Dystrophin and its isoforms in a sympathetic ganglion of normal and dystrophic mdx mice: Immunolocalization by electron microscopy and biochemical characterization

Neuroscience

Volumn 80, Issue 2, 1997, Pages 613-624

  De Stefano, M E ^a   Zaccaria, M L ^a   Cavaldesi, M ^b   Petrucci, T C ^b   Medori, R ^c   Paggi, P ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c Lilly Deutschland ^*  (Germany)

Author keywords

Cytoskeleton; Dystrophin; Dystrophin isoforms; Immunoelectron microscopy; mdx mouse; Mouse superior cervical ganglion

Indexed keywords

DYSTROPHIN; ISOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOELECTRON MICROSCOPY; MOUSE; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SUPERIOR CERVICAL GANGLION; SYMPATHETIC GANGLION;

ANIMALS; DYSTROPHIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GANGLIA, SYMPATHETIC; IMMUNOBLOTTING; ISOMERISM; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICROSCOPY, ELECTRON; MOLECULAR WEIGHT; MUSCULAR DYSTROPHY, ANIMAL; SUPERIOR CERVICAL GANGLION;

EID: 0030764004     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00003-1     Document Type: Article

References (44)

1. Beck K. A., Buchanan J. A., Malhotra V. and Nelson W. J. (1995) Golgi spectrin: identification of an erythroid β-spectrin homolog associated with the Golgi. J. Cell Biol. 127, 707-723.
2. Bennett V. (1990) Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Physiol. Rev. 70, 1029-1065.
3. Bonilla E., Samitt C. E., Miranda A. F., Hays A. P., Salviati G., DiMauro S., Kunkel L. M., Hoffman E. P. and Rowland L. P. (1988) Duchenne muscular dystrophy: deficiency of dystrophin at the muscle cell surface. Cell 54, 447-452.
4. Bradford M. M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein. Analyt. Biochem. 72, 248-254.
5. Byers T. J., Kunkel L. M. and Watkins S. C. (1991) The subcellular distribution of dystrophin in mouse skeletal, cardiac, and smooth muscle. J. Cell Biol. 115, 411-421.
6. Byers T. J., Lidov H. G. W. and Kunkel L. M. (1993) An alternative dystrophin transcript specific to peripheral nerve. Nat. Genet. 4, 77-81.
7. Chelly J., Hamard G., Koulakoff A., Kaplan J.-C., Kahn A. and Berwald-Netter Y. (1990) Dystrophin gene transcribed from different promoters in neuronal and glial cells. Nature 344, 64-65.
8. G119) in the kidney and muscle that binds βIΣ* spectrin and associates with the Golgi apparatus. J. Cell Biol. 133, 819-830.
9. Dickson G., Azad A., Morris G. E., Simon H., Noursadeghi M. and Walsh F. S. (1992) Colocalization and molecular association of dystrophin with laminin at the surface of mouse and human myotubes. J. Cell Sci. 103, 1223-1233.
10. D'Souza V. N., thi Man N., Morris G. E., Karges W., Pillers D. A. M. and Ray P. N. (1995) A novel dystrophin isoform is required for normal retinal electrophysiology. Hum. molec. Genet. 4, 837-842.
11. Ervasti G. M. and Campbell K. P. (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66, 1121-1131.
12. Fabbrizio E., Latouche J., Rivier F., Hugon G. and Mornet D. (1995) Re-evaluation of the distribution of dystrophin and utrophin in sciatic nerve. Biochem. J. 312, 309-314.
13. Feener C. A., Koenig M. and Kunkel L. M. (1989) Alternative splicing of human dystrophin mRNA generates isoforms at the carboxy terminus. Nature 338, 509-511.
14. Hoffman E. P., Brown H., Brown J. R. and Kunkel L. M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928.
15. Jasmin B. J., Cartaud A., Ludosky M. A., Changeux J. P. and Cartaud J. (1990) Asymmetric distribution of dystrophin in developing and adult Torpedo marmorata electrocyte: evidence for its association with the acetylcholine receptor-rich membrane. Proc. natn. Acad. Sci. U.S.A. 87, 3938-3941.
16. Kamakura K., Tadano Y., Kawai M., Ishiura S., Nakamura R., Miyamoto K., Nagata N. and Sugita H. (1994) Dystrophin-related protein is found in the central nervous system of mice at various developmental stages, especially at the postsynaptic membrane. J. Neurosci. Res. 37, 728-734.
17. Kim T. W., Wu K. and Black I. B. (1995) Deficiency of brain synaptic dystrophin in human Duchenne muscular dystrophy. Ann. Neurol. 38, 446-449.
18. Kim T. W., Wu K., Xu J. L. and Black I. B. (1992) Detection of dystrophin in the postsynaptic density of rat brain and deficiency in a mouse model of Duchenne muscular dystrophy. Proc. natn. Acad. Sci. U.S.A. 89, 11642-11644.
19. Koenig M., Monaco A. P. and Kunkel L. M. (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53, 219-228.
20. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
21. Lederfein D., Levy Z., Augier N., Mornet D., Morris G., Fuchs O., Yaffe D. and Nudel U. (1992) A 71 kd protein is a major product.of the Duchenne muscular dystrophy gene in brain and other non muscle tissue. Proc. natn. Acad. Sci. U.S.A. 89, 5346-5350.
