Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1996 Sep 1;134(5):1255–1270. doi: 10.1083/jcb.134.5.1255

Disruption of muscle architecture and myocardial degeneration in mice lacking desmin

PMCID: PMC2120972  PMID: 8794866

Abstract

Desmin, the muscle specific intermediate filament (IF) protein encoded by a single gene, is expressed in all muscle tissues. In mature striated muscle, desmin IFs surround the Z-discs, interlink them together and integrate the contractile apparatus with the sarcolemma and the nucleus. To investigate the function of desmin in all three muscle types in vivo, we generated desmin null mice through homologous recombination. Surprisingly, desmin null mice are viable and fertile. However, these mice demonstrated a multisystem disorder involving cardiac, skeletal, and smooth muscle. Histological and electron microscopic analysis in both heart and skeletal muscle tissues revealed severe disruption of muscle architecture and degeneration. Structural abnormalities included loss of lateral alignment of myofibrils and abnormal mitochondrial organization. The consequences of these abnormalities were most severe in the heart, which exhibited progressive degeneration and necrosis of the myocardium accompanied by extensive calcification. Abnormalities of smooth muscle included hypoplasia and degeneration. The present data demonstrate the essential role of desmin in the maintenance of myofibril, myofiber, and whole muscle tissue structural and functional integrity, and show that the absence of desmin leads to muscle degeneration.

Full Text

The Full Text of this article is available as a PDF (12.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen R. E., Rankin L. L., Greene E. A., Boxhorn L. K., Johnson S. E., Taylor R. G., Pierce P. R. Desmin is present in proliferating rat muscle satellite cells but not in bovine muscle satellite cells. J Cell Physiol. 1991 Dec;149(3):525–535. doi: 10.1002/jcp.1041490323. [DOI] [PubMed] [Google Scholar]
  2. Ariza A., Coll J., Fernández-Figueras M. T., López M. D., Mate J. L., García O., Fernández-Vasalo A., Navas-Palacios J. J. Desmin myopathy: a multisystem disorder involving skeletal, cardiac, and smooth muscle. Hum Pathol. 1995 Sep;26(9):1032–1037. doi: 10.1016/0046-8177(95)90095-0. [DOI] [PubMed] [Google Scholar]
  3. Arnold H. H., Braun T. The role of Myf-5 in somitogenesis and the development of skeletal muscles in vertebrates. J Cell Sci. 1993 Apr;104(Pt 4):957–960. doi: 10.1242/jcs.104.4.957. [DOI] [PubMed] [Google Scholar]
  4. Becker B., Bellin R. M., Sernett S. W., Huiatt T. W., Robson R. M. Synemin contains the rod domain of intermediate filaments. Biochem Biophys Res Commun. 1995 Aug 24;213(3):796–802. doi: 10.1006/bbrc.1995.2200. [DOI] [PubMed] [Google Scholar]
  5. Bennett G. S., Fellini S. A., Toyama Y., Holtzer H. Redistribution of intermediate filament subunits during skeletal myogenesis and maturation in vitro. J Cell Biol. 1979 Aug;82(2):577–584. doi: 10.1083/jcb.82.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bonifas J. M., Rothman A. L., Epstein E. H., Jr Epidermolysis bullosa simplex: evidence in two families for keratin gene abnormalities. Science. 1991 Nov 22;254(5035):1202–1205. doi: 10.1126/science.1720261. [DOI] [PubMed] [Google Scholar]
  7. Capetanaki Y. G., Ngai J., Lazarides E. Characterization and regulation in the expression of a gene coding for the intermediate filament protein desmin. Proc Natl Acad Sci U S A. 1984 Nov;81(22):6909–6913. doi: 10.1073/pnas.81.22.6909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Capetanaki Y., Smith S., Heath J. P. Overexpression of the vimentin gene in transgenic mice inhibits normal lens cell differentiation. J Cell Biol. 1989 Oct;109(4 Pt 1):1653–1664. doi: 10.1083/jcb.109.4.1653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cary R. B., Klymkowsky M. W. Disruption of intermediate filament organization leads to structural defects at the intersomite junction in Xenopus myotomal muscle. Development. 1995 Apr;121(4):1041–1052. doi: 10.1242/dev.121.4.1041. [DOI] [PubMed] [Google Scholar]
