β- and γ-cytoplasmic actins display distinct distribution and functional diversity

Journal of Cell Science

Volumn 122, Issue 16, 2009, Pages 2980-2988

  Dugina, Vera ^a   Zwaenepoel, Ingrid ^b,c   Gabbiani, Giulio ^b   Clément, Sophie ^b   Chaponnier, Christine ^b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c CNRS   (France)

Author keywords

Actin isoforms; Actin network; Cytoskeleton

Indexed keywords

ACTIN; BETA ACTIN; GAMMA ACTIN; ISOPROTEIN; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL ADHESION; CELL CONTACT; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CONTROLLED STUDY; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; LAMELLAR BODY; LAMELLIPODIUM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRESS FIBER; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CELL COMPARTMENTALIZATION; CELL FRACTIONATION; CELL MOTION; CELL SHAPE; CHEMISTRY; CYTOLOGY; CYTOPLASM; DRUG ANTAGONISM; GENE SILENCING; METABOLISM; MITOSIS; MOLECULAR GENETICS; PROTEIN TRANSPORT; PSEUDOPODIUM; RAT; SWINE;

ACTINS; ACTOMYOSIN; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; CELL COMPARTMENTATION; CELL MOVEMENT; CELL SHAPE; CYTOPLASM; EPITHELIAL CELLS; FIBROBLASTS; GENE SILENCING; HUMANS; MITOSIS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MONOMERIC GTP-BINDING PROTEINS; PROTEIN TRANSPORT; PSEUDOPODIA; RATS; SUBCELLULAR FRACTIONS; SUS SCROFA;

EID: 70350028849     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.041970     Document Type: Article

References (63)

