Cytoplasmic γ-actin and tropomodulin isoforms link to the sarcoplasmic reticulum in skeletal muscle fibers

Journal of Cell Biology

Volumn 194, Issue 1, 2011, Pages 105-120

  Gokhin, David S ^a   Fowler, Velia M ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ANKYRIN; CALCIUM ION; CYTOPLASMIC GAMMA ACTIN; TROPOMODULIN; TROPOMODULIN 1; TROPOMODULIN 3; TROPOMODULIN 4; TROPOMYOSIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; GENE DELETION; GENE TARGETING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; SARCOMERE; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE; WILD TYPE;

ACTINS; ANIMALS; CALCIUM; CYTOPLASM; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE FIBERS, SKELETAL; PROTEIN ISOFORMS; SARCOPLASMIC RETICULUM; TROPOMODULIN;

EID: 79960260136     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201011128     Document Type: Article

References (65)

1. Allen, P.G., C.B. Shuster, J. Käs, C. Chaponnier, P.A. Janmey, and I.M. Herman. 1996. Phalloidin binding and rheological differences among actin isoforms. Biochemistry. 35:14062-14069.
2. Almenar-Queralt, A., A. Lee, C.A. Conley, L. Ribas de Pouplana, and V.M. Fowler. 1999. Identification of a novel tropomodulin isoform, skeletal tropomodulin, that caps actin filament pointed ends in fast skeletal muscle. J. Biol. Chem. 274:28466-28475.
3. Bagnato, P., V. Barone, E. Giacomello, D. Rossi, and V. Sorrentino. 2003. Binding of an ankyrin-1 isoform to obscurin suggests a molecular link between the sarcoplasmic reticulum and myofibrils in striated muscles. J. Cell Biol. 160:245-253.
4. Bang, M.L., C. Gregorio, and S. Labeit. 2002. Molecular dissection of the interaction of desmin with the C-terminal region of nebulin. J. Struct. Biol. 137:119-127.
5. Belyantseva, I.A., B.J. Perrin, K.J. Sonnemann, M. Zhu, R. Stepanyan, J. McGee, G.I. Frolenkov, E.J. Walsh, K.H. Friderici, T.B. Friedman, and J.M. Ervasti. 2009. Gamma-actin is required for cytoskeletal maintenance but not development. Proc. Natl. Acad. Sci. USA. 106:9703-9708.
6. Bennett, V., and J. Healy. 2008. Being there: cellular targeting of voltagegated sodium channels in the heart. J. Cell Biol. 180:13-15.
7. Borzok, M.A., D.H. Catino, J.D. Nicholson, A. Kontrogianni-Konstantopoulos, and R.J. Bloch. 2007. Mapping the binding site on small ankyrin 1 for obscurin. J. Biol. Chem. 282:32384-32396.
8. Chu, X., J. Chen, M.C. Reedy, C. Vera, K.L. Sung, and L.A. Sung. 2003. E-Tmod capping of actin filaments at the slow-growing end is required to establish mouse embryonic circulation. Am. J. Physiol. Heart Circ. Physiol. 284:H1827-H1838.
9. Conley, C.A., K.L. Fritz-Six, A. Almenar-Queralt, and V.M. Fowler. 2001. Leiomodins: larger members of the tropomodulin (Tmod) gene family. Genomics. 73:127-139.
10. Conover, G.M., S.N. Henderson, and C.C. Gregorio. 2009. A myopathy-linked desmin mutation perturbs striated muscle actin filament architecture. Mol. Biol. Cell. 20:834-845.
11. Cox, P.R., and H.Y. Zoghbi. 2000. Sequencing, expression analysis, and mapping of three unique human tropomodulin genes and their mouse orthologs. Genomics. 63:97-107.
12. Craig, S.W., and J.V. Pardo. 1983. Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibrilto-sarcolemma attachment sites. Cell Motil. 3:449-462.
13. Cunha, S.R., and P.J. Mohler. 2009. Ankyrin protein networks in membrane formation and stabilization. J. Cell. Mol. Med. 13:4364-4376.
