CASPubMedWeb of Science®Google Scholar Brueckner JK, Itkis O, Porter JD. 1996. Spatial and temporal patterns of myosin heavy chain expression in developing rat extraocular muscle. J Muscle Res Cell Motil 17: 297–312. 10.1007/BF00240928 CASPubMedWeb of Science®Google Scholar Brueckner JK, Ashby LP, Prichard JR, Porter JD. 1999. Vestibulo-ocular pathways modulate extraocular muscle myosin expression patterns. Cell Tissue Res 295: 477–484. 10.1007/s004410051253 CASPubMedWeb of Science®Google Scholar Burden SJ. 1998. The formation of neuromuscular synapses. Genes Dev 12: 133–148. 10.1101/gad.12.2.133 CASPubMedWeb of Science®Google Scholar Campbell KP. 1995. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80: 675–679. 10.1016/0092-8674(95)90344-5 CASPubMedWeb of Science®Google Scholar Celio MR, Heizmann CW. 1982. Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres. Nature 297: 504–506. 10.1038/297504a0 CASPubMedWeb of Science®Google Scholar Clerk A, Morris GE, Dubowitz V, Davies KE, Sewry CA. 1993. Dystrophin-related protein, utrophin, in normal and dystrophic human fetal skeletal muscle. Histochem J 25: 554–561. 10.1007/BF02388063 CASPubMedWeb of Science®Google Scholar Close RI, Luff AR. 1974. Dynamic properties of inferior rectus muscle of the rat. J Physiol (London) 236: 259–270. 10.1113/jphysiol.1974.sp010434 CASPubMedWeb of Science®Google Scholar Collins CC, O'Meara D, Scott AB. 1975. Muscle tension during unrestrained human eye movements. J Physiol (London) 245: 351–369. 10.1113/jphysiol.1975.sp010850 CASPubMedWeb of Science®Google Scholar Couly GF, Coltey PM, Le Douarin NM. 1992. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114: 1–15. 10.1242/dev.114.1.1 PubMedWeb of Science®Google Scholar Crosbie RH, Lebakken CS, Holt KH, Venzke DP, Straub V, Lee JC, Grady RM, Chamberlain JS, Sanes JR, Campbell KP. 1999. Membrane targeting and stabilization of sarcospan is mediated by the sarcoglycan subcomplex. J Cell Biol 145: 153–165. 10.1083/jcb.145.1.153 CASPubMedWeb of Science®Google Scholar Deconinck N, Tinsley J, De Backer F, Fisher R, Kahn D, Phelps S, Kavies K, Gillis J-M. 1997. Expression of truncated eutrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nature Med 3: 1216–1221. 10.1038/nm1197-1216 CASPubMedWeb of Science®Google Scholar Di Constanzo A, Toreillo A, Mottola A, Di Iorio G, Bonavita V, Tedeschi G. 1997. Relative sparing of extraocular muscles in myotonic dystrophy. Acta Neurol Scand 95: 158–163. 10.1111/j.1600-0404.1997.tb00088.x PubMedWeb of Science®Google Scholar Disatnik M-H, Dhawan J, Yu Y, Beal MF, Whirl MM, Franco AA, Rando TA. 1998. Evidence of oxidative stress in mdx mouse muscle: studies of the pre-necrotic state. J Neurol Sci 161: 77–84. 10.1016/S0022-510X(98)00258-5 CASPubMedWeb of Science®Google Scholar Duclos F, Straub V, Moore SA, Venzke DP, Hrstka RF, Crosbie RH, Durbeej M, Lebakken CS, Ettinger AJ, van der Meulen J, Holt KH, Lim LE, Sanes JR, Davidson BL, Faulkner JA, Williamson R, Campbell KP. 1998. Progressive muscular dystrophy in α-sarcoglycan-deficient mice. J Cell Biol 142: 1461–1471. 10.1083/jcb.142.6.1461 CASPubMedWeb of Science®Google Scholar Duggan DJ, Hoffman EP. 1996. Autosomal recessive muscular dystrophy and mutations of the sarcoglycan complex. Neuromusc Disord 6: 475–482. 