Non-equilibrium dynamics of a nascent polypeptide during translation suppress its misfolding
Abstract
Protein folding can begin co-translationally. Due to the difference in timescale between folding and synthesis, co-translational folding is thought to occur at equilibrium for fastfolding domains. In this scenario, the folding kinetics of stalled ribosome-bound nascent chains should match the folding of nascent chains in real time. To test if this assumption is true, we compare the folding of a ribosome-bound, multi-domain calcium-binding protein stalled at different points in translation with the nascent chain as is it being synthesized in real-time, via optical tweezers. On stalled ribosomes, a misfolded state forms rapidly (1.5 s). However, during translation, this state is only attained after a long delay (63 s), indicating that, unexpectedly, the growing polypeptide is not equilibrated with its ensemble of accessible conformations. Slow equilibration on the ribosome can delay premature folding until adequate sequence is available and/or allow time for chaperone binding, thus promoting productive folding.
- Authors:
-
- Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States); Johns Hopkins Univ., Baltimore, MD (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1559262
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Alexander, Lisa M., Goldman, Daniel H., Wee, Liang M., and Bustamante, Carlos. Non-equilibrium dynamics of a nascent polypeptide during translation suppress its misfolding. United States: N. p., 2019.
Web. doi:10.1038/s41467-019-10647-6.
Alexander, Lisa M., Goldman, Daniel H., Wee, Liang M., & Bustamante, Carlos. Non-equilibrium dynamics of a nascent polypeptide during translation suppress its misfolding. United States. doi:https://doi.org/10.1038/s41467-019-10647-6
Alexander, Lisa M., Goldman, Daniel H., Wee, Liang M., and Bustamante, Carlos. Thu .
"Non-equilibrium dynamics of a nascent polypeptide during translation suppress its misfolding". United States. doi:https://doi.org/10.1038/s41467-019-10647-6. https://www.osti.gov/servlets/purl/1559262.
@article{osti_1559262,
title = {Non-equilibrium dynamics of a nascent polypeptide during translation suppress its misfolding},
author = {Alexander, Lisa M. and Goldman, Daniel H. and Wee, Liang M. and Bustamante, Carlos},
abstractNote = {Protein folding can begin co-translationally. Due to the difference in timescale between folding and synthesis, co-translational folding is thought to occur at equilibrium for fastfolding domains. In this scenario, the folding kinetics of stalled ribosome-bound nascent chains should match the folding of nascent chains in real time. To test if this assumption is true, we compare the folding of a ribosome-bound, multi-domain calcium-binding protein stalled at different points in translation with the nascent chain as is it being synthesized in real-time, via optical tweezers. On stalled ribosomes, a misfolded state forms rapidly (1.5 s). However, during translation, this state is only attained after a long delay (63 s), indicating that, unexpectedly, the growing polypeptide is not equilibrated with its ensemble of accessible conformations. Slow equilibration on the ribosome can delay premature folding until adequate sequence is available and/or allow time for chaperone binding, thus promoting productive folding.},
doi = {10.1038/s41467-019-10647-6},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {6}
}
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Works referenced in this record:
Quantitative determination of ribosome nascent chain stability
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Translational tuning optimizes nascent protein folding in cells
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The Geometry of the Ribosomal Polypeptide Exit Tunnel
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Entropic elasticity of lambda-phage DNA
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Transient ribosomal attenuation coordinates protein synthesis and co-translational folding
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Direct observation of multiple misfolding pathways in a single prion protein molecule
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α-Helical nascent polypeptide chains visualized within distinct regions of the ribosomal exit tunnel
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Protein folding within the cell is influenced by controlled rates of polypeptide elongation
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Calcium-induced folding of a fragment of calmodulin composed of EF-hands 2 and 3
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- Protein Science, Vol. 16, Issue 6
Limitations of Constant-Force-Feedback Experiments
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Prokaryotic calcium-binding protein of the calmodulin superfamily Calcium binding to a Saccharopolyspora erythraea 20 kDa protein
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Ribosome exit tunnel can entropically stabilize -helices
journal, December 2005
- Ziv, G.; Haran, G.; Thirumalai, D.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 52
The molten globule state is unusually deformable under mechanical force
journal, February 2012
- Elms, P. J.; Chodera, J. D.; Bustamante, C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 10
Quality over quantity: optimizing co-translational protein folding with non-‘optimal’ synonymous codons
journal, June 2016
- Jacobson, Giselle N.; Clark, Patricia L.
