Native Mass Spectrometry Analysis of Oligomerization States of Fluorescence Recovery Protein and Orange Carotenoid Protein: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle [Native Mass Spectrometry Analysis of Oligomerization States of FRP and OCP: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle]
Abstract
Here, the orange carotenoid protein (OCP) and fluorescence recovery protein (FRP) are present in many cyanobacteria, and regulate an essential photoprotection cycle in an antagonistic manner as a function of light intensity. We characterized the oligomerization states of OCP and FRP by using native mass spectrometry, a technique that has the capability of studying native proteins under a wide range of protein concentrations and molecular masses. We found that dimeric FRP (dFRP) is the predominant state at protein concentrations ranging from 3 μM to 180 μM, and that higher order oligomers gradually form at protein concentrations above this range. The OCP, however, demonstrates significantly different oligomerization behavior. Monomeric OCP (mOCP) dominates at low protein concentrations, with an observable population of dimeric OCP (dOCP). The ratio of dOCP to mOCP, however, increases proportionally with the protein concentration. Higher order OCP oligomers form at protein concentrations beyond 10 μM. Additionally, native mass spectrometry coupled with ion mobility allowed us to measure protein collisional cross sections (CCS) and interrogate the unfolding of different FRP and OCP oligomers. We found that monomeric FRP exhibits a one-stage unfolding process, which could be correlated with its C-terminal bent crystal structure. The structural domain compositions of FRPmore »
- Authors:
-
- Washington Univ. in St. Louis, St. Louis, MO (United States)
- Publication Date:
- Research Org.:
- Washington Univ., St. Louis, MO (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1465178
- Grant/Contract Number:
- FG02-07ER15902; SC0001035
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Volume: 56; Journal Issue: 1; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Lu, Yue, Liu, Haijun, Saer, Rafael G., Zhang, Hao, Meyer, Christine M., Li, Veronica L., Shi, Liuqing, King, Jeremy D., Gross, Michael L., and Blankenship, Robert E. Native Mass Spectrometry Analysis of Oligomerization States of Fluorescence Recovery Protein and Orange Carotenoid Protein: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle [Native Mass Spectrometry Analysis of Oligomerization States of FRP and OCP: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle]. United States: N. p., 2016.
Web. doi:10.1021/acs.biochem.6b01094.
Lu, Yue, Liu, Haijun, Saer, Rafael G., Zhang, Hao, Meyer, Christine M., Li, Veronica L., Shi, Liuqing, King, Jeremy D., Gross, Michael L., & Blankenship, Robert E. Native Mass Spectrometry Analysis of Oligomerization States of Fluorescence Recovery Protein and Orange Carotenoid Protein: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle [Native Mass Spectrometry Analysis of Oligomerization States of FRP and OCP: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle]. United States. https://doi.org/10.1021/acs.biochem.6b01094
Lu, Yue, Liu, Haijun, Saer, Rafael G., Zhang, Hao, Meyer, Christine M., Li, Veronica L., Shi, Liuqing, King, Jeremy D., Gross, Michael L., and Blankenship, Robert E. Thu .
"Native Mass Spectrometry Analysis of Oligomerization States of Fluorescence Recovery Protein and Orange Carotenoid Protein: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle [Native Mass Spectrometry Analysis of Oligomerization States of FRP and OCP: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle]". United States. https://doi.org/10.1021/acs.biochem.6b01094. https://www.osti.gov/servlets/purl/1465178.
