The superfast extraocular myosin (MYH13) is localized to the innervation zone in both the global and orbital layers of rabbit extraocular muscle

Journal of Experimental Biology

Volumn 205, Issue 20, 2002, Pages 3133-3142

  Briggs, Margaret M ^a   Schachat, Fred ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

EOM; Extraocular; Innervafion; Muscle; Myosin; Neuromuscular junction; Rabbit

Indexed keywords

ANTIBODY; MESSENGER RNA; MYOSIN;

ANIMAL; ARTICLE; CHEMISTRY; CHICKEN; ELECTROMYOGRAPHY; EXTRAOCULAR MUSCLE; EYE; EYE MOVEMENT; FEMALE; GENETICS; IMMUNOLOGY; INNERVATION; MUSCLE CELL; MUSCLE CONTRACTION; NEUROMUSCULAR SYNAPSE; ORBIT; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREGNANCY; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARCOPLASMIC RETICULUM; ULTRASTRUCTURE;

ANIMALS; ANTIBODIES; CHICKENS; ELECTROMYOGRAPHY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EYE; EYE MOVEMENTS; FEMALE; MUSCLE CONTRACTION; MUSCLE FIBERS; MYOSINS; NEUROMUSCULAR JUNCTION; OCULOMOTOR MUSCLES; ORBIT; PREGNANCY; RABBITS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SARCOPLASMIC RETICULUM;

