A direct interaction with calponin inhibits the actin-nucleating activity of gelsolin

Biochemical Journal

Volumn 396, Issue 3, 2006, Pages 461-468

  Ferjani, Imen ^a,b   Fattoum, Abdellatif ^c   Maciver, Sutherland K ^d   Bénistant, Christine ^c   Chahinian, Anne ^a   Manai, Mohamed ^b   Benyamin, Yves ^a   Roustan, Claude ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b FACULTÉ DES SCIENCES DE TUNIS   (Tunisia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d CNRS   (France)

Author keywords

Actin cytoskeleton; Actin nucleating activity; Calponin; Gelsolin; Gelsolin calponin complex

Indexed keywords

CHROMATOGRAPHY; FLUORESCENCE; IMMUNOLOGY; MODULATION; NUCLEATION; SIGNALING; TISSUE;

ACTIN CYTOSKELETON; ACTIN-NUCLEATING ACTIVITY; CALPONIN; GELSOLIN; GELSOLIN-CALPONIN COMPLEX;

PROTEINS;

ACTIN; CALPONIN; CYTOSKELETON PROTEIN; GELSOLIN; ACTIN BINDING PROTEIN; CALCIUM BINDING PROTEIN; FLUORESCENT DYE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; AFFINITY CHROMATOGRAPHY; AMINO TERMINAL SEQUENCE; ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; WESTERN BLOTTING; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; DRUG ANTAGONISM; HUMAN; METABOLISM; RAT; SPECTROFLUOROMETRY;

VERTEBRATA;

ACTINS; ANIMALS; CALCIUM-BINDING PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; FLUORESCENT DYES; GELSOLIN; HUMANS; MICROFILAMENT PROTEINS; RATS; SPECTROMETRY, FLUORESCENCE;

EID: 33745010035     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051690     Document Type: Article

References (46)

