The activation of gelsolin by low pH: The calcium latch is sensitive to calcium but not pH

European Journal of Biochemistry

Volumn 270, Issue 20, 2003, Pages 4105-4112

  Lagarrigue, Emeline ^a   Ternent, Diane ^b   Maciver, Sutherland K ^b   Fattoum, Abdellatif ^c   Benyamin, Yves ^a   Roustan, Claude ^a,c  

^a UNIVERSITÉ DE MONTPELLIER   (France)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c CNRS   (France)

Author keywords

Actin binding protein; Cytoskeleton; Gelsolin; Microfilament

Indexed keywords

ACTIN BINDING PROTEIN; CALCIUM; GELSOLIN; HISTIDINE;

ARTICLE; CHEMICAL BOND; CONFORMATION; PH; PRIORITY JOURNAL; PROTEIN DOMAIN;

ACTINS; ANIMALS; CALCIUM; GELSOLIN; HYDROGEN-ION CONCENTRATION; KINETICS; MUSCLE, SKELETAL; PROTEIN CONFORMATION; RABBITS; TIME FACTORS;

EID: 0142057159     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03803.x     Document Type: Article

References (49)

1. dos Remedios, C.G., Chhabra, D., Kekic, M., Dedova, I.V., Tsubakihara, M., Berry, D.A. & Noseworthy, N.J. (2003) Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83, 433-473.
2. Sun, H.Q., Yamamoto, M., Mejillano, M. & Yin, H.L. (1999) Gelsolin, a multifunctional actin regulatory protein. J. Biol. Chem. 274, 33179-33182.
3. Way, M. & Weeds, A.G. (1988) 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. 203, 1127-1133.
4. Burtnick, L.D., Koepf, E.K., Grimes, J., Jones, E.Y., Stuart, D.I., McLaughlin, P.J. & Robinson, R.C. (1997) The crystal structure of plasma gelsolin: Implications for actin severing, capping and nucleation. Cell. 90, 661-670.
5. Robinson, R.C., Mejillano, M., Le, V.P., Burtnick, L.D., Yin, H.L. & Choe, S. (1999) Domain movement in gelsolin: a calcium-activated switch. Science. 286, 1939-1942.
6. Bryan, J. (1988) Gelsolin has three actin-binding sites. J. Cell Biol. 106, 1553-1562.
7. Pope, B., Way, M. & Weeds, A.G. (1991) Two of the three actin-binding domains of gelsolin bind to the same subdomain of actin. FEBS Lett. 280, 70-74.
8. Pope, B., Maciver, S. & Weeds, A.G. (1995) Localization of the calcium-sensitive actin monomer binding site in gelsolin to segment 4 and identification of calcium-binding sites. Biochemistry. 34, 1583-1588.
9. Xu, Y.-S., Kantorow, M., Davis, J. & Piatigorsky, J. (2000) Evidence for gelsolin as a corneal crystallin in zebrafish. J. Biol. Chem. 275, 24645-24652.
10. Steed, P.M., Nagar, S. & Wennogle, L.P. (1996) Phospholipase D regulation by a physical interaction with the actin-binding protein gelsolin. Biochemistry. 35, 5229-5237.
11. Ohtsu, M., Sakai, N., Fujita, H., Kashiwagi, M., Gasa, S., Shimizu, S., Eguchi, Y., Tsujimoto, Y., Sakiyama, Y., Kobayashi, K. & Kuzumaki, N. (1997) Inhibition of apoptosis by the actin-regulatory protein gelsolin. EMBO J. 16, 4650-4656.
12. Harris, H.E., Bamburg, J.R. & Weeds, A.G. (1980) Actin filament disassembly in blood plasma. FEBS Lett. 123, 49-53.
13. Haddad, J.G., Harper, K.D., Guoth, M., Pietra, G.G. & Sanger, J.W. (1990) Angiogenic consequences of saturating the plasma scavenger system for actin. Proc. Nat. Acad. Sci. 87, 1381-1385.
14. Cunningham, C.C., Stossel, T.P. & Kwiatkowski, D.J. (1991) Enhanced motility in NIH 3T3 fibroblasts that overexpress gelsolin. Science. 251, 1233-1236.
15. Cunningham, C.C., Vegners, R., Bucki, R., Funaki, M., Korde, N., Hartwig, J.H., Stossel, T.P. & Janmey, P.A. (2001) Cell permeant polyphsophoinositide-binding peptides that block cell motililty and actin assembly. J. Biol. Chem. 276, 43390-43399.
16. Witke, W., Sharpe, A.H.H., Artwig, J.H., Azuma, T., Stossel, T.P. & Kwiatkowski, D.J. (1995) Hemostatic, inflammatory and fibroblast responses are blunted in mice lacking gelsolin. Cell. 81, 41-51.
17. Patkowski, A., Seils, J., Hinssen, H. & Dorfmuller, T. (1990) Size, shape parameters and calcium-induced conformational change of the gelsolin molecule. A dynamic light scattering study. Biopolymers. 30, 427-435.
18. 2+-induced conformational change of gelsolin is located in the carboxyl-terminal half of the molecule. Biophys. J. 65, 799-805.
19. Choe, H., Burtnick, L.D., Mejillano, M., Yin, H.L., Robinson, R.C. & Choe, S. (2002) The calcium activation of gelsolin: Insights from the 3Å structure of the G4-G6/actin complex. J. Mol. Evol. 324, 691-702.
20. Kolappan, S.P., Gooch, J.T., Weeds, A.G. & McLaughlin, P.J. (2003) Gelsolin domains 4-6 in active, actin free conformation identifies sites of regulatory calcium ions. J. Mol. Biol. 329, 85-92.
21. 2+ requirement. J. Biol. Chem. 268, 8999-9004.
