Inhibition of CapZ during myofibrillogenesis alters assembly of actin filaments

doi:10.1083/jcb.128.1.61

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Inhibition of CapZ during myofibrillogenesis alters assembly of actin filaments

DA Schafer, C Hug and JA Cooper
Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, Missouri 63110.

The actin filaments of myofibrils are highly organized; they are of a uniform length and polarity and are situated in the sarcomere in an aligned array. We hypothesized that the barbed-end actin-binding protein, CapZ, directs the process of actin filament assembly during myofibrillogenesis. We tested this hypothesis by inhibiting the actin- binding activity of CapZ in developing myotubes in culture using two different methods. First, injection of a monoclonal antibody that prevents the interaction of CapZ and actin disrupts the non-striated bundles of actin filaments formed during the early stages of myofibril formation in skeletal myotubes in culture. The antibody, when injected at concentrations lower than that required for disrupting the actin filaments, binds at nascent Z-disks. Since the interaction of CapZ and the monoclonal antibody are mutually exclusive, this result indicates that CapZ binds nascent Z-disks independent of an interaction with actin filaments. In a second approach, expression in myotubes of a mutant form of CapZ that does not bind actin results in a delay in the appearance of actin in a striated pattern in myofibrils. The organization of alpha-actinin at Z-disks also is delayed, but the organization of titin and myosin in sarcomeres is not significantly altered. We conclude that the interaction of CapZ and actin is important for the organization of actin filaments of the sarcomere.
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Schafer, D. A., Welch, M. D., Machesky, L. M., Bridgman, P. C., Meyer, S. M., Cooper, J. A. (1998). Visualization and Molecular Analysis of Actin Assembly in Living Cells. JCB 143: 1919-1930 [Abstract] [Full Text]
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Sussman, M. A., Baque, S., Uhm, C.-S., Daniels, M. P., Price, R. L., Simpson, D., Terracio, L., Kedes, L. (1998). Altered Expression of Tropomodulin in Cardiomyocytes Disrupts the Sarcomeric Structure of Myofibrils. Circ. Res. 82: 94-105 [Abstract] [Full Text]
Kuhlman, P. A., Hughes, C. A., Bennett, V., Fowler, V. M. (1996). A New Function for Adducin. J. Biol. Chem. 271: 7986-7991 [Abstract] [Full Text]
Mangan, M., Olmsted, J. (1996). A muscle-specific variant of microtubule-associated protein 4 (MAP4) is required in myogenesis. Development 122: 771-781 [Abstract]
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