Differential actin-regulatory activities of tropomodulin1 and tropomodulin3 with diverse tropomyosin and actin isoforms

Journal of Biological Chemistry

Volumn 289, Issue 17, 2014, Pages 11616-11629

  Yamashiro, Sawako ^a,b   Gokhin, David S ^a   Sui, Zhenhua ^a   Bergeron, Sarah E ^b   Rubenstein, Peter A ^c   Fowler, Velia M ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

ACTIN FILAMENT; ACTIN MONOMERS; CYTOSKELETAL DYNAMICS; ISOFORMS; TROPOMYOSIN;

PROTEINS;

ACTIN; ALPHA ACTIN; ALPHA TROPOMYOSIN; BETA ACTIN MONOMER; BETA TROPOMYOSIN; CYTOPLASMIC GAMMA ACTIN MONOMER; F ACTIN; G ACTIN; ISOPROTEIN; TROPOMODULIN; TROPOMODULIN 1; TROPOMODULIN 3; TROPOMYOSIN; TROPOMYOSIN 5B; TROPOMYOSIN 5NM1; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN REGULATORY ACTIVITY; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CELL FUNCTION; CELL STRUCTURE; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; MOLECULAR DYNAMICS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION, SYNTHESIS AND MODIFICATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN SEQEUSTRATION; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION;

ACTIN; ACTIN CAPPING; ACTIN-BINDING PROTEINS; CYTOSKELETON; PROTEIN CHEMISTRY; PROTEIN-PROTEIN INTERACTIONS; TROPOMODULIN; TROPOMYOSIN;

ACTINS; ANIMALS; CYTOSKELETON; MUSCLE, SKELETAL; PROTEIN BINDING; PROTEIN ISOFORMS; RABBITS; SARCOMERES; SPECTROMETRY, FLUORESCENCE; TROPOMODULIN; TROPOMYOSIN;

EID: 84899463909     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.555128     Document Type: Article

References (77)

