Slow axonal transport of soluble actin with actin depolymerizing factor, cofilin, and profilin suggests actin moves in an unassembled form

Journal of Neurochemistry

Volumn 67, Issue 3, 1996, Pages 1225-1234

  Mills, Roland G ^a   Minamide, Laurie S ^a,b   Yuan, Aidong ^a   Bamburg, James R ^a,b   Bray, John J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Actin; Actin depolymerizing factor; Axons; Cofilin; Profilin; Slow axonal transport; Specific activity

Indexed keywords

ACTIN; COFILIN; METHIONINE; PROFILIN; SULFUR 35;

ACTIN POLYMERIZATION; AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; DEPOLYMERIZATION; FLUOROGRAPHY; IMMUNOBLOTTING; MOTONEURON; NERVE FIBER TRANSPORT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SCIATIC NERVE;

ANIMALIA; GALLUS GALLUS;

EID: 0029799252     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1996.67031225.x     Document Type: Article

References (62)

1. Abe H., Ohshima S., and 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.
2. Abe H., Endo T., Yamamoto K., and 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, 7420-7425.
3. Adams M. E., Minamide L. S., Duester G., and Bamburg J. R. (1990) Nucleotide sequence and expression of a cDNA encoding chick brain actin depolymerizing factor. Biochemistry 29, 7414-7420.
4. Agnew B. J., Minamide L.S., and Bamburg J. R. (1995) Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J. Biol. Chem. 270, 17582-17587.
5. Baitinger C. and Willard M. (1987) Axonal transport of synapsin 1-like proteins in rabbit retinal ganglion cells. J. Neurosci. 7, 3723-3735.
6. Bamburg J. R. (1988) The axonal cytoskeleton: stationary or moving matrix? Trends Neurosci. 11, 248-249.
7. Bamburg J. R. and Bernstein B. W. (1991) Actin and actin-binding proteins in neurons, in The Neuronal Cytoskeleton (Burgoyne R., ed), pp. 121-160. John Wiley and Sons, New York.
8. Bamburg J. R. and Bray D. (1987) Distribution and cellular localization of actin depolymerizing factor. J. Cell Biol. 105, 2817-2825.
9. Bamburg J. R., Minamide L. S., Morgan T. E., Hayden S. M., Guilliano K. A., and Koffer A. (1991) Purification and characterization of low-molecular weight actin-depolarizing proteins from brain and cultured cells. Methods Enzymol. 196, 125-140.
10. Baorto D. M., Mellado W., and Shelanski M. L. (1992) Astrocyte process growth induction by actin breakdown. J. Cell Biol. 117, 357-367.
11. Black M. M. and Lasek R. J. (1979) Axonal transport of actin: slow component b is the principal source of actin for the axon. Brain Res. 171, 401-413.
12. Black M. M., Chestnut M. H., Pleasure I. T., and Keen J. H. (1991) Stable clathrin: uncoating protein (hsc70) complexes in intact neurons and their axonal transport. J. Neurosci. 11, 1163-1172.
13. Bray J. J., Fernyhough P., Bamburg J. R., and Bray D. (1992) Actin depolymerizing factor is a component of slow axonal transport. J. Neurochem. 58, 2081-2087.
14. Clark S. E., Moss D. J., and Bray D. (1983) Actin polymerization and synthesis in cultured neurones. Exp. Cell Res. 147, 303-314.
15. 2+. Biochem. J. 301, 41-47.
16. Fath K. R. and Lasek R. J. (1988) Two classes of actin microfilaments are associated with the inner cytoskeleton of axons. J. Cell Biol. 107, 613-621.
17. Filliatreau G., Denoulet P., de Nechaud B., and Di Giamberardino L. (1988) Stable and metastable cytoskeletal polymers carried by slow axonal transport. J. Neurosci. 8, 2227-2233.
18. Gandal C. P. (1969) Avian anesthesia. Fed. Proc. 28, 1533-1534.