  10. Chan Y. M., Yu Q. C., LeBlanc-Straceski J., Christiano A., Pulkkinen L., Kucherlapati R. S., Uitto J., Fuchs E. Mutations in the non-helical linker segment L1-2 of keratin 5 in patients with Weber-Cockayne epidermolysis bullosa simplex. J Cell Sci. 1994 Apr;107(Pt 4):765–774. doi: 10.1242/jcs.107.4.765. [DOI] [PubMed] [Google Scholar]
  11. Cheng J., Syder A. J., Yu Q. C., Letai A., Paller A. S., Fuchs E. The genetic basis of epidermolytic hyperkeratosis: a disorder of differentiation-specific epidermal keratin genes. Cell. 1992 Sep 4;70(5):811–819. doi: 10.1016/0092-8674(92)90314-3. [DOI] [PubMed] [Google Scholar]
  12. Chipev C. C., Korge B. P., Markova N., Bale S. J., DiGiovanna J. J., Compton J. G., Steinert P. M. A leucine----proline mutation in the H1 subdomain of keratin 1 causes epidermolytic hyperkeratosis. Cell. 1992 Sep 4;70(5):821–828. doi: 10.1016/0092-8674(92)90315-4. [DOI] [PubMed] [Google Scholar]
  13. Choi J., Costa M. L., Mermelstein C. S., Chagas C., Holtzer S., Holtzer H. MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7988–7992. doi: 10.1073/pnas.87.20.7988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Collard J. F., Côté F., Julien J. P. Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature. 1995 May 4;375(6526):61–64. doi: 10.1038/375061a0. [DOI] [PubMed] [Google Scholar]
  15. Colucci-Guyon E., Portier M. M., Dunia I., Paulin D., Pournin S., Babinet C. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell. 1994 Nov 18;79(4):679–694. doi: 10.1016/0092-8674(94)90553-3. [DOI] [PubMed] [Google Scholar]
  16. Coulombe P. A., Hutton M. E., Letai A., Hebert A., Paller A. S., Fuchs E. Point mutations in human keratin 14 genes of epidermolysis bullosa simplex patients: genetic and functional analyses. Cell. 1991 Sep 20;66(6):1301–1311. doi: 10.1016/0092-8674(91)90051-y. [DOI] [PubMed] [Google Scholar]
  17. Coulombe P. A., Hutton M. E., Vassar R., Fuchs E. A function for keratins and a common thread among different types of epidermolysis bullosa simplex diseases. J Cell Biol. 1991 Dec;115(6):1661–1674. doi: 10.1083/jcb.115.6.1661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Côté F., Collard J. F., Julien J. P. Progressive neuronopathy in transgenic mice expressing the human neurofilament heavy gene: a mouse model of amyotrophic lateral sclerosis. Cell. 1993 Apr 9;73(1):35–46. doi: 10.1016/0092-8674(93)90158-m. [DOI] [PubMed] [Google Scholar]
  19. Danto S. I., Fischman D. A. Immunocytochemical analysis of intermediate filaments in embryonic heart cells with monoclonal antibodies to desmin. J Cell Biol. 1984 Jun;98(6):2179–2191. doi: 10.1083/jcb.98.6.2179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Evans R. M. Intermediate filaments and lipoprotein cholesterol. Trends Cell Biol. 1994 May;4(5):149–151. doi: 10.1016/0962-8924(94)90189-9. [DOI] [PubMed] [Google Scholar]
  21. Forgacs G. On the possible role of cytoskeletal filamentous networks in intracellular signaling: an approach based on percolation. J Cell Sci. 1995 Jun;108(Pt 6):2131–2143. doi: 10.1242/jcs.108.6.2131. [DOI] [PubMed] [Google Scholar]
  22. Fuchs E. Intermediate filaments and disease: mutations that cripple cell strength. J Cell Biol. 1994 May;125(3):511–516. doi: 10.1083/jcb.125.3.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fuchs E., Weber K. Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem. 1994;63:345–382. doi: 10.1146/annurev.bi.63.070194.002021. [DOI] [PubMed] [Google Scholar]
  24. Gard D. L., Lazarides E. The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell. 1980 Jan;19(1):263–275. doi: 10.1016/0092-8674(80)90408-0. [DOI] [PubMed] [Google Scholar]