ANIMALIA; GALLUS GALLUS; MAMMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0036033571     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Akita, E. M. and Nakai, S. (1993). Comparison of four purification methods for the production of immunoglobulins from eggs laid by hens immunized with an enterotoxigenic E. coli strain. J. Immunol. Methods 160, 207-214.
2. Barmack, N. H. (1977). Recruitment and suprathreshold frequency modulation of single extraocular muscle fibers in the rabbit. J. Neurophysiol. 40, 779-790.
3. Blank, J. M. and Schachat, F. (1999). Extraocular and laryngeal muscles exhibit differential amplification of proteins involved in calcium homeostasis. Mol. Biol. Cell 10, 246a.
4. Briggs, M. and Schachat, F. (2000). Early specialization of the superfast myosin in extraocular and laryngeal muscles. J. Exp. Biol. 203, 2485-2494.
5. Briggs, M. M., Jacoby, J., Davidowitz, J. and Schachat, F. H. (1988). Expression of a novel combination of fast and slow troponin T isoforms in rabbit extraocular muscles. J. Mus. Res. Cell Motil. 9, 241-247.
6. Briggs, M. M., Lin, J. J. C. and Schachat, F. H. (1987). The extent of amino-terminal heterogeneity in rabbit fast skeletal muscle troponin T. J. Mus. Res. Cell Motil. 8, 1-12.
7. Briggs, M. M., McGinnis, H. D. and Schachat, F. (1990). Transitions from fetal to fast troponin T isoforms are coordinated with changes in tropomyosin and α-actinin isoforms in developing rabbit skeletal muscle. Dev. Biol. 140, 253-260.
8. Brueckner, J. K., Itkis, O. and Porter, J. D. (1996). Spatial and temporal patterns of myosin heavy chain expression in developing rat extraocular muscle. J. Mus. Res. Cell Motil. 17, 297-312.
9. Brueckner, J. K. and Porter, J. D. (1998). Visual system maldevelopment disrupts extraocular muscle-specific myosin expression. J. Appl. Physiol. 85, 584-592.
10. Cheng, G. and Porter, J. D. (2002). Transcriptional profile of rat extraocular muscle by serial analysis of gene expression. Invest. Ophthalmol. Vis. Sci. 43, 1048-1058.
11. Chiarandini, D. J. and Davidowitz, J. (1979). Structure and function of extraocular muscle fibers. In Current Topics in Eye Research, vol. 1 (ed. J. A. Zadunaisky and H. Davson), pp. 91-142. New York: Academic Press.
12. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol chloroform extraction. Anal. Biochem. 162, 156-159.
13. Close, R. L. and Luff, A. R. (1974). Dynamic properties of inferior rectus muscle of the rat. J. Physiol. 236, 259-270
14. Cooper, S. and Eccles, J. (1930). The isometric responses of mammalian muscles. J. Physiol. 69, 377-385.
15. Cuda, G., Pate, E., Cooke, R. and Sellers, J. R. (1997). In vitro actin filament sliding velocities produced by mixtures of different types of myosin. Biophys. J. 72, 1767-1779.
16. d'Albis, A., Couteaux, R., Janmot, C. and Roulet, A. (1989). Specific programs of myosin expression in the postnatal development of rat muscles. Eur. J. Biochem. 183, 583-590.
17. Davidowitz, J., Philips, G. and Breinin, G. M. (1977). Organization of the orbital surface layer in rabbit superior rectus. Invest. Ophthalmol. Vis. Sci. 16, 711-729.
18. Davidowitz, J., Rubinson, K., Jacoby, J. and Onejeme, A. (1996). Myofibril size variation along the length of extraocular muscle in rabbit and rat. II: Global layer. Tissue Cell 28, 77-87.
19. Davidowitz, J., Rubinson, K. and Onejeme, A. (2000). Location along the muscle's length is a determinant of myofibril size. Tissue Cell 32, 336-350.
20. Dean, P. (1996). Motor unit recruitment in a distributed model of extraocular muscle. J. Neurophysiol. 76, 727-742.
21. DelGaudio, J. M., Sciote, J. J., Carroll, W. R. and Escalmado, R. M. (1995). Atypical myosin heavy chain in rat laryngeal muscle. Ann. Otol. Rhinol. Laryngol. 104, 237-245.
22. Demer, J. L. (2002). The orbital pulley system: A revolution in concepts of orbital anatomy. Ann. NY Acad. Sci. 956, 17-32.
23. Demer, J. L., Miller, J. M., Poukens, V., Vinters, H. V. and Glasgow, B. J. (1995). Evidence for fibromuscular pulleys of the recti extraocular muscles. Invest. Ophthalmol. Vis. Sci. 36, 1125-1136.
24. Fischer, M. D., Gorospe, J. R., Felder, E., Bogdanovich, S., Pedrosa-Domellof, F., Ahima, R. S., Rubinstein, N. A., Hoffman, E. P. and Khurana, T. S. (2002). Expression profiling reveals metabolic and structural components of extraocular muscles. Physiol. Genomics 9, 71-84.
25. Fuchs, A. F., Kaneko, C. R. S. and Scudder, C. A. (1985). Brainstem control of saccadic eye movements Ann. Rev. Neurosci. 8, 307-337.
26. Gurahian, S. M. and Goldberg, S. J. (1987). Fatigue of lateral rectus and retractor bulbi motor units in cat. Brain Res. 415, 281-292.
27. Hamalainen, N. and Pette, D. (1997). Expression of an alpha-cardiac like myosin heavy chain in diaphragm, chronically stimulated, and denervated fast-twitch muscles of rabbit. J. Mus. Res. Cell Motil. 18, 401-411.
28. Jacoby, J., Chiarandini, D. J. and Stefani, E. (1989). Electrical properties and innervation of fibers in the orbital layer of rat extraocular muscles. J. Neurophysiol. 61, 116-125.
29. Jacoby, J., Ko, K., Weiss, C. and Rushbrook, J. I. (1990). Systematic variation in myosin expression along extraocular muscle fibers of the adult rat. J. Mus. Res. Cell Motil. 11, 2540.
30. Janmot, C. and d'Albis, A. (1994). Electrophoretic separation of developmental and adult rabbit skeletal muscle myosin heavy chain isoforms: Example of application to muscle denervation study. FEBS Lett. 353, 13-15.
31. Khanna, S. and Porter, J. D. (2001). Evidence for rectus extraocular muscle pulleys in rodents. Invest. Ophthahnol. Vis. Sci. 42, 1986-1992.
