Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-06-02T05:42:53.876Z Has data issue: false hasContentIssue false
  • English
  • Français

Myotubular Myopathy: Arrest of Morphogenesis of Myofibres Associated with Persistence of Fetal Vimentin and Desmin Four cases compared with fetal and neonatal muscle

Published online by Cambridge University Press:  18 September 2015

Harvey B. Sarnat
Harvey B. Sarnat*
Affiliation:
Departments of Pathology, Paediatrics, and Clinical Neurosciences, University of Calgary Faculty of Medicine, Calgary
*
Alberta Children's Hospital, 1820 Richmond Road S.W., Calgary, Alberta, Canada T2T 5C7
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Vastus lateralis muscle biopsies of four unrelated male neonates showing myotubular (i.e. centronuclear) myopathy (MM) were compared with muscle from four human fetuses in the myotubular stage of development, a 31 week preterm infant and four term neonates. The perimysium, blood vessels, spindles, myelinated intramuscular nerves, and motor end-plates in MM are as well developed as in term neonatal muscle. The cytoarchitecture of myofibres in MM is more mature than that of fetal myotubes in the spacing of central nuclei, Z-band registry, development of the sarcotubular system, and in the condensation of nuclear chromatin and nucleoli. Triads in MM may retain an immature oblique or longitudinal orientation. Myofibrillar ATPase shows normal differentiation of fibre types, consistent with nonnal innervation. Spinal motor neurons are nonnal in number and in RNA fluorescence. Immunoreactivity for vimentin and desmin in myofibres of MM is uniformly strong, as in fetal myotubes and unlike mature neonatal muscle. Maternal muscle biopsies of two cases also showed scattered small centronuclear myofibres reactive for vimentin and desmin. The arrest in morphogenesis of fibre architecture in MM is not a general arrest in muscle development. Persistence of fetal cytoskeletal proteins that preserve the immature central positions of nuclei and mitochondria may be important in pathogenesis. Vimentin/desmin studies of the infant and maternal muscle biopsies are useful in establishing the diagnosis.

Résumé:

RÉSUMÉ:

On a comparé des biopsies musculaires du vaste externe prélevées chez quatre nouveau-nés mâles sans lien de parenté, montrant une myopathie myotubulaire (centro-nucléaire MM), à des muscles provenant de quatre foetus humains durant l'étape myotubulaire de développement, d'un enfant prématuré âgé de 31 semaines, et de quatre nouveau-nés à terme. Le périmysium, les vaisseaux sanguins, les fuseaux musculaires, les nerfs myélinisés intramusculaires, et les jonctions neuro-musculaires sont aussi bien développés dans la MM que dans le muscle néo-natal à terme. La cyto-architecture des myofibres dans la MM a un niveau de maturité supérieur à celui des myotubes foetaux en ce qui a trait aux intervalles entre les noyaux centraux, à l'alignement des striations transversales, au développement du système sarcotubulaire, et à la condensation de la chromatine nucléaire et du nucléole. Les triades dans la MM conservent souvent l'orientation oblique ou longitudinale de l'état immature. La différenciation histochimique des myofibres selon l'ATPase myofibrillaire reste mature dans la MM, suggèrant une innervation normale. Les neurones moteurs spinaux sont normaux en nombre et à l'égard de la fluorescence pour l'ARN. L'immunoréactivité pour la vimentine et pour la desmine dans les myofibres de MM est uniformément forte, semblable aux myotubes foetaux et dissemblable au muscle mature néo-natal. Les biopsies musculaires des mères de deux cas montrèrent également des petites myofibres éparses à noyaux centraux, réactives pour la vimentine et pour la desmine. La MM représente un arrêt de la morphogenèse de l'architecture de la myofibre mais non arrêt général du développement musculaire. La pathogenèse est vraisemblablement une presévérance des protéines cytosquelettiques du foetus qui maintiennent la localisation centrale immature des noyaux et des mitochondries. Les études de la vimentine et de la desmine dans les biopsies musculaires de la mère et de l'enfant sont utiles pour établir le diagnostic.