19. Gao Y., Thomas J. O., Chow R. L., Lee G.-H., and Cowan N.J. (1992) A cytoplasmic chaperonin that catalyzes beta-actin folding. Cell 69, 1043-1050.
20. Harris H. E. and Weeds A. G. (1978) Platelet actin: sub-cellular distribution and association with profilin. FEBS Lett. 90, 84-88.
21. Hawkins M., Pope B., Maciver S. K., and Weeds A. G. (1993) Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry 32, 9985-9993.
22. Hayden S. M., Miller P. S., Brauweiler A., and Bamburg J. R. (1993) Analysis of the interactions of actin depolymerizing factor with G- and F-actin. Biochemistry 32, 9994-10004.
23. Heacock C. S. and Bamburg J. R. (1983) The quantitation of G-and F-actin in cultured cells. Anal. Biochem. 135, 22-36.
24. Hirokawa N. (1993) Axonal transport and the cytoskeleton. Curr. Opin. Neurobiol. 3, 724-731.
25. Joshi H. C. and Baas P. W. (1993) A new perspective on microtubules and axonal growth. J. Cell Biol. 121, 1191-1196.
26. Kanamori T., Hayakawa T., Suzuki M., and Titani K. (1995) Identification of two 17-kDa rat parotid gland phosphoproteins, subjects for dephosphorylation upon beta-adrenergic stimulation, as destrin- and cofilin-like proteins. J. Biol. Chem. 270, 8061-8067.
27. Kuznetsov S. A., Langford G. M., and Weiss D. G. (1992) Actin-dependent organelle movement in squid axoplasm. Nature 356, 722-725.
28. 4. Nature 227, 680-685.
29. Lasek R. J. (1986) Polymer sliding in axons. J. Cell Sci. Suppl. 5, 161-179.
30. Lasek R. J., Garner J. A., and Brady S. T. (1984) Axonal transport of the cytoplasmic matrix. J. Cell Biol. 99 (Suppl.), 212s-221s.
31. Maekawa S., Nishida E., Ohta Y., and Sakai H. (1984) Isolation of low molecular weight actin-binding proteins from porcine brain. J. Biochem. (Tokyo) 95, 377-385.
32. Markey F., Persson T., and Lindberg U. (1981) Characterization of platelet extracts before and after stimulation with respect to the possible role of profilin as microfilament precursor. Cell 23, 145-153.
33. MeQuarrie I. G., Brady S. T., and Lasek R. J. (1986) Diversity in the axonal transport of structural proteins: major differences between optic and spinal axons in the rat. J. Neurosci. 6, 1593-1605.
34. Minamide L. S. and Bamburg J. R. (1990) A filter paper dye-binding assay for quantitative determination of protein without interference from reducing agents or detergents. Anal. Biochem. 190, 66-70.
35. Moon A. and Drubin D. (1995) The ADF/cofilin proteins. Stimulus-responsive modulators of actin dynamics. Mol. Biol. Cell 6, 1423-1431.
36. Morgan T. E., Lockerbie R. O., Minamide L. S., Browning M. D., and Bamburg J. R. (1993) Isolation and characterization of a regulated form of actin depolymerizing factor. J. Cell Biol. 122, 623-633.
37. Moriyama K., Iida K., and Yahara I. (1996) Phosphorylalion of Ser-3 of cofilin regulates its essential function on actin. Genes Cells 1, 73-86.
38. Morris J. R. and Lasek R. J. (1984) Monomer-polymer equilibria in the axon: direct measurement of tubulin and actin as polymer and monomer in axoplasm. J. Cell Biol. 98, 2064-2076.
39. Morrissey J. H. (1981) Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal. Biochem. 117, 307-310.
40. Nishida E., Maekawa S., Muncyuki E., and Sakai H. (1984) Action of a 19K protein from porcine brain on actin polymerization: a new functional class of actin-binding proteins. J. Biochem. (Tokyo) 95, 387-398.
41. Nixon R. A. (1992) Slow axonal transport Curr. Opin. Cell Biol. 4, 8-14.