- Current Opinion in Structural Biology, Vol. 38
Cotranslational Protein Folding inside the Ribosome Exit Tunnel
journal, September 2015
- Nilsson, Ola B.; Hedman, Rickard; Marino, Jacopo
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Mechanical force releases nascent chain-mediated ribosome arrest in vitro and in vivo
journal, April 2015
- Goldman, D. H.; Kaiser, C. M.; Milin, A.
- Science, Vol. 348, Issue 6233
Nonmetric multidimensional scaling: A numerical method
journal, June 1964
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The Complex Folding Network of Single Calmodulin Molecules
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- Stigler, J.; Ziegler, F.; Gieseke, A.
- Science, Vol. 334, Issue 6055
Characterization of apo and partially saturated states of calerythrin, an EF-hand protein from S. erythraea: A molten globule when deprived of Ca2+
journal, January 2001
- Aitio, H.
- Protein Science, Vol. 10, Issue 1
Small protein domains fold inside the ribosome exit tunnel
journal, February 2016
- Marino, Jacopo; von Heijne, Gunnar; Beckmann, Roland
- FEBS Letters, Vol. 590, Issue 5
The ribosome destabilizes native and non-native structures in a nascent multidomain protein: EF-G Folding on the Ribosome
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- Liu, Kaixian; Rehfus, Joseph E.; Mattson, Elliot
- Protein Science, Vol. 26, Issue 7
Stretching DNA with optical tweezers
journal, March 1997
- Wang, M. D.; Yin, H.; Landick, R.
- Biophysical Journal, Vol. 72, Issue 3
In vivo translation rates can substantially delay the cotranslational folding of the Escherichia coli cytosolic proteome
journal, December 2012
- Ciryam, P.; Morimoto, R. I.; Vendruscolo, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 2
A tutorial on hidden Markov models and selected applications in speech recognition
journal, January 1989
- Rabiner, L. R.
- Proceedings of the IEEE, Vol. 77, Issue 2
On Some Criteria for Estimating the Order of a Markov Chain
journal, August 1981
- Katz, Richard W.
- Technometrics, Vol. 23, Issue 3
Calcium-dependent folding of single calmodulin molecules
journal, July 2012
- Stigler, J.; Rief, M.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 44
In vitro assays for the determination of aminoacyl-tRNA synthetase editing activity
journal, February 2008
- Splan, Kathryn E.; Musier-Forsyth, Karin; Boniecki, Michal T.
- Methods, Vol. 44, Issue 2
Direct single-molecule observation of calcium-dependent misfolding in human neuronal calcium sensor-1
journal, August 2014
- Heidarsson, P. O.; Naqvi, M. M.; Otazo, M. R.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 36
Cotranslational protein folding on the ribosome monitored in real time
journal, November 2015
- Holtkamp, W.; Kokic, G.; Jager, M.
- Science, Vol. 350, Issue 6264
Kinetic and structural comparison of a protein’s cotranslational folding and refolding pathways
journal, May 2018
- Samelson, Avi J.; Bolin, Eric; Costello, Shawn M.
- Science Advances, Vol. 4, Issue 5
Protein synthesis by pure translation systems
journal, July 2005
- Shimizu, Yoshihiro; Kanamori, Takashi; Ueda, Takuya
- Methods, Vol. 36, Issue 3
Translation and folding of single proteins in real time
journal, May 2017
- Wruck, Florian; Katranidis, Alexandros; Nierhaus, Knud H.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 22
The accuracy of codon recognition by polypeptide release factors
journal, February 2000
- Freistroffer, D. V.; Kwiatkowski, M.; Buckingham, R. H.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 5
The Ribosome Modulates Nascent Protein Folding
journal, December 2011
- Kaiser, C. M.; Goldman, D. H.; Chodera, J. D.