10.1016/S0960-8966(96)00388-4 CASPubMedWeb of Science®Google Scholar Edwards RH, Jones DA, Jackson MJ. 1984. An approach to treatment in muscular dystrophy with particular reference to agents influencing free radical damage. Med Biol 62: 143–147. CASPubMedWeb of Science®Google Scholar Emery AEH. 1987. Duchenne muscular dystrophy. Oxford: Oxford University Press. Google Scholar Emery AEH. 1994. Some unanswered questions in Duchenne muscular dystrophy. Neuromusc. Disord 4: 301–303. CASPubMedWeb of Science®Google Scholar Engel AG, Yamamoto M, Fischbeck K. 1994. Muscular dystrophies. In: A Engel, C Franzini-Armstrong, editors. Myology. New York: McGraw-Hill, Inc. p 1133–1187. Web of Science®Google Scholar Frueh BR, Hayes A, Lynch GS, Williams DA. 1994. Contractile properties and temperature sensitivity of the extraocular muscles, the levator and superior rectus, of the rabbit. J Physiol (London) 475: 327–336. 10.1113/jphysiol.1994.sp020073 CASPubMedWeb of Science®Google Scholar Fuchs AF, Binder MD. 1983. Fatigue resistance of human extraocular muscles. J Neurophysiol 49: 28–34. 10.1152/jn.1983.49.1.28 CASPubMedWeb of Science®Google Scholar Gailly P, Hermans E, Octave JN, Gillis JM. 1993. Specific increase of genetic expression of parvalbumin in fast skeletal muscles of mdx mice. FEBS Lett 326: 272–274. 10.1016/0014-5793(93)81806-B CASPubMedWeb of Science®Google Scholar Gamstorp I, Gustavson KH, Hellstrom O, Nordgren B. 1986. A trial of selenium and vitamin E in boys with muscular dystrophy. J Child Neurol 1: 211–214. 10.1177/088307388600100306 CASPubMedWeb of Science®Google Scholar Ginsberg J, Hamblet J, Menefee M. 1978. Ocular abnormality in myotonic dystrophy. Ann Ophthalmol 10: 1021–1028. CASPubMedWeb of Science®Google Scholar Guo W-XA, Nichol M, Merlie JP. 1996. Cloning and expression of full length mouse utrophin: the differential association of utrophin and dystrophin with AChR clusters. FEBS Lett 398: 259–264. 10.1016/S0014-5793(96)01216-1 CASPubMedWeb of Science®Google Scholar Hack AA, Ly CT, Jiang F, Clendenin CJ, Sigrist KS, Wollmann RL, McNally EM. 1998. γ-Sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J Cell Biol 142: 1279–1287. 10.1083/jcb.142.5.1279 CASPubMedWeb of Science®Google Scholar Halestrap AP, Griffiths EJ, Connern CP. 1993. Mitochondrial calcium handling and oxidative stress. Biochem Soc Trans 21: 353–358. 10.1042/bst0210353 CASPubMedWeb of Science®Google Scholar Helliwell TR, Man NT, Morris GE, Davies KE. 1992. The dystrophin-related protein, utrophin, is expressed on the sarcolemma of regenerating human skeletal muscle fibres in dystrophies and inflammatory myopathies. Neuromusc Disord 2: 177–184. 10.1016/0960-8966(92)90004-P CASPubMedWeb of Science®Google Scholar Hennig R, Lømo T. 1985. Firing patterns of motor units in normal rats. Nature 314: 164–166. 10.1038/314164a0 CASPubMedWeb of Science®Google Scholar Hodges BL, Hayashi YK, Nonaka I, Wang W, Arahata K, Kaufman SJ. 1997. Altered expression of the α7β1 integrin in human and murine muscular dystrophies. J Cell Sci 110: 2873–2881. 10.1242/jcs.110.22.2873 CASPubMedWeb of Science®Google Scholar Hunter MI, Mohamed JB. 1986. Plasma antioxidants and lipid peroxidation products in Duchenne muscular dystrophy. Clin Chim Acta 155: 123–131. 10.1016/0009-8981(86)90273-1 CASPubMedWeb of Science®Google Scholar Jackson MJ, Jones DA, Edwards RHT. 1984. Experimental skeletal muscle damage: the nature of the calcium-activated degenerative processes. Eur J Clin Invest 14: 369–374. 10.1111/j.1365-2362.1984.tb01197.x CASPubMedWeb of Science®Google Scholar Jackson MJ, Coakley J, Stokes M, Edwards RH, Oster O. 1989. Selenium metabolism and supplementation in patients with muscular dystrophy. Neurology 39: 655–659. 