14. Fischer, R.S., K.L. Fritz-Six, and V.M. Fowler. 2003. Pointed-end capping by tropomodulin3 negatively regulates endothelial cell motility. J. Cell Biol. 161:371-380.
15. Fowler, V.M. 1987. Identification and purification of a novel Mr 43,000 tropomyosin-binding protein from human erythrocyte membranes. J. Biol. Chem. 262:12792-12800.
16. Fowler, V.M. 1990. Tropomodulin: a cytoskeletal protein that binds to the end of erythrocyte tropomyosin and inhibits tropomyosin binding to actin. J. Cell Biol. 111:471-481.
17. Fowler, V.M., and V. Bennett. 1984. Tropomyosin: a new component of the erythrocyte membrane skeleton. Prog. Clin. Biol. Res. 159:57-71.
18. Fowler, V.M., M.A. Sussmann, P.G. Miller, B.E. Flucher, and M.P. Daniels. 1993. Tropomodulin is associated with the free (pointed) ends of the thin filaments in rat skeletal muscle. J. Cell Biol. 120:411-420.
19. Fritz-Six, K.L., P.R. Cox, R.S. Fischer, B. Xu, C.C. Gregorio, H.Y. Zoghbi, and V.M. Fowler. 2003. Aberrant myofibril assembly in tropomodulin1 null mice leads to aborted heart development and embryonic lethality. J. Cell Biol. 163:1033-1044.
20. Fukuzawa, A., S. Lange, M. Holt, A. Vihola, V. Carmignac, A. Ferreiro, B. Udd, and M. Gautel. 2008. Interactions with titin and myomesin target obscurin and obscurin-like 1 to the M-band: implications for hereditary myopathies. J. Cell Sci. 121:1841-1851.
21. Gallagher, P.G., and B.G. Forget. 1998. An alternate promoter directs expression of a truncated, muscle-specific isoform of the human ankyrin 1 gene. J. Biol. Chem. 273:1339-1348.
22. Gallagher, P.G., W.T. Tse, A.L. Scarpa, S.E. Lux, and B.G. Forget. 1997. Structure and organization of the human ankyrin-1 gene. Basis for complexity of pre-mRNA processing. J. Biol. Chem. 272:19220-19228.
23. Galustian, C., J. Dye, L. Leach, P. Clark, and J.A. Firth. 1995. Actin cytoskeletal isoforms in human endothelial cells in vitro: alteration with cell passage. In Vitro Cell. Dev. Biol. Anim. 31:796-802.
24. Gokhin, D.S., R.A. Lewis, C.R. McKeown, R.B. Nowak, N.E. Kim, R.S. Littlefield, R.L. Lieber, and V.M. Fowler. 2010. Tropomodulin isoforms regulate thin filament pointed-end capping and skeletal muscle physiology. J. Cell Biol. 189:95-109.
25. Gregorio, C.C., A. Weber, M. Bondad, C.R. Pennise, and V.M. Fowler. 1995. Requirement of pointed-end capping by tropomodulin to maintain actin filament length in embryonic chick cardiac myocytes. Nature. 377:83-86.
26. Hanft, L.M., I.N. Rybakova, J.R. Patel, J.A. Rafael-Fortney, and J.M. Ervasti. 2006. Cytoplasmic gamma-actin contributes to a compensatory remodeling response in dystrophin-deficient muscle. Proc. Natl. Acad. Sci. USA. 103:5385-5390.
27. Hanft, L.M., D.J. Bogan, U. Mayer, S.J. Kaufman, J.N. Kornegay, and J.M. Ervasti. 2007. Cytoplasmic gamma-actin expression in diverse animal models of muscular dystrophy. Neuromuscul. Disord. 17:569-574.
28. Jaeger, M.A., K.J. Sonnemann, D.P. Fitzsimons, K.W. Prins, and J.M. Ervasti. 2009. Context-dependent functional substitution of alpha-skeletal actin by gamma-cytoplasmic actin. FASEB J. 23:2205-2214.
29. Kee, A.J., G. Schevzov, V. Nair-Shalliker, C.S. Robinson, B. Vrhovski, M. Ghoddusi, M.R. Qiu, J.J. Lin, R. Weinberger, P.W. Gunning, and E.C. Hardeman. 2004. Sorting of a nonmuscle tropomyosin to a novel cytoskeletal compartment in skeletal muscle results in muscular dystrophy. J. Cell Biol. 166:685-696.
