Journal of Muscle Research & Cell Motility

, Volume 14, Issue 2, pp 195–204 | Cite as

Colocalization of ADF and cofilin in intranuclear actin rods of cultured muscle cells

  • Shoichiro Ono
  • Hiroshi Abe
  • Rie Nagaoka
  • Takashi Obinata
Papers

Summary

Immunofluorescence microscopy revealed that two actin-binding proteins of low molecular weight with different functional activity. ADF and cofilin, are transported into nuclei of cultured myogenic cells to form rod structures there together with actin, when the cells were incubated in medium containing dimethylsulfoxide. In most cases, ADF and cofilin colocalized in the same nuclear actin rods, but ADF appeared to predominate in mononucleated cells, while cofilin was present in multinucleated myotubes. In some mononucleated cells, the nuclear actin rods were composed of ADF and actin but devoid of cofilin. An ADF homologue in mammals, destrin, was also translocated into nuclear actin rods under similar conditions. As a nuclear transport signal sequence exists in cofilin and ADF but not in actin, ADF and/or cofilin may be responsible for the nuclear import of actin in myogenic cells under certain conditions.

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References

  1. ABE, H. & OBINATA, T. (1989) An actin-depolymerizing protein in embryonic chicken skeletal muscle: Purification and characterization. J. Biochem. (Tokyo) 106: 172–80.Google Scholar
  2. ABE, H., OHSHIMA, S. & OBINATA, T. (1989) A cofilin-like protein is involved in the regulation of actin assembly in developing skeletal muscle. J. Biochem. (Tokyo) 106, 696–702.Google Scholar
  3. ABE, H., ENDO, T., YAMAMOTO, K. & OBINATA, T. (1990) Sequence of cDNAs encoding actin depolymerizing factor and cofilin of embryonic chicken skeletal muscle: two functionally distinct actin-regulatory proteins exhibit high structural homology. Biochemistry 29, 7420–5.Google Scholar
  4. ABE, H., NAGAOKA, R. & OBINATA, T. (1991) Nuclear transport of cofilin in cultured muscle cells. Zool. Sci. (Tokyo) 8, 1128.Google Scholar
  5. ADAMS, M. E., MINAMIDE, L. S., DEUSTER, G. L. & BAMBURG, J. R. (1990) Nucleotide sequence and expression of a cDNA encoding chick brain actin depolymerizing factor. Biochemistry 29, 7413–19.Google Scholar
  6. BAMBURG, J. R., HARRIS, H. E. & WEEDS, A. G. (1980) Partial purification and characterization of an actin depolymerizing factor from brain. FEBS Lett. 121, 178–81.Google Scholar
  7. BAMBURG, J. R. & BRAY, D. (1987) Distribution and cellular localization of actin depolymerizing factor. J. Cell Biol. 105, 2817–25.Google Scholar
  8. COOPER, J. A., BLUM, J. D., WILLIAMS, R. C.Jr & POLLARD, T. D. (1986) Purification and characterization of actophorin, a new 15 000-dalton actin-binding protein from Acanthamoeba castellanii. J. Biol. Chem. 261, 477–85.Google Scholar
  9. DE, BLAS, A. L. & CHERWINSKI, H. M. (1983) Detection of antigens on nitrocellulose paper immunoblots with monoclonal antibodies. Anal. Biochem. 133, 214–19.Google Scholar
  10. FUKUI, Y. (1978) Intranuclear actin bundles induced by dimethyl sulfoxide in interphase nucleus of Dictyostelium. J. Cell Biol. 76, 146–57.Google Scholar
  11. FUKUI, Y. & KATSUMARU, H. (1980) Dynamics of nuclear actin bundle induction by dimethyl sulfoxide and factors affecting its development. J. Cell Biol. 84, 131–40.Google Scholar
