Reversible S-glutathionylation of Cys374 regulates actin filament formation by inducing structural changes in the actin molecule

Free Radical Biology and Medicine

Volumn 34, Issue 1, 2003, Pages 23-32

  Dalle Donne, Isabella ^a   Giustarini, D ^b   Rossi, R ^b   Colombo, R ^a   Milzani, A ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

Actin; Free radicals; Glutathione; Protein GSH mixed disulphides; S thiolation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYSTEINE; DEOXYRIBONUCLEASE I; F ACTIN; G ACTIN; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLYCINE; METHIONINE; SUBTILISIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; HYDROPHOBICITY; INHIBITION KINETICS; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN PROCESSING; RABBIT; RNA TRANSLATION; STRUCTURE ANALYSIS;

ACTINS; ADENOSINE TRIPHOSPHATE; ANIMALS; BIOPOLYMERS; CYSTEINE; GLUTATHIONE; OXIDATION-REDUCTION; PROTEIN CONFORMATION; RABBITS; SUBTILISINS;

EID: 12244311183     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(02)01182-6     Document Type: Article

References (66)

1. 2-treated actin assembly and polymer interactions with crosslinking proteins. Biophys J. 69:1995;2710-2719.
2. Dalle-Donne I., Milzani A., Colombo R. The t-butyl hydroperoxide-induced oxidation of actin Cys-374 is coupled with structural changes in distant regions of the protein. Biochemistry. 38:1999;12471-12480.
3. Dalle-Donne I., Rossi R., Giustarini D., Gagliano N., Lusini L., Milzani A., Di Simplicio P., Colombo R. Actin carbonylation from simple marker of protein oxidation to relevant sign of severe functional impairment. Free Radic Biol Med. 31:2001;1075-1083.
4. Milzani A., Dalle-Donne I., Colombo R. Prolonged oxidative stress on actin. Arch Biochem Biophys. 339:1997;267-274.
5. Milzani A., Rossi R., Di Simplicio P., Giustarini D., Colombo R., Dalle-Donne I. The oxidation produced by hydrogen peroxide on Ca-ATP-G-actin. Protein Sci. 9:2000;1774-1782.
6. Dalle-Donne I., Milzani A., Giustarini D., Di Simplicio P., Colombo R., Rossi R. S-NO-Actin S-nitrosylation kinetics and effect on isolated vascular smooth muscle. J Muscle Res Cell Motil. 21:2000;171-181.
7. Thomas J.A., Sies H. Protein S-thiolation and dethiolation. Tuboi S., Taniguchi N., Katunuma N. The post-translational modification of proteins roles in molecular and cellular biology. 1992;35-51 CRC Press, Boca Raton, FL.
8. Klatt P., Lamas S. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem. 267:2000;4928-4944.
9. Cotgreave I.A., Gerdes R.G. Recent trends in glutathione biochemistry-glutathione-protein interactions a molecular link between oxidative stress and cell proliferation? Biochem Biophys Res Comm. 242:1998;1-9.
10. Barrett W.C., DeGnore J.P., Koumlautnig S., Fales H.M., Keng Y.F., Zhang Z.Y., Yim M.B., Chock P.B. Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry. 38:1999;6699-6705.
11. Reddy S., Jones A.D., Cross C.E., Wong P.S.Y., van der Vliet A. Inactivation of creatine kinase by S-glutathionylation of the active-site cysteine residue. Biochem J. 347:2000;821-827.
12. Davis D.A., Dorsey K., Wingfield P.T., Stahl S.J., Kaufman J., Fales H.M., Levine R.L. Regulation of HIV-1 protease activity through cysteine modification. Biochemistry. 35:1996;2482-2488.
13. Davis D.A., Newcomb F.M., Starke D.W., Ott D.E., Mieyal J.J., Yarchoan R. Thioltransferase (glutaredoxin) is detected within HIV-1 and can regulate the activity of glutathionylated HIV-1 protease in vitro. J Biol Chem. 272:1997;25935-25940.
14. Klatt P., Molina E.S., Lacoba M.C., Padilla C.A., Martinez-Glaisteo E., Barcena J.A., Lamas S. Redox regulation of c-Jun DNA binding by reversible S-glutathiolation. FASEB J. 13:1999;1481-1490.
15. Klatt P., Molina E.S., Lamas S. Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation. J Biol Chem. 22:1999;15857-15864.
16. Schuppe-Koistinen I., Moldus P., Bergman T., Cotgreave I.A. Reversible S-thiolation of human endothelial cell actin accompanies a structural reorganization of the cytoskeleton. Endothelium. 3:1995;301-308.
17. Rokutan K., Johnston R.B. Jr., Kawai K. Oxidative stress induces S-thiolation of specific proteins in cultured gastric mucosal cells. Am J Physiol. 266:1994;G247-G254.