10.1212/WNL.39.5.655 CASPubMedWeb of Science®Google Scholar Jacoby J, Ko K. 1993. Sarcoplasmic reticulum fast Ca2+-pump and myosin heavy chain expression in extraocular muscles. Invest Ophthalmol Vis Sci 34: 2848–2858. CASPubMedWeb of Science®Google Scholar Kaminski H, Ruff R. 1997. Ocular muscle involvement by myasthenia gravis. Ann Neurol 41: 419–420. 10.1002/ana.410410402 CASPubMedWeb of Science®Google Scholar Kaminski HJ, Al-Hakim M, Leigh RJ, Katirji MB, Ruff RL. 1992. Extraocular muscles are spared in advanced Duchenne dystrophy. Ann Neurol 32: 586–588. 10.1002/ana.410320418 CASPubMedWeb of Science®Google Scholar Kaminski HJ, Fenstermaker RA, Abdul-Karim FW, Clayman J, Ruff RL. 1993. Acetylcholine receptor subunit gene expression in thymic tissue of myasthenic and non-myasthenics. Muscle Nerve 16: 1332–1337. 10.1002/mus.880161210 CASPubMedWeb of Science®Google Scholar Kar NC, Pearson CM. 1979. Catalase, superoxide dismutase, glutathione reductase and thiobarbituric acid-reactive products in normal and dystrophic human muscle. Clin Chim Acta 94: 277–280. 10.1016/0009-8981(79)90076-7 CASPubMedWeb of Science®Google Scholar Karpati G, Carpenter S. 1986. Small-caliber skeletal muscle fibers do not suffer deleterious consequences of dystrophic gene expression. Am J Med Genet 25: 653–658. 10.1002/ajmg.1320250407 PubMedWeb of Science®Google Scholar Karpati G, Carpenter S, Prescott S. 1988. Small-caliber skeletal muscle fibers do not suffer necrosis in mdx mouse dystrophy. Muscle Nerve 11: 795–803. 10.1002/mus.880110802 CASPubMedWeb of Science®Google Scholar Karpati G, Carpenter S, Morris GE, Davies KE, Guerin C, Holland P. 1993. Localization and quantitation of the chromosome 6-encoded dystrophin-related protein in normal and pathological human muscle. J Neuropathol Exp Neurol 52: 119–128. 10.1097/00005072-199303000-00004 CASPubMedWeb of Science®Google Scholar Katoh A, Kitazawa H, Itohara S, Nagao S. 1998. Dynamic characteristics and adaptability of mouse vestibulo-ocular and optokinetic response eye movements and the role of the flocculo-olivary system revealed by chemical lesions. Proc Natl Acad Sci USA 95: 7705–7710. 10.1073/pnas.95.13.7705 CASPubMedWeb of Science®Google Scholar Khurana TS, Hoffman EP, Kunkel LM. 1990. Identification of a chromosome 6-encoded dystrophin-related protein. J Biol Chem 265: 16717–16720. CASPubMedWeb of Science®Google Scholar Khurana TS, Watkins SC, Chafey P, Chelly J, Tomé FMS, Fardeau M, Kaplan J-C, Kunkel LM. 1991. Immunolocalization and developmental expression of dystrophin related proteins in skeletal muscle. Neuromusc Disord 1: 185–194. 10.1016/0960-8966(91)90023-L CASPubMedGoogle Scholar Khurana TS, Prendergast RA, Alameddine HS, Tomé FMS, Fardeau M, Arahata K, Sugita H, Kunkel LM. 1995. Absence of extraocular muscle pathology in Duchenne's muscular dystrophy: role for calcium homeostasis in extraocular muscle sparing. J Exp Med 182: 467–475. 10.1084/jem.182.2.467 CASPubMedWeb of Science®Google Scholar King WM, Fuchs AF, Magnin M. 1981. Vertical eye movement-related responses of neurons in midbrain near interstitial nucleus of Cajal. J Neurophysiol 46: 549–562. CASPubMedWeb of Science®Google Scholar Kuwabara T, Lessel S. 1976. Electron microscopic study of extraocular muscles in myotonic dystrophy. Am J Ophthalmol 82: 303–309. 