30. Knight, P.J., and J.A. Trinick. 1982. Preparation of myofibrils. Methods Enzymol. 85:9-12.
31. Kontrogianni-Konstantopoulos, A., E.M. Jones, D.B. Van Rossum, and R.J. Bloch. 2003. Obscurin is a ligand for small ankyrin 1 in skeletal muscle. Mol. Biol. Cell. 14:1138-1148.
32. Lange, S., K. Ouyang, G. Meyer, L. Cui, H. Cheng, R.L. Lieber, and J. Chen. 2009. Obscurin determines the architecture of the longitudinal sarcoplasmic reticulum. J. Cell Sci. 122:2640-2650.
33. Littlefield, R.S., and V.M. Fowler. 2008. Thin filament length regulation in striated muscle sarcomeres: pointed-end dynamics go beyond a nebulin ruler. Semin. Cell Dev. Biol. 19:511-519.
34. Littlefield, R., A. Almenar-Queralt, and V.M. Fowler. 2001. Actin dynamics at pointed ends regulates thin filament length in striated muscle. Nat. Cell Biol. 3:544-551.
35. McKeown, C.R., R.B. Nowak, J. Moyer, M.A. Sussman, and V.M. Fowler. 2008. Tropomodulin1 is required in the heart but not the yolk sac for mouse embryonic development. Circ. Res. 103:1241-1248.
36. Meyer, G.A., B. Kiss, S.R. Ward, D.L. Morgan, M.S. Kellermayer, and R.L. Lieber. 2010. Theoretical predictions of the effects of force transmission by desmin on intersarcomere dynamics. Biophys. J. 98:258-266.
37. Miller, J.B. 1991. Myoblasts, myosins, MyoDs, and the diversification of muscle fibers. Neuromuscul. Disord. 1:7-17.
38. Milner, D.J., G. Weitzer, D. Tran, A. Bradley, and Y. Capetanaki. 1996. Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J. Cell Biol. 134:1255-1270.
39. Mohler, P.J., J.Q. Davis, and V. Bennett. 2005. Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP3 receptor in a cardiac T-tubule/SR microdomain. PLoS Biol. 3:e423.
40. Monti, R.J., R.R. Roy, J.A. Hodgson, and V.R. Edgerton. 1999. Transmission of forces within mammalian skeletal muscles. J. Biomech. 32:371-380.
41. Moyer, J.D., R.B. Nowak, N.E. Kim, S.K. Larkin, L.L. Peters, J. Hartwig, F.A. Kuypers, and V.M. Fowler. 2010. Tropomodulin 1-null mice have a mild spherocytic elliptocytosis with appearance of tropomodulin 3 in red blood cells and disruption of the membrane skeleton. Blood. 116:2590-2599.
42. Nelson, W.J., and E. Lazarides. 1983. Expression of the beta subunit of spectrin in nonerythroid cells. Proc. Natl. Acad. Sci. USA. 80:363-367.
43. Nowak, R.B., R.S. Fischer, R.K. Zoltoski, J.R. Kuszak, and V.M. Fowler. 2009. Tropomodulin1 is required for membrane skeleton organization and hexagonal geometry of fiber cells in the mouse lens. J. Cell Biol. 186:915-928.
44. Otey, C.A., M.H. Kalnoski, and J.C. Bulinski. 1988. Immunolocalization of muscle and nonmuscle isoforms of actin in myogenic cells and adult skeletal muscle. Cell Motil. Cytoskeleton. 9:337-348.
45. Otterbein, L.R., P. Graceffa, and R. Dominguez. 2001. The crystal structure of uncomplexed actin in the ADP state. Science. 293:708-711.
46. 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.
47. Porter, G.A., G.M. Dmytrenko, J.C. Winkelmann, and R.J. Bloch. 1992. Dystrophin colocalizes with β-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J. Cell Biol. 117:997-1005.
48. Porter, G.A., M.G. Scher, W.G. Resneck, N.C. Porter, V.M. Fowler, and R.J. Bloch. 1997. Two populations of beta-spectrin in rat skeletal muscle. Cell Motil. Cytoskeleton. 37:7-19.
49. Porter, N.C., W.G. Resneck, A. O'Neill, D.B. Van Rossum, M.R. Stone, and R.J. Bloch. 2005. Association of small ankyrin 1 with the sarcoplasmic reticulum. Mol. Membr. Biol. 22:421-432.