Type
Original Articles
Information
Canadian Journal of Neurological Sciences , Volume 17 , Issue 2 , May 1990 , pp. 109 - 123
Copyright
Copyright © Canadian Neurological Sciences Federation 1990

References

REFERENCES

1. Spiro, AJ, Shy, GM, Gonatas, NK. Myotubular myopathy. Arch Neurol 1966; 14: 1–14.CrossRefGoogle ScholarPubMed
2. Kinoshita, M, Cadman, TE. Myotubular myopathy. Arch Neurol 1968; 18: 265–271.CrossRefGoogle ScholarPubMed
3. Badurska, B, Fidziańska, A, Kamieniecka, Z, et al. Myotubular myopathy. J Neurol Sci 1969; 8: 563–571.CrossRefGoogle ScholarPubMed
4. Edström, L, WrÓblewski, R, Mair, WGP. Genuine myotubular myopathy. Muscle Nerve 1982; 5: 604–613.CrossRefGoogle ScholarPubMed
5. Sarnat, HB, Roth, SI, Jimenez, JF. Neonatal myotubular myopathy: neuropathy and failure of postnatal maturation of fetal muscle. Can J Neurol Sci 1981; 8: 313–320.CrossRefGoogle ScholarPubMed
6. Sher, JH, Rimalovski, AB, Athanassiades, TJ, et al. Familial centronuclear myopathy: a clinical and pathological study. Neurology 1967; 17: 727–742.CrossRefGoogle ScholarPubMed
7. Munsat, TL, Thompson, LR, Coleman, RF. Centronuclear (“myotubular”) myopathy. Arch Neurol 1969; 20: 120–131.CrossRefGoogle ScholarPubMed
8. Ambler, MW, Neave, C, Singer, DB. X-linked recessive myotubular myopathy. II. Muscle morphology and human myogenesis. Hum Pathol 1984; 15: 1107–1120.CrossRefGoogle ScholarPubMed
9. Van Wijngaarden, GK, Fleury, P, Meijer AEFH. Familial “myotubular” myopathy. Neurology 1969; 19: 901–908.CrossRefGoogle Scholar
10. Myers, KR, Golomb, HM, Hansen, JL, et al. Familial neuromuscular disease with myotubes. Clin Genet 1974; 5: 327–337.CrossRefGoogle Scholar
11. Barth, PG, Van Wijngaarden, GK, Bethlem, J. X-linked myotubular myopathy with fatal neonatal asphyxia. Neurology 1975; 25: 531–536.CrossRefGoogle ScholarPubMed
12. Ilina, NA, Averyanov, UN, Potomskaya, LZ, et al. X-linked myotubular myopathy (in Russian). Zh Nevropathol Psikhiatr Im SS Korsakova 1979; 79: 1334–1338.Google Scholar
13. Bucher, HU, Boltshauser, E, Briner, J, et al. Severe neonatal centronuclear (myotubular) myopathy: an X-linked recessive disorder. Helv Paediatr Acta 1986; 41: 291–300.Google Scholar
14. Silver, MM, Gilbert, JJ, Stewart, S, et al. Morphologic and morphometric analysis of muscle in X-linked myotubular myopathy. Hum Pathol 1986; 17: 1167–1178.CrossRefGoogle ScholarPubMed
15. Keppen, LD, Husain, MM, Wood, RC. X-linked myotubular myopathy: intrafamilial variability and normal muscle biopsy in a heterozygous female. Clin Genet 1987; 32: 95–99.CrossRefGoogle Scholar
16. Palmucci, L, De Angelis, S, Leone, M, et al. Centronuclear myopathy: type of inheritance and clinical pattern in 268 cases. Clin Neuropathol 1988; 7: 194 (abstract).Google Scholar
17. Pépin, B, Mikol, J, Goldstein, B, et al. Forme familiale de myopathie centronuclaire de l’adulte. Rev Neurol (Paris) 1976; 132: 845–857.Google Scholar
18. Bradley, WG, Price, DL, Watanabe, CK. Familial centronuclear myopathy. J Neurol Neurosurg Psychiatry 1970; 33: 687–698.CrossRefGoogle ScholarPubMed