- Science, Vol. 334, Issue 6063
Hidden Markov Analysis of Trajectories in Single-Molecule Experiments and the Effects of Missed Events
journal, March 2012
- Stigler, Johannes; Rief, Matthias
- ChemPhysChem, Vol. 13, Issue 4
Secondary Structure Formation of a Transmembrane Segment in Kv Channels †
journal, June 2005
- Lu, Jianli; Deutsch, Carol
- Biochemistry, Vol. 44, Issue 23
Intrinsic Rates and Activation Free Energies from Single-Molecule Pulling Experiments
journal, March 2006
- Dudko, Olga; Hummer, Gerhard; Szabo, Attila
- Physical Review Letters, Vol. 96, Issue 10
A bacterial calcium-binding protein homologous to calmodulin
journal, September 1987
- Swan, David G.; Hale, Richard S.; Dhillon, Namrita
- Nature, Vol. 329, Issue 6134
Ionic effects on the elasticity of single DNA molecules
journal, June 1997
- Baumann, C. G.; Smith, S. B.; Bloomfield, V. A.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 12
tRNA concentration fine tunes protein solubility
journal, July 2012
- Fedyunin, Ivan; Lehnhardt, Lothar; Böhmer, Nadine
- FEBS Letters, Vol. 586, Issue 19
Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme
journal, January 2000
- Yang, G.; Cecconi, C.; Baase, W. A.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 1
Effects of protein size, thermodynamic stability, and net charge on cotranslational folding on the ribosome
journal, September 2018
- Farías-Rico, José Arcadio; Ruud Selin, Frida; Myronidi, Ioanna
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 40
Precision methylome characterization of Mycobacterium tuberculosis complex (MTBC) using PacBio single-molecule real-time (SMRT) technology
journal, December 2015
- Zhu, Lingxiang; Zhong, Jun; Jia, Xinmiao
- Nucleic Acids Research, Vol. 44, Issue 2
NMR assignments, secondary structure, and global fold of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea
journal, January 1999
- Aitio, Helena; Heikkinen, Sami; Äinen, Ilkka Kilpel
- Protein Science, Vol. 8, Issue 12
Ultrahigh-resolution optical trap with single-fluorophore sensitivity
journal, February 2011
- Comstock, Matthew J.; Ha, Taekjip; Chemla, Yann R.
- Nature Methods, Vol. 8, Issue 4
Differential detection of dual traps improves the spatial resolution of optical tweezers
journal, June 2006
- Moffitt, J. R.; Chemla, Y. R.; Izhaky, D.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 24
Co-Translational Folding Trajectory of the HemK Helical Domain
journal, May 2018
- Mercier, Evan; Rodnina, Marina V.
- Biochemistry, Vol. 57, Issue 25
A simple real-time assay for in vitro translation
journal, December 2014
- Capece, Mark C.; Kornberg, Guy L.; Petrov, Alexey
- RNA, Vol. 21, Issue 2
Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation
journal, November 1999
- Komar, Anton A.; Lesnik, Thierry; Reiss, Claude
- FEBS Letters, Vol. 462, Issue 3
NMR solution structure of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea
journal, June 2003
- Tossavainen, Helena; Permi, Perttu; Annila, Arto
- European Journal of Biochemistry, Vol. 270, Issue 11
Works referencing / citing this record:
Small protein domains fold inside the ribosome exit tunnel
journal, February 2016
- Marino, Jacopo; von Heijne, Gunnar; Beckmann, Roland
- FEBS Letters, Vol. 590, Issue 5
Hidden Markov Analysis of Trajectories in Single-Molecule Experiments and the Effects of Missed Events
journal, March 2012
- Stigler, Johannes; Rief, Matthias
- ChemPhysChem, Vol. 13, Issue 4
The ribosome destabilizes native and non-native structures in a nascent multidomain protein: EF-G Folding on the Ribosome
journal, May 2017
- Liu, Kaixian; Rehfus, Joseph E.; Mattson, Elliot
- Protein Science, Vol. 26, Issue 7
Nonmetric multidimensional scaling: A numerical method
journal, June 1964
- Kruskal, J. B.
- Psychometrika, Vol. 29, Issue 2
Prokaryotic calcium-binding protein of the calmodulin superfamily Calcium binding to a Saccharopolyspora erythraea 20 kDa protein
journal, March 1992
- Bylsma, Niels; Drakenberg, Torbjörn; Andersson, Ingrid
- FEBS Letters, Vol. 299, Issue 1
Protein folding within the cell is influenced by controlled rates of polypeptide elongation
journal, November 1992
- Crombie, Tanya; Swaffield, Jonathan C.; Brown, Alistair J. P.
- Journal of Molecular Biology, Vol. 228, Issue 1
Limitations of Constant-Force-Feedback Experiments
journal, October 2012
- Elms, Phillip J.; Chodera, John D.; Bustamante, Carlos J.