42. Oblinger M. M., Brady S. T., McQuarrie I. G., and Lasek J. (1987) Cytotopic differences in the protein composition of the axonally transported cytoskeleton in mammalian neurons. J. Neurosci. 7, 453-462.
43. O'Farrell P. H. (1975) High resolution two-dimensional eleclrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
44. O'Farrell P. Z., Goodman H. M., and O'Farrell P. H. (1977) High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 12, 1133-1142.
45. Pardee J. D. and Bamburg J. R. (1979) Actin from embryonic chick brain. Isolation in high yield and comparison of biochemical properties with chicken muscle actin. Biochemistry 18, 2245-2252.
46. Roobol A., Holmes F. E., Hayes N. V. L., Baines A. J., and Carden M. J. (1995) Cytoplasmic chaperonin complexes enter neuntes developing in vitro and differ in subunit composition within single cells. J. Cell Sci. 108, 1477-1488.
47. Sabry J., O'Conner T. P., and Kirschner M. W. (1995) Axonal transport of tubulin in Ti1 pioneer neurons in situ. Neuron 14, 1247-1256.
48. Safer D. and Nachmias V. T. (1994) Beta thymosins as actin binding peptides. Bioessays 16, 473-479.
49. Saito T., Lamy F., Roger P. P., Lecocq R., and Dumont J. (1994) Characterization and identification as cofilin and destrin of two thyrotropin- and phorbol ester-regulated phosphoproteins in thyroid cells. Exp. Cell Res. 212, 49-61.
50. Samstag Y., Eckerskorn C., Wesselborg S., Henning S., Wallach R., and Meuer S. C. (1994) Costimulatory signals for human T-cell activation induce nuclear translocation of pp19/cofilin. Proc. Natl. Acad. Sci. USA 91, 4494-4498.
51. Sun H.-Q., Kwiatkowska K., and Yin H. L. (1995) Actin monomer binding proteins. Curr. Opin. Cell Biol. 7, 102-110.
52. Takeda S., Funakoshi T., and Hirokawa N. (1995) Tubulin dynamics in neuronal axons of living zebrafish embryos. Neuron 14, 1257-1264.
53. Tanaka K., Tashiro T., Sekimoto S., and Komiya Y. (1994) Axonal transport of actin and actin-binding proteins in the rat sciatic nerve. Neurosci. Res. 19, 295-302.
54. Tashiro T. and Komiya Y. (1989) Stable and dynamic forms of cytoskeletal proteins in slow axonal transport. J. Neurosci. 9, 760-768.
55. Tashiro T. and Komiya Y. (1991) Changes in organization and axonal transport of cytoskeletal proteins during regeneration. J. Neurochem. 56, 1557-1563.
56. Towbin H., Staehelin T., and Gordon J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
57. Weber A., Pennise C. R., and Pring M. (1994) DNase I increases the rate constant of depolymerization at the pointed (-) end of actin filaments. Biochemistry 33, 4780-4786.
58. Weisenberg R. C., Flynn J., Goa B., Awodi S., Skee F., Goodman S. R., and Riederer B. M. (1987) Microtubule gelation-contraction: essential components and relation to slow axonal transport. Science 238, 1119-1122.
59. Weisenberg R. C., Flynn J., Goa B., and Awodi S. (1988) Microtubule gelation-contraction in vitro and its relationship to component a of slow axonal transport. Cell Motil. Cytoskeleton 10, 331-340.
60. Wessel D. and Flügge U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143.
61. Willard M., Wiseman M., Levine J., and Skene P. (1979) Axonal transport of actin in rabbit retinal ganglion cells. J. Cell Biol. 81, 581-591.
62. Yonezawa N., Nishida E., Iida K., Yahara I., and Sakai H. (1990) Inhibition of the interactions of cofilin, destrin and deoxyribonuclease I with actin by phosphoinositides. J. Biol. Chem. 265, 8382-8386.