A concerted ATPase cycle of the protein transporter AAA-ATPase Bcs1.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
11 10 2023
11 10 2023
Historique:
received:
16
03
2023
accepted:
18
09
2023
medline:
1
11
2023
pubmed:
12
10
2023
entrez:
11
10
2023
Statut:
epublish
Résumé
Bcs1, a homo-heptameric transmembrane AAA-ATPase, facilitates folded Rieske iron-sulfur protein translocation across the inner mitochondrial membrane. Structures in different nucleotide states (ATPγS, ADP, apo) provided conformational snapshots, but the kinetics and structural transitions of the ATPase cycle remain elusive. Here, using high-speed atomic force microscopy (HS-AFM) and line scanning (HS-AFM-LS), we characterized single-molecule Bcs1 ATPase cycling. While the ATP conformation had ~5600 ms lifetime, independent of the ATP-concentration, the ADP/apo conformation lifetime was ATP-concentration dependent and reached ~320 ms at saturating ATP-concentration, giving a maximum turnover rate of 0.17 s
Identifiants
pubmed: 37821516
doi: 10.1038/s41467-023-41806-5
pii: 10.1038/s41467-023-41806-5
pmc: PMC10567702
doi:
Substances chimiques
Adenosine Triphosphatases
EC 3.6.1.-
ATPases Associated with Diverse Cellular Activities
EC 3.6.4.-
Mitochondrial Proteins
0
Membrane Transport Proteins
0
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
6369Subventions
Organisme : NINDS NIH HHS
ID : R01 NS110790
Pays : United States
Organisme : NCCIH NIH HHS
ID : DP1 AT010874
Pays : United States
Informations de copyright
© 2023. Springer Nature Limited.
Références
Pilon, M. & Schekman, R. Protein translocation: how Hsp70 pulls it off. Cell 97, 679–682 (1999).
pubmed: 10380919
doi: 10.1016/S0092-8674(00)80780-1
Schatz, G. & Dobberstein, B. Common principles of protein translocation across membranes. Science 271, 1519–1526 (1996).
pubmed: 8599107
doi: 10.1126/science.271.5255.1519
Rapoport, T. A., Li, L. & Park, E. Structural and mechanistic insights into protein translocation. Annu. Rev. Cell Dev. Biol. 33, 369–390 (2017).
pubmed: 28564553
doi: 10.1146/annurev-cellbio-100616-060439
Lill, R. Function and biogenesis of iron-sulphur proteins. Nature 460, 831–838 (2009).
pubmed: 19675643
doi: 10.1038/nature08301
Graham, L. A., Brandt, U., Sargent, J. S. & Trumpower, B. L. Mutational analysis of assembly and function of the iron-sulfur protein of the cytochrome bc1 complex in Saccharomyces cerevisiae. J. Bioenerg. Biomembr. 25, 245–257 (1993).
pubmed: 8394320
doi: 10.1007/BF00762586
Brandt, U., Yu, L., Yu, C. A. & Trumpower, B. L. The mitochondrial targeting presequence of the Rieske iron-sulfur protein is processed in a single step after insertion into the cytochrome bc1 complex in mammals and retained as a subunit in the complex. J. Biol. Chem. 268, 8387–8390 (1993).
pubmed: 8386158
doi: 10.1016/S0021-9258(18)52883-0
Letts, J. A. & Sazanov, L. A. Clarifying the supercomplex: the higher-order organization of the mitochondrial electron transport chain. Nat. Struct. Mol. Biol. 24, 800–808 (2017).
pubmed: 28981073
doi: 10.1038/nsmb.3460
Xia, D. et al. Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science 277, 60–66 (1997).
pubmed: 9204897
doi: 10.1126/science.277.5322.60
Esser, L. et al. Surface-modulated motion switch: capture and release of iron–sulfur protein in the cytochrome bc1 complex. Proc. Natl Acad. Sci. USA 103, 13045–13050 (2006).
pubmed: 16924113
pmcid: 1551902
doi: 10.1073/pnas.0601149103
Wagener, N. & Neupert, W. Bcs1, a AAA protein of the mitochondria with a role in the biogenesis of the respiratory chain. J. Struct. Biol. 179, 121–125 (2012).
