Structural basis for active single and double ring complexes in human mitochondrial Hsp60-Hsp10 chaperonin.
Adenosine Diphosphate
/ chemistry
Adenosine Triphosphate
/ chemistry
Chaperonin 10
/ chemistry
Chaperonin 60
/ chemistry
Cryoelectron Microscopy
Crystallography, X-Ray
Cytosol
/ chemistry
Humans
Hydrogen Bonding
Hydrolysis
Mitochondria
/ chemistry
Mitochondrial Proteins
/ chemistry
Protein Binding
Protein Conformation
Protein Engineering
Protein Folding
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
21 04 2020
21 04 2020
Historique:
received:
22
10
2018
accepted:
17
03
2020
entrez:
23
4
2020
pubmed:
23
4
2020
medline:
4
8
2020
Statut:
epublish
Résumé
mHsp60-mHsp10 assists the folding of mitochondrial matrix proteins without the negative ATP binding inter-ring cooperativity of GroEL-GroES. Here we report the crystal structure of an ATP (ADP:BeF
Identifiants
pubmed: 32317635
doi: 10.1038/s41467-020-15698-8
pii: 10.1038/s41467-020-15698-8
pmc: PMC7174398
doi:
Substances chimiques
Chaperonin 10
0
Chaperonin 60
0
HSPD1 protein, human
0
Mitochondrial Proteins
0
Adenosine Diphosphate
61D2G4IYVH
Adenosine Triphosphate
8L70Q75FXE
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1916Subventions
Organisme : NIGMS NIH HHS
ID : P41 GM103310
Pays : United States
Organisme : NCRR NIH HHS
ID : P41 RR001209
Pays : United States
Organisme : NIH HHS
ID : S10 OD019994
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR026473
Pays : United States
Références
Levy-Rimler, G., Bell, R. E., Ben-Tal, N. & Azem, A. Type I chaperonins: not all are created equal. FEBS Lett. 529, 1–5 (2002).
pubmed: 12354603
doi: 10.1016/S0014-5793(02)03178-2
Cheng, M. Y. et al. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337, 620–625 (1989).
pubmed: 2645524
doi: 10.1038/337620a0
Christensen, J. H. et al. Inactivation of the hereditary spastic paraplegia-associated Hspd1 gene encoding the Hsp60 chaperone results in early embryonic lethality in mice. Cell Stress Chaperones 15, 851–863 (2010).
pubmed: 20393889
pmcid: 3024079
doi: 10.1007/s12192-010-0194-x
Cappello, F., Conway de Macario, E., Marasa, L., Zummo, G. & Macario, A. J. Hsp60 expression, new locations, functions and perspectives for cancer diagnosis and therapy. Cancer Biol. Ther. 7, 801–809 (2008).
pubmed: 18497565
doi: 10.4161/cbt.7.6.6281
Osterloh, A. et al. Lipopolysaccharide-free heat shock protein 60 activates T cells. J. Biol. Chem. 279, 47906–47911 (2004).
pubmed: 15371451
doi: 10.1074/jbc.M408440200
Johnson, B. J. et al. Heat shock protein 10 inhibits lipopolysaccharide-induced inflammatory mediator production. J. Biol. Chem. 280, 4037–4047 (2005).
pubmed: 15546885
doi: 10.1074/jbc.M411569200
Xanthoudakis, S. et al. Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J. 18, 2049–2056 (1999).
pubmed: 10205159
pmcid: 1171289
doi: 10.1093/emboj/18.8.2049
Knowlton, A. A. & Gupta, S. HSP60, Bax, and cardiac apoptosis. Cardiovas. Tox 3, 263–268 (2003).
doi: 10.1385/CT:3:3:263
Ban, H. S., Shimizu, K., Minegishi, H. & Nakamura, H. Identification of HSP60 as a primary target of o-carboranylphenoxyacetanilide, an HIF-1alpha inhibitor. J. Am. Chem. Soc. 132, 11870–11871 (2010).
pubmed: 20695501
doi: 10.1021/ja104739t
Chun, J. N. et al. Cytosolic Hsp60 is involved in the NF-kappaB-dependent survival of cancer cells via IKK regulation. PLoS ONE 5, e9422 (2010).
pubmed: 20351780
pmcid: 2843631
doi: 10.1371/journal.pone.0009422
Hansen, J. et al. A novel mutation in the HSPD1 gene in a patient with hereditary spastic paraplegia. J. Neurol. 254, 897–900 (2007).
