DOI: 10.1111/j.1432-1033.1994.tb20096.x. Interaction of Plant Profilin with Mammalian Actin

Interaction of Plant Profilin with Mammalian Actin

10.1111/j.1432-1033.1994.tb20096.x

Crossref journal-article

Wiley

European Journal of Biochemistry (311)

Abstract

The mode of interaction of birch and bovine profilins with actin was compared using a number of techniques. Birch profilin was purified from pollen or as a recombinant protein from Escherichia coli, using poly(l‐proline) affinity chromatography and a monoclonal antibody for the identification of the isolated product. On two‐dimensional gels, the genuine and recombinant proteins were identical in molecular mass and isoelectric point and revealed that birch profilin, in contrast to the basic profilins found in mammals, is an acidic protein, analogous to maize profilins. Bovine profilin was obtained from calf thymus.In viscometric assays, the birch protein was seen to modulate actin filament formation analogous to animal profilin. Birch profilin increased the critical concentration required for muscle and brain actin polymerization in a concentration‐dependent manner, supporting the notion of the formation of a heterologous complex between the plant protein and animal actin. The effect was Mg2+‐sensitive, as had been described for homologous complexes. The dissociation constants obtained for the plant/vertebrate and the vertebrate/vertebrate system were both in the micromolar range. The affinity of birch profilin for muscle actin was slightly lower than that for nonmuscle (brain) actin. A binary complex of birch profilin and skeletal muscle actin could be isolated by gel chromatography.Cross‐linking experiments with actin, birch profilin, the G‐actin binding peptide thymosin β4 and gelsolin segment 1, the N‐terminal fragment of an actin capping protein, showed that profilin competed with thymosin β4, but had no effect on segment 1 binding to actin.These data indicate that the actin‐binding domains in plant and animal profilins are functionally highly conserved, although the overall sequence similarity is less than 25%.

Bibliography

Giehl, K., Valenta, R., Rothkegel, M., Ronsiek, M., Mannherz, H., & Jockusch, B. M. (1994). Interaction of Plant Profilin with Mammalian Actin. European Journal of Biochemistry, 226(2), 681â689. Portico.

Authors 6

Klaudia Giehl (first)
Rudolf Valenta (additional)
Martin Rothkegel (additional)
Melanie Ronsiek (additional)
Hans‐Georg Mannherz (additional)
Brigitte M. Jockusch (additional)