10.1016/0002-9394(76)90438-4 CASPubMedWeb of Science®Google Scholar Law DJ, Allen DL, Tidball JG. 1994. Talin, vinculin and DRP (utrophin) concentrations are increased at mdx myotendinous junctions following onset of necrosis. J Cell Sci 107: 1477–1483. CASPubMedWeb of Science®Google Scholar Leberer E, Härtner K-T, Pette D. 1988. Postnatal development of Ca2+ sequestration by the sarcoplasmic reticulum of fast and slow muscles in normal and dystrophic mice. Eur J Biochem 174: 247–253. 10.1111/j.1432-1033.1988.tb14090.x CASPubMedWeb of Science®Google Scholar Lefaucheur JP, Pastoret C, Sebille A. 1995. Phenotype of dystrophinopathy in old mdx mice. Anat Rec 242: 70–76. 10.1002/ar.1092420109 CASPubMedWeb of Science®Google Scholar Love DR, Hill DF, Dickson G, Spurr NK, Byth BC, Marsden RF, Walsh FS, Edwards YH, Davies KE. 1989. An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339: 55–58. 10.1038/339055a0 CASPubMedWeb of Science®Google Scholar Luff AR. 1981. Dynamic properties of the inferior rectus, extensor digitorum longus, diaphragm and soleus muscles of the mouse. J Physiol (London) 313: 161–171. 10.1113/jphysiol.1981.sp013656 PubMedWeb of Science®Google Scholar Lynch GS, Frueh BR, Williams DA. 1994. Contractile properties of single skinned fibres from the extraocular muscles, the levator and superior rectus, of the rabbit. J Physiol (London) 475: 337–346. 10.1113/jphysiol.1994.sp020074 CASPubMedWeb of Science®Google Scholar Matsumura K, Campbell KP. 1994. Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 17: 2–15. 10.1002/mus.880170103 CASPubMedWeb of Science®Google Scholar Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP. 1992. Association of dystrophin-related protein with dystrophin associated proteins in mdx mouse muscle. Nature 360: 588–591. 10.1038/360588a0 CASPubMedWeb of Science®Google Scholar McArdle A, Helliwell TR, Beckett GJ, Catapano M, Davis A, Jackson MJ. 1998. Effect of propylthiouracil-induced hypothyroidism on the onset of skeletal muscle necrosis in dystrophin-deficient mdx mice. Clin Sci 95: 83–89. 10.1042/CS19980029 CASPubMedWeb of Science®Google Scholar McCutchan HJ, Schwappach JR, Enquist EG, Walden DL, Terada LS, Reiss OK, Leff JA, Repine JE. 1990. Xanthine oxidase-derived H2O2 contributes to reperfusion injury of ischemic skeletal muscle. Am J Physiol 258: H1415–H1419. 10.1152/ajpheart.1990.258.5.H1415 CASPubMedWeb of Science®Google Scholar Mechler F, Imre S, Dioszeghy P. 1984. Lipid peroxidation and superoxide dismutase activity in muscle and erythrocytes in Duchenne muscular dystrophy. J Neurol Sci 63: 279–283. 10.1016/0022-510X(84)90150-3 CASPubMedWeb of Science®Google Scholar Mendell JR, Sahenk Z, Prior TW. 1995. The childhood muscular dystrophies: diseases sharing a common pathogenesis of membrane instability. J Child Neurol 10: 150–159. 10.1177/088307389501000219 CASPubMedWeb of Science®Google Scholar Mitsumoto H, Chad DA, Pioro EP. 1998. Amyotrophic lateral sclerosis. Philadelphia: F.A. Davis. Google Scholar Morris GE. 1998. Dystrophin is replaced by utrophin in frog heart: implications for muscular dystrophy. Neuromusc Disord 7: 493–498. 10.1016/S0960-8966(97)00109-0 Web of Science®Google Scholar Pachter BR, Davidowitz J, Breinin GM. 1973. A light and electron microscopic study in serial sections of dystrophic extraocular muscle fibers. Invest Ophthalmol 12: 917–923. CASPubMedWeb of Science®Google Scholar Pastoret C, Sebille A. 1995. mdx Mice show progressive weakness and muscle deterioration with age. J Neurol Sci 129: 97–105. 