@article{osti_1465178,
title = {Native Mass Spectrometry Analysis of Oligomerization States of Fluorescence Recovery Protein and Orange Carotenoid Protein: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle [Native Mass Spectrometry Analysis of Oligomerization States of FRP and OCP: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle]},
author = {Lu, Yue and Liu, Haijun and Saer, Rafael G. and Zhang, Hao and Meyer, Christine M. and Li, Veronica L. and Shi, Liuqing and King, Jeremy D. and Gross, Michael L. and Blankenship, Robert E.},
abstractNote = {Here, the orange carotenoid protein (OCP) and fluorescence recovery protein (FRP) are present in many cyanobacteria, and regulate an essential photoprotection cycle in an antagonistic manner as a function of light intensity. We characterized the oligomerization states of OCP and FRP by using native mass spectrometry, a technique that has the capability of studying native proteins under a wide range of protein concentrations and molecular masses. We found that dimeric FRP (dFRP) is the predominant state at protein concentrations ranging from 3 μM to 180 μM, and that higher order oligomers gradually form at protein concentrations above this range. The OCP, however, demonstrates significantly different oligomerization behavior. Monomeric OCP (mOCP) dominates at low protein concentrations, with an observable population of dimeric OCP (dOCP). The ratio of dOCP to mOCP, however, increases proportionally with the protein concentration. Higher order OCP oligomers form at protein concentrations beyond 10 μM. Additionally, native mass spectrometry coupled with ion mobility allowed us to measure protein collisional cross sections (CCS) and interrogate the unfolding of different FRP and OCP oligomers. We found that monomeric FRP exhibits a one-stage unfolding process, which could be correlated with its C-terminal bent crystal structure. The structural domain compositions of FRP and OCP are compared and discussed.},
doi = {10.1021/acs.biochem.6b01094},
journal = {Biochemistry},
number = 1,
volume = 56,
place = {United States},
year = {Thu Dec 08 00:00:00 EST 2016},
month = {Thu Dec 08 00:00:00 EST 2016}
}
Web of Science
Works referenced in this record:
Oligomeric Characterization of the Photosynthetic Apparatus of Rhodobacter sphaeroides R26.1 by Nondenaturing Electrophoresis Methods
journal, January 2010
- D’Amici, Gian Maria; Rinalducci, Sara; Murgiano, Leonardo
- Journal of Proteome Research, Vol. 9, Issue 1
ExPASy: the proteomics server for in-depth protein knowledge and analysis
journal, July 2003
- Gasteiger, E.
- Nucleic Acids Research, Vol. 31, Issue 13
A Review Size-Exclusion Chromatography for the Analysis of Protein Biotherapeutics and Their Aggregates
journal, January 2012
- Hong, Paula; Koza, Stephan; Bouvier, Edouard S. P.
- Journal of Liquid Chromatography & Related Technologies, Vol. 35, Issue 20
From Ions In Solution To Ions In The Gas Phase
journal, November 1993
- Kebarle, Paul; Tang, Liang
- Analytical Chemistry, Vol. 65, Issue 22, p. 972A-986A
XX. On the equilibrium of liquid conducting masses charged with electricity
journal, September 1882
- Rayleigh, Lord
- The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science, Vol. 14, Issue 87
Evidence of functional trimeric chlorophyll a/c-peridinin proteins in the dinoflagellate Symbiodinium
journal, November 2014
- Jiang, Jing; Zhang, Hao; Orf, Gregory S.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 11
Twenty Years of Gas Phase Structural Biology
journal, September 2013
- Marcoux, Julien; Robinson, Carol V.
- Structure, Vol. 21, Issue 9
Ion mobility–mass spectrometry analysis of large protein complexes
journal, June 2008
- Ruotolo, Brandon T.; Benesch, Justin L. P.; Sandercock, Alan M.
- Nature Protocols, Vol. 3, Issue 7
Ion Mobility–Mass Spectrometry Reveals Long-Lived, Unfolded Intermediates in the Dissociation of Protein Complexes
journal, October 2007
- Ruotolo, Brandon T.; Hyung, Suk-Joon; Robinson, Paula M.
- Angewandte Chemie International Edition, Vol. 46, Issue 42
Mass spectrometry: come of age for structural and dynamical biology
journal, October 2011
- Benesch, Justin LP; Ruotolo, Brandon T.
- Current Opinion in Structural Biology, Vol. 21, Issue 5
Protein Complexes in the Gas Phase: Technology for Structural Genomics and Proteomics
journal, August 2007
- Benesch, Justin L. P.; Ruotolo, Brandon T.; Simmons, Douglas A.
- Chemical Reviews, Vol. 107, Issue 8
Naked Protein Conformations: Cytochrome c in the Gas Phase
journal, October 1995
- Clemmer, David E.; Hudgins, Robert R.; Jarrold, Martin F.
- Journal of the American Chemical Society, Vol. 117, Issue 40
The observation of non-covalent interactions in solution by electrospray ionization mass spectrometry: Promise, pitfalls and prognosis
journal, September 1993
- Smith, Richard D.; Light-Wahl, Karen J.
