Extraocular muscles have fundamentally distinct properties that make them selectively vulnerable to certain disorders

Neuromuscular Disorders

Volumn 15, Issue 1, 2005, Pages 17-23

  Yu Wai Man, C Y ^a,b   Chinnery, P F ^a   Griffiths, P G ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b ROYAL VICTORIA INFIRMARY   (United Kingdom)

Author keywords

CPEO; Extraocular muscles; Graves' ophthalmopathy; Myasthenia gravis

Indexed keywords

CHOLINERGIC RECEPTOR; MYOSIN;

CELL MEDIATED CYTOTOXICITY; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; ENDOCRINE OPHTHALMOPATHY; EXTRAOCULAR MUSCLE; EYE MOVEMENT; FATIGUE; HUMAN; IMMUNE RESPONSE; METABOLIC RATE; MOTOR UNIT; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE INNERVATION; MYASTHENIA GRAVIS; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; ADAPTATION; ANIMAL; BIOLOGICAL MODEL; CLASSIFICATION; GRAVES DISEASE; INNERVATION; METABOLISM; MUSCLE CONTRACTION; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; GRAVES DISEASE; HUMANS; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE FIBERS; MYASTHENIA GRAVIS; MYOSINS; OCULOMOTOR MUSCLES; OPHTHALMOPLEGIA, CHRONIC PROGRESSIVE EXTERNAL;

EID: 15044361428     PISSN: 09608966     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nmd.2004.10.002     Document Type: Article

References (55)