10.1016/0022-510X(94)00276-T CASPubMedWeb of Science®Google Scholar Pegoraro E, Marks H, Garcia CA, Crawford T, Mancias P, Connolly AM, Fanin M, Martinello F, Trevisan CP, Angelini C, Stella A, Scavina M, Munk RL, Servidei S, Bönnemann CC, Bertorini T, Acsadi G, Thompson CE, Gagnon D, Hoganson G, Carver V, Zimmerman RA, Hoffman EP. 1998. Laminin α2 muscular dystrophy. Genotype/phenotype studies of 22 patients. Neurology 51: 101–110. 10.1212/WNL.51.1.101 CASPubMedWeb of Science®Google Scholar Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL. 1993. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90: 3710–3714. 10.1073/pnas.90.8.3710 CASPubMedWeb of Science®Google Scholar Pons F, Robert A, Marini JF, Léger JJ. 1994. Does utrophin expression in muscles of mdx mice during postnatal development functionally compensate for dystrophin deficiency. J Neurol Sci 122: 162–170. 10.1016/0022-510X(94)90295-X CASPubMedWeb of Science®Google Scholar Porter JD. 1998. Extraocular muscle sparing in muscular dystrophy: a critical evaluation of potential protective mechanisms. Neuromusc. Disord. 8: 198–203. 10.1016/S0960-8966(98)00015-7 CASPubMedWeb of Science®Google Scholar Porter JD, Baker RS. 1992. Prenatal morphogenesis of primate extraocular muscle: neuromuscular junction formation and fiber type differentiation. Invest. Ophthalmol. Vis. Sci. 33: 657–670. CASPubMedWeb of Science®Google Scholar Porter JD, Baker RS. 1996. Muscles of a different “color”: the unusual properties or the extraocular muscles may predispose or protect them in neurogenic and myogenic disease. Neurology 46: 30–37. 10.1212/WNL.46.1.30 CASPubMedWeb of Science®Google Scholar Porter JD, Karathanasis P. 1998. Extraocular muscle in merosin-deficient muscular dystrophy: cation homeostasis is maintained but is not mechanistic in muscle sparing. Cell Tissue Res 292: 495–501. 10.1007/s004410051078 CASPubMedWeb of Science®Google Scholar Porter JD, Karathanasis P. 1999. The development of extraocular muscle calcium homeostasis parallels visuomotor system maturation. Biochem Biophys Res Commun 257: 678–683. 10.1006/bbrc.1999.0536 CASPubMedWeb of Science®Google Scholar Porter JD, Edney DP, McMahon EJ, Burns LA. 1988. Extraocular myotoxicity of the retrobulbar anesthetic bupivacaine hydrochloride. Invest Ophthalmol Vis Sci 29: 163–174. CASPubMedWeb of Science®Google Scholar Porter JD, Baker RS, Ragusa RJ, Brueckner JK. 1995. Extraocular muscles: basic and clinical aspects of structure and function. Surv Ophthalmol 39: 451–484. 10.1016/S0039-6257(05)80055-4 CASPubMedWeb of Science®Google Scholar Porter JD, Karathanasis P, Bonner PH, Brueckner JK. 1997. The oculomotor periphery: the clinician's focus is no longer a basic science stepchild. Curr Opin Neurobiol 7: 880–887. 10.1016/S0959-4388(97)80150-X CASPubMedWeb of Science®Google Scholar Porter JD, Rafael JA, Ragusa RJ, Brueckner JK, Trickett JI, Davies KE. 1998. The sparing of extraocular muscle in dystrophinopathy is lost in mice lacking utrophin and dystrophin. J Cell Sci 111: 1801–1811. CASPubMedWeb of Science®Google Scholar Ragusa RJ, Chow CK, St. Clair DK, Porter JD. 1996. Extraocular, limb and diaphragm muscle group-specific antioxidant enzyme activity patterns in control and mdx mice. J Neurol Sci 139: 180–186. 10.1016/S0022-510X(96)00066-4 CASPubMedWeb of Science®Google Scholar Ragusa RJ, Chow CK, Porter JD. 1997. Oxidative stress as a potential pathogenic mechanism in an animal model of Duchenne muscular dystrophy. Neuromusc Disord 7: 379–386. 10.1016/S0960-8966(97)00096-5 CASPubMedWeb of Science®Google Scholar Robinson DA. 1970. Oculomotor unit behavior in the monkey. J Neurophysiol 33: 393–404. 