Home LiteratureArticle Details
PMID: 2547804 Published · ppublish English Journal Article

Expression of human plasma gelsolin in Escherichia coli and dissection of actin binding sites by segmental deletion mutagenesis.

The Journal of cell biology ·Vol. 109 ·No. 2 ·1989-08-00 ·Pages 593-605

Way M, Gooch J, Pope B, Weeds AG

Abstract

Human plasma gelsolin has been expressed in high yield and soluble form in Escherichia coli. The protein has nucleating and severing activities identical to those of plasma gelsolin and is fully calcium sensitive in its interactions with monomeric actin. A number of deletion mutants have been expressed to explore the function of the three actin binding sites. Their design is based on the sixfold segmental repeat in the protein sequence. (These sites are located in segment 1, segments 2-3, and segments 4-6). Two mutants, S1-3 and S4-6, are equivalent to the NH2- and COOH-terminal halves of the molecule obtained by limited proteolysis. S1-3 binds two actin monomers in the presence or absence of calcium, it severs and caps filaments but does not nucleate polymerization. S4-6 binds a single actin monomer but only in calcium. These observations confirm and extend current knowledge on the properties of the two halves of gelsolin. Two novel constructs have also been studied that provide a different pairwise juxtaposition of the three sites. S2-6, which lacks the high affinity site of segment 1 (equivalent to the 14,000-Mr proteolytic fragment) and S1,4-6, which lacks segments 2-3 (the actin filament binding domain previously identified using the 28,000-Mr proteolytic fragment). S2-6 binds two actin monomers in calcium and nucleates polymerization; it associates laterally with filaments in the presence or absence of calcium and has a weak calcium-dependent fragmenting activity. S1,4-6 also binds two actin monomers in calcium and one in EGTA, has weak severing activity but does not nucleate polymerization. A model is presented for the involvement of the three binding sites in the various activities of gelsolin.