1. Fischer, R. S., and Fowler, V. M. (2003) Tropomodulins: life at the slowend. Trends Cell Biol. 13, 593-601
2. Yamashiro, S., Gokhin, D. S., Kimura, S., Nowak, R. B., and Fowler, V. M. (2012) Tropomodulins: pointed-end capping proteins that regulate actin filament architecture in diverse cell types. Cytoskeleton 69, 337-370
3. Gokhin, D. S., and Fowler, V. M. (2011) Tropomodulin capping of actin filaments in striated muscle development and physiology. J. Biomed. Biotechnol. 2011, 103069
4. Fischer, R. S., Fritz-Six, K. L., and Fowler, V. M. (2003) Pointed-end capping by tropomodulin3 negatively regulates endothelial cell motility. J. Cell Biol. 161, 371-380 (Pubitemid 36529854)
5. Sui, Z., Nowak, R. B., Bacconi, A., Kim, N. E., Liu, H., Li, J., Wickrema, A., An, X. L., and Fowler, V. M. (2014) Tropomodulin3-null mice are embryonic lethal with anemia due to impaired erythroid terminal differentiation in the fetal liver. Blood 123, 758-767
6. Weber, K. L., Fischer, R. S., and Fowler, V. M. (2007) Tmod3 regulates polarized epithelial cell morphology. J. Cell Sci. 120, 3625-3632 (Pubitemid 350120954)
7. Gokhin, D. S., and Fowler, V. M. (2011) Cytoplasmicγ-actin and tropomodulin isoforms link to the sarcoplasmic reticulum in skeletal muscle fibers. J. Cell Biol. 194, 105-120
8. Moyer, J. D., Nowak, R. B., Kim, N. E., Larkin, S. K., Peters, L. L., Hartwig, J., Kuypers, F. A., and Fowler, V. M. (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
9. Nowak, R. B., Fischer, R. S., Zoltoski, R. K., Kuszak, J. R., and Fowler, V. M. (2009) Tropomodulin1 is required for membrane skeleton organization and hexagonal geometry of fiber cells in the mouse lens. J. Cell Biol. 186,915-928
10. 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 (Pubitemid 17147271)
11. Sung, L. A., and Lin, J. J. (1994) Erythrocyte tropomodulin binds to the N-terminus of hTM5, a tropomyosin isoform encoded by the γ-tropomyosin gene. Biochem. Biophys. Res. Commun. 201, 627-634 (Pubitemid 24206918)
12. Vera, C., Sood, A., Gao, K. M., Yee, L. J., Lin, J. J., and Sung, L. A. (2000) Tropomodulin-binding site mapped to residues 7-14 at the N-terminal heptad repeats of tropomyosin isoform 5. Arch. Biochem. Biophys. 378, 16-24 (Pubitemid 30350459)
13. Gunning, P., O'Neill, G., and Hardeman, E. (2008) Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol. Rev. 88,1-35
14. 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
15. Greenfield, N. J., Kostyukova, A. S., and Hitchcock-DeGregori, S. E. (2005) Structure and tropomyosin binding properties of the N-terminal capping domain of tropomodulin 1. Biophys. J. 88, 372-383 (Pubitemid 40070683)
16. Kostyukova, A. S., Hitchcock-Degregori, S. E., and Greenfield, N. J. (2007) Molecular basis of tropomyosin binding to tropomodulin, an actin-capping protein. J. Mol. Biol. 372, 608-618 (Pubitemid 47313477)
17. Gunning, P. W., Schevzov, G., Kee, A. J., and Hardeman, E. C. (2005) Tropomyosin isoforms: divining rods for actin cytoskeleton function. Trends Cell Biol. 15, 333-341 (Pubitemid 40805330)
18. Weber, A., Pennise, C. R., Babcock, G. G., and Fowler, V. M. (1994) Tropomodulin caps the pointed ends of actin filaments. J. Cell Biol. 127,1627-1635 (Pubitemid 24380901)
19. Weber, A., Pennise, C. R., and Fowler, V. M. (1999) Tropomodulin increases the critical concentration of barbed end-capped actin filaments by converting ADP·Pi-actin to ADP-actin at all pointed filament ends. J. Biol.Chem. 274, 34637-34645 (Pubitemid 129509501)
20. Kostyukova, A. S., and Hitchcock-DeGregori, S. E. (2004) Effect of the structure of the N terminus of tropomyosin on tropomodulin function. J. Biol. Chem. 279, 5066-5071 (Pubitemid 38220522)