1. dos Remedies, C. G., Chhabra, D., Kekic, M., Dedova, I. V., Tsubakihara, M., Berry, D. A. and Noseworthy, N. J. (2003) Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83, 433-473
2. Yin, H. L. and Stossel, T. P. (1979) Control of cytoplasmic actin gel-sol transformation by gelsolin, a calcium dependent regulatory protein. Nature (London) 281, 583-586
3. 2+ requirement. J. Biol. Chem. 268, 8999-9004
4. Lagarrigue, E., Ternent, D., Maciver, S. K., Fattoum, A., Benyamin, Y. and Roustan, C. (2003) The activation of gelsolin by low pH: the calcium latch is sensitive to calcium but not pH. Eur. J. Biochem. 270, 4105-4112
5. Wang, Q., Xie, Y., Du, Q.-S., Wu, X.-J., Feng, X., Mei, L., McDonald, J. M. and Xiong, W.-C. (2003) Regulation of the formation of osteoclastic actin rings by protine-rich tyrosine kinase 2 interacting with gelsolin. J. Cell Biol. 160, 565-575
6. c-src catalysed phosphorylation of gelsolin and related actin-binding proteins. FEBS Lett. 401, 191-196
7. Janmey, P. A. and Stossel, T. P. (1987) Modulation of gelsolin function by Phosphatidylinositol 4,5-bisphosphate. Nature (London) 325, 362-364
8. Mere, J., Chahinian, A., Maciver, S. K., Fattoum, A., Bettache, N., Benyamin, Y. and Roustan, C. (2005) Gelsolin binds to polyphosphoinositide-free lipid vesicles and simultaneously to actin microfilaments. Biochem. J. 386, 47-56
9. ++-dependent regulatory protein of actin gel-sol transformation and its intracellular distribution in a variety of cells and tissues. J. Cell Biol. 91, 901-906
10. Kwiatkowski, D. J., Mehl, R., Izumo, S., Nadal-Ginard, N. and Yin, H. L. (1988) Muscle is the major source of plasma gelsolin. J. Biol. Chem. 263, 8239-8243
11. Lind, S. E., Smith, D. B., Janmey, P. A. and Stossel, T. P. (1986) Role of plasma gelsolin and vitamin D-binding protein in clearing actin from the circulation. J. Clin. Invest. 78, 736-742
12. Cunningham, C. C., Stossel, T. P. and Kwiatkowski, D. J. (1991) Enhanced motility in NIH 3T3 fibroblasts that overexpress gelsolin. Science 251, 1233-1236
13. Kwiatkowski, D. J. (1999) Functions of gelsolin: motility, signaling, apoptosis, cancer. Curr. Opin. Cell Biol. 11, 103-108
14. Witke, W., Sharpe, A. H., Hartwig, J. H., Azuma, T., Stossel, T. P. and Kwiatkowski, D. J. (1995) Hemostatic, inflammatory and fibroblast responses are blunted in mice lacking gelsolin. Cell 81, 41-51
15. Chellaiah, M., Kizer, N., Suva, M., Alvarez, U., Kwiatkowski, D. and Hruska, K. A. (2000) Gelsolin deficiency blocks podosome assembly and produces increased bone mass and strength. J. Cell Biol. 148, 665-678
16. Becker, P. M., Kazi, A. A., Wadgaonkar, R., Pearse, D. B., Kwiatkowski, D. and Garcia, J. G. N. (2003) Pulmonary vascular permeability and ischemic injury in gelsolin-deficient mice. Am. J. Respir. Cell Mol. Biol. 28, 478-484
17. Koepf, E. K. and Burtnick, L. D. (1992) Interaction of plasma gelsolin with tropomyosin. FEBS Lett. 309, 56-58
18. Winder, S. J. and Walsh, M. P. (1993) Calponin: Thin filament-linked regulation of smooth muscle contraction. Cell. Signalling 5, 677-686
19. Plantier, M., Fattoum, A., Menn, B., Ben-Ari, Y., Der Terrosian, E. and Represa, A. (1999) Acidic calponin immunoreactivity in postnatal rat brain and cultures: subcellular localization in growth cones, under the plasma membrane and along actin and glial filaments. Eur. J. Neurosci. 11, 2810-2812
20. Leinweber, B. D., Leavis, P. C., Grabarek, Z., Wang, C.-L. A. and Morgan, K. G. (1999) Extracellular regulated kinase (ERK) interaction with actin and the calponin homology (CH) domain of actin-binding proteins. Biochem. J. 344, 117-123
21. Parker, C. A., Takahashi, K., Tao, T. and Morgan, K. G. (1994) Agonist-induced redistribution of calponin in contractile vascular smooth muscle cells. Am. J. Physiol. 267, C1262-C1270
22. Menice, C. B., Hulvershorn, J., Adam, L. P., Wang, C.-L. A. and Morgan, K. G. (1997) Calponin and mitogen-activated protein kinase signaling in differentiated vascular smooth muscle. J. Biol. Chem. 272, 25157-25161
23. Patil, S. B., Pawar, M. D. and Bitar, K. N. (2004) Direct association and translocation of PKC-α with calponin. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G954-G963
24. Fujii, T., Yamana, K., Ogoma, Y. and Kondo, Y. (1995) Interaction of calponin with phospholipids. J. Biochem. 117, 999-1003