19. Torres, CF, Griggs, RC, Goetz, JP. Severe neonatal centronuclear myopathy with autosomal dominant inheritance. Arch Neurol 1985; 42: 1011–1014.CrossRefGoogle ScholarPubMed
20. Radu, H, Killyen, I, Ionescu, V, et al. Myotubular (centronuclear) (neuro-) myopathy. I. Clinical, genetical and morphological studies. Eur Neurol 1977; 15: 285–300.CrossRefGoogle ScholarPubMed
21. Martin, JJ, Ceuterick, J, Joris, C, et al. Myopathie centro-nucléaire. Acta Neurol Belg 1977; 77: 285’299.Google Scholar
22. Raju, TNK, Vidyasagar, D, Reyes, MG, et al. Centronuclear myopathy in the newborn period causing severe respiratory distress syndrome. Pediatrics 1977; 59: 29–34.CrossRefGoogle Scholar
23. Palmucci, L, Bertolotto, A, Monga, G, et al. Histochemical and ultrastructural findings in a case of centronuclear myopathy. Eur Neurol 1978; 17: 327–332.CrossRefGoogle Scholar
24. PeBenito, R, Sher, JH, Cracco, JB. Centronuclear myopathy: clinical and pathologic features. Clin Pediatr 1978; 17: 259–265.CrossRefGoogle ScholarPubMed
25. Larbrisseau, A, Brochu, P, Vanasse, M, et al. Les myopathies congénitales. Observation de 9 cas et revue générale. L’Union Méd Canada 1980; 109: 256–276.Google Scholar
26. Collins, JE, Collins, A, Radford, MR, et al. Perinatal diagnosis of myotubular (centronuclear) myopathy: a case report. Clin Neuropathol 1983; 2: 79–82.Google ScholarPubMed
27. Heckmatt, JZ, Sewry, CA, Hodes, D, et al. Congenital centronuclear (myotubular) myopathy. Brain 1985; 108: 941–964.CrossRefGoogle ScholarPubMed
28. Strom, EH, Tangsrud, SE. Craniopharyngioma in a boy with centronuclear (myotubular) myopathy: clinical and postmortem findings. Clin Neuropathol 1986; 5: 84–87.Google Scholar
29. Inokuchi, T, Umezaki, H, Santa, T. A case of type I muscle fibre hypotrophy and internal nuclei. J Neurol Neurosurg Psychiatry 1975; 38: 475–482.CrossRefGoogle Scholar
30. Jandro-Santel, D. Centronuclear myopathy with type I fibre hypotrophy and fingerprint inclusions associated with Marian’s syndrome. J Neurol Sci 1980; 45: 43–56.CrossRefGoogle Scholar
31.. Tomanek, RJ, Colling-Saltin, A-S. Cytological differentiation of human fetal skeletal muscle. Am J Anat 1977; 149: 227–246.CrossRefGoogle ScholarPubMed
32. Fidziańska, A. Human ontogenesis. I. Ultrastructural characteristics of developing human muscle. J Neuropathol Exp Neurol 1980; 39: 476–486.CrossRefGoogle ScholarPubMed
33. Minguetti, G, Mair, WGP. Ultrastructure of developing muscle. Biol Neonate 1981; 40: 276–294.CrossRefGoogle Scholar
34. Sarnat, HB. Ontogenesis of striated muscle. In: Polin, RA, Fox, WW, eds. Neonatal and Fetal Medicine: Physiology and Pathophysiology. Orlando, Florida: WB Saunders 1990; (in press).Google Scholar
35. Pages, M, Cesari, JB, Pages, AM. La myopathie centronucléaire. Revue complète de la littérature á propos d’un cas. Ann Pathol (Paris) 1982; 2: 301–310.Google Scholar
36. Zimmermann, P, Weber, V. Familial centronuclear myopathy: a haploid DNA disease? Acta Neuropathol 1979; 46: 209–214.CrossRefGoogle ScholarPubMed