  25. Georgatos S. D., Maison C. Integration of intermediate filaments into cellular organelles. Int Rev Cytol. 1996;164:91–138. doi: 10.1016/s0074-7696(08)62385-2. [DOI] [PubMed] [Google Scholar]
  26. Goebel H. H., Bornemann A. Desmin pathology in neuromuscular diseases. Virchows Arch B Cell Pathol Incl Mol Pathol. 1993;64(3):127–135. doi: 10.1007/BF02915105. [DOI] [PubMed] [Google Scholar]
  27. Granger B. L., Lazarides E. Desmin and vimentin coexist at the periphery of the myofibril Z disc. Cell. 1979 Dec;18(4):1053–1063. doi: 10.1016/0092-8674(79)90218-6. [DOI] [PubMed] [Google Scholar]
  28. Granger B. L., Lazarides E. Synemin: a new high molecular weight protein associated with desmin and vimentin filaments in muscle. Cell. 1980 Dec;22(3):727–738. doi: 10.1016/0092-8674(80)90549-8. [DOI] [PubMed] [Google Scholar]
  29. Granger B. L., Lazarides E. The existence of an insoluble Z disc scaffold in chicken skeletal muscle. Cell. 1978 Dec;15(4):1253–1268. doi: 10.1016/0092-8674(78)90051-x. [DOI] [PubMed] [Google Scholar]
  30. Grounds M. D., Yablonka-Reuveni Z. Molecular and cell biology of skeletal muscle regeneration. Mol Cell Biol Hum Dis Ser. 1993;3:210–256. doi: 10.1007/978-94-011-1528-5_9. [DOI] [PubMed] [Google Scholar]
  31. Guo L., Degenstein L., Dowling J., Yu Q. C., Wollmann R., Perman B., Fuchs E. Gene targeting of BPAG1: abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell. 1995 Apr 21;81(2):233–243. doi: 10.1016/0092-8674(95)90333-x. [DOI] [PubMed] [Google Scholar]
  32. Herrmann H., Fouquet B., Franke W. W. Expression of intermediate filament proteins during development of Xenopus laevis. II. Identification and molecular characterization of desmin. Development. 1989 Feb;105(2):299–307. doi: 10.1242/dev.105.2.299. [DOI] [PubMed] [Google Scholar]
  33. Hill C. S., Duran S., Lin Z. X., Weber K., Holtzer H. Titin and myosin, but not desmin, are linked during myofibrillogenesis in postmitotic mononucleated myoblasts. J Cell Biol. 1986 Dec;103(6 Pt 1):2185–2196. doi: 10.1083/jcb.103.6.2185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Holtzer H., Bennett G. S., Tapscott S. J., Croop J. M., Toyama Y. Intermediate-size filaments: changes in synthesis and distribution in cells of the myogenic and neurogenic lineages. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):317–329. doi: 10.1101/sqb.1982.046.01.033. [DOI] [PubMed] [Google Scholar]
  35. Horowitz S. H., Schmalbruch H. Autosomal dominant distal myopathy with desmin storage: a clinicopathologic and electrophysiologic study of a large kinship. Muscle Nerve. 1994 Feb;17(2):151–160. doi: 10.1002/mus.880170204. [DOI] [PubMed] [Google Scholar]
  36. Ingber D. E. The riddle of morphogenesis: a question of solution chemistry or molecular cell engineering? Cell. 1993 Dec 31;75(7):1249–1252. doi: 10.1016/0092-8674(93)90612-t. [DOI] [PubMed] [Google Scholar]
  37. Ishikawa H., Bischoff R., Holtzer H. Mitosis and intermediate-sized filaments in developing skeletal muscle. J Cell Biol. 1968 Sep;38(3):538–555. doi: 10.1083/jcb.38.3.538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kachinsky A. M., Dominov J. A., Miller J. B. Intermediate filaments in cardiac myogenesis: nestin in the developing mouse heart. J Histochem Cytochem. 1995 Aug;43(8):843–847. doi: 10.1177/43.8.7542682. [DOI] [PubMed] [Google Scholar]
  39. Kachinsky A. M., Dominov J. A., Miller J. B. Myogenesis and the intermediate filament protein, nestin. Dev Biol. 1994 Sep;165(1):216–228. doi: 10.1006/dbio.1994.1248. [DOI] [PubMed] [Google Scholar]
  40. Kaufman S. J., Foster R. F. Replicating myoblasts express a muscle-specific phenotype. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9606–9610. doi: 10.1073/pnas.85.24.9606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Klymkowsky M. W. Intermediate filaments: new proteins, some answers, more questions. Curr Opin Cell Biol. 1995 Feb;7(1):46–54. doi: 10.1016/0955-0674(95)80044-1. [DOI] [PubMed] [Google Scholar]