MeSH Terms
Actins/analysis,metabolism Binding Sites/drug effects Calcium/metabolism Calcium-Binding Proteins/blood,genetics Chromosome Deletion Chymotrypsin/pharmacology Deoxyribonucleases/antagonists & inhibitors Escherichia coli/metabolism Gelsolin Gene Expression Regulation Humans Intermediate Filaments/metabolism,ultrastructure Microfilament Proteins/blood,genetics Microscopy, Electron Mutation Viscosity
Chemicals
Actins Calcium-Binding Proteins Gelsolin Microfilament Proteins Deoxyribonucleases Chymotrypsin Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Way M
Medical Research Council Laboratory of Molecular Biology, Cambridge, England.
Gooch J
Pope B
Weeds A G
References (47)
47 references, click to expand
  1. Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin.
    J Cell Sci. 1986 Dec;86:217-32 PMID: 3308928
  2. Villin sequence and peptide map identify six homologous domains.
    Proc Natl Acad Sci U S A. 1988 Jul;85(14):4986-90 PMID: 2839826
  3. Gelsolin: calcium- and polyphosphoinositide-regulated actin-modulating protein.
    Bioessays. 1987 Oct;7(4):176-9 PMID: 2825660
  4. Association of deoxyribonuclease I with the pointed ends of actin filaments in human red blood cell membrane skeletons.
    J Biol Chem. 1988 Jan 15;263(2):638-45 PMID: 3335517
  5. Severin, gelsolin, and villin share a homologous sequence in regions presumed to contain F-actin severing domains.
    J Biol Chem. 1988 Jan 15;263(2):722-7 PMID: 2826459
  6. Binding of phosphate to F-ADP-actin and role of F-ADP-Pi-actin in ATP-actin polymerization.
    J Biol Chem. 1988 Jan 15;263(2):817-25 PMID: 3335528
  7. Synthesis and sequence-specific proteolysis of hybrid proteins produced in Escherichia coli.
    Methods Enzymol. 1987;153:461-81 PMID: 3323806
  8. Identification of a polyphosphoinositide-modulated domain in gelsolin which binds to the sides of actin filaments.
    J Cell Biol. 1988 Mar;106(3):805-12 PMID: 2831234
  9. The F-actin capping proteins of Physarum polycephalum: cap42(a) is very similar, if not identical, to fragmin and is structurally and functionally very homologous to gelsolin; cap42(b) is Physarum actin.
    EMBO J. 1987 Dec 20;6(13):4149-57 PMID: 2832154
  10. Muscle is the major source of plasma gelsolin.
    J Biol Chem. 1988 Jun 15;263(17):8239-43 PMID: 2836420
  11. Gelsolin has three actin-binding sites.
    J Cell Biol. 1988 May;106(5):1553-62 PMID: 2836434
  12. Sequence of human villin: a large duplicated domain homologous with other actin-severing proteins and a unique small carboxy-terminal domain related to villin specificity.
    J Cell Biol. 1988 Nov;107(5):1759-66 PMID: 2846586
  13. Nucleotide sequence of pig plasma gelsolin. Comparison of protein sequence with human gelsolin and other actin-severing proteins shows strong homologies and evidence for large internal repeats.
    J Mol Biol. 1988 Oct 20;203(4):1127-33 PMID: 2850369
  14. Identification of critical functional and regulatory domains in gelsolin.
    J Cell Biol. 1989 May;108(5):1717-26 PMID: 2541138
  15. Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli.
    Biochemistry. 1968 Jun;7(6):2143-52 PMID: 4873173
  16. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  17. Re-examination of the apparent binding constant of ethylene glycol bis(beta-aminoethyl ether)-N,N,N',N'-tetraacetic acid with calcium around neutral pH.
    J Biochem. 1980 May;87(5):1305-12 PMID: 6771253
  18. Ca2+ control of actin gelation. Interaction of gelsolin with actin filaments and regulation of actin gelation.
    J Biol Chem. 1980 Oct 10;255(19):9494-500 PMID: 6251091
  19. An actin depolymerizing protein from pig plasma.
    FEBS Lett. 1981 Jan 12;123(1):49-53 PMID: 6894126
  20. Ca2+ control of actin filament length. Effects of macrophage gelsolin on actin polymerization.
    J Biol Chem. 1981 Sep 25;256(18):9693-7 PMID: 6270098
  21. The depolymerization of actin by specific proteins from plasma and brain: a quantitative assay.
    Anal Biochem. 1982 Jan 1;119(1):102-14 PMID: 7072932
  22. Tropomyosin binding to F-actin protects the F-actin from disassembly by brain actin-depolymerizing factor (ADF).
    Cell Motil. 1982;2(1):1-8 PMID: 6890875
  23. Plasma actin depolymerizing factor has both calcium-dependent and calcium-independent effects on actin.
    Biochemistry. 1983 May 24;22(11):2728-41 PMID: 6871158
  24. Platelet activation induces the formation of a stable gelsolin-actin complex from monomeric gelsolin.
    J Biol Chem. 1984 Jun 25;259(12):7473-9 PMID: 6330059
  25. Actin-gelsolin interactions. Evidence for two actin-binding sites.
    J Biol Chem. 1984 Jun 25;259(12):7480-7 PMID: 6330060
  26. Generation of beta-globin by sequence-specific proteolysis of a hybrid protein produced in Escherichia coli.
    Nature. 1984 Jun 28-Jul 4;309(5971):810-2 PMID: 6330564
  27. Actin polymerization. The effect of brevin on filament size and rate of polymerization.
    J Biol Chem. 1984 Oct 10;259(19):11868-75 PMID: 6480587
  28. Calcium dependence of villin-induced actin depolymerization.
    Biochemistry. 1984 Dec 4;23(25):6099-102 PMID: 6525347
  29. Improved oligonucleotide site-directed mutagenesis using M13 vectors.
    Nucleic Acids Res. 1985 Jun 25;13(12):4431-43 PMID: 2989795
  30. Lack of nucleotide cleavage on the binding of G-actin-ATP to plasma gelsolin.
    FEBS Lett. 1985 Oct 7;190(1):81-3 PMID: 2995131
  31. Kinetic analysis of F-actin depolymerization in the presence of platelet gelsolin and gelsolin-actin complexes.
    J Cell Biol. 1985 Oct;101(4):1236-44 PMID: 2995403
  32. Interaction of plasma gelsolin with G-actin and F-actin in the presence and absence of calcium ions.
    J Biol Chem. 1985 Dec 5;260(28):15033-41 PMID: 2999102
  33. Isolation and properties of two actin-binding domains in gelsolin.
    J Biol Chem. 1985 Dec 5;260(28):15232-8 PMID: 2999108
  34. Definition of an N-terminal actin-binding domain and a C-terminal Ca2+ regulatory domain in human brevin.
    J Cell Biol. 1986 Apr;102(4):1439-46 PMID: 3082893
  35. Sequential binding of actin monomers to plasma gelsolin and its inhibition by vitamin D-binding protein.
    Biochem Biophys Res Commun. 1986 Apr 14;136(1):72-9 PMID: 3010978
  36. Rate of treadmilling of actin filaments in vitro.
    J Mol Biol. 1986 Feb 20;187(4):627-31 PMID: 3012095
  37. Plasma and cytoplasmic gelsolins are encoded by a single gene and contain a duplicated actin-binding domain.
    Nature. 1986 Oct 2-8;323(6087):455-8 PMID: 3020431
  38. The actin filament-severing domain of plasma gelsolin.
    J Cell Biol. 1986 Oct;103(4):1473-81 PMID: 3021782
  39. Gelsolin inhibits nucleotide exchange from actin.
    Biochemistry. 1986 Sep 23;25(19):5799-804 PMID: 3022803
  40. Preparation and characterization of pig plasma and platelet gelsolins.
    Eur J Biochem. 1986 Nov 17;161(1):69-76 PMID: 3023087
  41. Interactions of pig plasma gelsolin with G-actin.
    Eur J Biochem. 1986 Nov 17;161(1):77-84 PMID: 3023088
  42. Binding of pig plasma gelsolin to F-actin and partial fractionation into calcium-dependent and calcium-independent forms.
    Eur J Biochem. 1986 Nov 17;161(1):85-93 PMID: 3023089
  43. Kinetics of actin monomer exchange at the slow growing ends of actin filaments and their relation to the elongation of filaments shortened by gelsolin.
    J Muscle Res Cell Motil. 1986 Oct;7(5):446-54 PMID: 3025252
  44. Study of actin filament ends in the human red cell membrane.
    J Mol Biol. 1986 Oct 5;191(3):461-8 PMID: 3029384
  45. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes.
    J Biol Chem. 1987 Jul 25;262(21):10035-8 PMID: 3611052
  46. The binary complex of pig plasma gelsolin with Mg2+-G-actin in ATP and ADP.
    FEBS Lett. 1988 Jun 20;233(2):359-62 PMID: 2838335
  47. pH-dependent rate of formation of the gelsolin-actin complex from gelsolin and monomeric actin.
    Eur J Biochem. 1987 Oct 1;168(1):111-5 PMID: 2822398
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1989-08-00
Pages
593-605
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2115723
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]