pubmed: 22575765
doi: 10.1016/j.jsb.2012.04.019
Cruciat, C. M., Hell, K., Fölsch, H., Neupert, W. & Stuart, R. A. Bcs1p, an AAA-family member, is a chaperone for the assembly of the cytochrome bc(1) complex. Embo J. 18, 5226–5233 (1999).
pubmed: 10508156
pmcid: 1171593
doi: 10.1093/emboj/18.19.5226
Nobrega, F. G., Nobrega, M. P. & Tzagoloff, A. BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae. Embo J. 11, 3821–3829 (1992).
pubmed: 1327750
pmcid: 556891
doi: 10.1002/j.1460-2075.1992.tb05474.x
De Meirleir, L. et al. Clinical and diagnostic characteristics of complex III deficiency due to mutations in the BCS1L gene. Am. J. Med. Genet. A 121a, 126–131 (2003).
pubmed: 12910490
doi: 10.1002/ajmg.a.20171
Fernandez-Vizarra, E. et al. Impaired complex III assembly associated with BCS1L gene mutations in isolated mitochondrial encephalopathy. Hum. Mol. Genet. 16, 1241–1252 (2007).
pubmed: 17403714
doi: 10.1093/hmg/ddm072
Ogura, T. & Wilkinson, A. J. AAA+ superfamily ATPases: common structure–diverse function. Genes Cells 6, 575–597 (2001).
pubmed: 11473577
doi: 10.1046/j.1365-2443.2001.00447.x
Sauer, R. T. et al. Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 119, 9–18 (2004).
pubmed: 15454077
pmcid: 2717008
doi: 10.1016/j.cell.2004.09.020
Truscott, K. N., Lowth, B. R., Strack, P. R. & Dougan, D. A. Diverse functions of mitochondrial AAA+ proteins: protein activation, disaggregation, and degradation. Biochem. Cell Biol. 88, 97–108 (2010).
pubmed: 20130683
doi: 10.1139/O09-167
Gates, S. N. & Martin, A. Stairway to translocation: AAA+ motor structures reveal the mechanisms of ATP-dependent substrate translocation. Protein Sci. 29, 407–419 (2020).
pubmed: 31599052
doi: 10.1002/pro.3743
Lee, S. et al. Cryo-EM structures of the Hsp104 protein disaggregase captured in the ATP conformation. Cell Rep. 26, 29–36.e23 (2019).
pubmed: 30605683
pmcid: 6347426
doi: 10.1016/j.celrep.2018.12.037
Monroe, N., Han, H., Shen, P. S., Sundquist, W. I. & Hill, C. P. Structural basis of protein translocation by the Vps4-Vta1 AAA ATPase. eLife 6, e24487 (2017).
pubmed: 28379137
pmcid: 5413351
doi: 10.7554/eLife.24487
Twomey, E. C. et al. Substrate processing by the Cdc48 ATPase complex is initiated by ubiquitin unfolding. Science 365, eaax1033 (2019).
pubmed: 31249135
pmcid: 6980381
doi: 10.1126/science.aax1033
Majumder, P. et al. Cryo-EM structures of the archaeal PAN-proteasome reveal an around-the-ring ATPase cycle. Proc. Natl Acad. Sci. USA 116, 534–539 (2019).
pubmed: 30559193
doi: 10.1073/pnas.1817752116
Kater, L. et al. Structure of the Bcs1 AAA-ATPase suggests an airlock-like translocation mechanism for folded proteins. Nat. Struct. Mol. Biol. 27, 142–149 (2020).
pubmed: 31988523
doi: 10.1038/s41594-019-0364-1
Tang, W. K. et al. Structures of AAA protein translocase Bcs1 suggest translocation mechanism of a folded protein. Nat. Struct. Mol. Biol. 27, 202–209 (2020).
pubmed: 32042153
doi: 10.1038/s41594-020-0373-0
Uchihashi, T., Iino, R., Ando, T. & Noji, H. High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333, 755–758 (2011).
pubmed: 21817054
doi: 10.1126/science.1205510
Maruyama, S. et al. Metastable asymmetrical structure of a shaftless V1 motor. Sci. Adv. 5, eaau8149 (2019).