  12. GRAESSER, F. A., SCHIEDTMANN, K. H., TUAZON, P. T., TRAIGH, J. A. & WALTER, G. (1988) In vitro phosphorylation of SV40 T antigen. Virology 165, 13–22.Google Scholar
  13. II, I., KIMURA, I. & OZAWA, E. (1982) A myotropic protein from chick embryo extract; first purification, identity to transferrin, and indispensability for avian myogenesis. Dev. Biol. 94, 366–77.Google Scholar
  14. IIDA, K., IIDA, H. & YAHARA, I. (1986) Heat shock induction of intranuclear actin rods in cultured mammalian cells. Exp. Cell Res. 165, 207–15.Google Scholar
  15. IIDA, K., MATSUMOTO, S. & YAHARA, I. (1992) The KKRKK sequence is involved in heat shock-induced nuclear translocation of the 18-kDa actin-binding protein, cofilin. Cell Struct. Funct. 17, 39–46.Google Scholar
  16. JANS, D. A., ACKERMANN, M. J., BISCHOFF, J. R., BEACH, D. H. & PETERS, R. (1991) p34çdc2-mediated phosphorylation at T124 inhibits nuclear import of SV-40 T antigen proteins. J. Cell Biol. 115, 1203–12.Google Scholar
  17. KALDERON, D., ROBERTS, B. L., RICHARDSON, W. D., & SMITH, A. E. (1984) A short amino acid sequence able to specify nuclear location. Cell 39, 499–509.Google Scholar
  18. KENNELLY, P. J. & KREBS, E. G. (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266, 15555–8.Google Scholar
  19. LAEMMLI, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.Google Scholar
  20. LANFORD, R. E. & BUTEL, J. S. (1984) Construction and characterization of an SV40 mutant defective in nuclear transport of T antigen. Cell 37, 801–13.Google Scholar
  21. MABUCHI, I. (1983) An actin-depolymerizing protein (depactin) from starfish oocyte: Properties and interaction with actin. J. Cell Biol. 97, 1612–21.Google Scholar
  22. MACIVER, S. K., AMPE, C., RIMM, D. L., ALMO, S. C., Van Damme, J., VANDEKERCKHOVE, J. S. & POLLARD, T. D. (1990) The cDNA sequence of actophorin, an actin severing protein from Acanthamoeba. J. Cell Biol. 111, 28a.Google Scholar
  23. MAEKAWA, S., NISHIDA, E., OHTA, Y. & SAKAI, H. (1984) Isolation of low molecular weight actin-binding proteins from porcine brain. J. Biochem. (Tokyo) 95, 377–85.Google Scholar
  24. MATSUZAKI, F., MATSUMOTO, S., YAHARA, I., YONEZAWA, N., NISHIDA, E. & SAKAI, H. (1988) Cloning and characterization of porcine brain cofilin cDNA. Cofilin contains the nuclear transport signal sequence. J. Biol. Chem. 263, 11564–8.Google Scholar
  25. MORGAN, T. E. (1990) Regulation of the amount and activity of actin depolymerizing factor in developing brain and muscle. Ph.D. Thesis, Colorado State University, Fort Collins, CO.Google Scholar
  26. MORIYAMA, K., NISHIDA, E., YONEZAWA, N., SAKAI, H., MATSUMOTO, S., IIDA, K., & YAHARA, I. (1990) Destrin, a mammalian actin-depolymerizing protein, is closely related to cofilin. J. Biol. Chem. 265, 5768–73.Google Scholar
  27. NISHIDA, E., MAEKAWA, S. & SAKAI, H. (1984) Cofilin, a protein in porcine brain that binds to actin filaments and inhibits their interaction with myosin and tropomyosin. Biochemistry 23, 5307–13.Google Scholar
  28. NISHIDA, E., MUNEYUKI, E., MAEKAWA, S., OHTA, Y. & SAKAI, H. (1985) An actin-depolymerizing protein (destrin) from porcine kidney. Its action on F-actin containing or lacking tropomyosin. Biochemistry 24, 6624–30.Google Scholar
  29. NISHIDA, E., IIDA, K., YONEZAWA, N., KOYASU, S., YAHARA, I. & SAKAI, H. (1987) Cofilin is a component of intranuclear and cytoplasmic actin rods induced in cultured cells. Proc. Natl. Acad. Sci. USA 84, 5262–6.Google Scholar