18. Chai Y.C., Ashraf S.S., Rokutan K., Johnston R.B. Jr., Thomas J.A. S-thiolation of individual human neutrophil proteins including actin by stimulation of the respiratory burst evidence against a role for glutathione disulfide. Arch Biochem Biophys. 310:1994;273-281.
19. Ghezzi P., Romines B., Fratelli M., Eberini I., Gianazza E., Casagrande S., Laragione T., Mengozzi M., Herzenberg L.A. Protein glutathionylation coupling and uncoupling of glutathione to protein thiol groups in lymphocytes under oxidative stress and HIV infection. Mol Immunol. 38:2002;773-780.
20. Fratelli M., Demol H., Puype M., Casagrande S., Eberini I., Salmona M., Bonetto V., Mengozzi M., Duffieux F., Miclet E., Bachi A., Vandekerckhove J., Gianazza E., Ghezzi P. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc. Natl. Acad. Sci. USA. 99:2002;3505-3510.
21. Stournaras C. Exposure of thiol groups and bound nucleotide in G-actin thiols as an indicator for the native state of actin. Anticancer Res. 10:1990;1651-1659.
22. Wang J., Boja E.S., Tan W., Tekle E., Fales H.M., English S., Mieyal J.J., Chock P.B. Reversible glutathionylation regulates actin polymerization in A431 cells. J Biol Chem. 276:2001;47763-47766.
23. Milzani A., Dalle-Donne I. Effects of chlorpromazine on actin polymerization slackening of filament elongation and filament annealing. Arch Biochem Biophys. 369:1999;59-67.
24. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:1976;248-254.
25. Colombo R., Dalle-Donne I., Milzani A. Alpha-actinin increases actin filament end concentration by inhibiting annealing. J Mol Biol. 230:1993;1151-1158.
26. Newton G.L., Fahey R.C. Determination of biothiols by bromobimane labeling and high-performance liquid chromatography. Methods Enzymol. 251:1995;148-166.
27. Giustarini D., Capoccia G., Fanetti G., Rossi R., Giannerini F., Lusini L., Di Simplicio P. Minor thiols cysteine and cysteinylglycine regulate the competition between glutathione and protein SH groups in human platelets subjected to oxidative stress. Arch Biochem Biophys. 380:2000;1-10.
28. Lusini L., Tripodi S.A., Rossi R., Giannerini F., Giustarini D., Del Vecchio M.T., Barbanti G., Cintorino M., Tosi P., Di Simplicio P. Altered glutathione antioxidant metabolism during tumor progression in renal cell carcinoma. Int. J. Cancer. 91:2001;55-59.
29. Chao C.C., Ma Y.S., Stadtman E.R. Modification of protein surface hydrophobicity and methionine oxidation by oxidative systems. Proc. Natl. Acad. Sci. USA. 94:1997;2969-2974.
30. Miki M., Ohnuma H., Mihashi K. Interaction of actin water epsilon-ATP. FEBS Lett. 46:1974;17-19.
31. Estes J.E., Selden L.A., Gershman L.C. Mechanism of action of phalloidin on the polimerization of muscle actin. Biochemistry. 20:1981;708-712.
32. Drewes G., Faulstich H. The enhanced ATPase activity of glutathione-substituted actin provides a quantitative approach to filament stabilization. J Biol Chem. 265:1990;3017-3021.
33. Drewes G., Faulstich H. Cooperative effects on filament stability in actin modified at the C-terminus by substitution or truncation. Eur J Biochem. 212:1993;247-253.
34. Faulstich H., Merkler I., Blackholm H., Stournaras C. Nucleotide in monomeric actin regulates the reactivity of the thiol groups. Biochemistry. 23:1984;1608-1612.
35. Pollard T.D. Actin. Anal Biochem. 134:1983;406-412.
36. Stournaras C., Drewes G., Blackholm H., Merkler I., Faulstich H. Glutathionyl(cysteine-374) actin forms filaments of low mechanical stability. Biochim. Biophys. Acta. 1037:1990;86-91.
37. O'Donoghue S.I., Miki M., dos Remedios C.G. Removing the two C-terminal residues of actin affects the filament structure. Arch Biochem Biophys. 293:1992;110-116.
38. Mossakowska M., Moraczewska J., Khaitlina S., Strzelecka-Golaszewska H. Proteolytic removal of three C-terminal residues of actin alters the monomer-monomer interactions. Biochem J. 289:1993;897-902.
39. Cooper J.A., Walker S.B., Pollard T.D. Pyrene actin documentation of the validity of a sensitive assay for actin polymerization. J Muscle Res Cell Motil. 4:1983;253-262.
