Sorting of a nonmuscle tropomyosin to a novel cytoskeletal compartment in skeletal muscle results in muscular dystrophy

Journal of Cell Biology

Volumn 166, Issue 5, 2004, Pages 685-696

  Kee, Anthony J ^a   Schevzov, Galina ^b,d   Nair Shalliker, Visalini ^a   Robinson, C Stephen ^a   Vrhovski, Bernadette ^b   Ghoddusi, Majid ^a   Qiu, Min Ru ^b   Lin, Jim J C ^c   Weinberger, Ron ^b,d   Gunning, Peter W ^b   Hardeman, Edna C ^a  

^a CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^b CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Muscles; Muscular dystrophies; Sarcomeres; Transgenic mice; Tropomyosin

Indexed keywords

ACTIN; ISOPROTEIN; TROPOMYOSIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; GENE MUTATION; IMMUNOHISTOCHEMISTRY; MOUSE; MUSCLE FIBRIL; MUSCULAR DYSTROPHY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TARGETING; SARCOMERE; SKELETAL MUSCLE; THIN FILAMENT;

ANIMALS; CELL COMPARTMENTATION; CELL MEMBRANE; CYTOSKELETON; DISEASE MODELS, ANIMAL; FEMALE; MICE; MICE, TRANSGENIC; MUSCLE FIBERS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUTATION; PHENOTYPE; PROTEIN ISOFORMS; PROTEIN TRANSPORT; SARCOMERES; TROPOMYOSIN;

ANIMALIA; MAMMALIA; MUS MUSCULUS;

EID: 4444219750     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200406181     Document Type: Article

References (70)