- Biological Mass Spectrometry, Vol. 22, Issue 9
A photoactive carotenoid protein acting as light intensity sensor
journal, August 2008
- Wilson, A.; Punginelli, C.; Gall, A.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
Do Charge State Signatures Guarantee Protein Conformations?
journal, May 2012
- Hall, Zoe; Robinson, Carol V.
- Journal of The American Society for Mass Spectrometry, Vol. 23, Issue 7
T-wave Ion Mobility-mass Spectrometry: Basic Experimental Procedures for Protein Complex Analysis
journal, January 2010
- Michaelevski, Izhak; Kirshenbaum, Noam; Sharon, Michal
- Journal of Visualized Experiments, Issue 41
Crystal structure of the FRP and identification of the active site for modulation of OCP-mediated photoprotection in cyanobacteria
journal, May 2013
- Sutter, M.; Wilson, A.; Leverenz, R. L.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 24
Local and global structural drivers for the photoactivation of the orange carotenoid protein
journal, September 2015
- Gupta, Sayan; Guttman, Miklos; Leverenz, Ryan L.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 41
Structural Determinants Underlying Photoprotection in the Photoactive Orange Carotenoid Protein of Cyanobacteria
journal, April 2010
- Wilson, Adjele; Kinney, James N.; Zwart, Petrus H.
- Journal of Biological Chemistry, Vol. 285, Issue 24
Investigation of intact protein complexes by mass spectrometry
journal, January 2004
- Heck, Albert J. R.; van den Heuvel, Robert H. H.
- Mass Spectrometry Reviews, Vol. 23, Issue 5
Probing the oligomeric structure of an enzyme by electrospray ionization time-of-flight mass spectrometry.
journal, July 1996
- Fitzgerald, M. C.; Chernushevich, I.; Standing, K. G.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 14
Structural, Mechanistic and Genomic Insights into OCP-Mediated Photoprotection
book, January 2013
- Kerfeld, Cheryl A.; Kirilovsky, Diana
- Advances in Botanical Research
Preliminary crystallographic analysis of 4-oxalocrotonate tautomerase reveals the oligomeric structure of the enzyme
journal, November 1994
- Roper, David I.; Subramanya, Hosahalli S.; Shingler, Victoria
- Journal of Molecular Biology, Vol. 243, Issue 4
Temperature-dependent H/D exchange of compact and elongated cytochrome c ions in the gas phase
journal, May 2002
- Valentine, Stephen J.; Clemmer, David E.
- Journal of the American Society for Mass Spectrometry, Vol. 13, Issue 5
A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II
journal, July 2006
- Nishiyama, Yoshitaka; Allakhverdiev, Suleyman I.; Murata, Norio
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 7
Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria
journal, June 2010
- Boulay, C.; Wilson, A.; D'Haene, S.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 25
Structural Symmetry and Protein Function
journal, June 2000
- Goodsell, David S.; Olson, Arthur J.
- Annual Review of Biophysics and Biomolecular Structure, Vol. 29, Issue 1
Characterization of the Synechocystis PCC 6803 Fluorescence Recovery Protein involved in photoprotection
journal, March 2013
- Gwizdala, Michal; Wilson, Adjélé; Omairi-Nasser, Amin
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 3
Travelling wave ion mobility mass spectrometry studies of protein structure: biological significance and comparison with X-ray crystallography and nuclear magnetic resonance spectroscopy measurements
journal, October 2008
- Scarff, Charlotte A.; Thalassinos, Konstantinos; Hilton, Gillian R.