- Biophysical Journal, Vol. 103, Issue 7
Cotranslational Protein Folding inside the Ribosome Exit Tunnel
journal, September 2015
- Nilsson, Ola B.; Hedman, Rickard; Marino, Jacopo
- Cell Reports, Vol. 12, Issue 10
tRNA concentration fine tunes protein solubility
journal, July 2012
- Fedyunin, Ivan; Lehnhardt, Lothar; Böhmer, Nadine
- FEBS Letters, Vol. 586, Issue 19
The Geometry of the Ribosomal Polypeptide Exit Tunnel
journal, July 2006
- Voss, N. R.; Gerstein, M.; Steitz, T. A.
- Journal of Molecular Biology, Vol. 360, Issue 4
Quality over quantity: optimizing co-translational protein folding with non-‘optimal’ synonymous codons
journal, June 2016
- Jacobson, Giselle N.; Clark, Patricia L.
- Current Opinion in Structural Biology, Vol. 38
Protein synthesis by pure translation systems
journal, July 2005
- Shimizu, Yoshihiro; Kanamori, Takashi; Ueda, Takuya
- Methods, Vol. 36, Issue 3
In vitro assays for the determination of aminoacyl-tRNA synthetase editing activity
journal, February 2008
- Splan, Kathryn E.; Musier-Forsyth, Karin; Boniecki, Michal T.
- Methods, Vol. 44, Issue 2
Stretching DNA with optical tweezers
journal, March 1997
- Wang, M. D.; Yin, H.; Landick, R.
- Biophysical Journal, Vol. 72, Issue 3
Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation
journal, November 1999
- Komar, Anton A.; Lesnik, Thierry; Reiss, Claude
- FEBS Letters, Vol. 462, Issue 3
Co-Translational Folding Trajectory of the HemK Helical Domain
journal, May 2018
- Mercier, Evan; Rodnina, Marina V.
- Biochemistry, Vol. 57, Issue 25
Secondary Structure Formation of a Transmembrane Segment in Kv Channels †
journal, June 2005
- Lu, Jianli; Deutsch, Carol
- Biochemistry, Vol. 44, Issue 23
A bacterial calcium-binding protein homologous to calmodulin
journal, September 1987
- Swan, David G.; Hale, Richard S.; Dhillon, Namrita
- Nature, Vol. 329, Issue 6134
Ultrahigh-resolution optical trap with single-fluorophore sensitivity
journal, February 2011
- Comstock, Matthew J.; Ha, Taekjip; Chemla, Yann R.
- Nature Methods, Vol. 8, Issue 4
Transient ribosomal attenuation coordinates protein synthesis and co-translational folding
journal, February 2009
- Zhang, Gong; Hubalewska, Magdalena; Ignatova, Zoya
- Nature Structural & Molecular Biology, Vol. 16, Issue 3
α-Helical nascent polypeptide chains visualized within distinct regions of the ribosomal exit tunnel
journal, February 2010
- Bhushan, Shashi; Gartmann, Marco; Halic, Mario
- Nature Structural & Molecular Biology, Vol. 17, Issue 3
NMR solution structure of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea
journal, June 2003
- Tossavainen, Helena; Permi, Perttu; Annila, Arto
- European Journal of Biochemistry, Vol. 270, Issue 11
The accuracy of codon recognition by polypeptide release factors
journal, February 2000
- Freistroffer, D. V.; Kwiatkowski, M.; Buckingham, R. H.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 5
Ribosome exit tunnel can entropically stabilize -helices
journal, December 2005
- Ziv, G.; Haran, G.; Thirumalai, D.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 52
Differential detection of dual traps improves the spatial resolution of optical tweezers
journal, June 2006
- Moffitt, J. R.; Chemla, Y. R.; Izhaky, D.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 24
Direct observation of multiple misfolding pathways in a single prion protein molecule
journal, March 2012
- Yu, H.; Liu, X.; Neupane, K.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 14
The molten globule state is unusually deformable under mechanical force
journal, February 2012
- Elms, P. J.; Chodera, J. D.; Bustamante, C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 10
Calcium-dependent folding of single calmodulin molecules
journal, July 2012
- Stigler, J.; Rief, M.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 44
In vivo translation rates can substantially delay the cotranslational folding of the Escherichia coli cytosolic proteome
journal, December 2012
- Ciryam, P.; Morimoto, R. I.; Vendruscolo, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 2
