Insulin hexamer dissociation dynamics revealed by photoinduced T -jumps and time-resolved X-ray solution scattering

Rimmerman, Dolev; Leshchev, Denis; Hsu, Darren J.; Hong, Jiyun; Abraham, Baxter; Kosheleva, Irina; Henning, Robert; Chen, Lin X.

doi:10.1039/c8pp00034d

Insulin hexamer dissociation dynamics revealed by photoinduced T -jumps and time-resolved X-ray solution scattering

Journal Article · Sun Dec 31 23:00:00 EST 2017 · Photochemical & Photobiological Sciences

DOI:https://doi.org/10.1039/c8pp00034d· OSTI ID:1471508

Rimmerman, Dolev ^[1]; Leshchev, Denis ^[1]; Hsu, Darren J. ^[1]; Hong, Jiyun ^[1]; Abraham, Baxter ^[2]; Kosheleva, Irina ^[3]; Henning, Robert ^[3]; ^[4]

Department of Chemistry; Northwestern University; Evanston; USA
Department of Chemistry and Biochemistry; University of Delaware; Newark; USA
Center for Advanced Radiation Sources; The University of Chicago; USA
Department of Chemistry; Northwestern University; Evanston; USA; Chemical Sciences and Engineering Division

The structural dynamics of insulin hexamer dissociation were studied by the photoinduced temperature jump technique and monitored by time-resolved X-ray scattering.

Research Organization:: Argonne National Laboratory (ANL)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science - Office of Basic Energy Sciences

DOE Contract Number:: AC02-06CH11357

OSTI ID:: 1471508

Journal Information:: Photochemical & Photobiological Sciences, Journal Name: Photochemical & Photobiological Sciences Journal Issue: 7 Vol. 17; ISSN PPSHCB; ISSN 1474-905X

Publisher:: Royal Society of Chemistry

Country of Publication:: United States

Language:: English

References (48)

