Hydrogen peroxide induces the dissociation of GroEL into monomers that can facilitate the reactivation of oxidatively inactivated rhodanese

International Journal of Biochemistry and Cell Biology

Volumn 36, Issue 3, 2004, Pages 505-518

  Melkani, Girish C ^a   McNamara, Case ^a,c   Zardeneta, Gustavo ^b   Mendoza, Jose A ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chaperonin; Dissociation; GroEL; Monomers; Oxidative stress; Protein protein interaction; Reactivation; Rhodanese

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN; HYDROGEN PEROXIDE; MONOMER; THIOSULFATE SULFURTRANSFERASE; UREA;

ARTICLE; CIRCULAR DICHROISM; COMPARATIVE STUDY; DISSOCIATION; ENZYME DENATURATION; ENZYME INACTIVATION; ENZYME METABOLISM; ENZYME REACTIVATION; FLUORESCENCE SPECTROSCOPY; GEL ELECTROPHORESIS; HYDROPHOBICITY; LIGHT SCATTERING; MONITORING; OXIDATION; OXIDATIVE STRESS; PROTEIN FOLDING; PROTEIN STRUCTURE; SEDIMENTATION; STRUCTURE ANALYSIS;

EID: 0348110316     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2003.08.012     Document Type: Article

References (60)