  42. Kuisk I. R., Li H., Tran D., Capetanaki Y. A single MEF2 site governs desmin transcription in both heart and skeletal muscle during mouse embryogenesis. Dev Biol. 1996 Feb 25;174(1):1–13. doi: 10.1006/dbio.1996.0046. [DOI] [PubMed] [Google Scholar]
  43. Lane E. B., Rugg E. L., Navsaria H., Leigh I. M., Heagerty A. H., Ishida-Yamamoto A., Eady R. A. A mutation in the conserved helix termination peptide of keratin 5 in hereditary skin blistering. Nature. 1992 Mar 19;356(6366):244–246. doi: 10.1038/356244a0. [DOI] [PubMed] [Google Scholar]
  44. Lazarides E., Hubbard B. D. Immunological characterization of the subunit of the 100 A filaments from muscle cells. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4344–4348. doi: 10.1073/pnas.73.12.4344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Lazarides E. Intermediate filaments as mechanical integrators of cellular space. Nature. 1980 Jan 17;283(5744):249–256. doi: 10.1038/283249a0. [DOI] [PubMed] [Google Scholar]
  46. Li H., Capetanaki Y. An E box in the desmin promoter cooperates with the E box and MEF-2 sites of a distal enhancer to direct muscle-specific transcription. EMBO J. 1994 Aug 1;13(15):3580–3589. doi: 10.1002/j.1460-2075.1994.tb06665.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Li H., Capetanaki Y. Regulation of the mouse desmin gene: transactivated by MyoD, myogenin, MRF4 and Myf5. Nucleic Acids Res. 1993 Jan 25;21(2):335–343. doi: 10.1093/nar/21.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Li H., Choudhary S. K., Milner D. J., Munir M. I., Kuisk I. R., Capetanaki Y. Inhibition of desmin expression blocks myoblast fusion and interferes with the myogenic regulators MyoD and myogenin. J Cell Biol. 1994 Mar;124(5):827–841. doi: 10.1083/jcb.124.5.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Li Z., Colucci-Guyon E., Pinçon-Raymond M., Mericskay M., Pournin S., Paulin D., Babinet C. Cardiovascular lesions and skeletal myopathy in mice lacking desmin. Dev Biol. 1996 May 1;175(2):362–366. doi: 10.1006/dbio.1996.0122. [DOI] [PubMed] [Google Scholar]
  50. Lin Z., Lu M. H., Schultheiss T., Choi J., Holtzer S., DiLullo C., Fischman D. A., Holtzer H. Sequential appearance of muscle-specific proteins in myoblasts as a function of time after cell division: evidence for a conserved myoblast differentiation program in skeletal muscle. Cell Motil Cytoskeleton. 1994;29(1):1–19. doi: 10.1002/cm.970290102. [DOI] [PubMed] [Google Scholar]
  51. Lloyd C., Yu Q. C., Cheng J., Turksen K., Degenstein L., Hutton E., Fuchs E. The basal keratin network of stratified squamous epithelia: defining K15 function in the absence of K14. J Cell Biol. 1995 Jun;129(5):1329–1344. doi: 10.1083/jcb.129.5.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Lockard V. G., Bloom S. Trans-cellular desmin-lamin B intermediate filament network in cardiac myocytes. J Mol Cell Cardiol. 1993 Mar;25(3):303–309. doi: 10.1006/jmcc.1993.1036. [DOI] [PubMed] [Google Scholar]
  53. Mayo M. L., Bringas P., Jr, Santos V., Shum L., Slavkin H. C. Desmin expression during early mouse tongue morphogenesis. Int J Dev Biol. 1992 Jun;36(2):255–263. [PubMed] [Google Scholar]
  54. McLean W. H., Lane E. B. Intermediate filaments in disease. Curr Opin Cell Biol. 1995 Feb;7(1):118–125. doi: 10.1016/0955-0674(95)80053-0. [DOI] [PubMed] [Google Scholar]
  55. Muguruma M., Kobayashi K., Fukazawa T., Ohashi K., Maruyama K. A new 220,000 dalton protein located in the Z lines of vertebrate skeletal muscle. J Biochem. 1981 Jun;89(6):1981–1984. doi: 10.1093/oxfordjournals.jbchem.a133401. [DOI] [PubMed] [Google Scholar]