1. Arai, A., J.A. Spencer, and E.N. Olson. 2002. STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription. J. Biol. Chem. 277:24453-24459.
2. Bang, M.L., R.E. Mudry, A.S. McElhinny, K. Trombitas, A.J. Geach, R. Yamasaki, H. Sorimachi, H. Granzier, C.C. Gregorio, and S. Labeit. 2001. Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J. Cell Biol. 153:413-427.
3. Banker, B.Q., and A.G. Engel. 1994. Basic Reactions of Muscle. In Myology. A.G. Engel and Franzini-Armstrong C., editors. McGraw-Hill, Inc., New York. 832-888.
4. Bittner, R.E., L.V. Anderson, E. Burkhardt, R. Bashir, E. Vafiadaki, S. Ivanova, T. Raffelsberger, I. Maerk, H. Hoger, M. Jung, et al. 1999. Dysferlin deletion in SJL mice (SJL-Dysf) defines a natural model for limb girdle muscular dystrophy 2B. Nat. Genet. 23:141-142.
5. Borrione, A.C., A.M. Zanellato, L. Saggin, M. Mazzoli, G. Azzarello, and S. Sartore. 1988. Neonatal myosin heavy chains are nor expressed in Ni-induced rat rhabdomyosarcoma. Differentiation. 38:49-59.
6. Bottinelli, R., D.A. Coviello, C.S. Redwood, M.A. Pellegrino, B.J. Maron, P. Spirito, H. Watkins, and C. Reggiani. 1998. A mutant tropomyosin that causes hypertrophic cardiomyopathy is expressed in vivo and associated with an increased calcium sensitivity. Circ. Res. 82:106-115.
7. Boyd, J., J.I. Risinger, R.W. Wiseman, B.A. Merrick, J.K. Selkirk, and J.C. Barrett. 1995. Regulation of microfilament organization and anchorage-independent growth by tropomyosin 1. Proc. Natl. Acad. Sci. USA. 92:11534-11538.
8. Bryce, N.S., G. Schevzov, V. Ferguson, J.M. Percival, J.J. Lin, F. Matsumura, J.R. Bamburg, P.L. Jeffrey, E.C. Hardeman, P. Gunning, and R.P. Weinberger. 2003. Specification of actin filament function and molecular composition by tropomyosin isoforms. Mol. Biol. Cell. 14:1002-1016.
9. Capetanaki, Y. 2002. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc. Med. 12:339-348.
10. Clark, K.A., A.S. McElhinny, M.C. Beckerle, and C.C. Gregorio. 2002. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18:637-706.
11. Coghill, I.D., S. Brown, D.L. Cottle, M.J. McGrath, P.A. Robinson, H.H. Nandurkar, J.M. Dyson, and C.A. Mitchell. 2003. FHL3 is an actin-binding protein that regulates alpha-actinin-mediated actin bundling: FHL3 localizes to actin stress fibers and enhances cell spreading and stress fiber disassembly. J. Biol. Chem. 278:24139-24152.
12. Craig, S.W., and J.V. Pardo. 1983. Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibril-to-sarcolemma attachment sites. Cell Motil. 3:449-462.
13. Dalby-Payne, J.R., E.V. O'Loughlin, and P. Gunning. 2003. Polarization of specific tropomyosin isoforms in gastrointestinal epithelial cells and their impact on CFTR at the apical surface. Mol. Biol. Cell. 14:4365-4375.
14. Dalkilic, I., and L.M. Kunkel. 2003. Muscular dystrophies: genes to pathogenesis. Curr. Opin. Genet. Dev. 13:231-238.
15. Dufour, C., R.P. Weinberger, and P. Gunning. 1998a. Tropomyosin isoform diversity and neuronal morphogenesis. Immunol. Cell Biol. 76:424-429.
16. Dufour, C., R.P. Weinberger, G. Schevzov, P.L. Jeffrey, and P. Gunning. 1998b. Splicing of two internal and four carboxyl-terminal alternative exons in non-muscle tropomyosin 5 pre-mRNA is independently regulated during development. J. Biol. Chem. 273:18547-18555.
17. Engel, W.K., and G.G. Cunningham. 1963. Rapid examination of muscle tissue. An improved trichrome method for fresh-frozen biopsy sections. Neurology. 13:919-923.
18. Erdelyi, M., A.M. Michon, A. Guichet, J.B. Glotzer, and A. Ephrussi. 1995. Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization. Nature. 377:524-527.
19. Ervasti, J.M. 2003. Costameres: the Achilles' heel of Herculean muscle. J. Biol. Chem. 278:13591-13594.
20. Fanning, A.S., J.S. Wolenski, M.S. Mooseker, and J.G. Izant. 1994. Differential regulation of skeletal muscle myosin-II and brush border myosin-I enzymology and mechanochemistry by bacterially produced tropomyosin isoforms. Cell Motil. Cytoskeleton. 29:29-45.
21. Flicker, P.F., G.N. Phillips Jr., and C. Cohen. 1982. Troponin and its interactions with tropomyosin. An electron microscope study. J. Mol. Biol. 162:495-501.
22. Gimona, M., J.A. Kazzaz, and D.M. Helfman. 1996. Forced expression of tropomyosin 2 or 3 in v-Ki-ras-transformed fibroblasts results in distinct phenotypic effects. Proc. Natl. Acad. Sci. USA. 93:9618-9623.
23. Griffiths, G., A. McDowall, R. Back, and J. Dubochet. 1984. On the preparation of cryosection for immunocytochemistry. J. Ultrastruct. Res. 89:65-78.