1. Hoh JFY, Hughes S, Hugh G, Pozgaj I. Three hierarchies in skeletal muscle fibre classification: allotype, isotype and phenotype. In: Kedes LH, Stockdale FE, editors. Cellular and molecular biology of muscle development. New York: Liss; 1989. p. 15-26.
2. Porter JD, Baker RS. Muscles of a different 'color': the unusual properties of the extraocular muscles may predispose or protect them in neurogenic and myogenic disease. Neurology 1996;46(1): 30-7.
3. Mayr R. Structure and distribution of fiber types in the external eye muscles of the rat. Tissue Cell 1971;3:433-62.
4. Spencer RF, Porter JD. Structural organization of the extraocular muscles. In: Buttner-Enever JA, editor. Reviews in oculomotor research. New York: Elsevier; 1988.
5. Khanna S, Richmonds CR, Kaminski HJ, Porter JD. Molecular organization of the extraocular muscle neuromuscular junction: partial conservation of and divergence from the skeletal muscle prototype. Invest Ophthalmol Vis Sci 2003;44(5):1918-26.
6. Chiarandini DJ, Stefani E. Electrophysiological identification of two types of fibres in rat extraocular muscles. J Physiol 1979;290(2): 453-65.
7. Jacoby J, Ko K, Weiss C, Rushbrook JI. Systematic variation in myosin expression along extraocular muscle fibres of the adult rat. J Muscle Res Cell Motility 1990;11(1):25-40.
8. Salpeter MM. Vertebrate neuromuscular junctions: general morphology, molecular organisation, and functional consequences. In: Salpeter MM, editor. The vertebrate neuromuscular junction. New York: Alan R. Liss; 1987. p. 1-54.
9. kim Y, Zahm D, Liu H, Johns T. Safety margin of neuromuscular transmission in rat extraocular muscle. Noc Neurosci 1982;8:616.
10. Kaminski HJ, Maas E, Spiegel P, Ruff RL. Why are eye muscles frequently involved in myasthenia gravis? Neurology 1990;40(11): 1663-9.
11. Kaminski HJ, Richmonds CR, Kusner LL, Mitsumoto H. Differential susceptibility of the ocular motor system to disease. Ann N Y Acad Sci 2002;956:42-54.
12. Porter JD, Khanna S, Kaminski HJ, et al. Extraocular muscle is defined by a fundamentally distinct gene expression profile. Proc Natl Acad Sci USA 2001;98(21):12062-7.
13. Robinson DA. Oculomotor unit behavior in the monkey. J Neurophysiol 1970;33(3):393-403.
14. Burke RE. The structure and function of motor units. In: Karpati G, Hilton-Jones D, Griggs RC, editors. Disorders of voluntary muscle. Cambridge: Cambridge University Press; 2001. p. 3-25.
15. Nelson JS, Goldberg SJ, McClung JR. Motoneuron electrophysiological and muscle contractile properties of superior oblique motor units in cat. J Neurophysiol 1986;55(4):715-26.
16. Brueckner JK, Itkis O, Porter JD. Spatial and temporal patterns of myosin heavy chain expression in developing rat extraocular muscle. J Muscle Res Cell Motility 1996;17(3):297-312.
17. Rubinstein NA, Hoh JF. The distribution of myosin heavy chain isoforms among rat extraocular muscle fiber types. Invest Ophthalmol Vis Sci 2000;41(11):3391-8.
18. Wieczorek DF, Periasamy M, Butler-Browne GS, Whalen RG, Nadal-Ginard B. Co-expression of multiple myosin heavy chain genes, in addition to a tissue-specific one, in extraocular musculature. J Cell Biol 1985;101(2):618-29.
19. McLoon LK, Rios L, Wirtschafter JD. Complex three-dimensional patterns of myosin isoform expression: differences between and within specific extraocular muscles. J Muscle Res Cell Motility 1999; 20(8):771-83.
20. Rushbrook JI, Weiss C, Ko K, et al. Identification of alpha-cardiac myosin heavy chain mRNA and protein in extraocular muscle of the adult rabbit. J Muscle Res Cell Motility 1994;15(5):505-15.
21. Briggs MM, Schachat F. Early specialization of the superfast myosin in extraocular and laryngeal muscles. J Exp Biol 2000;203(Pt 16): 2485-94.
22. Briggs MM, Schachat F. The superfast extraocular myosin (MYH13) is localized to the innervation zone in both the global and orbital layers of rabbit extraocular muscle. J Exp Biol 2002;205(Pt 20):3133-42.
23. Fuchs AF, Binder MD. Fatigue resistance of human extraocular muscles. J Neurophysiol 1983;49(1):28-34.
24. Wooten GF, Reis DJ. Blood flow in extraocular muscle of cat. Arch Neurol 1972;26(4):350-2.
25. Carry MR, Ringel SP, Starcevich JM. Mitochondrial morphometrics of histochemically identified human extraocular-muscle fibers. Anatomical Record 1986;214(1):8-16.
26. Chang TS, Johns DR, Walker D, de la Cruz Z, Maumence IH, Green WR. Ocular clinicopathologic study of the mitochondrial encephalomyopathy overlap syndromes. Arch Ophthalmology 1993; 111(9):1254-62.
27. Demer JL, Oh SY, Poukens V. Evidence for active control of rectus extraocular muscle pulleys. Invest Ophthalmol Vis Sci 2000;41(6): 1280-90.
28. Mullerhocker J, Seibel P, Schneiderbanger K, Kadenbach B. Different insitu hybridization patterns of mitochondrial-DNA in cytochrome-c oxidase-deficient extraocular-muscle fibers in the elderly. Virchows Arch a-Pathol Anat Histopathol 1993;422(1): 7-15.