References 58 Referenced 57

10.1002/j.1460-2075.1987.tb02761.x
10.1016/S0021-9258(20)71174-9 / J. Biol. Chem. / The amino acid sequence of Acanthamoeba profilin by Ampe C. (1985)
10.1016/0014-5793(94)80262-9
10.1002/cm.970140209
10.1016/0014-5793(93)80388-B
10.1128/jvi.65.9.4598-4608.1991 / J. Virol. / Sequence analysis, expression and deletion of a vaccinia virus gene encoding a homolog of profilin, a eukaryotic actin‐binding protein by Blasco R. (1991)
10.1016/0014-5793(89)80009-2
10.1002/cm.970220106
10.1073/pnas.90.11.5034
10.1016/0022-2836(77)90166-8
10.1016/0076-6879(82)85021-0
10.1016/S0021-9258(17)39622-9 / J. Biol. Chem. / Effects of macrophage profilin on actin in the presence and absence of acumentin and gelsolin by DiNubile U. J. (1985)
10.1126/science.1848725
10.1083/jcb.113.5.1081
10.1016/S0021-9258(17)33270-2 / J. Biol. Chem. / Characterization of cytoplasmic actin isolated from Acanthamoeba castellanii by a new method by Gordon D. J. (1976)
10.1002/cm.970170202
10.1016/0003-9861(89)90498-0
10.1083/jcb.109.4.1571
10.1242/jcs.100.3.481 / J. Cell Sci. / Dictyostelium discoideum contains two profilin isoforms that differ in structure and function by Haugwitz M. (1991)
{'key': 'e_1_2_2_21_1', 'first-page': '97', 'article-title': 'Expression and localisation of profilin and plant actin in E. coli: an immunoelectron microscopic study, Eur. J. Cell Biol. 63', 'volume': '40', 'author': 'Heimann P.', 'year': '1991', 'journal-title': 'Suppl.'} / Suppl. / Expression and localisation of profilin and plant actin in E. coli: an immunoelectron microscopic study, Eur. J. Cell Biol. 63 by Heimann P. (1991)
10.1016/0003-2697(74)90367-4
10.1016/0167-4838(88)90013-1
10.1002/jcb.240370302
10.1083/jcb.105.2.833
10.1016/0962-8924(93)90087-H
10.1007/BF00712116
10.1038/364685a0
10.1021/bi00213a010
10.1016/S0021-9258(17)41821-7 / J. Biol. Chem. / Identification of the poly‐l‐proline‐binding site on human profilin by Metzler W. J. (1994)
10.1021/bi00564a033
10.1021/bi00326a015
10.1016/S0021-9258(19)41496-8 / J. Biol. Chem. / High resolution two‐dimensional electrophoresis of proteins by O'Farell P. H. (1975)
10.1093/oxfordjournals.jbchem.a134167
10.1016/0092-8674(93)90544-Z
10.1021/bi00321a054
10.1002/cm.970200209
{'key': 'e_1_2_2_38_1', 'first-page': '220', 'article-title': 'A simple procedure to produce monospecific polyclonal antibodies of high affinity against actin from muscular sources', 'volume': '50', 'author': 'Polzar B.', 'year': '1989', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. / A simple procedure to produce monospecific polyclonal antibodies of high affinity against actin from muscular sources by Polzar B. (1989)
10.1016/0955-0674(94)90121-X
10.1016/S0021-9258(20)64278-8 / J. Biol.Chem. / Thymosin β4 and Fx, an actin sequestering peptide, are indistinguishable by Safer D. (1991)
10.1016/0003-2697(87)90587-2
10.1083/jcb.90.1.222
10.1038/365810a0
10.1016/0003-2697(85)90442-7
10.1016/S0021-9258(18)62016-2
10.1046/j.1365-313X.1993.04040631.x
10.1016/S0960-9822(00)00050-6
10.1016/0076-6879(90)85008-C
10.1111/j.1432-1033.1985.tb09099.x
10.1016/0092-8674(93)90527-W
10.1016/S0021-9258(18)34701-X / J. Biol. Chem. / The regulation of actin polymerization and the inhibition of monomeric actin ATPase activity by Acanthamoeba castellanii profilin by Tobacman L. S. (1982)
10.1083/jcb.94.1.213
10.1006/bbrc.1994.1201
10.1126/science.1857985
10.1016/S0021-9258(18)41594-3 / J. Biol. Chem. / Identification of profilin as an actin‐binding protein in higher plants by Valenta R. (1993)
10.1083/jcb.109.2.619
10.1083/jcb.122.6.1277
10.1002/j.1460-2075.1990.tb07632.x
10.1016/0076-6879(82)85036-2

Dates

Type	When
Created	20 years, 6 months ago (March 4, 2005, 6:25 a.m.)
Deposited	1 year, 9 months ago (Nov. 22, 2023, 10:29 p.m.)
Indexed	1 year, 1 month ago (July 10, 2024, 1:58 p.m.)
Issued	30 years, 9 months ago (Dec. 1, 1994)
Published	30 years, 9 months ago (Dec. 1, 1994)
Published Online	17 years, 2 months ago (June 28, 2008)
Published Print	30 years, 9 months ago (Dec. 1, 1994)

Funders 0

None

BibTeX

@article{Giehl_1994, title={Interaction of Plant Profilin with Mammalian Actin}, volume={226}, ISSN={1432-1033}, url={http://dx.doi.org/10.1111/j.1432-1033.1994.tb20096.x}, DOI={10.1111/j.1432-1033.1994.tb20096.x}, number={2}, journal={European Journal of Biochemistry}, publisher={Wiley}, author={Giehl, Klaudia and Valenta, Rudolf and Rothkegel, Martin and Ronsiek, Melanie and Mannherz, Hans‐Georg and Jockusch, Brigitte M.}, year={1994}, month=dec, pages={681–689} }

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