pubmed: 30729160
pmcid: 6353620
doi: 10.1126/sciadv.aau8149
Uchihashi, T. et al. Dynamic structural states of ClpB involved in its disaggregation function. Nat. Commun. 9, 2147 (2018).
pubmed: 29858573
pmcid: 5984625
doi: 10.1038/s41467-018-04587-w
Cho, C. et al. Structural basis of nucleosome assembly by the Abo1 AAA+ ATPase histone chaperone. Nat. Commun. 10, 5764 (2019).
pubmed: 31848341
pmcid: 6917787
doi: 10.1038/s41467-019-13743-9
Matin, T. R., Heath, G. R., Huysmans, G. H. M., Boudker, O. & Scheuring, S. Millisecond dynamics of an unlabeled amino acid transporter. Nat. Commun. 11, 5016 (2020).
pubmed: 33024106
pmcid: 7538599
doi: 10.1038/s41467-020-18811-z
Heath, G. R. & Scheuring, S. High-speed AFM height spectroscopy reveals µs-dynamics of unlabeled biomolecules. Nat. Commun. 9, 4983 (2018).
pubmed: 30478320
pmcid: 6255864
doi: 10.1038/s41467-018-07512-3
Ando, T. et al. High-speed AFM and nano-visualization of biomolecular processes. Pflügers Archiv. Eur. J. Physiol. 456, 211–225 (2008).
doi: 10.1007/s00424-007-0406-0
Heath, G. R. & Scheuring, S. Advances in high-speed atomic force microscopy (HS-AFM) reveal dynamics of transmembrane channels and transporters. Curr. Opin. Struct. Biol. 57, 93–102 (2019).
pubmed: 30878714
pmcid: 7216758
doi: 10.1016/j.sbi.2019.02.008
Shen, C. Analysis of detrended time-lagged cross-correlation between two nonstationary time series. Phys. Lett. A 379, 680–687 (2015).
doi: 10.1016/j.physleta.2014.12.036
Ruan, Y. et al. Direct visualization of glutamate transporter elevator mechanism by high-speed AFM. Proc. Natl Acad. Sci. USA 114, 1584–1588 (2017).
pubmed: 28137870
pmcid: 5320997
doi: 10.1073/pnas.1616413114
Oguntunde, P., Odetunmibi, O. & Adejumo, A. On the sum of exponentially distributed random variables: a convolution approach. Eur. J. Stat. Prob. 2, 1–8 (2014).
Neubig, R. R., Spedding, M., Kenakin, T. & Christopoulos, A. International union of pharmacology committee on receptor nomenclature and drug classification. XXXVIII. Update on terms and symbols in quantitative pharmacology. Pharmacol. Rev. 55, 597 (2003).
pubmed: 14657418
doi: 10.1124/pr.55.4.4
Phillips, R., Ursell, T., Wiggins, P. & Sens, P. Emerging roles for lipids in shaping membrane-protein function. Nature 459, 379–385 (2009).
pubmed: 19458714
pmcid: 3169427
doi: 10.1038/nature08147
Ursell, T., Huang, K. C., Peterson, E. & Phillips, R. Cooperative gating and spatial organization of membrane proteins through elastic interactions. PLoS Comput. Biol. 3, e81 (2007).
pubmed: 17480116
pmcid: 1864995
doi: 10.1371/journal.pcbi.0030081
Wiggins, P. & Phillips, R. Membrane-protein interactions in mechanosensitive channels. Biophys. J. 88, 880–902 (2005).
pubmed: 15542561
doi: 10.1529/biophysj.104.047431
Cooney, I. et al. Structure of the Cdc48 segregase in the act of unfolding an authentic substrate. Science 365, 502–505 (2019).
pubmed: 31249134
pmcid: 7362759
doi: 10.1126/science.aax0486
Fei, X. et al. Structures of the ATP-fueled ClpXP proteolytic machine bound to protein substrate. eLife 9, e52774 (2020).
pubmed: 32108573
pmcid: 7112951
doi: 10.7554/eLife.52774
Tsai, F. T. F. & Hill, C. P. Same structure, different mechanisms? Elife 9, e56501 (2020).
pubmed: 32321627
pmcid: 7180051
doi: 10.7554/eLife.56501
Ripstein, Z. A., Vahidi, S., Houry, W. A., Rubinstein, J. L. & Kay, L. E. A processive rotary mechanism couples substrate unfolding and proteolysis in the ClpXP degradation machinery. eLife 9, e52158 (2020).
pubmed: 31916936
pmcid: 7112952
doi: 10.7554/eLife.52158
Rosing, J. & Slater, E. C. The value of G degrees for the hydrolysis of ATP. Biochim. Biophys. Acta 267, 275–290 (1972).
pubmed: 4402900
doi: 10.1016/0005-2728(72)90116-8
Tran, Q. H. & Unden, G. Changes in the proton potential and the cellular energetics of Escherichia coli during growth by aerobic and anaerobic respiration or by fermentation. Eur. J. Biochem. 251, 538–543 (1998).
pubmed: 9492330
doi: 10.1046/j.1432-1327.1998.2510538.x
Wackerhage, H. et al. Recovery of free ADP, Pi, and free energy of ATP hydrolysis in human skeletal muscle. J. Appl. Physiol. (1985) 85, 2140–2145 (1998).
pubmed: 9843537
doi: 10.1152/jappl.1998.85.6.2140
Smith, P. K. et al. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76–85 (1985).
pubmed: 3843705
doi: 10.1016/0003-2697(85)90442-7
Miyagi, A. & Scheuring, S. Automated force controller for amplitude modulation atomic force microscopy. Rev. Sci. Instrum. 87, 053705 (2016).
pubmed: 27250433
doi: 10.1063/1.4950777
Miyagi, A. & Scheuring, S. A novel phase-shift-based amplitude detector for a high-speed atomic force microscope. Rev. Sci. Instrum. 89, 083704 (2018).
pubmed: 30184715
doi: 10.1063/1.5038095
Perrino, A. P., Miyagi, A. & Scheuring, S. Single molecule kinetics of bacteriorhodopsin by HS-AFM. Nat. Commun. 12, 7225 (2021).
pubmed: 34893646
pmcid: 8664958
doi: 10.1038/s41467-021-27580-2
Ping, X., Bao-Shan, W., Wei, Z., Jian-Min, L. & Yong, C. Estimating seismic attenuation using cross-correlation function. Chin. J. Geophys.-Chin. Ed. 49, 1738–1744 (2006).
Gonçalves, R. R., Zullo, J. Jr, Romani, L. A., Nascimento, C. R. & Traina, A. J. Analysis of NDVI time series using cross-correlation and forecasting methods for monitoring sugarcane fields in Brazil. Int. J. Remote Sens. 33, 4653–4672 (2012).
doi: 10.1080/01431161.2011.638334
Li, H., Futch, S. H. & Syvertsen, J. P. Cross‐correlation patterns of air and soil temperatures, rainfall and Diaprepes abbreviatus root weevil in citrus. Pest Manag. Sci.: Formerly Pesticide Sci. 63, 1116–1123 (2007).
doi: 10.1002/ps.1431
Yoon, D.-B., Park, J.-H. & Shin, S.-H. Improvement of cross-correlation technique for leak detection of a buried pipe in a tonal noisy environment. Nuclear Eng. Technol. 44, 977–984 (2012).
doi: 10.5516/NET.09.2011.067
Mei, D. C., Du, L. C. & Wang, C. J. The effects of time delay on stochastic resonance in a bistable system with correlated noises. J. Stat. Phys. 137, 625–638 (2009).
doi: 10.1007/s10955-009-9864-4
Du, L. & Mei, D. Stochastic resonance in a bistable system with global delay and two noises. Eur. Phys. J. B 85, 1–5 (2012).
doi: 10.1140/epjb/e2012-21053-0
Schmidpeter, P. A. M., Gao, X., Uphadyay, V., Rheinberger, J. & Nimigean, C. M. Ligand binding and activation properties of the purified bacterial cyclic nucleotide-gated channel SthK. J Gen Physiol 150, 821–834 (2018).
pubmed: 29752414
pmcid: 5987880
doi: 10.1085/jgp.201812023
Turner, M. S. & Sens, P. Gating-by-tilt of mechanically sensitive membrane channels. Phys. Rev. Lett. 93, 118103 (2004).
pubmed: 15447384
doi: 10.1103/PhysRevLett.93.118103