1. Atmane, N., Dairou, J., Paul, A., Dupret, J. M., & Rodrigues-Lima, F. Redox regulation of the human xenobiotic-metabolizing enzyme arylamine N-acetyltransferase 1 (NAT1) reversible inactivation by hydrogen peroxide. Journal of Biological Chemistry, in press.
2. Barbirz S., Jakob U., Glocker M. Mass spectrometry unravels disulfide bond formation as the mechanism that activates a molecular chaperone. Journal of Biological Chemistry. 275:2000;18759-18766.
3. Borutaite V., Brown G.C. Caspases are reversibly inactivated by hydrogen peroxide. FEBS Letters. 500:2001;114-118.
4. 2+ GroEL interactions. Journal of Biological Chemistry. 273:1998;3257-3263.
5. Cabiscol E., Belli G., Tamarit J., Echave P., Herrero E., Ros J. Mitochondrial Hsp60, resistance to oxidative stress, and the labile iron pool are closely connected in Saccharomyces cerevisiae. Journal of Biological Chemistry. 277:2002;44531-44538.
6. Cabiscol E., Piulats E., Echave P., Herrero E., Ros J. Oxidative stress promotes specific protein damage in saccharomyces cerevisiae. Journal of Biological Chemistry. 275:2000;27393-27398.
7. Chen S.J., Sun T.X., Akhtar N.J., Liang J.N. Oxidation of human lens recombinants αA-crystallin and cysteine-deficient mutants. Journal of Molecular Biology. 305:2001;969-976.
8. Clark A.C., Hugo E., Frieden C. Determination of regions in the dihydrofolate reductase structure that interact with the molecular chaperonin GroEL. Biochemistry. 35:1996;5893-5901.
9. Clark A.C., Ramanathan R., Frieden C. Purification of GroEL with low fluorescence background. Methods in Enzymology. 290:1998;100-118.
10. Conconi M., SzwedaL L.A., Levine R.L., Stadtman E.R., Friguet B. Age-related decline of rat liver multicatalytic proteinase activity and protection from oxidative inactivation by heatshock protein 90. Archives of Biochemistry and Biophysics. 331:1996;232-240.
11. Cuzzocrea S., Riley D.P., Caputi A.P., Salvemini D. Antioxidant therapy: A new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacological Review. 53:2001;135-159.
12. Del Fierro D., Zardeneta G., Mendoza J.A. Alpha-crystallin facilitates the reactivation of hydrogen peroxide-inactivated rhodanese. Biochemical and Biophysical Research Communications. 274:2000;461-466.
13. Dukan S., Farewell A., Ballesteros M., Taddei F., Radman M., Nystrom T. Protein oxidation in response to increased transcriptional or translational errors. Proceedings of the National Academy of Sciences of the United States of America. 97:2000;5746-5749.
14. Ericsson M.C., Tarnvik A., Kuoppa K., Sandstrom G., Sjostedt A. Increased synthesis of DnaK, GroEL, and GroES homologs by Francisella tularensis LVS in response to heat and hydrogen peroxide. Infections and Immunity. 62:1994;178-183.
15. Falke S., Fisher M.T., Gogol E.P. Structural changes in GroEL effected by binding a denatured protein substrate. Journal of Molecular Biology. 11:2001;569-577.
16. Fisher M.T. Promotion of the in vitro renaturation of dodecameric glutamine synthetase from Escherichia coli in the presence of GroEL (chaperonin-60) and ATP. Biochemistry. 31:1992;3955-3963.
17. Fliss H., Weissbach H., Brot N. Oxidation of methionine residues in proteins of activated human neutrophils. Proceedings of the National Academy of Sciences of the United States of America. 80:1983;7160-7164.
18. Gibbons D.L., Horowitz P.M. Exposure of hydrophobic surfaces on the chaperonin GroEL oligomer by protonation or modification of His-401. Journal of Biological Chemistry. 270:1995;7335-7340.
19. Gibbons D.L., Horowitz P.M. Ligand-induced conformational changes in the apical domain of the chaperonin GroEL. Journal of Biological Chemistry. 271:1996;238-243.
20. Giulivi C., Pacifici R.E., Davies K.J.A. Exposure of hydrophobic moieties promotes the selective degradation of hydrogen peroxide-modified hemoglobin by the multicatalytic proteinase complex, proteasome. Archives of Biochemistry and Biophysics. 311:1994;329-341.
21. Gorovits B.M., Seale J.W., Horowitz P.M. Residual structure in urea-denatured chaperonin GroEL. Biochemistry. 34:1995;13928-13933.
22. Graumann J., Lilie H., Tang X., Tucker K.A., Hoffmann J.H., Vijayalakshmi J., Saper M., Bardwell J.C., Jakob U. Activation of the redox-regulated molecular chaperone Hsp33-a two-step mechanism. Structure. 9:2001;377-387.
23. Gustavson N., Harndahl U., Emanuelsson A., Roepstorf P., Sundby C. Methionine sulfoxidation of the chloroplast small heat shock protein and conformational changes in the oligomer. Protein Science. 8:1999;2506-2512.
24. Hanawa T., Yamamoto T., Kamiya S. Listeria monocytogenes can grow in macrophages without the aid of proteins induced by environmental stresses. Infections and Immunity. 63:1995;4595-4599.
25. Hanson S.R., Chen A.A., Smith J.B., Lou M.F. Thiolation of the gamma B-crystallins in intact bovine lens exposed to hydrogen peroxide. Journal of Biological Chemistry. 274:1999;4735-4742.
26. Hemmingsen S.M., Woolford C., van der Vies S.M., Tilly K., Dennis D.T., Georgopoulos C.P., Hendrix R.W., Ellis R.J. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature. 333:1988;330-334.
27. Hiner A.N.P., Hernandez Ruiz J., Rodriguez Lopez J.N., Garcia Canovas F., Brisset N.C., Smith A.T., Arnao M.B., Acosta M. Reactions of the class II peroxidases, lignin peroxidase and Arthromyces ramosus peroxidase, with hydrogen peroxidase. Journal of Biological Chemistry. 277:2002;26879-26885.
28. Holl-Neugebauer B., Rudolph R. Reconstitution of a heat shock effect in vitro: Influence of GroE on the thermal aggregation of alpha-glucosidase from yeast. Biochemistry. 30:1991;11609-11614.