37. Sarnat, HB. L’acridine-orange: un fluorochrome pour l’étude des cellules musculaires et nerveuses. Rev Neurol (Paris) 1985; 141: 120–127.Google Scholar
38. Kelly, DE. Myofibrillogenesis and Z-band differentiation. Anat Rec 1969; 163: 403–426.CrossRefGoogle ScholarPubMed
39. Larson, PF, Hudgson, P, Walton, JN. Morphological relationship of polyribosomes and myosin filaments in developing and regenerating skeletal muscle. Nature 1969; 222: 1168–1169.CrossRefGoogle Scholar
40. Askanas, V, Engel, WK, Reddy, NB, et al. X-linked recessive congenital muscle fiber hypotrophy with central nuclei. Abnormalities of growth and adeylate cyclase in muscle tissue cultures. Arch Neurol 1979; 36: 604–609.CrossRefGoogle ScholarPubMed
41. Edge, MB. Development of apposed sarcoplasmic reticulum at the T-system and sarcolemma and the change in orientation of triads in rat skeletal muscle. Dev Biol 1970; 23: 634–650.CrossRefGoogle ScholarPubMed
42. Walker, SM, Schrodt, GR, Currier, GJ, et al. Relationship of the sarcoplasmic reticulum to fibril and triadic junction development in skeletal muscle fibers of fetal monkeys and humans. J Morphol 1975; 146: 97–128.CrossRefGoogle Scholar
43. Tokuyasu, KT, Dutton, AH, Singer, SJ. Immunoelectron microscopic studies of desmin (skeletin) localization and intermediate filament organization in chicken skeletal muscle. J Cell Biol 1983; 96: 1727–1735.CrossRefGoogle ScholarPubMed
44. Bill, PLA, Cole, G, Proctor NSF. Centronuclear myopathy. J Neurol Neurosurg Psychiatry 1979; 42: 548–556.CrossRefGoogle Scholar
45. Hayes, VE, Hikida, RS. Naturally-occurring degeneration in chick muscle development; ultrastructure of the M. complexus. J Anat 1976; 122: 67–76.Google ScholarPubMed
46. Webb, JN. The development of human skeletal muscle with particular reference to muscle cell death. J Pathol 1972; 106: 221–229.CrossRefGoogle ScholarPubMed
47. Goulon, L, Fardeau, M, Got, C, et al. Myopathie centro-nucléaire d’expression tardive. Étude clinique, histologique et ultrastructurale. Rev Neurol (Paris) 1976; 132: 275–290.Google Scholar
48. Campbell, MJ, Rebeiz, JJ, Walton, JN. Myotubular, centronuclear or pericentronuclear myopathy? J Neurol Sci 1969; 8: 425–443.CrossRefGoogle ScholarPubMed
49. Headington, JT, McNamara, JO, Brownell, AK. Centronuclear myopathy: histochemistry and electron microscopy. Report of 2 cases. Arch Pathol 1975; 99: 16–24.Google Scholar
50. Schochet, SS, Zellweger, H, lonasescu, V, et al. Centronuclear myopathy: disease entity or a syndrome? J Neurol Sci 1972; 16: 215–228.CrossRefGoogle ScholarPubMed
51. Engel, WK, Karpati, G. Impaired skeletal muscle maturation following neonatal neurectomy. Dev Biol 1968; 17: 713–723.CrossRefGoogle ScholarPubMed
52. Pongratz, D, Heuser, M, Mittelbach, F, et al. Die sogenannte congénitale centronucleäre Myopathie — eine primare Neuropathie? Acta Neuropathol 1975; 32: 9–19.CrossRefGoogle Scholar