  56. Nelson W. J., Lazarides E. Goblin (ankyrin) in striated muscle: identification of the potential membrane receptor for erythroid spectrin in muscle cells. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3292–3296. doi: 10.1073/pnas.81.11.3292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Olson E. N., Capetanaki Y. G. Developmental regulation of intermediate filament and actin mRNAs during myogenesis is disrupted by oncogenic ras genes. Oncogene. 1989 Jul;4(7):907–913. [PubMed] [Google Scholar]
  58. Porter R. M., Leitgeb S., Melton D. W., Swensson O., Eady R. A., Magin T. M. Gene targeting at the mouse cytokeratin 10 locus: severe skin fragility and changes of cytokeratin expression in the epidermis. J Cell Biol. 1996 Mar;132(5):925–936. doi: 10.1083/jcb.132.5.925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Price M. G., Lazarides E. Expression of intermediate filament-associated proteins paranemin and synemin in chicken development. J Cell Biol. 1983 Dec;97(6):1860–1874. doi: 10.1083/jcb.97.6.1860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Reis A., Hennies H. C., Langbein L., Digweed M., Mischke D., Drechsler M., Schröck E., Royer-Pokora B., Franke W. W., Sperling K. Keratin 9 gene mutations in epidermolytic palmoplantar keratoderma (EPPK). Nat Genet. 1994 Feb;6(2):174–179. doi: 10.1038/ng0294-174. [DOI] [PubMed] [Google Scholar]
  61. Richardson F. L., Stromer M. H., Huiatt T. W., Robson R. M. Immunoelectron and immunofluorescence localization of desmin in mature avian muscles. Eur J Cell Biol. 1981 Dec;26(1):91–101. [PubMed] [Google Scholar]
  62. Rothnagel J. A., Dominey A. M., Dempsey L. D., Longley M. A., Greenhalgh D. A., Gagne T. A., Huber M., Frenk E., Hohl D., Roop D. R. Mutations in the rod domains of keratins 1 and 10 in epidermolytic hyperkeratosis. Science. 1992 Aug 21;257(5073):1128–1130. doi: 10.1126/science.257.5073.1128. [DOI] [PubMed] [Google Scholar]
  63. Rugg E. L., McLean W. H., Lane E. B., Pitera R., McMillan J. R., Dopping-Hepenstal P. J., Navsaria H. A., Leigh I. M., Eady R. A. A functional "knockout" of human keratin 14. Genes Dev. 1994 Nov 1;8(21):2563–2573. doi: 10.1101/gad.8.21.2563. [DOI] [PubMed] [Google Scholar]
  64. Sassoon D. A. Myogenic regulatory factors: dissecting their role and regulation during vertebrate embryogenesis. Dev Biol. 1993 Mar;156(1):11–23. doi: 10.1006/dbio.1993.1055. [DOI] [PubMed] [Google Scholar]
  65. Schmid E., Osborn M., Rungger-Brändle E., Gabbiani G., Weber K., Franke W. W. Distribution of vimentin and desmin filaments in smooth muscle tissue of mammalian and avian aorta. Exp Cell Res. 1982 Feb;137(2):329–340. doi: 10.1016/0014-4827(82)90034-9. [DOI] [PubMed] [Google Scholar]
  66. Schultheiss T., Lin Z. X., Ishikawa H., Zamir I., Stoeckert C. J., Holtzer H. Desmin/vimentin intermediate filaments are dispensable for many aspects of myogenesis. J Cell Biol. 1991 Sep;114(5):953–966. doi: 10.1083/jcb.114.5.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Sejersen T., Lendahl U. Transient expression of the intermediate filament nestin during skeletal muscle development. J Cell Sci. 1993 Dec;106(Pt 4):1291–1300. doi: 10.1242/jcs.106.4.1291. [DOI] [PubMed] [Google Scholar]
  68. Shibuki K., Gomi H., Chen L., Bao S., Kim J. J., Wakatsuki H., Fujisaki T., Fujimoto K., Katoh A., Ikeda T. Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron. 1996 Mar;16(3):587–599. doi: 10.1016/s0896-6273(00)80078-1. [DOI] [PubMed] [Google Scholar]
  69. Small J. V., Fürst D. O., Thornell L. E. The cytoskeletal lattice of muscle cells. Eur J Biochem. 1992 Sep 15;208(3):559–572. doi: 10.1111/j.1432-1033.1992.tb17220.x. [DOI] [PubMed] [Google Scholar]
  70. Smith T. H., Kachinsky A. M., Miller J. B. Somite subdomains, muscle cell origins, and the four muscle regulatory factor proteins. J Cell Biol. 1994 Oct;127(1):95–105. doi: 10.1083/jcb.127.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Steinert P. M., Roop D. R. Molecular and cellular biology of intermediate filaments. Annu Rev Biochem. 1988;57:593–625. doi: 10.1146/annurev.bi.57.070188.003113. [DOI] [PubMed] [Google Scholar]