- Rapid Communications in Mass Spectrometry, Vol. 22, Issue 20
Average Cross-Sectional Areas of Molecules by Gaseous Diffusion Methods
journal, October 1925
- Mack, Edward
- Journal of the American Chemical Society, Vol. 47, Issue 10
The Crystal Structure of a Cyanobacterial Water-Soluble Carotenoid Binding Protein
journal, January 2003
- Kerfeld, Cheryl A.; Sawaya, Michael R.; Brahmandam, Vishnu
- Structure, Vol. 11, Issue 1
Protein oligomerization: How and why
journal, September 2005
- Ali, Mayssam H.; Imperiali, Barbara
- Bioorganic & Medicinal Chemistry, Vol. 13, Issue 17
The purple Trp288Ala mutant of Synechocystis OCP persistently quenches phycobilisome fluorescence and tightly interacts with FRP
journal, January 2017
- Sluchanko, Nikolai N.; Klementiev, Konstantin E.; Shirshin, Evgeny A.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 1
Ion Mobility Mass Spectrometry of Two Tetrameric Membrane Protein Complexes Reveals Compact Structures and Differences in Stability and Packing
journal, November 2010
- Wang, Sheila C.; Politis, Argyris; Di Bartolo, Natalie
- Journal of the American Chemical Society, Vol. 132, Issue 44
Toward Understanding Insulin Fibrillation
journal, May 1997
- Brange, Jens; Andersen, Lennart; Laursen, Erik D.
- Journal of Pharmaceutical Sciences, Vol. 86, Issue 5
Characterization of the Oligomeric States of Insulin in Self-Assembly and Amyloid Fibril Formation by Mass Spectrometry
journal, August 2000
- Nettleton, Ewan J.; Tito, Paula; Sunde, Margaret
- Biophysical Journal, Vol. 79, Issue 2
The power of ion mobility-mass spectrometry for structural characterization and the study of conformational dynamics
journal, March 2014
- Lanucara, Francesco; Holman, Stephen W.; Gray, Christopher J.
- Nature Chemistry, Vol. 6, Issue 4
Structural Modeling of Heteromeric Protein Complexes from Disassembly Pathways and Ion Mobility-Mass Spectrometry
journal, September 2012
- Hall, Zoe; Politis, Argyris; Robinson, Carol V.
- Structure, Vol. 20, Issue 9
Molecular Mechanism of Photoactivation and Structural Location of the Cyanobacterial Orange Carotenoid Protein
journal, December 2013
- Zhang, Hao; Liu, Haijun; Niedzwiedzki, Dariusz M.
- Biochemistry, Vol. 53, Issue 1
Native mass spectrometry of photosynthetic pigment-protein complexes
journal, January 2013
- Zhang, Hao; Cui, Weidong; Gross, Michael L.
- FEBS Letters, Vol. 587, Issue 8
An exact hard-spheres scattering model for the mobilities of polyatomic ions
journal, October 1996
- Shvartsburg, Alexandre A.; Jarrold, Martin F.
- Chemical Physics Letters, Vol. 261, Issue 1-2
Charge-State Dependent Compaction and Dissociation of Protein Complexes: Insights from Ion Mobility and Molecular Dynamics
journal, February 2012
- Hall, Zoe; Politis, Argyris; Bush, Matthew F.
- Journal of the American Chemical Society, Vol. 134, Issue 7
4-Oxalocrotonate tautomerase, an enzyme composed of 62 amino acid residues per monomer.
journal, September 1992
- Chen, L. H.; Kenyon, G. L.; Curtin, F.
- Journal of Biological Chemistry, Vol. 267, Issue 25
Works referencing / citing this record:
OCP–FRP protein complex topologies suggest a mechanism for controlling high light tolerance in cyanobacteria
journal, September 2018
- Sluchanko, Nikolai N.; Slonimskiy, Yury B.; Shirshin, Evgeny A.
- Nature Communications, Vol. 9, Issue 1
Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs
journal, July 2017
- Kerfeld, Cheryl A.; Melnicki, Matthew R.; Sutter, Markus
- New Phytologist, Vol. 215, Issue 3
OCP–FRP protein complex topologies suggest a mechanism for controlling high light tolerance in cyanobacteria
text, January 2018
- Sluchanko, Nikolai N.; Slonimskiy, Yury B.; Shirshin, Evgeny A.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
High intracellular stability of the spidroin N‐terminal domain in spite of abundant amyloidogenic segments revealed by in‐cell hydrogen/deuterium exchange mass spectrometry
journal, December 2019
- Kaldmäe, Margit; Leppert, Axel; Chen, Gefei
- The FEBS Journal, Vol. 287, Issue 13
Interdomain interactions reveal the molecular evolution of the orange carotenoid protein
journal, September 2019
- Muzzopappa, Fernando; Wilson, Adjélé; Kirilovsky, Diana
- Nature Plants, Vol. 5, Issue 10