53. Coërs, C, Telerman-Toppet, N, Gérard, JM, et al. Changes in motor innervation and histochemical pattern of muscle fibers in some congenital myopathies. Neurology 1976; 26: 1046–1053.CrossRefGoogle ScholarPubMed
54. Sugie, H, Rasmussen, GE, Verity, MA. Adult onset type 11 fiber centronuclear neuromyopathy with segmental demyelination. Brain Dev (Tokyo) 1982; 4: 7–12.Google Scholar
55. Elder, GB, Dean, D, McComas, AJ, et al. Infantile centronuclear myopathy. Evidence suggesting incomplete innervation. J Neurol Sci 1983; 60: 79–88.CrossRefGoogle ScholarPubMed
56. Sasaki, T, Shikura, K, Sugai, K, et al. Muscle histochemistry in myotubular (centronuclear) myopathy. Brain Dev (Tokyo) 1989; 11: 26–32.Google Scholar
57. Sarnat, HB, Jacob, P, Jiménez, M. Atrophie spinale musculaire: l’évanouissement de la fluorescence á l’ARN des neurones moteurs en dégénérescence: une étude à l’acridine-orange. Rev Neurol (Paris) 1989; 145: 305–311.Google Scholar
58. Sarnat, HB. Hypoxic alterations in neonatal neurons: an acridine orange fluorochromic study of nucleic acids. Brain Dev (Tokyo) 1987; 9: 43–47.CrossRefGoogle ScholarPubMed
59. Bender, AN, Bender, MB. Muscle fiber hypotrophy with intact neuromuscular junctions. Neurology 1977; 27: 206–212.CrossRefGoogle ScholarPubMed
60. Bergen, BJ, Carry, MP, Wilson, WB, et al. Centronuclear myopathy: extraocular- and limb-muscle findings in an adult. Muscle Nerve 1980; 3: 165–171.CrossRefGoogle ScholarPubMed
61. Ringel, SP, Bender, AN, Engel, WK. Extrajunctional acetylcholine receptors. Arch Neurol 1976; 33: 751–758.CrossRefGoogle ScholarPubMed
62. Dubowitz, V. Enzymatic maturation of skeletal muscle. Nature 1963; 197: 1215.CrossRefGoogle Scholar
63. Fenichel, GM. A histochemical study of developing human skeletal muscle. Neurology 1966; 16: 741–745.CrossRefGoogle Scholar
64. Farkas-Bargeton, E, Diebler, MF, Arsénio-Nunes ML, et al. àtude de la maturation histochimique, quantitative et ultrastructurale du muscle foetal humain. J Neurol Sci 1977; 31: 245–259.CrossRefGoogle Scholar
65. Colling-Saltin, A-S. Enzyme histochemistry on skeletal muscle of the human foetus. J Neurol Sci 1978; 39: 169–185.CrossRefGoogle ScholarPubMed
66. Kumagai, T, Hakamada, S, Hara, K, et al.Development of human fetal muscles: a comparative histochemical analysis of the psoas and the quadriceps muscles. Neuropediatrics 1984; 15: 198–202.CrossRefGoogle ScholarPubMed
67. Engel, WK, Gold, GN, Karpati, G. Type I fiber hypotrophy and central nuclei. Arch Neurol 1968; 18: 435–444.CrossRefGoogle ScholarPubMed
68. Bethlem, J, Van Wijngaarden, GK, Meijer AEFH. Neuromuscular disease with type I fiber atrophy, central nuclei, and myotube-like structures. Neurology 1969; 19: 705–710.Google Scholar
69. Karpati, G, Carpenter, S, Nelson, RF. Type I fibre atrophy and central nuclei: a rare familial neuromuscular disease. J Neurol Sci 1970; 10: 489–500.CrossRefGoogle ScholarPubMed
70. Kinoshita, M, Satoyoshi, E, Matsuo, N. “Myotubular myopathy” and “type I fibre atrophy” in a family. J Neurol Sci 1975; 26: 575–582.CrossRefGoogle Scholar