1. Abercrombie, M., Heaysman, J. E. and Pegrum, S. M. (1970). The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp. Cell Res. 59, 393-398.
2. Abercrombie, M., Heaysman, J. E. and Pegrum, S. M. (1971). The locomotion of fibroblasts in culture. IV. Electron microscopy of the leading lamella. Exp. Cell Res. 67, 359-367.
3. Antecol, M. H., Darveau, A., Sonenberg, N. and Mukherjee, B. B. (1986). Altered biochemical properties of actin in normal skin fibroblasts from individuals predisposed to dominantly inherited cancers. Cancer Res. 46, 1867-1873.
4. Bassell, G. J., Zhang, H., Byrd, A. L., Femino, A. M., Singer, R. H., Taneja, K. L., Lifshitz, L. M., Herman, I. M. and Kosik, K. S. (1998). Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18, 251-265.
5. Chaponnier, C. and Gabbiani, G. (2004). Pathological situations characterized by altered actin isoform expression. J. Pathol. 204, 386-395.
6. Chaponnier, C., Goethals, M., Janmey, P. A., Gabbiani, F., Gabbiani, G. and Vandekerckhove, J. (1995). The specific NH2-terminal sequence Ac-EEED of alpha-smooth muscle actin plays a role in polymerization in vitro and in vivo. J. Cell Biol. 130, 887-895.
7. Chhabra, E. S. and Higgs, H. N. (2007). The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9, 1110-1121.
8. Clement, S., Chaponnier, C. and Gabbiani, G. (1999). A subpopulation of cardiomyocytes expressing alpha-skeletal actin is identified by a specific polyclonal antibody. Circ. Res. 85, e51-e58.
9. Clement, S., Hinz, B., Dugina, V., Gabbiani, G. and Chaponnier, C. (2005). The Nterminal Ac-EEED sequence plays a role in alpha-smooth-muscle actin incorporation into stress fibers. J. Cell Sci. 118, 1395-1404.
10. Condeelis, J. and Singer, R. H. (2005). How and why does beta-actin mRNA target? Biol. Cell 97, 97-110.
11. Desmouliere, A., Geinoz, A., Gabbiani, F. and Gabbiani, G. (1993). Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol. 122, 103-111.
12. Even-Ram, S., Doyle, A. D., Conti, M. A., Matsumoto, K., Adelstein, R. S. and Yamada, K. M. (2007). Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat. Cell Biol. 9, 299-309.
13. Fenteany, G., Janmey, P. A. and Stossel, T. P. (2000). Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr. Biol. 10, 831-838.
14. Gao, Y., Dickerson, J. B., Guo, F., Zheng, J. and Zheng, Y. (2004). Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA 101, 7618-7623.
15. Gimona, M., Vandekerckhove, J., Goethals, M., Herzog, M., Lando, Z. and Small, J. V. (1994). Beta-actin specific monoclonal antibody. Cell Motil. Cytoskeleton 27, 108-116.
16. Goeckeler, Z. M., Bridgman, P. C. and Wysolmerski, R. B. (2008). Nonmuscle myosin II is responsible for maintaining endothelial cell basal tone and stress fiber integrity. Am. J. Physiol. Cell Physiol. 295, C994-C1006.
17. Hanft, L. M., Rybakova, I. N., Patel, J. R., Rafael-Fortney, J. A. and Ervasti, J. M. (2006). Cytoplasmic gamma-actin contributes to a compensatory remodeling response in dystrophin-deficient muscle. Proc. Natl. Acad. Sci. USA 103, 5385-5390.
18. Harborth, J., Elbashir, S. M., Bechert, K., Tuschl, T. and Weber, K. (2001). Identification of essential genes in cultured mammalian cells using small interfering RNAs. J. Cell Sci. 114, 4557-4565.
19. Heath, J. P. and Holifield, B. F. (1993). On the mechanisms of cortical actin flow and its role in cytoskeletal organisation of fibroblasts. Symp. Soc. Exp. Biol. 47, 35-56.
20. Hill, M. A. and Gunning, P. (1993). Beta and gamma actin mRNAs are differentially located within myoblasts. J. Cell Biol. 122, 825-832.
21. Hinz, B., Alt, W., Johnen, C., Herzog, V. and Kaiser, H. W. (1999). Quantifying lamella dynamics of cultured cells by SACED, a new computer-assisted motion analysis. Exp. Cell Res. 251, 234-243.
22. Hinz, B., Gabbiani, G. and Chaponnier, C. (2002). The NH2-terminal peptide of alpha-smooth muscle actin inhibits force generation by the myofibroblast in vitro and in vivo. J. Cell Biol. 157, 657-663.
23. Hofer, D., Ness, W. and Drenckhahn, D. (1997). Sorting of actin isoforms in chicken auditory hair cells. J. Cell Sci. 110, 765-770.
24. Hoock, T. C., Newcomb, P. M. and Herman, I. M. (1991). Beta actin and its mRNA are localized at the plasma membrane and the regions of moving cytoplasm during the cellular response to injury. J. Cell Biol. 112, 653-664.
25. Kilpatrick, K. E., Wring, S. A., Walker, D. H., Macklin, M. D., Payne, J. A., Su, J. L., Champion, B. R., Caterson, B. and McIntyre, G. D. (1997). Rapid development of affinity matured monoclonal antibodies using RIMMS. Hybridoma 16, 381-389.
26. Kislauskis, E. H., Zhu, X. and Singer, R. H. (1994). Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J. Cell Biol. 127, 441-451.
27. Kovacs, M., Toth, J., Hetenyi, C., Malnasi-Csizmadia, A. and Sellers, J. R. (2004). Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279, 35557-35563.
28. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
29. Lambrechts, A., Van Troys, M. and Ampe, C. (2004). The actin cytoskeleton in normal and pathological cell motility. Int. J. Biochem. Cell Biol. 36, 1890-1909.
30. Latham, V. M., Yu, E. H., Tullio, A. N., Adelstein, R. S. and Singer, R. H. (2001). A Rho-dependent signaling pathway operating through myosin localizes beta-actin mRNA in fibroblasts. Curr. Biol. 11, 1010-1016.
31. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