  30. OBINATA, T., OOI, A. & TAKANO-OHMURO, H. (1983) Myosin and actin from ascidian smooth muscle and their interaction. Comp. Biochem. Physiol. 76B, 437–42.Google Scholar
  31. OBINATA, T. & ABE, H. (1991) Regulation of actin assembly in embryonic chicken skeletal muscle by three different actin-binding proteins. In Frontiers in Muscle Research (edited by Ozawa, E., Masaki, T. & Nabeshima, Y.) pp. 325–47. Amsterdam, Elsevier Science Publishers.Google Scholar
  32. OSBORN, M. & WEBER, K. (1980a) Dimethylsulfoxide and the inophore A23187 affect the arrangement of actin and induce nuclear actin paracrystals in PtK2 cells. Exp. Cell Res. 129, 103–14.Google Scholar
  33. OSBORN, M. & WEBER, K. (1980b) Damage of cellular functions by trifluoperazine, a calmodulin-specific drug. Exp. Cell Res. 130, 484–8.Google Scholar
  34. OSBORN, M. & WEBER, K. (1984) Actin paracrystal induction by forskolin and by db-AMP in CHO cells. Exp. Cell Res. 150, 408–18.Google Scholar
  35. POLLARD, T. D. & COOPER, J. A. (1986) Actin and actin binding proteins. A critical evaluation of mechanisms and functions. Annu. Rev. Biochem. 55, 987–1035.Google Scholar
  36. RIHS, H-P. & PETERS, R. (1989) Nuclear transport kinetics depend on phosphorylation-site-containing sequences flanking the karyophilic signal of the simian virus 40 T-antigen. EMBO J. 8, 1479–84.Google Scholar
  37. SANGER, J. W., SANGER, J. M., KREIS, T. E. & JOCKUSCH, B. M. (1980) Reversible translocation of cytoplasmic actin into the nucleus caused by dimethylsulfoxide. Proc. Natl. Acad. Sci. USA 77, 5268–72.Google Scholar
  38. TAKAGI, T., KONISHI, K. & MABUCHI, I. (1988) Amino acid sequence of starfish oocyte depactin. J. Biol. Chem. 263, 3097–102.Google Scholar
  39. TOWBIN, H. T., STAHELIN, H. M. & GORDON, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4.Google Scholar
  40. WAY, M. & WEEDS, A. (1990) Cytoskeletal ups and downs. Nature 344, 292–4.Google Scholar
  41. WELCH, W. J. & SUHAN, J. P. (1985) Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibloblasts after heat-shock treatment. J. Cell Biol. 101, 1198–211.Google Scholar
  42. YAHARA, I., HARADA, F., SEKITA, S., YOSHIHIRA, K. & NATORI, S. (1982) Correlation between effects of 24 different cytochalasins on cellular structures and cellular events and those on actin in vitro. J. Cell Biol. 92, 69–78.Google Scholar
  43. YONEZAWA, N., NISHIDA, E. & SAKAI, H. (1985) pH control of actin polymerization by cofilin. J. Biol. Chem. 260, 14410–12.Google Scholar
  44. YONEZAWA, N., NISHIDA, E., KOYASU, S., MAEKAWA, S., OHTA, Y., YAHARA, I. & SAKAI, H. (1987) Distribution among tissues and intracellular localization of cofilin, a 21 kDa actin-binding protein. Cell Struct. Funct. 2, 443–52.Google Scholar
  45. YONEZAWA, N., NISHIDA, E., IIDA, K., KUMAGAI, H., YAHARA, I. & SAKAI, H. (1991) Inhibition of actin polymerization by a synthetic dodecapeptide patterned on the sequence around the actin-binding site of cofilin. J. Biol. Chem. 266, 10485–9.Google Scholar

Copyright information

© Chapman & Hall 1993

Authors and Affiliations

  • Shoichiro Ono
    • 1
  • Hiroshi Abe
    • 1
  • Rie Nagaoka
    • 1
  • Takashi Obinata
    • 1
  1. 1.Department of Biology, Faculty of ScienceChiba UniversityChibaJapan

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