24. Gunning, P., M. Gordon, R. Wade, R. Gahlmann, C.S. Lin, and E. Hardeman. 1990. Differential control of tropomyosin mRNA levels during myogenesis suggests the existence of an isoform competition-autoregulatory compensation control mechanism. Dev. Biol. 138:443-453.
25. Gunning, P., E. Hardeman, P. Jeffrey, and R. Weinberger. 1998a. Creating intracellular structural domains: spatial segregation of actin and tropomyosin isoforms in neurons. Bioessays. 20:892-900.
26. Gunning, P., R. Weinberger, P. Jeffrey, and E. Hardeman. 1998b. Isoform sorting and the creation of intracellular compartments. Annu. Rev. Cell Dev. Biol. 14:339-372.
27. Guy, P.M., D.A. Kenny, and G.N. Gill. 1999. The PDZ domain of the LIM protein enigma binds to beta-tropomyosin. Mol. Biol. Cell. 10:1973-1984.
28. Hall, Z.W., B.W. Lubit, and J.H. Schwartz. 1981. Cytoplasmic actin in postsynaptic structures at the neuromuscular junction. J. Cell Biol. 90:789-792.
29. Hannan, A.J., P. Gunning, P.L. Jeffrey, and R.P. Weinberger. 1998. Structural compartments within neurons: developmentally regulated organization of microfilament isoform mRNA and protein. Mol. Cell. Neurosci. 11:289-304.
30. Heimann, K., J.M. Percival, R. Weinberger, P. Gunning, and J.L. Stow. 1999. Specific isoforms of actin-binding proteins on distinct populations of Golgi-derived vesicles. J. Biol. Chem. 274:10743-10750.
31. Herman, I.M. 1993. Actin isoforms. Curr. Opin. Cell Biol. 5:48-55.
32. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the Mouse Embryo. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 332 pp.
33. Hook, J., F. Lemckert, H. Qin, G. Schevzov, and P. Gunning. 2004. Gamma tropomyosin gene products are required for embryonic development. Mol. Cell. Biol. 24:2318-2323.
34. 2+. Potentiation of the annealing process by caldesmon. J. Biol. Chem. 264:16764-16770.
35. Ishikawa, R., S. Yamashiro, and F. Matsumura. 1989b. Differential modulation of actin-severing activity of gelsolin by multiple isoforms of cultured rat cell tropomyosin. Potentiation of protective ability of tropomyosins by 83-kDa nonmuscle caldesmon. J. Biol. Chem. 264:7490-7497.
36. Kislauskis, E.H., X. Zhu, and R.H. Singer. 1997. β-Actin messenger RNA localization and protein synthesis augment cell motility. J. Cell Biol. 136:1263-1270.
37. Kojima, H., A. Ishijima, and T. Yanagida. 1994. Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc. Natl. Acad. Sci. USA. 91:12962-12966.
38. Kumar, A., K. Crawford, L. Close, M. Madison, J. Lotenz, T. Doetschman, S. Pawlowski, J. Duffy, J. Neumann, J. Robbins, et al. 1997. Rescue of cardiac alpha-actin-deficient mice by enteric smooth muscle gamma-actin. Proc. Natl. Acad. Sci. USA. 94:4406-4411.
39. Lehman, W., V. Hatch, V. Korman, M. Rosol, L. Thomas, R. Maytum, M.A. Geeves, J.E. Van Eyk, L.S. Tobacman, and R. Craig. 2000. Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments. J. Mol. Biol. 302:593-606.
40. Lin, J.J., T.E. Hegmann, and J.L. Lin. 1988. Differential localization of tropomyosin isoforms in cultured nonmuscle cells. J. Cell Biol. 107:563-572.
41. Lin, J.J., K.S. Warren, D.D. Wamboldt, T. Wang, and J.L. Lin. 1997. Tropomyosin isoforms in nonmuscle cells. Int. Rev. Cytol. 170:1-38.
42. Lubit, B.W. 1984. Association of beta-cytoplasmic actin with high concentrations of acetylcholine receptor (AChR) in normal and anti-AChR-treated primary rat muscle cultures. J. Histochem. Cytochem. 32:973-981.
43. Matsumura, F., and S. Yamashiro-Matsumura. 1985. Purification and characterization of multiple isoforms of tropomyosin from rat cultured cells. J. Biol. Chem. 260:13851-13859.
44. Matsumura, F., S. Yamashiro-Matsumura, and J.J. Lin. 1983. Isolation and characterization of tropomyosin-containing microfilaments from cultured cells. J. Biol. Chem. 258:6636-6644.
45. Milner, D.J., M. Mavroidis, N. Weisleder, and Y. Capetanaki. 2000. Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J. Cell Biol. 150:1283-1298.
46. Miyado, K., M. Kimura, and S. Taniguchi. 1996. Decreased expression of a single tropomyosin isoform, TM5/TM30nm, results in reduction in motility of highly metastatic B16-F10 mouse melanoma cells. Biochem. Biophys. Res. Commun. 225:427-435.
47. Moreira, E.S., T.J. Wiltshire, G. Faulkner, A. Nilforoushan, M. Vainzof, O.T. Suzuki, G. Valle, R. Reeves, M. Zatz, M.R. Passos-Bueno, and D.E. Jenne. 2000. Limb-girdle muscular dystrophy type 2G is caused by mutations in the gene encoding the sarcomeric protein telethonin. Nat. Genet. 24:163-166.
48. Muthuchamy, M., K. Pieples, P. Rethinasamy, B. Hoit, I.L. Grupp, G.P. Boivin, B. Wolska, C. Evans, R.J. Solaro, and D.F. Wieczorek. 1999. Mouse model of a familial hypertrophic cardiomyopathy mutation in alpha-tropomyosin manifests cardiac dysfunction. Circ. Res. 85:47-56.
49. Nakata, T., Y. Nishina, and H. Yorifuji. 2001. Cytoplasmic gamma actin as a Z-disc protein. Biochem. Biophys. Res. Commun. 286:156-163.
50. North, K.N., and A.H. Beggs. 1996. Deficiency of a skeletal muscle isoform of alpha-actinin (alpha-actinin-3) in merosin-positive congenital muscular dystrophy. Neuromuscul. Disord. 6:229-235.
51. North, A.J., M. Gimona, Z. Lando, and J.V. Small. 1994. Actin isoform compartments in chicken gizzard smooth muscle cells. J. Cell Sci. 107:445-455.
52. Pardo, J.V., M.F. Pittenger, and S.W. Craig. 1983. Subcellular sorting of isoactins: selective association of gamma-actin with skeletal muscle mitochondria. Cell. 32:1093-1103.
53. Palmer, S., N. Groves, A. Schindeler, T. Yeoh, C. Biben, C.C. Wang, D.B. Sparrow, L. Barnett, N.A. Jenkins, N.G. Copeland, et al. 2001. The small muscle-specific protein Csl modifies cell shape and promotes myocyte fusion in an insulin-like growth factor 1-dependent manner. J. Cell Biol. 153:985-998.
54. Percival, J.M., G. Thomas, T.A. Cock, E.M. Gardiner, P.L. Jeffrey, J.J. Lin, R.P. Weinberger, and P. Gunning. 2000. Sorting of tropomyosin isoforms in synchronised NIH 3T3 fibroblasts: evidence for distinct microfilament populations. Cell Motil. Cytoskeleton. 47:189-208.
55. Percival, J.M., J.A.I. Hughes, D.L. Brown, G. Schevzov, K. Heimann, B. Vrhovski, N. Bryce, J.L. Stow, and P.W. Gunning. 2004. Targeting of a tropomyosin isoform to short microfilaments associated with the Golgi complex. Mol. Biol. Cell. 15:268-280.
56. Pittenger, M.F., J.A. Kazzaz, and D.M. Helfman. 1994. Functional properties of non-muscle tropomyosin isoforms. Curr. Opin. Cell Biol. 6:96-104.
57. Pittenger, M.F., A. Kistler, and D.M. Helfman. 1995. Alternatively spliced exons of the beta tropomyosin gene exhibit different affinities for F-actin and effects with nonmuscle caldesmon. J. Cell Sci. 108:3253-3265.
58. Prasad, G.L., R.A. Fuldner, and H.L. Cooper. 1993. Expression of transduced tropomyosin 1 cDNA suppresses neoplastic growth of cells transformed by the ras oncogene. Proc. Natl. Acad. Sci. USA. 90:7039-7043.
59. Richard, I., O. Broux, V. Allamand, F. Fougerousse, N. Chiannilkulchai, N. Bourg, L. Brenguier, C. Devaud, P. Pasturaud, C. Roudaut, et al. 1995. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell. 81:27-40.
60. Ronnov-Jessen, L., and O.W. Petersen. 1996. A function for filamentous α-smooth muscle actin: retardation of motility in fibroblasts. J. Cell Biol. 134:67-80.
61. Rybakova, I.N., J.R. Patel, and J.M. Ervasti. 2000. The dystrophin complex forms a mechanically strong link between the sarcolemma and costametic actin. J. Cell Biol. 150:1209-1214.
62. Schevzov, G., C. Lloyd, and P. Gunning. 1992. High level expression of transfected β- and γ-actin genes differentially impacts on myoblast cytoarchitecture. J. Cell Biol. 117:775-785.
63. Schevzov, G., P. Gunning, P.L. Jeffrey, C. Temm-Grove, D.M. Helfman, J.J. Lin, and R.P. Weinberger. 1997. Tropomyosin localization reveals distinct populations of microfilaments in neurites and growth cones. Mol. Cell. Neurosci. 8:439-454.
64. Seward, D.J., J.C. Haney, M.A. Rudnicki, and S.J. Swoap. 2001. bHLH transcription factor MyoD affects myosin heavy chain expression pattern in a muscle-specific fashion. Am. J. Physiol. Cell Physiol. 280:C408-C413.
65. Temm-Grove, C.J., B.M. Jockusch, R.P. Weinberger, G. Schevzov, and D.M. Helfman. 1998. Distinct localizations of tropomyosin isoforms in LLC-PK1 epithelial cells suggests specialized function at cell-cell adhesions. Cell Motil. Cytoskeleton. 40:393-407.
66. Thietfelder, L., H. Watkins, C. MacRae, R. Lamas, W. McKenna, H.P. Vosberg, J.G. Seidman, and C.E. Seidman. 1994. Alpha-tropomyosin and cardiac troponin T mutations cause familial hypertrophic cardiomyopathy: a disease of the sarcomere. Cell. 77:701-712.
67. Tsukamoto, Y., T. Senda, T. Nakano, C. Nakada, T. Hida, N. Ishiguro, G. Kondo, T. Baba, K. Sato, M. Osaki, et al. 2002. Arpp, a new homolog of carp, is preferentially expressed in type 1 skeletal muscle fibers and is markedly induced by denervation. Lab. Invest. 82:645-655.
68. von Arx, P., S. Bantle, T. Soldati, and J.C. Perriard. 1995. Dominant negative effect of cytoplasmic actin isoproteins on cardiomyocyte cytoarchitecture and function. J. Cell Biol. 131:1759-1773.
69. Weinberger, R., G. Schevzov, P. Jeffrey, K. Gordon, M. Hill, and P. Gunning. 1996. The molecular composition of neuronal microfilaments is spatially and temporally regulated. J. Neurosci. 16:238-252.
70. Wieczorek, D.F., M. Periasamy, G.S. Butler-Browne, R.G. Whalen, and B. Nadal-Ginard. 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.