32. Lunn, J. A., Wong, H., Rozengurt, E. and Walsh, J. H. (2000). Requirement of cortical actin organization for bombesin, endothelin, and EGF receptor internalization. Am. J. Physiol. Cell Physiol. 279, C2019-C2027.
33. Nelson, W. J. (2003). Adaptation of core mechanisms to generate cell polarity. Nature 422, 766-774.
34. Otey, C. A., Kalnoski, M. H., Lessard, J. L. and Bulinski, J. C. (1986). Immunolocalization of the gamma isoform of nonmuscle actin in cultured cells. J. Cell Biol. 102, 1726-1737.
35. Pawlak, G. and Helfman, D. M. (2001). Cytoskeletal changes in cell transformation and tumorigenesis. Curr. Opin. Genet. Dev. 11, 41-47.
36. Pellegrin, S. and Mellor, H. (2007). Actin stress fibres. J. Cell Sci. 120, 3491-3499.
37. Peterson, J. R., Bickford, L. C., Morgan, D., Kim, A. S., Ouerfelli, O., Kirschner, M. W. and Rosen, M. K. (2004). Chemical inhibition of N-WASP by stabilization of a native autoinhibited conformation. Nat. Struct. Mol. Biol. 11, 747-755.
38. Pollack, R., Osborn, M. and Weber, K. (1975). Patterns of organization of actin and myosin in normal and transformed cultured cells. Proc. Natl. Acad. Sci. USA 72, 994-998.
39. Revenu, C., Athman, R., Robine, S. and Louvard, D. (2004). The co-workers of actin filaments: from cell structures to signals. Nat. Rev. Mol. Cell Biol. 5, 635-646.
40. Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
41. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
42. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
43. Rubin, R. W., Warren, R. H., Lukeman, D. S. and Clements, E. (1978). Actin content and organization in normal and transformed cells in culture. J. Cell Biol. 78, 28-35.
44. Sandquist, J. C., Swenson, K. I., Demali, K. A., Burridge, K. and Means, A. R. (2006). Rho kinase differentially regulates phosphorylation of nonmuscle myosin II isoforms A and B during cell rounding and migration. J. Biol. Chem. 281, 35873-35883.
45. Sarmiento, C., Wang, W., Dovas, A., Yamaguchi, H., Sidani, M., El-Sibai, M., Desmarais, V., Holman, H. A., Kitchen, S., Backer, J. M. et al. (2008). WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J. Cell Biol. 180, 1245-1260.
46. Schevzov, G., Vrhovski, B., Bryce, N. S., Elmir, S., Qiu, M. R., O'Neill, G. M., Yang, N., Verrills, N. M., Kavallaris, M. and Gunning, P. W. (2005). Tissue-specific tropomyosin isoform composition. J. Histochem. Cytochem. 53, 557-570.
47. Shawlot, W., Deng, J. M., Fohn, L. E. and Behringer, R. R. (1998). Restricted beta-galactosidase expression of a hygromycin-lacZ gene targeted to the beta-actin locus and embryonic lethality of beta-actin mutant mice. Transgenic Res. 7, 95-103.
48. Skalli, O., Ropraz, P., Trzeciak, A., Benzonana, G., Gillessen, D. and Gabbiani, G. (1986). A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation. J. Cell Biol. 103, 2787-2796.
49. Skalli, O., Vandekerckhove, J. and Gabbiani, G. (1987). Actin-isoform pattern as a marker of normal or pathological smooth-muscle and fibroblastic tissues. Differentiation 33, 232-238.
50. Small, J. V. (1981). Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks. J. Cell Biol. 91, 695-705.
51. Small, J. V., Rottner, K., Kaverina, I. and Anderson, K. I. (1998). Assembling an actin cytoskeleton for cell attachment and movement. Biochim. Biophys. Acta 1404, 271-281.
52. Sonnemann, K. J., Fitzsimons, D. P., Patel, J. R., Liu, Y., Schneider, M. F., Moss, R. L. and Ervasti, J. M. (2006). Cytoplasmic gamma-actin is not required for skeletal muscle development but its absence leads to a progressive myopathy. Dev. Cell 11, 387-397.
53. Spector, I., Shochet, N. R., Blasberger, D. and Kashman, Y. (1989). Latrunculins-novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil. Cytoskeleton 13, 127-144.
54. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R. and Mitchison, T. J. (2003). Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299, 1743-1747.
55. Svitkina, T. M. and Borisy, G. G. (1999). Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145, 1009-1026.
56. Svitkina, T. M., Verkhovsky, A. B. and Borisy, G. G. (1995). Improved procedures for electron microscopic visualization of the cytoskeleton of cultured cells. J. Struct. Biol. 115, 290-303.
57. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M. et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
58. Vandekerckhove, J. and Weber, K. (1978). At least six different actins are expressed in a higher mammal: an analysis based on the amino acid sequence of the amino-terminal tryptic peptide. J. Mol. Biol. 126, 783-802.
59. Verderame, M., Alcorta, D., Egnor, M., Smith, K. and Pollack, R. (1980). Cytoskeletal F-actin patterns quantitated with fluorescein isothiocyanate-phalloidin in normal and transformed cells. Proc. Natl. Acad. Sci. USA 77, 6624-6628.
60. Watanabe, H., Kislauskis, E. H., Mackay, C. A., Mason-Savas, A. and Marks, S. C., Jr (1998). Actin mRNA isoforms are differentially sorted in normal osteoblasts and sorting is altered in osteoblasts from a skeletal mutation in the rat. J. Cell Sci. 111, 1287-1292.
61. Winder, S. J. and Ayscough, K. R. (2005). Actin-binding proteins. J. Cell Sci. 118, 651-654.
62. Yao, X., Chaponnier, C., Gabbiani, G. and Forte, J. G. (1995). Polarized distribution of actin isoforms in gastric parietal cells. Mol. Biol. Cell 6, 541-557.
63. Yeaman, C., Grindstaff, K. K. and Nelson, W. J. (1999). New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol. Rev. 79, 73-98.