Studying Protein–Protein Binding through T-Jump Induced Dissociation: Transient 2D IR Spectroscopy of Insulin Dimer Zhang, Xin-Xing; Jones, Kevin C.; Fitzpatrick, Ann The Journal of Physical Chemistry B, Vol. 120, Issue 23 https://doi.org/10.1021/acs.jpcb.6b03246	journal	May 2016
Thermodynamics of Formation of the Insulin Hexamer: Metal-Stabilized Proton-Coupled Assembly of Quaternary Structure Carpenter, Margaret C.; Wilcox, Dean E. Biochemistry, Vol. 53, Issue 8 https://doi.org/10.1021/bi4016567	journal	February 2014
Protein Folding and Unfolding at Atomic Resolution Fersht, Alan R.; Daggett, Valerie Cell, Vol. 108, Issue 4 https://doi.org/10.1016/S0092-8674(02)00620-7	journal	February 2002
Molecular dynamics simulations of unfolding and refolding of a -hairpin fragment of protein G Pande, V. S.; Rokhsar, D. S. Proceedings of the National Academy of Sciences, Vol. 96, Issue 16 https://doi.org/10.1073/pnas.96.16.9062	journal	August 1999
Conformational Substates of Myoglobin Intermediate Resolved by Picosecond X-ray Solution Scattering Oang, Key Young; Kim, Jong Goo; Yang, Cheolhee The Journal of Physical Chemistry Letters, Vol. 5, Issue 5 https://doi.org/10.1021/jz4027425	journal	February 2014
Protein folding and unfolding on a complex energy landscape Leeson, D. T.; Gai, F.; Rodriguez, H. M. Proceedings of the National Academy of Sciences, Vol. 97, Issue 6 https://doi.org/10.1073/pnas.040580397	journal	February 2000
Protein structural dynamics in solution unveiled via 100-ps time-resolved x-ray scattering Cho, H. S.; Dashdorj, N.; Schotte, F. Proceedings of the National Academy of Sciences, Vol. 107, Issue 16 https://doi.org/10.1073/pnas.1002951107	journal	April 2010
Structural Characterisation and Functional Significance of Transient Protein–Protein Interactions Nooren, Irene M. A.; Thornton, Janet M. Journal of Molecular Biology, Vol. 325, Issue 5 https://doi.org/10.1016/S0022-2836(02)01281-0	journal	January 2003
Probing Cytochrome c Folding Transitions upon Phototriggered Environmental Perturbations Using Time-Resolved X-ray Scattering Rimmerman, Dolev; Leshchev, Denis; Hsu, Darren J. The Journal of Physical Chemistry B, Vol. 122, Issue 20 https://doi.org/10.1021/acs.jpcb.8b03354	journal	April 2018
Multimerization and Aggregation of Native-State Insulin: Effect of Zinc Xu, Yisheng; Yan, Yunfeng; Seeman, Daniel Langmuir, Vol. 28, Issue 1 https://doi.org/10.1021/la202902a	journal	December 2011
Prediction of the association state of insulin using spectral parameters Uversky, Vladimir N.; Garriques, Liza Nielsen; Millett, Ian S. Journal of Pharmaceutical Sciences, Vol. 92, Issue 4 https://doi.org/10.1002/jps.10355	journal	April 2003
Application of Singular Value Decomposition to the Analysis of Time-Resolved Macromolecular X-Ray Data Schmidt, Marius; Rajagopal, Sudarshan; Ren, Zhong Biophysical Journal, Vol. 84, Issue 3 https://doi.org/10.1016/S0006-3495(03)75018-8	journal	March 2003
Advances in X-ray scattering: from solution SAXS to achievements with coherent beams Pérez, Javier; Nishino, Yoshinori Current Opinion in Structural Biology, Vol. 22, Issue 5 https://doi.org/10.1016/j.sbi.2012.07.014	journal	October 2012
Impulsive solvent heating probed by picosecond x-ray diffraction Cammarata, M.; Lorenc, M.; Kim, T. K. The Journal of Chemical Physics, Vol. 124, Issue 12 https://doi.org/10.1063/1.2176617	journal	March 2006
Anisotropic Picosecond X-ray Solution Scattering from Photoselectively Aligned Protein Molecules Kim, Jeongho; Kim, Kyung Hwan; Kim, Jong Goo The Journal of Physical Chemistry Letters, Vol. 2, Issue 5 https://doi.org/10.1021/jz101503r	journal	February 2011
Sequential conformational transitions and α-helical supercoiling regulate a sensor histidine kinase Berntsson, Oskar; Diensthuber, Ralph P.; Panman, Matthijs R. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00300-5	journal	August 2017
Characterization of the nanoscale properties of individual amyloid fibrils Smith, J. F.; Knowles, T. P. J.; Dobson, C. M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 43 https://doi.org/10.1073/pnas.0604035103	journal	October 2006
Structure of human insulin monomer in water/acetonitrile solution Bocian, Wojciech; Sitkowski, Jerzy; Bednarek, Elżbieta Journal of Biomolecular NMR, Vol. 40, Issue 1 https://doi.org/10.1007/s10858-007-9206-2	journal	November 2007
Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle x-ray scattering Akiyama, S.; Takahashi, S.; Kimura, T. Proceedings of the National Academy of Sciences, Vol. 99, Issue 3 https://doi.org/10.1073/pnas.012458999	journal	January 2002