  72. Tao J. X., Ip W. Site-specific antibodies block kinase A phosphorylation of desmin in vitro and inhibit incorporation of myoblasts into myotubes. Cell Motil Cytoskeleton. 1991;19(2):109–120. doi: 10.1002/cm.970190206. [DOI] [PubMed] [Google Scholar]
  73. Thomas K. R., Capecchi M. R. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell. 1987 Nov 6;51(3):503–512. doi: 10.1016/0092-8674(87)90646-5. [DOI] [PubMed] [Google Scholar]
  74. Thornell L. E., Edström L., Eriksson A., Henriksson K. G., Angqvist K. A. The distribution of intermediate filament protein (skeletin) in normal and diseased human skeletal muscle--an immunohistochemical and electron-microscopic study. J Neurol Sci. 1980 Aug;47(2):153–170. doi: 10.1016/0022-510x(80)90001-5. [DOI] [PubMed] [Google Scholar]
  75. Thornell L. E., Eriksson A., Johansson B., Kjörell U., Franke W. W., Virtanen I., Lehto V. P. Intermediate filament and associated proteins in heart Purkinje fibers: a membrane-myofibril anchored cytoskeletal system. Ann N Y Acad Sci. 1985;455:213–240. doi: 10.1111/j.1749-6632.1985.tb50414.x. [DOI] [PubMed] [Google Scholar]
  76. Tokuyasu K. T., Dutton A. H., Singer S. J. Immunoelectron microscopic studies of desmin (skeletin) localization and intermediate filament organization in chicken cardiac muscle. J Cell Biol. 1983 Jun;96(6):1736–1742. doi: 10.1083/jcb.96.6.1736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Tokuyasu K. T., Dutton A. H., Singer S. J. Immunoelectron microscopic studies of desmin (skeletin) localization and intermediate filament organization in chicken skeletal muscle. J Cell Biol. 1983 Jun;96(6):1727–1735. doi: 10.1083/jcb.96.6.1727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Tokuyasu K. T., Maher P. A., Singer S. J. Distributions of vimentin and desmin in developing chick myotubes in vivo. I. Immunofluorescence study. J Cell Biol. 1984 Jun;98(6):1961–1972. doi: 10.1083/jcb.98.6.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Torchard D., Blanchet-Bardon C., Serova O., Langbein L., Narod S., Janin N., Goguel A. F., Bernheim A., Franke W. W., Lenoir G. M. Epidermolytic palmoplantar keratoderma cosegregates with a keratin 9 mutation in a pedigree with breast and ovarian cancer. Nat Genet. 1994 Jan;6(1):106–110. doi: 10.1038/ng0194-106. [DOI] [PubMed] [Google Scholar]
  80. Traub P., Shoeman R. L. Intermediate filament proteins: cytoskeletal elements with gene-regulatory function? Int Rev Cytol. 1994;154:1–103. doi: 10.1016/s0074-7696(08)62198-1. [DOI] [PubMed] [Google Scholar]
  81. Vajsar J., Becker L. E., Freedom R. M., Murphy E. G. Familial desminopathy: myopathy with accumulation of desmin-type intermediate filaments. J Neurol Neurosurg Psychiatry. 1993 Jun;56(6):644–648. doi: 10.1136/jnnp.56.6.644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Vassar R., Coulombe P. A., Degenstein L., Albers K., Fuchs E. Mutant keratin expression in transgenic mice causes marked abnormalities resembling a human genetic skin disease. Cell. 1991 Jan 25;64(2):365–380. doi: 10.1016/0092-8674(91)90645-f. [DOI] [PubMed] [Google Scholar]
  83. Wang N., Butler J. P., Ingber D. E. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 1993 May 21;260(5111):1124–1127. doi: 10.1126/science.7684161. [DOI] [PubMed] [Google Scholar]
  84. Weitzer G., Milner D. J., Kim J. U., Bradley A., Capetanaki Y. Cytoskeletal control of myogenesis: a desmin null mutation blocks the myogenic pathway during embryonic stem cell differentiation. Dev Biol. 1995 Dec;172(2):422–439. doi: 10.1006/dbio.1995.8070. [DOI] [PubMed] [Google Scholar]
  85. Xu Z., Cork L. C., Griffin J. W., Cleveland D. W. Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell. 1993 Apr 9;73(1):23–33. doi: 10.1016/0092-8674(93)90157-l. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES