DOI: 10.1002/pro.5560070705. MgATP binding to the nucleotide‐binding domains of the eukaryotic cytoplasmic chaperonin induces conformational changes in the putative substrate‐binding domains

MgATP binding to the nucleotide‐binding domains of the eukaryotic cytoplasmic chaperonin induces conformational changes in the putative substrate‐binding domains

10.1002/pro.5560070705

Crossref journal-article

Wiley

Protein Science (311)

Abstract

AbstractThe eukaryotic cytosolic chaperonins are large heterooligomeric complexes with a cylindrical shape, resembling that of the homooligomeric bacterial counterpart, GroEL. In analogy to GroEL, changes in shape of the cytosolic chaperonin have been detected in the presence of MgATP using electron microscopy but, in contrast to the nucleotide‐induced conformational changes in GroEL, no details are available about the specific nature of these changes. The present study identifies the structural regions of the cytosolic chaperonin that undergo conformational changes when MgATP binds to the nucleotide binding domains. It is shown that limited proteolysis with trypsin in the absence of MgATP cleaves each of the eight subunits approximately in half, generating two fragments of ∼ 30 kDa. Using mass spectrometry (MS) and N‐terminal sequence analysis, the cleavage is found to occur in a narrow span of the amino acid sequence, corresponding to the peptide binding regions of GroEL and to the helical protrusion, recently identified in the structure of the substrate binding domain of the archeal group I1 chaperonin. This proteolytic cleavage is prevented by MgATP but not by ATP in the absence of magnesium, ATP analogs (MgATPyS and MgAMP‐PNP) or MgADP. These results suggest that, in analogy to GroEL, binding of MgATP to the nucleotide binding domains of the cytosolic chaperonin induces long range conformational changes in the polypeptide binding domains. It is postulated that despite their different subunit composition and substrate specificity, group I and group I1 chaperonins may share similar, functionally‐important, conformational changes. Additional conformational changes are likely to involve a flexible helix‐loop‐helix motif, which is characteristic for all group II chaperonins.

Bibliography

Szpikowska, B. K., Sherman, M. A., Mas, M. T., & Swiderek, K. M. (1998). MgATP binding to the nucleotideâbinding domains of the eukaryotic cytoplasmic chaperonin induces conformational changes in the putative substrateâbinding domains. Protein Science, 7(7), 1524â1530. Portico.

Authors 4

Barbara K. Szpikowska (first)
Mark A. Sherman (additional)
Maria T. Mas (additional)
Kristine M. Swiderek (additional)

References 31 Referenced 28

10.1073/pnas.93.20.11115
10.1038/nsb0296-170
10.1038/nsb1295-1083
10.1073/pnas.90.9.3978
10.1021/ac00120a019
10.1016/1044-0305(95)00192-G
{'key': 'e_1_2_1_8_1', 'first-page': '304', 'volume-title': 'Methods: A companion to Methods in Enzymology', 'author': 'Davis MT', 'year': '1994'} / Methods: A companion to Methods in Enzymology by Davis MT (1994)
{'key': 'e_1_2_1_9_1', 'volume-title': 'The chaperonins', 'author': 'Ellis RJ', 'year': '1996'} / The chaperonins by Ellis RJ (1996)
10.1002/j.1460-2075.1992.tb05582.x
10.1016/0092-8674(92)90622-J / Cell / A cytoplasmic chaperonin that catalyzes ß‐actin folding by Gao Y (1992)
10.1038/355033a0
10.1074/jbc.271.1.238
10.1006/abio.1995.1070
10.1016/0014-5793(94)01408-S
10.1096/fasebj.10.1.8566534 / FASEB J / Peptide mass fingerprinting of chaperonin‐containing TCP‐I (CCT) and copurifying proteins by Hynes G (1996)
10.1016/0968-0004(94)90058-2
10.1016/S0092-8674(00)80408-0
10.1016/S0960-9822(94)00024-2
10.1111/j.1432-1033.1995.0003i.x
10.1016/0378-1119(94)00880-2
10.1038/358249a0
10.1016/S0006-3495(94)80489-8
10.1021/bi962830o
10.1128/MCB.14.5.2895
{'key': 'e_1_2_1_26_1', 'first-page': '2895', 'article-title': 'Chaperonin‐mediated folding of vertebrate actin‐related protein and gamma‐globulin', 'volume': '14', 'author': 'Melki R', 'year': '1993', 'journal-title': 'J Cell Biol'} / J Cell Biol / Chaperonin‐mediated folding of vertebrate actin‐related protein and gamma‐globulin by Melki R (1993)
10.1002/pro.5560050715
10.1073/pnas.90.24.11975
10.1016/S0092-8674(00)81342-2
10.1016/1044-0305(96)00057-8
10.1038/41944
10.1038/358245a0

Dates

Type	When
Created	16 years, 6 months ago (Feb. 10, 2009, 1:34 a.m.)
Deposited	1 year, 9 months ago (Oct. 28, 2023, 8:25 p.m.)
Indexed	1 year, 2 months ago (June 4, 2024, 1:12 a.m.)
Issued	27 years, 1 month ago (July 1, 1998)
Published	27 years, 1 month ago (July 1, 1998)
Published Online	16 years, 7 months ago (Dec. 31, 2008)
Published Print	27 years, 1 month ago (July 1, 1998)

Funders 0

None

BibTeX

@article{Szpikowska_1998, title={MgATP binding to the nucleotide‐binding domains of the eukaryotic cytoplasmic chaperonin induces conformational changes in the putative substrate‐binding domains}, volume={7}, ISSN={1469-896X}, url={http://dx.doi.org/10.1002/pro.5560070705}, DOI={10.1002/pro.5560070705}, number={7}, journal={Protein Science}, publisher={Wiley}, author={Szpikowska, Barbara K. and Sherman, Mark A. and Mas, Maria T. and Swiderek, Kristine M.}, year={1998}, month=jul, pages={1524–1530} }

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