32. Kranjc, B. S., Sketelj, J., d'Albis, A., Ambroz, M. and Erzen, I. (2000). Fibre types and myosin heavy chain expression in the ocular medial rectus muscle of the adult rat. J. Mus. Res. Cell Motil. 21, 753-761.
33. Kranjc, B. S., Sketelj, J., d'Albis, A. and Erzen, I. (2001). Long-term changes in myosin heavy chain composition after botulinum toxin a injection into rat medial rectus muscle. Invest. Ophthalmol. Vis. Sci. 42, 3158-3164.
34. Li, Z. B., Rossmanith, G. H. and Hoh, J. F. (2000). Cross-bridge kinetics of rabbit single extraocular and limb muscle fibers. Invest. Ophthalmol. Vis. Sci. 41, 3770-3774.
35. Lucas, C. A., Rughani, A. and Hoh, J. F. (1995). Expression of extraocular myosin heavy chain in rabbit laryngeal muscle. J. Mus. Res. Cell Motil. 16, 368-378.
36. McKoy, G., Leger, M. E., Bacou, F. and Goldspink, G. (1998). Differential expression of myosin heavy chain mRNA and protein isoforms in four functionally diverse rabbit skeletal muscles during pre- and postnatal development. Dev. Dyn. 211, 193-203.
37. McLoon, L. K., Rios, L. and Wirtschafter, J. D. (1999). Complex three-dimensional patterns of myosin isoform expression: Differences between and within specific extraocular muscles. J. Mus. Res. Cell Motil. 20, 771-783.
38. McNally, E., Sohn, R., Frankel, S. and Leinwand, L. (1991). Expression of myosin and actin in Escherichia coli. Methods Enzymol. 196, 368-389.
39. Merati, A. L., Bodine, S. C., Bennett, T., Jung, H. H., Furuta, H. and Ryan, A. F. (1996). Identification of a novel myosin heavy chain gene expressed in the rat larynx. Biochim. Biophys. Acta 1306, 153-159.
40. Pierobon-Bormioli, S., Torresan, P., Sartore, S., Moschini, G. B. and Schiaffino, S. (1979). Immunohistochemical identification of slow-tonic fibers in human extrinsic eye muscles. Invest. Ophthalmol. Vis. Sci. 18, 303-306.
41. Porter, J. D., Khanna, S., Kaminski, H. J., Rao, J. S., Merriam, A. P., Richmonds, C. R., Leahy, P., Li, J. and Andrade, F. H. (2001). Extraocular muscle is defined by a fundamentally distinct gene expression profile. Proc. Natl. Acad. Sci. USA 98, 12062-12067.
42. Reiser, P. J., Moss, R. L., Giulian, G. G. and Greaser, M. L. (1985). Shortening velocity in single fibers from adult rabbit soleus muscles is correlated with myosin heavy chain composition. J. Biol. Chem. 260, 9077-9080.
43. Rosser, B. W., Farrar, C. M., Crellin, N. K., Andersen, L. B. and Bandman, E. (2000). Repression of myosin isoforms in developing and denervated skeletal muscle fibers originates near motor endplates. Dev. Dyn. 217, 50-61.
44. Rubinstein, N. A. and Hoh, J. F. (2000). The distribution of myosin heavy chain isoforms among rat extraocular muscle fiber types. Invest. Ophthalmol. Vis. Sci. 41, 3391-3398.
45. Rushbrook, J. I., Weiss, C., Ko, K., Feurman, M. H., Carleton, S., Ing, A. and Jacoby, J. (1994). Identification of alpha-cardiac myosin heavy chain mRNA and protein in extraocular muscle of the adult rabbit. J. Mus. Res. Cell Motil. 15, 505-515.
46. Sartore, S., Mascarello, F., Rowlerson, A., Gorza, L., Ausoni, S., Vianello, M. and Schiaffino, S. (1987). Fibre types in extraocular muscles: A new myosin isoform in the fast fibres. J. Mus. Res. Cell Motil. 8, 161-172.
47. Schachat, F. and Briggs, M. (2002). Phylogenetic implications of the superfast myosin in extraocular muscles. J. Exp. Biol. 205, 2189-2201.
48. Schachat, F., Williams, R. S. and Schnurr, C. A. (1988). Coordinate changes in fast thin filament and Z-line protein expression in the early response to chronic stimulation. J. Biol. Chem. 263, 13975-13978.
49. Schachat, F. H., Bronson, D. D. and McDonald, O. B. (1985a). Heterogeneity of contractile proteins: A continuum of troponin-tropomyosin expression in mammalian skeletal muscle. J. Biol. Chem. 260, 1108-1113.
50. Schachat, F. H., Canine, A. C., Briggs, M. M. and Reedy, M. C. (1985b). The presence of two skeletal muscle alpha-actinins correlates with troponin-tropomyosin expression and Z-line width. J. Cell Biol. 101, 1001-1008.
51. Schachat, F. H., Diamond, M. S. and Brandt, P. W. (1987). The effect of different troponin T-tropomyosin combinations on thin filament activation. J. Mol. Biol. 198, 551-554.
52. Scott, A. B. and Collins, C. C. (1973). Division of labor in human extraocular muscle. Arch. Ophthalmol. 90, 319-322.
53. Shall, M. S. and Goldberg, S. J. (1992). Extraocular motor units: Type classification and motoneuron stimulation frequency-muscle unit force relationships. Brain Res. 587, 291-300.
54. Shall, M. S. and Goldberg, S. J. (1995). Lateral rectus EMG and contractile responses elicited by cat abducens motoneurons. Muscle Nerve 18, 948-955.
55. Spencer, R. F. and Porter, J. D. (1988). Structural organization of the extraocular muscles. In Neuroanatomy of the Oculomotor System (ed. J. A. Buttner-Ennever), pp. 33-79. Amsterdam: Elsevier Science.
56. Talmadge, R. J. and Roy, R. R. (1993). Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol. 75, 2337-2340.
57. Wasicky, R., Ziya-Ghazvini, F., Blumer, R., Lukas, J. R. and Mayr, R. (2000). Muscle fiber types of human extraocular muscles: A histochemical and immunohistochemical study. Invest. Ophthalmol. Vis. Sci. 41, 980-990.
58. Weiss, A., McDonough, D., Wertman, B., Acakpo-Satchivi, L., Montgomery, K., Kucherlapati, R., Leinwand, L. and Krauter, K. (1999). Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proc. Natl. Acad. Sci. USA 96, 2958-2963.
59. Wieczorek, D. F., Periasamy, M., Butler-Browne, G., Whalen, R. G. and 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.
60. Winters, L. M., Briggs, M. M. and Schachat, F. (1998). The human extraocular muscle myosin heavy chain gene (MYH13) maps to the cluster of fast and developmental myosin genes on chromosome 17. Genomics 54, 188-189.