21. Kostyukova, A. S., Choy, A., and Rapp, B. A. (2006) Tropomodulin binds two tropomyosins: a novel model for actin filament capping. Biochemistry 45, 12068-12075 (Pubitemid 44497832)
22. Kostyukova, A. S., Rapp, B. A., Choy, A., Greenfield, N. J., and Hitchcock- DeGregori, S. E. (2005) Structural requirements of tropomodulin for tropomyosin binding and actin filament capping. Biochemistry 44,4905- 4910 (Pubitemid 40396768)
23. Moroz, N. A., Novak, S. M., Azevedo, R., Colpan, M., Uversky, V. N., Gregorio, C. C., and Kostyukova, A. S. (2013) Alteration of tropomyosinbinding properties of tropomodulin-1 affects its capping ability and localization in skeletal myocytes. J. Biol. Chem. 288, 4899-4907
24. Tsukada, T., Kotlyanskaya, L., Huynh, R., Desai, B., Novak, S. M., Kajava, A. V., Gregorio, C. C., and Kostyukova, A. S. (2011) Identification of residues within tropomodulin-1 responsible for its localization at the pointed ends of the actin filaments in cardiac myocytes. J. Biol. Chem. 286, 2194-2204
25. Kostyukova, A. S. (2008) Tropomodulin/tropomyosin interactions regulate actin pointed end dynamics. Adv. Exp. Med. Biol. 644, 283-292
26. Kostyukova, A. S. (2008) Tropomodulins and tropomodulin/tropomyosin interactions. Cell. Mol. Life Sci. 65, 563-569 (Pubitemid 351294812)
27. Babcock, G. G., and Fowler, V. M. (1994) Isoform-specific interaction of tropomodulin with skeletal muscle and erythrocyte tropomyosins. J. Biol. Chem. 269, 27510-27518 (Pubitemid 24346580)
28. Perrin, B. J., and Ervasti, J. M. (2010) The actin gene family: functionfollows isoform. Cytoskeleton 67, 630-634
29. Prins, K. W., Call, J. A., Lowe, D. A., and Ervasti, J. M. (2011) Quadriceps myopathy caused by skeletal muscle-specific ablation of βcyto-actin. J. Cell Sci. 124, 951-957
30. Pinder, J. C., and Gratzer, W. B. (1983) Structural and dynamic states ofactin in the erythrocyte. J. Cell Biol. 96, 768-775 (Pubitemid 13131339)
31. Pinder, J. C., Ungewickell, E., Bray, D., and Gratzer, W. B. (1978) The spectrin-actin complex and erythrocyte shape. J. Supramol. Struct. 8, 439-445 (Pubitemid 9053805)
32. Sung, L. A., Gao, K. M., Yee, L. J., Temm-Grove, C. J., Helfman, D. M., Lin, J. J., and Mehrpouryan, M. (2000) Tropomyosin isoform 5b is expressed in human erythrocytes: implications of tropomodulin-TM5 or tropomodulin-TM5b complexes in the protofilament and hexagonal organization of membrane skeletons. Blood 95, 1473-1480 (Pubitemid 30099863)
33. Ursitti, J. A., and Fowler, V. M. (1994) Immunolocalization of tropomodulin, tropomyosin and actin in spread human erythrocyte skeletons. J. Cell Sci. 107, 1633-1639 (Pubitemid 24198481)
34. Fowler, V. M., Davis, J. Q., and Bennett, V. (1985) Human erythrocyte myosin: identification and purification. J. Cell Biol. 100, 47-55
35. Fischer, R. S., Yarmola, E. G., Weber, K. L., Speicher, K. D., Speicher, D. W., Bubb, M. R., and Fowler, V. M. (2006) Tropomodulin 3 binds to actin monomers. J. Biol. Chem. 281, 36454-36465 (Pubitemid 46041379)
36. Yamashiro, S., Speicher, K. D., Speicher, D. W., and Fowler, V. M. (2010) Mammalian tropomodulins nucleate actin polymerization via their actin monomer binding and filament pointed end-capping activities. J. Biol.Chem. 285, 33265-33280
37. Gupton, S. L., Anderson, K. L., Kole, T. P., Fischer, R. S., Ponti, A., Hitchcock- DeGregori, S. E., Danuser, G., Fowler, V. M., Wirtz, D., Hanein, D., and Waterman-Storer, C. M. (2005) Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropomyosin. J. Cell Biol. 168, 619-631
38. DesMarais, V., Ichetovkin, I., Condeelis, J., and Hitchcock-DeGregori,S. E. (2002) Spatial regulation of actin dynamics: a tropomyosin-free, actin- rich compartment at the leading edge. J. Cell Sci. 115, 4649-4660 (Pubitemid 36007758)
39. Pardee, J. D., and Spudich, J. A. (1982) Purification of muscle actin. Methods Cell Biol. 24, 271-289 (Pubitemid 12055905)