22. Lagarrique, E., Maciver, S.K., Fattoum, A., Benyamin, Y. & Roustan, C. (2003) Co-operation of domain-binding and calcium-binding sites in the activation of gelsolin. Eur. J. Biochem. 270, 2236-2243.
23. Spudich, J.A. & Watt, S. (1971) The regulation of rabbit skeletal muscle contraction. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871.
24. Kouyama, T. & Mihashi, K. (1981) Fluorimetry study of N-(1-pyrenyl) iodoacetamide-labelled F-actin. Eur. J. Biochem. 114, 33-38.
25. Way, M., Pope, B., Gooch, J., Hawkins, M. & Weeds, A.G. (1990) Identification of a region of segment 1 of gelsolin critical for actin binding. EMBO J. 9, 4103-4109.
26. Way, M., Pope, B. & Weeds, A.G. (1992) Evidence for functional homology in the F-actin binding domains of gelsolin and alpha-actinin: implications for the requirements of severing and capping. J. Cell Biol. 119, 835-842.
27. Way, M., Gooch, J., Pope, B. & Weeds, A.G. (1989) Expression of human plasma gelsolin in E. coli and dissection of actin binding sites by segmental deletion mutagenesis. J. Cell Biol. 109, 593-605.
28. Kurokawa, H., Fujii, W., Ohmi, K., Sakurai, T. & Nonomura, Y. (1990) Simple and rapid purification of brevin. Biochem. Biophys. Res. Comm. 168, 451-457.
29. Renoult, C., Blondin, L., Fattoum, A., Ternent, D., Maciver, S.K., Raynaud, F., Benyamin, Y. & Roustan, C. (2001) Binding of gelsolin domain 2 to actin. An actin interface distinct from that of gelsolin domain 1 and from ADF/cofilin. Eur. J. Biochem. 268, 6165-6175.
30. Miki, M. & dos Remedios, C.G. (1988) Fluorescence quenching studies of fluorescein attached to Lys-61 or Cys-374 in actin: effects of polymerization, myosin subfragment-1 binding, and tropomyosin-troponin binding. J. Biochem. 104, 232-235.
31. Papa, I., Astier, C., Kwiatek, O., Lebart, M.-C., Raynaud, F., Benyamin, Y. & Roustan, C. (1999) Use of a chaotropic anion iodide in the purification of Z-line proteins: isolation of CapZ. from fish white muscle. Prot. Expr Purif. 17, 1-7.
32. Engvall, E. (1980) Enzyme immunoassay ELISA and EMIT. Meth. Enzymol. 70, 419-439.
33. Méjean, C., Lebart, M.C., Poyer, M., Roustan, C. & Benyamin, Y. (1992) Localization and identification of actin structures involved in the filamin-actin interaction. Eur. J. Biochem. 209, 555-562.
34. Lakowicz, J.R. (1983) Principles of Fluorescence Spectroscopy. Plenum Publishing Corp, New York.
35. Gill, S.C. & von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
36. 2+-sensitive interface in the plasma gelsolin-actin complex. Biochem. J. 274, 753-757.
37. 2+ regulation of gelsolin by its C-terminal. Biol. Chem. 275, 27746-27752.
38. Maciver, S.K., Ternent, D. & McLaughlin, P.J. (2000) Domain 2 of gelsolin binds directly to tropomyosin. FEBS Lett. 473, 71-75.
39. Kwiatkowski, D.J., Janmey, P.A. & Yin, H.L. (1989) Identification of critical functional and regulatory domains in gelsolin. J. Cell Biol. 108, 1717-1726.
40. Lueck, A., Yin, H.L., Kwiatkowski, D.J. & Allen, P.G. (2000) Calcium regulation of gelsolin and adseverin: a natural test of the helix latch hypothesis. Biochemistry. 39, 5274-5279.
41. Hesterkamp, T., Weeds, A.G. & Mannherz, H.G. (1993) The actin monomers in the ternary gelsolin: 2 actin complex are in anti-parallel orientation. Eur. J. Biochem. 218, 507-513.
42. McLaughlin, P.J., Gooch, J.T., Mannherz, H.G. & Weeds, A.G. (1993) Structure of gelsolin segment-1-actin complex and the mechanism of filament severing. Nature. 364, 685-692.
43. Chaponnier, C., Janmey, P.A. & Yin, H.L. (1986) The actin filament-severing domain of plasma gelsolin. J. Cell Biol. 103, 1473-1481.
44. Selve, N. & Wegner, A. (1987) pH-dependent rate of formation of the gelsolin-actin complex from gelsolin and monomeric actin. Eur. J. Biochem. 161, 111-115.
45. Watanabe, K., Hamaguchi, M.S. & Hamaguchi, Y. (1997) Effects of intracellular pH on the mitotic apparatus and mitoitc stage in the sand dollar egg. Cell Mot. Cytoskel. 37, 263-270.
46. Van Duijn. B. & Inouye, K. (1991) Regulation of movement speed by intracellular pH during Dictyostelium discoideum chemotaxis. Proc. Nat. Acad. Sci. 88, 4951-4955.
47. Schwiening, C.J. & Willoughby, D. (2002) Depolarization-induced pH microdomains and their relationship to calcium transients in isolated snail neurones. J. Physiol. 538, 371-382.
48. Yonezawa, N., Nishida, E. & Sakai, H. (1985) pH control of actin polymerization by cofilin. J. Biol. Chem. 260, 14410-14412.
49. Edmonds, B.T., Murray, J. & Condeelis, J. (1995) pH regulation of the F-actin binding properties of Dictyostelium elongation factor 1a. J. Biol. Chem. 270, 15222-15230.