pubmed: 17420924
doi: 10.1007/s00415-006-0470-y
Hansen, J. J. et al. Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am. J. Hum. Genet. 70, 1328–1332 (2002).
pubmed: 11898127
pmcid: 447607
doi: 10.1086/339935
Magen, D. et al. Mitochondrial hsp60 chaperonopathy causes an autosomal-recessive neurodegenerative disorder linked to brain hypomyelination and leukodystrophy. Am. J. Hum. Genet. 83, 30–42 (2008).
pubmed: 18571143
pmcid: 2443844
doi: 10.1016/j.ajhg.2008.05.016
Briones, P. et al. A new case of multiple mitochondrial enzyme deficiencies with decreased amount of heat shock protein 60. J. Inherit. Metab. Dis. 20, 569–577 (1997).
pubmed: 9266394
doi: 10.1023/A:1005303008439
Venner, T. J. & Gupta, R. S. Nucleotide sequence of mouse HSP60 (chaperonin, GroEL homolog) cDNA. Biochim Biophys. Acta 1087, 336–338 (1990).
pubmed: 1979012
doi: 10.1016/0167-4781(90)90008-P
Venner, T. J., Singh, B. & Gupta, R. S. Nucleotide sequences and novel structural features of human and Chinese hamster hsp60 (chaperonin) gene families. DNA Cell Biol. 9, 545–552 (1990).
pubmed: 1980192
doi: 10.1089/dna.1990.9.545
Rye, H. S. et al. Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388, 792–798 (1997).
pubmed: 9285593
doi: 10.1038/42047
Xu, Z., Horwich, A. L. & Sigler, P. B. The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388, 741–750 (1997).
pubmed: 9285585
doi: 10.1038/41944
Horovitz, A., Fridmann, Y., Kafri, G. & Yifrach, O. Review: allostery in chaperonins. J. Struct. Biol. 135, 104–114 (2001).
pubmed: 11580260
doi: 10.1006/jsbi.2001.4377
Saibil, H. R., Fenton, W. A., Clare, D. K. & Horwich, A. L. Structure and allostery of the chaperonin GroEL. J. Mol. Biol. 425, 1476–1487 (2013).
pubmed: 23183375
doi: 10.1016/j.jmb.2012.11.028
Levy-Rimler, G. et al. The effect of nucleotides and mitochondrial chaperonin 10 on the structure and chaperone activity of mitochondrial chaperonin 60. Eur. J. Biochem./FEBS 268, 3465–3472 (2001).
doi: 10.1046/j.1432-1327.2001.02243.x
Yifrach, O. & Horovitz, A. Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34, 5303–5308 (1995).
pubmed: 7727391
doi: 10.1021/bi00016a001
Sameshima, T., Iizuka, R., Ueno, T. & Funatsu, T. Denatured proteins facilitate the formation of the football-shaped GroEL-(GroES)2 complex. Biochem. J. 427, 247–254 (2010).
pubmed: 20121703
doi: 10.1042/BJ20091845
Ye, X. & Lorimer, G. H. Substrate protein switches GroE chaperonins from asymmetric to symmetric cycling by catalyzing nucleotide exchange. Proc. Natl Acad. Sci. USA 110, E4289–E4297 (2013).
pubmed: 24167257
doi: 10.1073/pnas.1317702110
Yang, D., Ye, X. & Lorimer, G. H. Symmetric GroEL:GroES2 complexes are the protein-folding functional form of the chaperonin nanomachine. Proc. Natl Acad. Sci. USA 110, E4298–E4305 (2013).
pubmed: 24167279
doi: 10.1073/pnas.1318862110
Nielsen, K. L. & Cowan, N. J. A single ring is sufficient for productive chaperonin-mediated folding in vivo. Mol. Cell 2, 93–99 (1998).
pubmed: 9702195
doi: 10.1016/S1097-2765(00)80117-3
Weiss, C., Jebara, F., Nisemblat, S. & Azem, A. Dynamic Complexes in the Chaperonin-Mediated Protein Folding Cycle. Front. Mol. Biosci. 3, 80 (2016).
pubmed: 28008398
pmcid: 5143341
doi: 10.3389/fmolb.2016.00080
Nisemblat, S., Yaniv, O., Parnas, A., Frolow, F. & Azem, A. Crystal structure of the human mitochondrial chaperonin symmetrical football complex. Proc. Natl Acad. Sci. USA 112, 6044–6049 (2015).
pubmed: 25918392
doi: 10.1073/pnas.1411718112
Parnas, A. et al. Identification of elements that dictate the specificity of mitochondrial Hsp60 for its co-chaperonin. PLoS ONE 7, e50318 (2012).
pubmed: 23226518
pmcid: 3514286
doi: 10.1371/journal.pone.0050318
Scheres, S. H. & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 9, 853–854 (2012).
pubmed: 22842542
pmcid: 22842542
doi: 10.1038/nmeth.2115
Hunt, J. F., Weaver, A. J., Landry, S. J., Gierasch, L. & Deisenhofer, J. The crystal structure of the GroES co-chaperonin at 2.8 A resolution. Nature 379, 37–45 (1996).
pubmed: 8538739
doi: 10.1038/379037a0
Parnas, A. et al. The MitCHAP-60 disease is due to entropic destabilization of the human mitochondrial Hsp60 oligomer. J. Biol. Chem. 284, 28198–28203 (2009).
pubmed: 19706612
pmcid: 2788871
doi: 10.1074/jbc.M109.031997
Ma, J. & Karplus, M. The allosteric mechanism of the chaperonin GroEL: a dynamic analysis. Proc. Natl Acad. Sci. USA 95, 8502–8507 (1998).
pubmed: 9671707
doi: 10.1073/pnas.95.15.8502
Braig, K. et al. The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 371, 578–586, https://doi.org/10.1038/371578a0 (1994).
doi: 10.1038/371578a0
pubmed: 7935790
Yifrach, O. & Horovitz, A. Allosteric control by ATP of non-folded protein binding to GroEL. J. Mol. Biol. 255, 356–361 (1996).
pubmed: 8568880
doi: 10.1006/jmbi.1996.0028
Fei, X., Yang, D., LaRonde-LeBlanc, N. & Lorimer, G. H. Crystal structure of a GroEL-ADP complex in the relaxed allosteric state at 2.7 A resolution. Proc. Natl Acad. Sci. USA 110, E2958–E2966 (2013).
pubmed: 23861496
doi: 10.1073/pnas.1311996110
Fei, X., Ye, X., LaRonde, N. A. & Lorimer, G. H. Formation and structures of GroEL:GroES2 chaperonin footballs, the protein-folding functional form. Proc. Natl Acad. Sci. USA 111, 12775–12780 (2014).
pubmed: 25136110
doi: 10.1073/pnas.1412922111
Gruber, R., Levitt, M. & Horovitz, A. Sequential allosteric mechanism of ATP hydrolysis by the CCT/TRiC chaperone is revealed through Arrhenius analysis. Proc. Natl Acad. Sci. USA 114, 5189–5194 (2017).
pubmed: 28461478
doi: 10.1073/pnas.1617746114
pmcid: 28461478
Lorimer, G. H., Fei, X. & Ye, X. The GroEL chaperonin: a protein machine with pistons driven by ATP binding and hydrolysis. Philos. Trans. R Soc. Lond. B Biol. Sci. 373, https://doi.org/10.1098/rstb.2017.0179 (2018).
Todd, M. J., Viitanen, P. V. & Lorimer, G. H. Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265, 659–666 (1994).
pubmed: 7913555
doi: 10.1126/science.7913555
Sewell, B. T. et al. A mutant chaperonin with rearranged inter-ring electrostatic contacts and temperature-sensitive dissociation. Nat. Struct. Mol. Biol. 11, 1128–1133 (2004).
pubmed: 15475965
doi: 10.1038/nsmb844
Sot, B. et al. Ionic interactions at both inter-ring contact sites of GroEL are involved in transmission of the allosteric signal: a time-resolved infrared difference study. Protein Sci. 14, 2267–2274 (2005).
pubmed: 16081650
pmcid: 2253480
doi: 10.1110/ps.051469605
Bandyopadhyay, B., Mondal, T., Unger, R. & Horovitz, A. Contact order is a determinant for the dependence of GFP folding on the chaperonin GroEL. Biophys. J. 116, 42–48 (2019).
pubmed: 30577980
doi: 10.1016/j.bpj.2018.11.019
Viitanen, P. V. et al. Purification of mammalian mitochondrial chaperonin 60 through in vitro reconstitution of active oligomers. Methods Enzymol. 290, 203–217 (1998).
pubmed: 9534164
doi: 10.1016/S0076-6879(98)90020-9
Horwich, A. L. & Fenton, W. A. Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding. Q Rev. Biophys. 42, 83–116 (2009).