40. Kouyama, T., and Mihashi, K. (1981) Fluorimetry study of N-(1-pyrenyl)iodoacetamide- labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur.J. Biochem. 114, 33-38 (Pubitemid 11101489)
41. Bergeron, S. E., Zhu, M., Thiem, S. M., Friderici, K. H., and Rubenstein,P. A. (2010) Ion-dependent polymerization differences between mammalianβ- and γ-nonmuscle actin isoforms. J. Biol. Chem. 285, 16087-16095
42. Smillie, L. B. (1982) Preparation and identification of α- and β-tropomyosins.Methods Enzymol. 85, 234-241
43. Maytum, R., Bathe, F., Konrad, M., and Geeves, M. A. (2004) Tropomyosin exon 6b is troponin-specific and required for correct acto-myosin regulation. J. Biol. Chem. 279, 18203-18209 (Pubitemid 38623233)
44. Hitchcock-DeGregori, S. E., Song, Y., and Moraczewska, J. (2001) Importance of internal regions and the overall length of tropomyosin for actin binding and regulatory function. Biochemistry 40, 2104-2112 (Pubitemid 32165681)
45. Gokhin, D. S., Lewis, R. A., McKeown, C. R., Nowak, R. B., Kim, N. E., Littlefield, R. S., Lieber, R. L., and Fowler, V. M. (2010) Tropomodulin isoforms regulate thin filament pointed-end capping and skeletal muscle physiology. J. Cell Biol. 189, 95-109
46. Ilkovski, B., Mokbel, N., Lewis, R. A., Walker, K., Nowak, K. J., Domazetovska, A., Laing, N. G., Fowler, V. M., North, K. N., and Cooper, S. T. (2008) Disease severity and thin filament regulation in M9R TPM3 nemaline myopathy. J. Neuropathol. Exp. Neurol. 67, 867-877
47. Laemmli, U. K. (1970) Cleavage of structural proteins during the assemblyof the head of bacteriophage T4. Nature 227, 680-685
48. Hitchcock-DeGregori, S. E., and Heald, R. W. (1987) Altered actin and troponin binding of amino-terminal variants of chicken striated muscleα-tropomyosin expressed in Escherichia coli. J. Biol. Chem. 262,9730-9735
49. Fowler, V. M., Greenfield, N. J., and Moyer, J. (2003) Tropomodulin contains two actin filament pointed end-capping domains. J. Biol. Chem. 278,40000-40009 (Pubitemid 37248565)
50. Young, C. L., Southwick, F. S., and Weber, A. (1990) Kinetics of the interactionof a 41-kilodalton macrophage capping protein with actin: promotion of nucleation during prolongation of the lag period. Biochemistry 29,2232-2240 (Pubitemid 20095465)
51. Safer, D. (1989) An electrophoretic procedure for detecting proteins that bind actin monomers. Anal. Biochem. 178, 32-37 (Pubitemid 19096000)
52. Wegner, A. (1979) Equilibrium of the actin-tropomyosin interaction. J.Mol. Biol. 131, 839-853 (Pubitemid 9254677)
53. Yang, Y. Z., Korn, E. D., and Eisenberg, E. (1979) Cooperative binding oftropomyosin to muscle and Acanthamoeba actin. J. Biol. Chem. 254,7137-7140 (Pubitemid 9243566)
54. Pittenger, M. F., and Helfman, D. M. (1992) In vitro and in vivo characterizationof four fibroblast tropomyosins produced in bacteria: TM-2, TM-3, TM-5a, and TM-5b are co-localized in interphase fibroblasts.J. Cell Biol. 118, 841-858
55. Temm-Grove, C. J., Guo, W., and Helfman, D. M. (1996) Low molecularweight rat fibroblast tropomyosin 5 (TM-5): cDNA cloning, actin-binding,localization, and coiled-coil interactions. Cell Motil. Cytoskeleton 33,223-240 (Pubitemid 26108414)
56. Maytum, R., Konrad, M., Lehrer, S. S., and Geeves, M. A. (2001) Regulatoryproperties of tropomyosin effects of length, isoform, and N-terminalsequence. Biochemistry 40, 7334-7341
57. Urbancikova, M., and Hitchcock-DeGregori, S. E. (1994) Requirement ofamino-terminal modification for striated muscleα-tropomyosin function.J. Biol. Chem. 269, 24310-24315
58. Skoumpla, K., Coulton, A. T., Lehman, W., Geeves, M. A., and Mulvihill,D. P. (2007) Acetylation regulates tropomyosin function in the fissionyeast Schizosaccharomyces pombe. J. Cell Sci. 120, 1635-1645 (Pubitemid 46831793)