Direct single-molecule observation of calcium-dependent misfolding in human neuronal calcium sensor-1
journal, August 2014
- Heidarsson, P. O.; Naqvi, M. M.; Otazo, M. R.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 36
Quantitative determination of ribosome nascent chain stability
journal, November 2016
- Samelson, Avi J.; Jensen, Madeleine K.; Soto, Randy A.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 47
Translation and folding of single proteins in real time
journal, May 2017
- Wruck, Florian; Katranidis, Alexandros; Nierhaus, Knud H.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 22
Effects of protein size, thermodynamic stability, and net charge on cotranslational folding on the ribosome
journal, September 2018
- Farías-Rico, José Arcadio; Ruud Selin, Frida; Myronidi, Ioanna
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 40
Ionic effects on the elasticity of single DNA molecules
journal, June 1997
- Baumann, C. G.; Smith, S. B.; Bloomfield, V. A.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 12
Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme
journal, January 2000
- Yang, G.; Cecconi, C.; Baase, W. A.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 1
Precision methylome characterization of Mycobacterium tuberculosis complex (MTBC) using PacBio single-molecule real-time (SMRT) technology
journal, December 2015
- Zhu, Lingxiang; Zhong, Jun; Jia, Xinmiao
- Nucleic Acids Research, Vol. 44, Issue 2
Intrinsic Rates and Activation Free Energies from Single-Molecule Pulling Experiments
journal, March 2006
- Dudko, Olga; Hummer, Gerhard; Szabo, Attila
- Physical Review Letters, Vol. 96, Issue 10
A tutorial on hidden Markov models and selected applications in speech recognition
journal, January 1989
- Rabiner, L. R.
- Proceedings of the IEEE, Vol. 77, Issue 2
Calcium-induced folding of a fragment of calmodulin composed of EF-hands 2 and 3
journal, June 2007
- Lakowski, Ted M.; Lee, Gregory M.; Okon, Mark
- Protein Science, Vol. 16, Issue 6
Characterization of apo and partially saturated states of calerythrin, an EF-hand protein from S. erythraea: A molten globule when deprived of Ca2+
journal, January 2001
- Aitio, H.
- Protein Science, Vol. 10, Issue 1
NMR assignments, secondary structure, and global fold of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea
journal, January 1999
- Aitio, Helena; Heikkinen, Sami; Äinen, Ilkka Kilpel
- Protein Science, Vol. 8, Issue 12
Kinetic and structural comparison of a protein’s cotranslational folding and refolding pathways
journal, May 2018
- Samelson, Avi J.; Bolin, Eric; Costello, Shawn M.
- Science Advances, Vol. 4, Issue 5
The Complex Folding Network of Single Calmodulin Molecules
journal, October 2011
- Stigler, J.; Ziegler, F.; Gieseke, A.
- Science, Vol. 334, Issue 6055
The Ribosome Modulates Nascent Protein Folding
journal, December 2011
- Kaiser, C. M.; Goldman, D. H.; Chodera, J. D.
- Science, Vol. 334, Issue 6063
Mechanical force releases nascent chain-mediated ribosome arrest in vitro and in vivo
journal, April 2015
- Goldman, D. H.; Kaiser, C. M.; Milin, A.
- Science, Vol. 348, Issue 6233
Entropic elasticity of lambda-phage DNA
journal, September 1994
- Bustamante, C.; Marko, J.; Siggia, E.
- Science, Vol. 265, Issue 5178
Translational tuning optimizes nascent protein folding in cells
journal, April 2015
- Kim, S. J.; Yoon, J. S.; Shishido, H.
- Science, Vol. 348, Issue 6233
Cotranslational protein folding on the ribosome monitored in real time
journal, November 2015
- Holtkamp, W.; Kokic, G.; Jager, M.
- Science, Vol. 350, Issue 6264
A simple real-time assay for in vitro translation
journal, December 2014
- Capece, Mark C.; Kornberg, Guy L.; Petrov, Alexey
- RNA, Vol. 21, Issue 2
On Some Criteria for Estimating the Order of a Markov Chain
journal, August 1981
- Katz, Richard W.
- Technometrics, Vol. 23, Issue 3
Cotranslational Folding of Proteins on the Ribosome
journal, January 2020
- Liutkute, Marija; Samatova, Ekaterina; Rodnina, Marina V.
- Biomolecules, Vol. 10, Issue 1