29. Huang F.Y., Chia C.M., Ho Y. The formation of oxidatively induced high-molecular-weight aggregate of alpha-/gamma-crystallins. Biochemical and Biophysical Research Communications. 260:1999;60-65.
30. Iametti S., Bera A.K., Vecchio G., Grinberg A., Bernhardt R., Bonomi F. GroEL-assisted refolding of adrenodoxin during chemical cluster insertion. European Journal of Biochemistry. 268:2001;2421-2429.
31. Jacob U., Eser M., Bardwell J.C. Redox switch of hsp33 has a novel zinc-binding motif. Journal of Biological Chemistry. 275:2000;38302-38310.
32. Jakob U., Muse W., Eser M., Bardwell J.C. Chaperone activity with a redox switch. Cell. 96:1999;341-352.
33. Kalapos M.P. Methylglyoxal in living organisms: Chemistry, biochemistry, toxicology and biological implications. Toxicology Letters. 110(3):1999;145-175.
34. Kurzban G.P., Horowitz P.M. Purification of bovine liver rhodanese by low-pH column chromatography. Protein Expression and Purification. 2:1991;379-384.
35. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
36. Li S., Nguyen T.H., Schoneich C., Borchardt R.T. Aggregation and precipitation of human relaxin induced by metal-catalyzed oxidation. Biochemistry. 34:1995;5762-5772.
37. Lissin N.M. In vitro dissociation and self-assembly of three chaperonin 60s: The role of ATP. FEBS Letters. 361:1995;55-60.
38. Lissin N.M., Venyaminov S.Yu., Girshovivh A.S. (Mg-ATP)-dependent self-assembly of molecular chaperone GroEL. Nature. 348:1990;339-342.
39. Lundrigan M.D., Arceneaux J.E., Zhu W., Byers B.R. Enhanced hydrogen peroxide sensitivity and altered stress protein expression in iron-starved mycobacterium smegmatis. Biometals. 3:1997;215-225.
40. Martin J., Hartl F.U. Chaperone-assisted protein folding. Current Opinion Structural Biology. 7:1997;41-52.
41. Martin J., Horwich A.L., Hartl F.U. Prevention of protein denaturation under heat stress by the chaperonin Hsp60. Science. 258:1992;995-998.
42. Melkani G.C., Zardeneta G., Mendoza J.A. GroEL interacts transiently with oxidatively inactivated rhodanese facilitating its reactivation. Biochemical and Biophysical Research Communications. 294:2002;893-899.
43. Mendoza J.A., Del Campo G. Ligand-induced conformational changes of GroEL are dependent on the bound substrate polypeptide. Journal of Biological Chemistry. 271:1996;16344-16349.
44. Mendoza J.A., Demeler B., Horowitz P.M. Bound substrate polypeptides can generally stabilize the tetradecameric structure of Cpn60 and induce its reassembly from monomers. Journal of Biological Chemistry. 269:1994;2447-2451.
45. Mendoza J.A., Horowitz P.M. Sulfhydryl modification of E. coli Cpn60 leads to loss of its ability to support refolding of rhodanese but not to form a binary complex. Journal of Protein Chemistry. 11:1992;589-594.
46. Mendoza J.A., Lorimer G.H., Horowitz P.M. Chaperonin cpn60 from Escherichia coli protects the mitochondrial enzyme rhodanese against heat inactivation and supports folding at elevated temperatures. Journal of Biological Chemistry. 267:1992;17631-17634.
47. Mendoza J.A., Martinez J.L., Horowitz P.M. Tetradecameric chaperonin 60 can be assembled in vitro from monomers in a process that is ATP independent. Biochimica et Biophysica Acta. 1247:1995;209-214.
48. Mendoza J.A., Rogers E., Lorimer G.H., Horowitz P.M. Chaperonins facilitate the in vitro folding of monomeric mitochondrial rhodanese. Journal of Biological Chemistry. 266:1991;13044-13049.
49. Mendoza J.A., Wilson M., Joves F., Ackermann E. Thermostabilization of enzymes by the chaperonin GroEL. Biotechnical Techniques. 10:1996;535-540.
50. Milzani A., Rossi R., Simplicio P.D., Giustarini D., Colombo R., Dalledonne I. The oxidation produced by hydrogen peroxide on Ca-ATP-G-actin. Protein Science. 9:2000;1774-1782.
51. Ploegman J.H., Drent G.H., Kalk K.H., Hol W.G.J., Heinrikson R.L., Keim P., Weng L., Russell J. The covalent and tertiary structure of bovine liver rhodanese. Nature. 273:1978;1245-1249.
52. Raman B., Siva Kumar L.V., Ramakrishna T., Mohan Rao Ch. Redox-regulated chaperone function and conformational changes of Escherichia coli Hsp33. FEBS Letters. 489:2001;19-24.
53. Rosen C.G., Weber G. Dimer formation from 1-amino-8-naphthalenesulfonate catalyzed by bovine serum albumin. A new fluorescent molecule with exceptional binding properties. Biochemistry. 8:1969;3915-3920.
54. Siezen R.J., Coppin C.M., Kaplan E.D., Dwyer D., Thompson J.A. Oxidative modifications of crystallins induced in calf lenses in vitro by hydrogen peroxide. Experimental Eye Research. 48:1989;225-235.
55. Teshima S., Rokutan K., Takahashi M., Nikawa T., Kishi K. Induction of heat shock proteins and their possible roles in macrophages during activation by macrophage colony-stimulating factor. Biochemical Journal. 315:1996;497-504.
56. Vogt W. Oxidation of methionyl residues in proteins: Tools, targets, and reversal. Free Radical Biology and Medicine. 18:1995;93-105.
57. Voziyan P.A., Fisher M.T. Polyols induce ATP-independent folding of GroEL-bound bacterial glutamine synthetase. Archives of Biochemistry and Biophysics. 397:2002;293-29743.
58. Wang K., Spector A. Alpha-crystallin can act as a chaperone under conditions of oxidative stress. Investigation of Opthalmological and Visual Sciences. 36:1995;3111-3121.
59. Whitelegge J.P., Penn B., To T., Johnson J., Waring A., Sherman M., Stevens R.L., Fluharty C.B., Faull K.F., Fluharty A.L. Methionine oxidation within the cerebroside-sulfate activator protein (CSAct or Saposin B). Protein Science. 9:2000;1618-1630.
60. Zhang S., Li J., Wang C.C. GroEL-assisted dehydrogenase folding mediated by coenzyme is ATP-independent. Biochemical and Biophysical Research Communications. 285:2001;277-282.