Cooperative Subunit Refolding of a Light-Harvesting Protein through a Self-Chaperone Mechanism

Laos, Alistair J.; Dean, Jacob C.; Toa, Zi S.  D.; Wilk, Krystyna E.; Scholes, Gregory D.; Curmi, Paul M.  G.; Thordarson, Pall

doi:10.1002/anie.201607921

Cooperative Subunit Refolding of a Light-Harvesting Protein through a Self-Chaperone Mechanism

Journal Article · Fri Jan 27 00:00:00 EST 2017 · Angewandte Chemie (International Edition)

DOI:https://doi.org/10.1002/anie.201607921· OSTI ID:1388635

Laos, Alistair J. ^[1]; Dean, Jacob C. ^[2]; Toa, Zi S. D. ^[2]; Wilk, Krystyna E. ^[3]; Scholes, Gregory D. ^[2]; Curmi, Paul M. G. ^[3]; ^[4]

Univ. of New South Wales, Sydney, NSW (Australia). School of Chemistry, the Australian Centre for NanoMedicine, the ARC Centre of Excellence in Convergent Bio-Nano Science and Technology, and School of Physics
Princeton Univ., NJ (United States). Dept. of Chemistry
Univ. of New South Wales, Sydney, NSW (Australia). School of Physics
Univ. of New South Wales, Sydney, NSW (Australia). School of Chemistry, the Australian Centre for NanoMedicine, and the ARC Centre of Excellence in Convergent Bio-Nano Science and Technology

The fold of a protein is encoded by its amino acid sequence, but how complex multimeric proteins fold and assemble into functional quaternary structures remains unclear. Here we show that two structurally different phycobiliproteins refold and reassemble in a cooperative manner from their unfolded polypeptide subunits, without biological chaperones. Refolding was confirmed by ultrafast broadband transient absorption and two-dimensional electronic spectroscopy to probe internal chromophores as a marker of quaternary structure. Our results demonstrate a cooperative, self-chaperone refolding mechanism, whereby the β-subunits independently refold, thereby templating the folding of the α-subunits, which then chaperone the assembly of the native complex, quantitatively returning all coherences. Finally, our results indicate that subunit self-chaperoning is a robust mechanism for heteromeric protein folding and assembly that could also be applied in self-assembled synthetic hierarchical systems.

View Accepted Manuscript (DOE)

Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0001035

OSTI ID:: 1388635

Alternate ID(s):: OSTI ID: 1400468

Journal Information:: Angewandte Chemie (International Edition), Journal Name: Angewandte Chemie (International Edition) Journal Issue: 29 Vol. 56; ISSN 1433-7851

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (25)