50. Prins, K.W., D.A. Lowe, and J.M. Ervasti. 2008. Skeletal muscle-specific ablation of gamma(cyto)-actin does not exacerbate the mdx phenotype. PLoS ONE. 3:e2419.
51. Renley, B.A., I.N. Rybakova, K.J. Amann, and J.M. Ervasti. 1998. Dystrophin binding to nonmuscle actin. Cell Motil. Cytoskeleton. 41:264-270.
52. Repasky, E.A., B.L. Granger, and E. Lazarides. 1982. Widespread occurrence of avian spectrin in nonerythroid cells. Cell. 29:821-833.
53. Rybakova, I.N., J.R. Patel, and J.M. Ervasti. 2000. The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J. Cell Biol. 150:1209-1214.
54. Shah, S.B., F.C. Su, K. Jordan, D.J. Milner, J. Fridén, Y. Capetanaki, and R.L. Lieber. 2002. Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle. J. Exp. Biol. 205:321-325.
55. Shah, S.B., J. Davis, N. Weisleder, I. Kostavassili, A.D. McCulloch, E. Ralston, Y. Capetanaki, and R.L. Lieber. 2004. Structural and functional roles of desmin in mouse skeletal muscle during passive deformation. Biophys. J. 86:2993-3008.
56. Sonnemann, K.J., D.P. Fitzsimons, J.R. Patel, Y. Liu, M.F. Schneider, R.L. Moss, and J.M. Ervasti. 2006. Cytoplasmic gamma-actin is not required for skeletal muscle development but its absence leads to a progressive myopathy. Dev. Cell. 11:387-397.
57. Sung, L.A., V.M. Fowler, K. Lambert, M.A. Sussman, D. Karr, and S. Chien. 1992. Molecular cloning and characterization of human fetal liver tropomodulin. A tropomyosin-binding protein. J. Biol. Chem. 267:2616-2621.
58. Tonino, P., C.T. Pappas, B.D. Hudson, S. Labeit, C.C. Gregorio, and H. Granzier. 2010. Reduced myofibrillar connectivity and increased Z-disk width in nebulin-deficient skeletal muscle. J. Cell Sci. 123:384-391.
59. Vlahovich, N., G. Schevzov, V. Nair-Shaliker, B. Ilkovski, S.T. Artap, J.E. Joya, A.J. Kee, K.N. North, P.W. Gunning, and E.C. Hardeman. 2008. Tropomyosin 4 defines novel filaments in skeletal muscle associated with muscle remodelling/regeneration in normal and diseased muscle. Cell Motil. Cytoskeleton. 65:73-85.
60. Vlahovich, N., A.J. Kee, C. Van der Poel, E. Kettle, D. Hernandez-Deviez, C. Lucas, G.S. Lynch, R.G. Parton, P.W. Gunning, and E.C. Hardeman. 2009. Cytoskeletal tropomyosin Tm5NM1 is required for normal excitation-contraction coupling in skeletal muscle. Mol. Biol. Cell. 20:400-409.
61. Watakabe, A., R. Kobayashi, and D.M. Helfman. 1996. N-tropomodulin: a novel isoform of tropomodulin identified as the major binding protein to brain tropomyosin. J. Cell Sci. 109:2299-2310.
62. Weber, K.L., R.S. Fischer, and V.M. Fowler. 2007. Tmod3 regulates polarized epithelial cell morphology. J. Cell Sci. 120:3625-3632.
63. Williams, M.W., W.G. Resneck, T. Kaysser, J.A. Ursitti, C.S. Birkenmeier, J.E. Barker, and R.J. Bloch. 2001. Na,K-ATPase in skeletal muscle: two populations of beta-spectrin control localization in the sarcolemma but not partitioning between the sarcolemma and the transverse tubules. J. Cell Sci. 114:751-762.
64. Woo, M.K., A. Lee, R.S. Fischer, J. Moyer, and V.M. Fowler. 2000. The lens membrane skeleton contains structures preferentially enriched in spectrin-actin or tropomodulin-actin complexes. Cell Motil. Cytoskeleton. 46:257-268.
65. Yamashiro, S., K.D. Speicher, D.W. Speicher, and V.M. Fowler. 2010. Mammalian tropomodulins nucleate actin polymerization via their actin monomer binding and filament pointed end-capping activities. J. Biol. Chem. 285:33265-33280.