22. Lenk U., Oexle K., Voit T., Ancker U., Hellner K.-A., Speer A. and Hubner C. (1996) A cysteine 3340 substitution in the dystroglycan-binding domain of dystrophin associated with Duchenne muscular dystrophy, mental retardation and absence of the ERG b-wave. Hum. molec. Genet. 5, 973-975.
23. Lidov H. G. W., Byers T. J. and Kunkel L. M. (1993) The distribution of dystrophin in the murine central nervous system: an immunocytochemical study. Neuroscience 54, 167-187.
24. Lidov H. G. W., Byers T. J., Watkins S. C. and Kunkel L. M. (1990) Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nature 348, 725-728.
25. Lidov H. G. W., Selig S. and Kunkel L. M. (1995) Dp140: a novel 140 kDa CNS transcript from the dystrophin locus. Hum. molec. Genet. 4, 329-335.
26. Luna E. J. and Hitt A. L. (1992) Cytoskeleton-plasma membrane interactions. Science 258, 955-963.
27. Matthews M. R. (1983) The ultrastructure of junctions in sympathetic ganglia of mammals. In Autonomic Ganglia (ed. Elfvin L. G.), pp. 27-66. Wiley, New York.
28. Miranda A. F., Bonilla E., Mastucci G., Moraes C. T., Hays A. P. and DiMauro S. (1988) Immunocytochemical study of dystrophin in muscle from patients with Duchenne muscular dystrophy and unaffected control patients. Am. J. Path. 132, 410-416.
29. Mokri B. and Engel A. G. (1975) Duchenne dystrophy: electron microscopic findings pointing to a basic or early abnormality in the plasma membrane of the muscle fiber. Neurology 25, 1111-1120.
30. Montanaro F., Carbonetto S., Campbell K. P. and Lindenbaum M. (1995) Dystroglycan expression in the wild type and mdx mouse neural retina: synaptic colocalization with dystrophin, dystrophin-related protein but not laminin. J. Neurosci. 42, 528-538.
31. Nudel U., Zuk D., Einat P., Zeelon E., Levy Z., Neuman S. and Yaffe D. (1989) Duchenne muscular dystrophy gene product is not identical in muscle and brain. Nature 337, 76-78.
32. Petrucci T. C., lacovacci G. and Ceccarini M. (1994) Segregation of dystrophin and β-spectrin isoform at the postsynaptic densities in murine brain. Bas. appl. Myol. 4, 239-246.
33. Phillips W. D., Noakes P. G., Roberds S. L., Campbell P. K. and Merlie J. P. (1993) Clustering and immobilization of acetylcholine receptors by the 43-kD protein: a possible role for dystrophin-related protein. J. Cell Biol. 123, 729-740.
34. Porter G. A., Dmytrenko G. M., Winkelmann J. C. and Bloch R. J. (1992) Dystrophin colocalizes with β-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J. Cell Biol. 117, 997-1005.
35. Rafael J. A., Cox G. A., Corrado K., Jung D., Campbell K. P. and Chamberlain J. S. (1996) Forced expression of dystrophin deletion constructs reveals structure-function correlations. J. Cell Biol. 134, 93-102.
36. Sharp A. H., Imagawa T., Leung A. T. and Campbell K. P. (1987) Identification and characterization of the dihydropyridine-binding subunits of the skeletal muscle dihydropyridine receptor. J. biol. Chem. 262, 12309-12315.
37. Sherrat T. G., Vulliamy T., Dubowitz V., Sewry C. A. and Strong P. N. (1993) Exon skipping and translation in patients with frameshift deletion in the dystrophin gene. Am. J. Hum. Genet. 53, 1007-1015.
38. Sherrat T. G., Vulliamy T. and Strong P. (1992) Evolutionary conservation of the dystrophin central rod domain. Biochem. J. 287, 755-759.
39. Sicinski O., Geng Y., Ryder-Cook A. S., Barnard E. A., Darlison M. G. and Barnard P. J. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244, 1578-1580.
40. Suzuki A., Yoshida M., Yamamoto H. and Ozawa E. (1992) Glycoprotein binding site of dystrophin is confined to the cysteine-rich domain and the first half of the carboxy-terminal domain. Fedn Eur. biochem. Socs Lett. 308, 154-160.
41. Towbin M., Staehelin T. and Gordon J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc. natn. Acad. Sci. U.S.A. 76, 4350-4354.
42. Uchino M., Teramoto H., Naoe H., Miike T., Yoshioka K. and Ando M. (1994) Dystrophin and dystrophin-related protein in the central nervous system of normal controls and Duchenne muscular dystrophy. Acta neuropath. 87, 129-134.
43. Uchino M., Teramoto H., Naoe H., Yoshioka K., Miike T. and Ando M. (1994) Localisation and characterisation of dystrophin in the central nervous system of controls and patients with Duchenne muscular dystrophy. J. Neurol. Neurosurg. Psychiat. 57, 426-429.
44. Yokota R. and Yamauchi A. (1974) Ultrastructure of the mouse superior cervical ganglion, with particular reference to the pre-and postganglionic elements covering the soma of its principal neurons. Am. J. Anat. 140, 281-298.