The Levinthal paradox: yesterday and today Karplus, Martin Folding and Design, Vol. 2 https://doi.org/10.1016/S1359-0278(97)00067-9	journal	June 1997
Developing a Structure–Function Model for the Cryptophyte Phycoerythrin 545 Using Ultrahigh Resolution Crystallography and Ultrafast Laser Spectroscopy Doust, Alexander B.; Marai, Christopher N. J.; Harrop, Stephen J. Journal of Molecular Biology, Vol. 344, Issue 1 https://doi.org/10.1016/j.jmb.2004.09.044	journal	November 2004
Broadband Transient Absorption and Two-Dimensional Electronic Spectroscopy of Methylene Blue Dean, Jacob C.; Rafiq, Shahnawaz; Oblinsky, Daniel G. The Journal of Physical Chemistry A, Vol. 119, Issue 34 https://doi.org/10.1021/acs.jpca.5b06126	journal	August 2015
Structural Basis for the Self-Chaperoning Function of an RNA Collapsed State ^† Garcia, Ivelitza; Weeks, Kevin M. Biochemistry, Vol. 43, Issue 48 https://doi.org/10.1021/bi048626f	journal	December 2004
Coherent Oscillations in the PC577 Cryptophyte Antenna Occur in the Excited Electronic State McClure, Scott D.; Turner, Daniel B.; Arpin, Paul C. The Journal of Physical Chemistry B, Vol. 118, Issue 5 https://doi.org/10.1021/jp411924c	journal	January 2014
(Mg–ATP)-dependent self-assembly of molecular chaperone GroEL Lissin, N. M.; Venyaminov, S. Yu.; Girshovich, A. S. Nature, Vol. 348, Issue 6299 https://doi.org/10.1038/348339a0	journal	November 1990
Coupled chaperone action in folding and assembly of hexadecameric Rubisco Liu, Cuimin; Young, Anna L.; Starling-Windhof, Amanda Nature, Vol. 463, Issue 7278 https://doi.org/10.1038/nature08651	journal	January 2010
Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature Collini, Elisabetta; Wong, Cathy Y.; Wilk, Krystyna E. Nature, Vol. 463, Issue 7281 https://doi.org/10.1038/nature08811	journal	February 2010
Lessons from nature about solar light harvesting Scholes, Gregory D.; Fleming, Graham R.; Olaya-Castro, Alexandra Nature Chemistry, Vol. 3, Issue 10 https://doi.org/10.1038/nchem.1145	journal	September 2011
Electronic coherence lineshapes reveal hidden excitonic correlations in photosynthetic light harvesting Wong, Cathy Y.; Alvey, Richard M.; Turner, Daniel B. Nature Chemistry, Vol. 4, Issue 5 https://doi.org/10.1038/nchem.1302	journal	March 2012
Shaping quaternary assemblies of water-soluble non-peptide helical foldamers by sequence manipulation Collie, Gavin W.; Pulka-Ziach, Karolina; Lombardo, Caterina M. Nature Chemistry, Vol. 7, Issue 11 https://doi.org/10.1038/nchem.2353	journal	September 2015
Cooperativity in macromolecular assembly Williamson, James R. Nature Chemical Biology, Vol. 4, Issue 8 https://doi.org/10.1038/nchembio.102	journal	July 2008
Opposing effects of folding and assembly chaperones on evolvability of Rubisco Durão, Paulo; Aigner, Harald; Nagy, Péter Nature Chemical Biology, Vol. 11, Issue 2 https://doi.org/10.1038/nchembio.1715	journal	January 2015
Cooperativity and biological complexity Whitty, Adrian Nature Chemical Biology, Vol. 4, Issue 8 https://doi.org/10.1038/nchembio0808-435	journal	August 2008
From Levinthal to pathways to funnels Dill, Ken A.; Chan, Hue Sun Nature Structural & Molecular Biology, Vol. 4, Issue 1 https://doi.org/10.1038/nsb0197-10	journal	January 1997
Spinophilin directs protein phosphatase 1 specificity by blocking substrate binding sites Ragusa, Michael J.; Dancheck, Barbara; Critton, David A. Nature Structural & Molecular Biology, Vol. 17, Issue 4 https://doi.org/10.1038/nsmb.1786	journal	March 2010
Natural supramolecular protein assemblies Pieters, Bas J. G. E.; van Eldijk, Mark B.; Nolte, Roeland J. M. Chemical Society Reviews, Vol. 45, Issue 1 https://doi.org/10.1039/C5CS00157A	journal	January 2016
Single-residue insertion switches the quaternary structure and exciton states of cryptophyte light-harvesting proteins Harrop, Stephen J.; Wilk, Krystyna E.; Dinshaw, Rayomond Proceedings of the National Academy of Sciences, Vol. 111, Issue 26 https://doi.org/10.1073/pnas.1402538111	journal	June 2014
Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: Crystal structure of a cryptophyte phycoerythrin at 1.63-A resolution Wilk, K. E.; Harrop, S. J.; Jankova, L. Proceedings of the National Academy of Sciences, Vol. 96, Issue 16 https://doi.org/10.1073/pnas.96.16.8901	journal	August 1999
Role of Small Subunit in Mediating Assembly of Red-type Form I Rubisco Joshi, Jidnyasa; Mueller-Cajar, Oliver; Tsai, Yi-Chin C. Journal of Biological Chemistry, Vol. 290, Issue 2 https://doi.org/10.1074/jbc.M114.613091	journal	November 2014
Translocation of a Phycoerythrin α Subunit across Five Biological Membranes Gould, Sven B.; Fan, Enguo; Hempel, Franziska Journal of Biological Chemistry, Vol. 282, Issue 41 https://doi.org/10.1074/jbc.M701869200	journal	August 2007
Models of cooperativity in protein folding Chan, Hue Sun; Bromberg, Sarina; Dill, Ken A. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 348, Issue 1323, p. 61-70 https://doi.org/10.1098/rstb.1995.0046	journal	April 1995
Principles that Govern the Folding of Protein Chains Anfinsen, C. B. Science, Vol. 181, Issue 4096 https://doi.org/10.1126/science.181.4096.223	journal	July 1973
Principles of assembly reveal a periodic table of protein complexes Ahnert, S. E.; Marsh, J. A.; Hernandez, H. Science, Vol. 350, Issue 6266 https://doi.org/10.1126/science.aaa2245	journal	December 2015
Structure, Dynamics, Assembly, and Evolution of Protein Complexes Marsh, Joseph A.; Teichmann, Sarah A. Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-034142	journal	June 2015

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Assessing cooperativity in supramolecular systems von Krbek, Larissa K. S.; Schalley, Christoph A.; Thordarson, Pall Chemical Society Reviews, Vol. 46, Issue 9 https://doi.org/10.1039/c7cs00063d	journal	January 2017
Determination of the protonation preferences of bilin pigments in cryptophyte antenna complexes Corbella, Marina; Toa, Zi S. D.; Scholes, Gregory D. Physical Chemistry Chemical Physics, Vol. 20, Issue 33 https://doi.org/10.1039/c8cp02541j	journal	January 2018

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