29. Mullerhocker J, Schneiderbanger K, Stefani FH, Kadenbach B. Progressive loss of cytochrome-c-oxidase in the human extraocular-muscles in aging-a cytochemical-immunohistochemical study. Mutation Res 1992;275(3-6):115-24.
30. Muller-Hocker J. Cytochrome c oxidase deficient fibres in the limb muscle and diaphragm of man without muscular disease: an age-related alteration. J Neurological Sci 1990;100(1-2):14-21.
31. Wallace DC. Mitochondrial DNA mutations in diseases of energy metabolism. J Bioenerg Biomembranes 1994;26(3):241-50.
32. Brierley EJ, Johnson MA, James OF, Turnbull DM. Effects of physical activity and age on mitochondrial function. Q J Med 1996; 89(4):251-8.
33. McLoon LK, Wirtschafter JD. Continuous myonuclear addition to single extraocular myofibers in uninjured adult rabbits. Muscle Nerve 2002;25(3):348-58.
34. McLoon LK, Wirtschafter J. Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci 2003;44(5):1927-32.
35. McLoon LK, Wirtschafter J. Activated satellite cells are present in uninjured extraocular muscles of mature mice. Trans Am Ophthalmological Soc 2002; 100:119-23 (discussion 123-124).
36. Clark KM, Bindoff LA, Lightowlers RN, et al. Reversal of a mitochondrial DNA defect in human skeletal muscle. Nature Genet 1997;16(3):222-4.
37. Blau HM, Kaplan I, Tao TW, Kriss JP. Thyroglobulin-independent, cell-mediated cytotoxicity of human eye muscle cells in tissue culture by lymphocytes of a patient with Graves' ophthalmopathy. Life Sci 1983;32(1-2):45-53.
38. Wang PW, Hiromatsu Y, Laryea E, Wosu L, How J, Wall JR. Immunologically mediated cytotoxicity against human eye muscle cells in Graves' ophthalmopathy. J Clin Endocrinology Metabolism 1986;63(2):316-22.
39. Bahn RS, Heufelder AE. Pathogenesis of Graves' ophthalmopathy. New England J Med 1993;329(20):1468-75.
40. Hufnagel TJ, Hickey WF, Cobbs WH, Jakobiec FA, Iwamoto T, Eagle RC. Immunohistochemical and ultrastructural studies on the exenterated orbital tissues of a patient with Graves' disease. Ophthalmology 1984;91(11):1411-9.
41. Tallstedt L, Norberg R. Immunohistochemical staining of normal and Graves' extraocular muscle. Invest Ophthalmol Vis Sci 1988;29(2): 175-84.
42. Newsom-Davis J, Vincent A, Willcox HN. Autoimmune disorders of the neuromuscular junction. In: Lachmann PJ, Peters DK, Rosen FS, Walport NJ, editors. Clinical aspects of immunology, 5th ed. Oxford: Blackwell Scientific Publications; 1993. p. 2091-111.
43. Horton RM, Manfredi AA, Conti-Tronconi BM. The 'embryonic' gamma subunit of the nicotinic acetylcholine receptor is expressed in adult extraocular muscle, [comment]. Neurology 1993;43(5): 983-6.
44. Kaminski HJ, Kusner LL, Block CH. Expression of acetylcholine receptor isoforms at extraocular muscle endplates. Invest Ophthalmol Vis Sci 1996;37(2):345-51.
45. Missias AC, Chu GC, Klocke BJ, Sanes JR, Merlie JP. Maturation of the acetylcholine receptor in skeletal muscle: regulation of the AChR gamma-to-epsilon switch. Dev Biol 1996;179(1):223-38.
46. Kaminski HJ, Kusner LL, Nash KV, Ruff RL. The gamma-subunit of the acetylcholine receptor is not expressed in the levator palpebrae superioris. Neurology 1995;45(3 Pt 1):516-8.
47. Gasque P, Morgan BP, Legoedec J, Chan P, Fontaine M. Human skeletal myoblasts spontaneously activate allogeneic complement but are resistant to killing. J Immunol 1996;156(9):3402-11.
48. Lang TJ, Shin ML. Activation of the alternative complement pathway and production of Factor-H by skeletal myotubes. J Neurophysiol 1993;44(2):185-92.
49. Navenot JM, Villanova M, LucasHeron B, Malandrini A, Blanchard D, Louboutin JP. Expression of CD59, a regulator of the membrane attack complex of complement, on human skeletal muscle fibers. Muscle Nerve 1997;20(1):92-6.
50. Burke RE. Motor units: anatomy, physiology, and functional organization. In: Brooks VB, editor. Handbook of physiology, section 1, the nervous system. Bethesda: American Physiological Society; 1981. p. 345-422.
51. Barmack NH. Recruitment and suprathreshold frequency modulation of single extraocular muscle fibers in the rabbit. J Neurophysiol 1977; 40(4):779-90.
52. Hanson J, Lennerstrand G. Contractile and histochemical properties of the inferior oblique muscle in the rat and in the cat. Acta Ophthalmologica 1977;55(1):88-102.
53. Gurahian SM, Goldberg SJ. Fatigue of lateral rectus and retractor bulbi motor units in cat. Brain Res 1987;415(2): 281-92.
54. Meredith MA, Goldberg SJ. Contractile differences between muscle units in the medial rectus and lateral rectus muscles in the cat. J Neurophysiol 1986;56(1):50-62.
55. Close RI, Luff AR. Dynamic properties of inferior rectus muscle of the rat. J Physiol (Lond) 1974;236:259-70.