10.1152/jn.1970.33.3.393 CASPubMedWeb of Science®Google Scholar Robinson DA. 1981. Control of eye movements. In: VB Brooks, editor. Handbook of physiology, Section 1: the nervous system. Bethesda, MD: American Physiological Society. p 1275–1320. Google Scholar Rodemann HP, Waxman L, Goldberg AL. 1982. The stimulation of protein degradation in muscle by Ca++ is mediated by prostaglandin E2 and does not require the calcium-activated protease. J Biol Cheml 257: 8716–8723. CASPubMedWeb of Science®Google Scholar Rome LC. 1998. Some advances in integrative muscle physiology. Comp Biochem Physioll B120: 51–72. 10.1016/S0305-0491(98)00023-6 CASWeb of Science®Google Scholar Sartore S, Mascarello F, Rowlerson A, Gorza L, Ausoni S, Vianello M, Schiaffino S. 1987. Fibre types in extraocular muscles: a new myosin isoform in the fast fibres. J Muscle Res Cell Motil 8: 161–172. 10.1007/BF01753992 CASPubMedWeb of Science®Google Scholar Scelsa S, Simpson D, Reichler B, Dai M. 1996. Extraocular muscle involvement in Becker muscular dystrophy. Neurology 46: 564–566. 10.1212/WNL.46.2.564 CASPubMedWeb of Science®Google Scholar Schachat FH, Diamond MS, Brandt PW. 1987. Effect of different troponin T-tropomyosin combinations on thin filament activation. J Mol Biol 198: 551–554. 10.1016/0022-2836(87)90300-7 CASPubMedWeb of Science®Google Scholar Settles DL, Cihak RA, Erickson HP. 1996. Tenascin-C expression in dystrophin-related muscular dystrophy. Muscle Nerve 19: 147–154. 10.1002/(SICI)1097-4598(199602)19:2 3.0.CO;2-E CASPubMedWeb of Science®Google Scholar Sewry CA, Taylor J, Anderson LVB, Ozawa E, Pogue R, Piccolo G, Bushby K, Dubowitz V, Muntoni F. 1996. Abnormalities in α-, β- and γ-sarcoglycan in patients with limb-girdle muscular dystrophy. Neuromusc Disord 6: 467–474. 10.1016/S0960-8966(96)00389-6 CASPubMedWeb of Science®Google Scholar Sohal GS, Ali AA, Ali MM. 1998. Ventral neural tube cells differentiate into craniofacial skeletal muscles. Biochem Biophys Res Commun 252: 675–678. 10.1006/bbrc.1998.9715 CASPubMedWeb of Science®Google Scholar Spencer RF, Porter JD. 1988. Structural organization of the extraocular muscles. In: JA Büttner-Ennever, editor. Neuroanatomy of the oculomotor system. New York: Elsevier Science Publishers. p 33–79. Google Scholar Stern LZ, Ringel SP, Ziter FA, Menander-Huber KB, Ionasescu V, Pellegrino RJ, Snyder RD. 1982. Drug trial of superoxide dismutase in Duchenne's muscular dystrophy. Arch Neurol 39: 342–346. 10.1001/archneur.1982.00510180020004 CASPubMedWeb of Science®Google Scholar Straub V, Campbell KP. 1997. Muscular dystrophies and the dystrophin-glycoprotein complex. Curr Opin Neurol 10: 168–175. 10.1097/00019052-199704000-00016 CASPubMedWeb of Science®Google Scholar Straub V, Rafael JA, Chamberlain JS, Campbell KP. 1997. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J Cell Biol 139: 375–385. 10.1083/jcb.139.2.375 CASPubMedWeb of Science®Google Scholar Takemitsu M, Ishiura S, Koga R, Kamakura K, Arahata K, Nonaka I, Sugita H. 1991. Dystrophin-related protein in the fetal and denervated skeletal muscles of normal and mdx mice. Biochem Biophys Res Commun 180: 1179–1186. 10.1016/S0006-291X(05)81320-8 CASPubMedWeb of Science®Google Scholar Tanaka J, Ishiguro I, Efuchi C, Saito K, Ozawa E. 1991. Expression of a dystrophin-related protein associated with the skeletal muscle cell membrane. Histochemistry 96: 1–5. 10.1007/BF00266753 CASPubMedWeb of Science®Google Scholar Taylor J, Muntoni F, Dubowitz V, Sewry CA. 1997. The abnormal expression of utrophin in Duchenne and Becker muscular dystrophy is age related. Neuropathol Appl Neurobiol 23: 399–405. 