25. Agassandian, C., Plantier, M., Fattoum, A., A. R. and Der Terrosian, E. (2000) Subcellular distribution of calponin and caldesmon in rat hippocampus. Brain Res. 887, 444-449
26. Childs, T. J., Watson, M. H., Novy, R. E., Lin, J. J.-C. and Mak, A. S. (1992) Calponin and tropomyosin interactions. Biochim. Biophys. Acta 1121, 41-46
27. Way, M., Pope, B., Gooch, J., Hawkins, M. and Weeds, A. G. (1990) Identification of a region of segment 1 of gelsolin critical for actin binding. EMBO J. 9, 4103-4109
28. Mezgueldi, M., Fattoum, A., Derancourt, J. and Kassab, R. (1992) Mapping of the functional domains in the amino-terminal region of calponin. J. Biol. Chem. 267, 15943-15951
29. Burgstaller, G., Kranewitter, W. J. and Gimona, M. (2002) The molecular basis for the autoregulation of calponin by isoform-specific C-terminal tail sequences. J. Cell Sci. 115, 2021-2029
30. Spudich, J. A. and 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
31. Kouyama, T. and Mihashi, K. (1981) Fluorimetry study of N-(1-pyrenyl) iodoacetamide-labelled F-actin: local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur. J. Biochem. 114, 33-38
32. Feinberg, J., Kwiatek, O., Astier, C., Diennet, S., Mercy, J., Heitz, F., Benyamin, Y. and Roustan, C. (1998) Capping and dynamic relation between domains 1 and 2 of gelsolin. J. Pept. Sci. 4, 116-127
33. Mezgueldi, M., Mendre, C., Calas, B., Kassab, R. and Fattoum, A. (1995) Characterization of the regulatory domain of gizzard calponin. J. Biol. Chem. 270, 8867-8876
34. Abouzaglou, J., Benistant, C., Gimona, M., Roustan, C., Kassab, R. and Fattoum, A. (2004) Tyrosine phosphorylation of calponins: inhibition of the interaction with F-actin. Eur. J. Biochem. 271, 2615-2623
35. Valentin-Ranc, C., Combeau, C., Carlier, M. F. and Pantaloni, O. (1991) Myosin subfragment-1 interacts with two G-actin molecules in the absence of ATP. J. Biol. Chem. 266, 17872-17879
36. Méjean, C., Lebart, M. C., Poyer, M., Roustan, C. and Benyamin, Y. (1992) Localization and identification of actin structures involved in the filamin-actin interaction. Eur. J. Biochem. 209, 555-562
37. Bryan, J. and Coluccio, L. M. (1985) Kinetic analysis of F-actin depolymerization in the presence of platelet gelsolin and gelsolin-actin complexes. J. Cell Biol. 101, 1236-1244
38. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326
39. Dissmann, E. and Hinssen, H. (1994) Immunocytochemical localization of gelsolin in fibroblasts, myogenic cells, and isolated myofibrils. Eur. J. Cell Biol. 63, 336-344
40. Gimona, M., Kaverina, I., Resch, G. P., Vignal, E. and Burgstaller, G. (2003) Calponin repeats regulate actin filament stability and formation of podosomes in smooth muscle cells. Mol. Biol. Cell. 14, 2482-2491
41. Leinweber, B., Tang, Z. X., Stafford, W. F. and Chalovich, J. M. (1999) Calponin interaction with α-actinin-actin: evidence for a structural role for calponin. Biophys. J. 77, 3208-3217
42. Mino, T., Yuasa, U., Nakamura, F., Naka, M. and Tanaka, T. (1998) Two distinct actin-binding sites of smooth muscle calponin. Eur. J. Biochem. 251, 262-268
43. Taniguchi, S., Takeoka, M., Ehara, T., Hashimoto, S., Shibuki, H., Yoshimura, N., Shigematsu, H., Takahashi, K. and Katsuki, M. (2001) Structural fragility of blood vessels and peritoneum in calponin h1-deficient mice, resulting in an increase in hematogenous metastasis and peritoneal dissemination of malignant tumor cells. Cancer Res. 61, 7627-7634
44. Becker, P. M., Kazi, A. A., Wadgaonkar, R., Pearse, D. B., Kwiatkowski, D. and Garcia, J. G. N. (2003) Pulmonary vascular permeability and ischemic injury in gelsolin-deficient mice. Am. J. Respir. Cell Mol. Biol. 28, 478-484
45. Chan, M. W. C., El Sayegh, T. Y., Arora, P. D., Laschinger, C. A., Overall, C. M., Morrison, C. and McCulloch, C. A. G. (2004) Regulation of intercellular adhesion strength in fibroblasts. J. Biol. Chem. 279, 41047-41057
46. Yoshikawa, H., Taniguchi, S.-i., Yamamura, H., Mori, S., Sugimoto, M., Miyado, K., Nakamura, K., Nakao, K., Katsuki, M., Shibata, N. and Takahashi, K. (1998) Mice lacking smooth muscle calponin display increased bone formation that is associated with enhancement of bone morphogenetic protein responses. Genes Cells 3, 685-695