40. Crosbie R.H., Miller C., Cheung P., Goodnight T., Muhlrad A., Reisler E. Structural connectivity in actin effect of C-terminal modifications on the properties of actin. Biophys J. 67:1994;1957-1964.
41. Schwyter D., Phillips M., Reisler E. Subtilisin-cleaved actin polymerization and interaction with myosin subfragment 1. Biochemistry. 28:1989;5889-5895.
42. Grant C.M. Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol. 39:2001;533-541.
43. Eaton P., Byers H. L.; Leeds, N.; Ward, M. A.; Shattock, M. J. Detection, quantitation, purification, and identification of cardiac proteins S-thiolated during ischemia and reperfusion. J Biol Chem. 277:2002;9806-9811.
44. Eaton P., Fuller W., Shattock M.J. S-thiolation of HSP27 regulates its multimeric aggregate size independently of phosphorylation. J Biol Chem. 277:2002;21189-21196.
45. Vandekerckhove J., Weber K. Mammalian cytoplasmic actins are the products of at least two genes and differ in primary structure in at least 25 identified positions from skeletal muscle actins. Proc. Natl. Acad. Sci. USA. 75:1978;1106-1110.
46. Elzinga M., Collins J.H., Kuehl W.M., Adelstein R.S. Complete amino-acid sequence of actin of rabbit skeletal muscle. Proc. Natl. Acad. Sci. USA. 70:1973;2687-2691.
47. Milligan R.A., Whittaker M., Safer D. Molecular structure of F-actin and location of surface binding sites. Nature. 348:1990;217-221.
48. Orlova A., Egelman E.H. Structural dynamics of F-actin. I. Changes in the C terminus. J Mol Biol. 245:1995;582-597.
49. Egelman E.H., Orlova A. New insights into actin filament dynamics. Curr Opin Struct Biol. 5:1995;172-180.
50. Holmes K.C., Popp D., Gebhard W., Kabsch W. Atomic model of the actin filament. Nature. 347:1990;44-49.
51. Lorenz M., Popp D., Holmes K.C. Refinement of the F-actin model against x-ray fiber diffraction data by the use of a directed mutation algorithm. J Mol Biol. 234:1993;826-836.
52. Tirion M.M., ben-Avraham D., Lorenz M., Holmes K.C. Normal modes as refinement parameters for the F-actin model. Biophys J. 68:1995;5-12.
53. Hegyi G., Michel H., Shabanowitz J., Hunt D.E., Chatterjie N., Healy-Louie G., Elzinga M. Gln-41 is intermolecularly cross-linked to Lys-113 in F-actin by N-(4-azidobenzoyl)-putrescine. Protein Sci. 1:1992;132-144.
54. Egelman E.H. Actin allostery again? Nat Struct Biol. 8:2001;735-736.
55. Otterbein L.R., Graceffa P., Dominguez R. The crystal structure of uncomplexed actin in the ADP state. Science. 293:2001;708-711.
56. Kabsch W., Mannherz H.G., Suck D., Pai E.F., Holmes K.C. Atomic structure of the actin DNase I complex. Nature. 347:1990;37-44.
57. Orlova A., Prochniewicz E., Egelman E.H. Structural dynamics of F-actin II. Cooperativity in structural transitions. J Mol Biol. 245:1995;598-607.
58. Kuznetsova I., Antropova O. Turoverov, K.; Khaitlina, S. Conformational changes in subdomain I of actin induced by proteolytic cleavage within the DNase I-binding loop energy transfer from tryptophan to AEDANS. FEBS Lett. 383:1996;105-108.
59. Kim E., Reisler E. Intermolecular coupling between loop 38-52 and the C-teminus in actin filaments. Biophys J. 71:1996;1914-1919.
60. Kim E., Reisler E. Intermolecular dynamics and function in actin filaments. Biophys Chem. 86:2000;191-201.
61. Cheung P., Allis C.D., Sassone-Corsi P. Signaling to chromatin through histone modifications. Cell. 103:2000;263-271.
62. Dalle-Donne I., Rossi R., Milzani A., Di Simplicio P., Colombo R. The actin cytoskeleton response to oxidants from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radic Biol Med. 31:2001;1624-1632.
63. Powell S.A., Gurzenda E.M., Wahezi S.E. Actin is oxidized during myocardial ischemia. Free Radic Biol Med. 30:2001;1171-1176.
64. Schwalb H., Olivson A., Li J., Houminer E., Wahezi S.E., Opie L.H., Maulik D., Borman J.B., Powell S.R. Nicorandil decreases postischemic actin oxidation. Free Radic Biol Med. 31:2001;607-614.
65. Barbato R., Menab R., Dainese P., Carafoli E., Schiaffino S., Di Lisa F. Binding of cytosolic proteins to myofibrils in ischemic rat hearts. Circ Res. 78:1996;821-828.
66. Huot J., Houle F., Rousseau S., Deschesnes R.G., Shah G.M., Landry J. SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. J Cell Biol. 143:1998;1361-1373.