59. Greenfield, N. J., and Fowler, V. M. (2002) Tropomyosin requires an intactN-terminal coiled coil to interact with tropomodulin. Biophys. J. 82,2580-2591 (Pubitemid 34441296)
60. Uversky, V. N., Shah, S. P., Gritsyna, Y., Hitchcock-DeGregori, S. E., andKostyukova, A. S. (2011) Systematic analysis of tropomodulin/tropomyosin interactions uncovers fine-tuned binding specificity of intrinsically disordered proteins. J. Mol. Recognit. 24, 647-655
61. Kostyukova, A., Maeda, K., Yamauchi, E., Krieger, I., and Maéda, Y. (2000) Domain structure of tropomodulin: distinct properties of the N-terminal and C-terminal halves. Eur. J. Biochem. 267, 6470-6475
62. Ochala, J., Gokhin, D. S., Iwamoto, H., and Fowler, V. M. (2014) Pointedend capping by tropomodulin modulates actomyosin crossbridge formation in skeletal muscle fibers. FASEB J. 28, 408-415
63. Carlier, M. F., Valentin-Ranc, C., Combeau, C., Fievez, S., and Pantoloni, D. (1994) Actin polymerization: regulation by divalent metal ion and nucleotide binding, ATP hydrolysis and binding of myosin. Adv. Exp. Med. Biol. 358, 71-81 (Pubitemid 24284913)
64. Haviv, L., Gillo, D., Backouche, F., and Bernheim-Groswasser, A. (2008) A cytoskeletal demolition worker: myosin II acts as an actin depolymerization agent. J. Mol. Biol. 375, 325-330
65. Almenar-Queralt, A., Gregorio, C. C., and Fowler, V. M. (1999) Tropomodulin assembles early in myofibrillogenesis in chick skeletal muscle: evidence that thin filaments rearrange to form striated myofibrils. J. Cell Sci. 112, 1111-1123 (Pubitemid 29218901)
66. Tzima, E., Trotter, P. J., Orchard, M. A., and Walker, J. H. (2000) Annexin V relocates to the platelet cytoskeleton upon activation and binds to a specific isoform of actin. Eur. J. Biochem. 267, 4720-4730
67. Larsson, H., and Lindberg, U. (1988) The effect of divalent cations on the interaction between calf spleen profilin and different actins. Biochim. Biophys. Acta 953, 95-105 (Pubitemid 18051929)
68. De La Cruz, E. M. (2005) Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. J. Mol. Biol. 346, 557-564
69. Weber, A., Nachmias, V. T., Pennise, C. R., Pring, M., and Safer, D. (1992) Interaction of thymosinβ4 with muscle and platelet actin: implications for actin sequestration in resting platelets. Biochemistry 31, 6179-6185
70. Namba, Y., Ito, M., Zu, Y., Shigesada, K., and Maruyama, K. (1992) Human T cell L-plastin bundles actin filaments in a calcium-dependent manner. J. Biochem. 112, 503-507
71. Yao, X., Cheng, L., and Forte, J. G. (1996) Biochemical characterization of ezrin-actin interaction. J. Biol. Chem. 271, 7224-7229 (Pubitemid 26104164)
72. Shuster, C. B., Lin, A. Y., Nayak, R., and Herman, I. M. (1996) βCap73: a novelβactin-specific binding protein. Cell Motil. Cytoskeleton 35, 175-187 (Pubitemid 26363864)
73. Bunnell, T. M., and Ervasti, J. M. (2011) Structural and functional properties of the actin gene family. Crit. Rev. Eukaryot. Gene. Expr. 21, 255-266
74. McKane, M., Wen, K. K., Boldogh, I. R., Ramcharan, S., Pon, L. A., and Rubenstein, P. A. (2005) A mammalian actin substitution in yeast actin (H372R) causes a suppressible mitochondria/vacuole phenotype. J. Biol. Chem. 280, 36494-36501
75. McKane, M., Wen, K. K., Meyer, A., and Rubenstein, P. A. (2006) Effect of the substitution of muscle actin-specific subdomain 1 and 2 residues in yeast actin on actin function. J. Biol. Chem. 281, 29916-29928 (Pubitemid 44537000)
76. Small, J. V., Stradal, T., Vignal, E., and Rottner, K. (2002) The lamellipodium: where motility begins. Trends Cell Biol. 12, 112-120 (Pubitemid 34164650)
77. Prasain, N., and Stevens, T. (2009) The actin cytoskeleton in endothelial cell phenotypes. Microvasc. Res. 77, 53-63