10.1111/j.1365-2990.1997.tb01314.x CASPubMedWeb of Science®Google Scholar Tinsley JM, Davies KE. 1993. Utrophin: a potential replacement for dystrophin? Neuromusc Disord 3: 537–539. 10.1016/0960-8966(93)90111-V CASPubMedWeb of Science®Google Scholar Tinsley JM, Blake DJ, Roche A, Fairbrother U, Riss J, Byth BC, Knight AE, Kendrick-Jones J, Suthers GK, Love DR, Edwards YH, Davies KE. 1992. Primary structure of dystrophin-related protein. Nature 360: 591–593. 10.1038/360591a0 CASPubMedWeb of Science®Google Scholar Tinsley JM, Potter AC, Phelps SR, Fisher R, Trickett JI, Davies KE. 1996. Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384: 349–353. 10.1038/384349a0 CASPubMedWeb of Science®Google Scholar Tullis A, Block BA. 1996. Expression of sarcoplasmic reticulum Ca2+-ATPase isoforms in marlin and swordfish muscle and heater cells. Am J Physiol 271: R262–R275. CASPubMedWeb of Science®Google Scholar Turner PR, Westwood T, Regen CM, Steinhardt RA. 1988. Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335: 735–738. 10.1038/335735a0 CASPubMedWeb of Science®Google Scholar Turner PR, Fong P, Denetclaw WF, Steinhardt RA. 1991. Increased calcium influx in dystrophic muscle. J Cell Biol 115: 1701–1712. 10.1083/jcb.115.6.1701 CASPubMedWeb of Science®Google Scholar van de Water B, Zoeteweij JP, de Bont HJGM, Mulder GJ, Nagelkerke JF. 1994. Role of mitochondrial Ca2+ in the oxidative stress-induced dissipation of the mitochondrial membrane potential. J Biol Chem 269: 14546–14552. CASPubMedWeb of Science®Google Scholar Voit T. 1998. Congenital muscular dystrophies: 1997 update. Brain Dev 20: 65–74. 10.1016/S0387-7604(97)00094-6 CASPubMedWeb of Science®Google Scholar Wahl CM, Noden DM, Baker R. 1994. Developmental relations between sixth nerve motor neurons and their targets in the chick embryos. Dev Dyn 201: 191–202. 10.1002/aja.1002010209 CASPubMedWeb of Science®Google Scholar Webster C, Silberstein L, Hays AP, Blau HM. 1988. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52: 503–513. 10.1016/0092-8674(88)90463-1 CASPubMedWeb of Science®Google Scholar Wehling M, Stull JT, McCabe TJ, Tidball JG. 1998. Sparing of mdx extraocular muscles from dystrophic pathology is not attributable to normalized concentration or distribution of neuronal nitric oxide synthase. Neuromusc Disord 8: 22–29. 10.1016/S0960-8966(97)00136-3 CASPubMedWeb of Science®Google Scholar Weller B, Karpati G, Carpenter S. 1990. Dystrophin-deficient mdx muscle fibers are preferentially vulnerable to necrosis induced by experimental lengthening contractions. J Neurol Sci 100: 9–13. 10.1016/0022-510X(90)90005-8 CASPubMedWeb of Science®Google Scholar Wieczorek DF, Periasamy M, Butler-Browne GS, Whalen RG, Nadal-Ginard B. 1985. Co-expression of multiple myosin heavy chain genes, in addition to a tissue-specific one, in extraocular musculature. J Cell Biol 101: 618–629. 10.1083/jcb.101.2.618 CASPubMedWeb of Science®Google Scholar Winder SJ, Gibson TJ, Kendrick-Jones J. 1995. Dystrophin and utrophin: the missing links!. FEBS Lett 369: 27–33. 10.1016/0014-5793(95)00398-S CASPubMedWeb of Science®Google Scholar Wrogemann K, Peña SDJ. 1976. MItochondrial calcium overload: a general mechanism for cell-necrosis in muscle diseases. Lancet 1: 672–674. 10.1016/S0140-6736(76)92781-1 CASPubMedWeb of Science®Google Scholar Citing Literature Volume48, Issue3-4Special Issue: Muscular Dystrophy1 ‐ 15 February 2000Pages 192-203 ReferencesRelatedInformation
Referência(s)