pubmed: 19638247
doi: 10.1017/S0033583509004764
Koike-Takeshita, A., Arakawa, T., Taguchi, H. & Shimamura, T. Crystal structure of a symmetric football-shaped GroEL:GroES2-ATP14 complex determined at 3.8A reveals rearrangement between two GroEL rings. J. Mol. Biol. 426, 3634–3641 (2014).
pubmed: 25174333
doi: 10.1016/j.jmb.2014.08.017
Goodsell, D. S. & Olson, A. J. Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29, 105–153 (2000).
pubmed: 10940245
doi: 10.1146/annurev.biophys.29.1.105
Andre, I., Strauss, C. E., Kaplan, D. B., Bradley, P. & Baker, D. Emergence of symmetry in homooligomeric biological assemblies. Proc. Natl Acad. Sci. USA 105, 16148–16152 (2008).
pubmed: 18849473
doi: 10.1073/pnas.0807576105
Yan, X. et al. GroEL ring separation and exchange in the chaperonin reaction. Cell 172, 605–617 e611 (2018).
pubmed: 29336887
doi: 10.1016/j.cell.2017.12.010
Farr, G. W. et al. Folding with and without encapsulation by cis- and trans-only GroEL-GroES complexes. EMBO J. 22, 3220–3230 (2003).
pubmed: 12839985
pmcid: 165638
doi: 10.1093/emboj/cdg313
Bigman, L. S. & Horovitz, A. Reconciling the controversy regarding the functional importance of bullet- and football-shaped GroE complexes. J. Biol. Chem. 294, 13527–13529 (2019).
pubmed: 31371450
doi: 10.1074/jbc.AC119.010299
Opatowsky, Y., Chomsky-Hecht, O., Kang, M. G., Campbell, K. P. & Hirsch, J. A. The voltage-dependent calcium channel beta subunit contains two stable interacting domains. J. Biol. Chem. 278, 52323–52332 (2003).
pubmed: 14559910
doi: 10.1074/jbc.M303564200
Goloubinoff, P., Diamant, S., Weiss, C. & Azem, A. GroES binding regulates GroEL chaperonin activity under heat shock. FEBS Lett. 407, 215–219 (1997).
pubmed: 9166902
doi: 10.1016/S0014-5793(97)00348-7
Sokolovski, M., Bhattacherjee, A., Kessler, N., Levy, Y. & Horovitz, A. Thermodynamic protein destabilization by GFP tagging: a case of interdomain allostery. Biophysical J. 109, 1157–1162 (2015).
doi: 10.1016/j.bpj.2015.04.032
Kabsch, W. Xds. Acta Crystallogr D. Biol. Crystallogr 66, 125–132 (2010).
pubmed: 20124692
pmcid: 2815665
doi: 10.1107/S0907444909047337
Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D. Biol. Crystallogr. 68, 352–367 (2012).
pubmed: 22505256
pmcid: 3322595
doi: 10.1107/S0907444912001308
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126–2132 (2004).
pubmed: 15572765
doi: 10.1107/S0907444904019158
Glaeser, R. M., Typke, D., Tiemeijer, P. C., Pulokas, J. & Cheng, A. Precise beam-tilt alignment and collimation are required to minimize the phase error associated with coma in high-resolution cryo-EM. J. Struct. Biol. 174, 1–10 (2011).
pubmed: 21182964
doi: 10.1016/j.jsb.2010.12.005
Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41–60 (2005).
pubmed: 15890530
pmcid: 15890530
doi: 10.1016/j.jsb.2005.03.010
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 5494038
pmcid: 5494038
doi: 10.1038/nmeth.4193
Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
pubmed: 26278980
pmcid: 26278980
doi: 10.1016/j.jsb.2015.08.008
Roseman, A. M. FindEM—a fast, efficient program for automatic selection of particles from electron micrographs. J. Struct. Biol. 145, 91–99 (2004).
pubmed: 15065677
doi: 10.1016/j.jsb.2003.11.007
Lander, G. C. et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95–102 (2009).
pubmed: 19263523
pmcid: 2775544
doi: 10.1016/j.jsb.2009.01.002
Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
pubmed: 23000701
pmcid: 23000701
doi: 10.1016/j.jsb.2012.09.006
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
doi: 10.1038/nmeth.4169
Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63–65 (2014).
doi: 10.1038/nmeth.2727
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213–221 (2010).
pubmed: 20124702
pmcid: 2815670
doi: 10.1107/S0907444909052925