71. Serratrice, G, Pellissier, JF, Faugére, MC, et al. Centronuclear myopathy: possible central nervous system origin. Muscle Nerve 1978; 1: 62–69.CrossRefGoogle ScholarPubMed
72. Bennett, GS, Fellini, SA, Toyama, Y, et al. Redistribution of intermediate filament subunits during skeletal myogenesis and maturation in vitro. J Cell Biol 1979; 82: 577–584.CrossRefGoogle ScholarPubMed
73. Gard, DL, Lazarides, E. The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell 1980; 19: 263–275.CrossRefGoogle ScholarPubMed
74. Tokuyasu, KT, Dutton, AH, Singer, SJ. Distribution of vimentin and desmin in developing chick myotubes in vivo. I. Immunofluorescence study. J Cell Biol 1984; 98: 1961–1972.CrossRefGoogle ScholarPubMed
75. Tassin, A-M, PinÇon-Raymond, M, Paulin, D, et al. Unusual organization of desmin intermediate filaments in muscular dysgenesis and TTX-treated myotubes. Dev Biol 1988; 129: 37–47.CrossRefGoogle ScholarPubMed
76. Holtzer, H, Bennett, GS, Tapscott, SJ, et al. Intermediate-size fila-ments: change in synthesis and distribution in cells of the myogenic and neurogenic lineages. Quant Biol 1982; 46: 317–329.CrossRefGoogle Scholar
77. Tokuyasu, KT, Maher, PA, Dutton, AH, et al. Intermediate filaments in skeletal and cardiac muscle tissue in embryonic and adult chicken. Ann. NY Acad Sci 1985; 455: 200–212.CrossRefGoogle ScholarPubMed
78. Tassin, A-M, Maro, B, Bornens, M. Fate of microtubule organizing centers during myogenesis in vitro. J Cell Biol 1985; 100: 35–46.CrossRefGoogle ScholarPubMed
79. Berner, PF, Frank, E, Holtzer, H, et al.The intermediate filament proteins of rabbit vascular smooth muscle: immunofluorescent studies of desmin and vimentin. J Muscle Res Cell Motil 1981; 2: 439–452.CrossRefGoogle Scholar
80. Schmid, E, Osborn, M, Rungger-Brandle, E, et al. Distribution of vimentin and desmin filaments in smooth muscle tissue of mammalian and avian aorta. Exp Cell Res 1982; 137: 329–340.CrossRefGoogle ScholarPubMed
81. Fujimoto, T, Singer, SJ. Immunocytochemical studies of desmin and vimentin in pericapillary cells of chicken. J Histochem Cytochem 1987; 35: 1105–1112.CrossRefGoogle ScholarPubMed
82. Osinska, HE, Lemanski, LF. Immunofluorescent localization of desmin and vimentin in developing cardiac muscle of Syrian hamster. Anat Rec 1989; 223: 406–413.CrossRefGoogle ScholarPubMed
83. Battifora, H. Desmin and sarcomeric myosins in the diagnosis of rhabdomyosarcoma. In: De Lei lis, RA, ed: Advances in Immunohistochemistry. New York: Raven Press 1988.Google Scholar
84. Tokuyasu, KT, Maher, SA, Singer, SJ. Distributions of vimentin and desmin in developing chick myotubes in vivo. II. Immunoelectron microscopic study. J Cell Biol 1985; 100: 1157–1166.CrossRefGoogle ScholarPubMed
85. Lewis, SA, Balcarek, JM, Krek, V, et al. Sequence of a cDNA clone encoding mouse glial fibrillary acidic protein: structural conservation of intermediate filaments. Proc Natl Acad Sci USA 1984; 81: 2743–2746.CrossRefGoogle ScholarPubMed
86. Clark, AW, Krekoski, CA, Parhad, IM, et al. Altered expression of genes for amyloid and cytoskeletal proteins in Alzheimer cortex. Ann Neurol 1989; 25: 331–339.CrossRefGoogle ScholarPubMed
87. Sarnat, HB, Silbert, SW. Maturational arrest of fetal muscle in neonatal myotonic dystrophy. A pathologic study of four cases. Arch Neurol 1976; 33: 466–474.CrossRefGoogle ScholarPubMed
88. Farkas-Bargeton, E, Barbet, JP, Dancea, S, et al. Immaturity of muscle fibres in the congenital form of myotonic dystrophy: its consequences and its origin. J Neurol Sci 1988; 83: 145–159.CrossRefGoogle Scholar
89. Sarnat, HB. Le cerveau influence-t-il le développement musculaire du foetus humain? Mise en évidence de 21 cas. Can J Neurol Sci 1985; 12: 111–120.CrossRefGoogle Scholar
90. Fardeau, M, Godet-Guillain, J, Tomé, FMS, et al. Une nouvelle affection musculaire familiale definie par l’accumulation intrasarcoplasmique d’un materiel granulofilamentaire dense en microscopie électronique. Rev Neurol (Paris) 1978; 134: 411–425.Google Scholar
91. Edström, L, Thornell, LE, Eriksson, A. A new type of hereditary distal myopathy with characteristic sarcoplasmic bodies and intermediate (skeletin) filaments. J Neurol Sci 1980; 47: 171–190.CrossRefGoogle ScholarPubMed
92. Fidziańska, A, Goebel, M, Osborn, M, et al. Mallory body-like inclusions in a hereditary congenital neuromuscular disease. Muscle Nerve 1983; 6: 195–200.CrossRefGoogle Scholar
93. Osborn, M, Goebel, HH. The cytoplasmic bodies in a congenital myopathy can be stained with antibodies to desmin, the muscle-specific intermediate filament protein. Acta Neuropathol 1983; 62: 149–152.CrossRefGoogle Scholar
94. Pellissier, JF, Pouget, J, Charpin, C, et al. Myopathy associated with desmin type intermediate filaments. An immunoelectron microscopic study. J Neurol Sci 1989; 89: 49–61.CrossRefGoogle ScholarPubMed
95. Stoeckel, M-E, Osborn, M, Porte, A, et al. An unusual familial cardiomyopathy characterized by aberrant accumulations of desmin-type intermediate filaments. Virch Arch Pathol Anat 1981; 393: 53–60.CrossRefGoogle ScholarPubMed
96. Coleman, FR, Thompson, LR, Neihuis, AW, et al. Histochemical investigation of myotubular myopathy. Arch Pathol 1968; 86: 365–375.Google Scholar
97. Thomas, NST, Sarfarazi, M, Roberts, K, et al. X-linked myotubular myopathy: evidence for linkage to Xq28 DNA markers. Cytogenet Cell Genet 1987; 46: 704 (abstract).Google Scholar
98. Darfors, C, Borje Larsson, HE, Oldfors, A, et al. X-linked myotubular myopathy. A linkage study. Cytogenet Cell Genet 1989; 51: 983 (abstract).Google Scholar
99. Quax, W, Meera Khan, P, Quax-Jeuken, Y, et al. The human desmin and vimentin genes are located on different chromosomes. Gene 1985; 38: 189–196.CrossRefGoogle ScholarPubMed
100. Ferrari, S, Cannizzaro, LA, Battini, R, et al. The gene encoding human vimentin is located on the short arm of chromosome 10. Am J Hum Genet 1987; 41: 616–626.Google ScholarPubMed
101. Viegas-Péquignot, E, Zhen Lin, L, Dutrillaux, B, et al. Assignment of human desmin gene to band 2q35 by nonradioactive in situ hybridization. Hum Genet 1989; 83: 33–36.CrossRefGoogle ScholarPubMed