Thermal Dissociation and Unfolding of Insulin Huus, Kasper; Havelund, Svend; Olsen, Helle B. Biochemistry, Vol. 44, Issue 33 https://doi.org/10.1021/bi0507940	journal	August 2005
Visualizing Solution-Phase Reaction Dynamics with Time-Resolved X-ray Liquidography Ihee, Hyotcherl Accounts of Chemical Research, Vol. 42, Issue 2 https://doi.org/10.1021/ar800168v	journal	February 2009
Microscopic Reversibility of Protein Folding in Molecular Dynamics Simulations of the Engrailed Homeodomain ^† McCully, Michelle E.; Beck, David A. C.; Daggett, Valerie Biochemistry, Vol. 47, Issue 27 https://doi.org/10.1021/bi800118b	journal	July 2008
Time-Resolved X-Ray Solution Scattering Reveals the Structural Photoactivation of a Light-Oxygen-Voltage Photoreceptor Berntsson, Oskar; Diensthuber, Ralph P.; Panman, Matthijs R. Structure, Vol. 25, Issue 6 https://doi.org/10.1016/j.str.2017.04.006	journal	June 2017
Insulin Loaded PLGA Microspheres: Effect of Zinc Salts on Encapsulation, Release, and Stability Manoharan, Chandrasekar; Singh, Jagdish Journal of Pharmaceutical Sciences, Vol. 98, Issue 2 https://doi.org/10.1002/jps.21445	journal	February 2009
SVD-aided pseudo principal-component analysis: A new method to speed up and improve determination of the optimum kinetic model from time-resolved data Oang, Key Young; Yang, Cheolhee; Muniyappan, Srinivasan Structural Dynamics, Vol. 4, Issue 4 https://doi.org/10.1063/1.4979854	journal	July 2017
Time-resolved methods in biophysics. 9. Laser temperature-jump methods for investigating biomolecular dynamics Kubelka, Jan Photochemical & Photobiological Sciences, Vol. 8, Issue 4 https://doi.org/10.1039/b819929a	journal	January 2009
Direct Observation of Insulin Association Dynamics with Time-Resolved X-ray Scattering Rimmerman, Dolev; Leshchev, Denis; Hsu, Darren J. The Journal of Physical Chemistry Letters, Vol. 8, Issue 18 https://doi.org/10.1021/acs.jpclett.7b01720	journal	September 2017
BioCARS: a synchrotron resource for time-resolved X-ray science Graber, T.; Anderson, S.; Brewer, H. Journal of Synchrotron Radiation, Vol. 18, Issue 4 https://doi.org/10.1107/S0909049511009423	journal	May 2011
The role of assembly in insulin's biosynthesis Dodson, Guy; Steiner, Don Current Opinion in Structural Biology, Vol. 8, Issue 2 https://doi.org/10.1016/S0959-440X(98)80037-7	journal	April 1998
Amyloid Fibrillation of Insulin under Water-Limited Conditions Choi, Tae Su; Lee, Jong Wha; Jin, Kyeong Sik Biophysical Journal, Vol. 107, Issue 8 https://doi.org/10.1016/j.bpj.2014.09.008	journal	October 2014
pH-dependent self-association of zinc-free insulin characterized by concentration-gradient static light scattering Attri, Arun K.; Fernández, Cristina; Minton, Allen P. Biophysical Chemistry, Vol. 148, Issue 1-3 https://doi.org/10.1016/j.bpc.2010.02.002	journal	May 2010
The structure of T ₆ bovine insulin Smith, G. David; Pangborn, Walter A.; Blessing, Robert H. Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 11 https://doi.org/10.1107/S0907444905025771	journal	October 2005
Protein Structural Dynamics of Photoactive Yellow Protein in Solution Revealed by Pump–Probe X-ray Solution Scattering Kim, Tae Wu; Lee, Jae Hyuk; Choi, Jungkweon Journal of the American Chemical Society, Vol. 134, Issue 6 https://doi.org/10.1021/ja210435n	journal	February 2012
A practical guide to small angle X-ray scattering (SAXS) of flexible and intrinsically disordered proteins Kikhney, Alexey G.; Svergun, Dmitri I. FEBS Letters, Vol. 589, Issue 19PartA https://doi.org/10.1016/j.febslet.2015.08.027	journal	August 2015
Picosecond Photobiology: Watching a Signaling Protein Function in Real Time via Time-Resolved Small- and Wide-Angle X-ray Scattering Cho, Hyun Sun; Schotte, Friedrich; Dashdorj, Naranbaatar Journal of the American Chemical Society, Vol. 138, Issue 28 https://doi.org/10.1021/jacs.6b03565	journal	July 2016
Time-resolved photothermal methods: accessing time-resolved thermodynamics of photoinduced processes in chemistry and biologyDedicated to Professor Silvia Braslavsky, to mark her great contribution to photochemistry and photobiology particularly in the field of photothermal methods. Gensch, Thomas; Viappiani, Cristiano Photochemical & Photobiological Sciences, Vol. 2, Issue 7 https://doi.org/10.1039/b303177b	journal	January 2003
Tracking the structural dynamics of proteins in solution using time-resolved wide-angle X-ray scattering Cammarata, Marco; Levantino, Matteo; Schotte, Friedrich Nature Methods, Vol. 5, Issue 10 https://doi.org/10.1038/nmeth.1255	journal	September 2008
Insulin dimer dissociation and unfolding revealed by amide I two-dimensional infrared spectroscopy Ganim, Ziad; Jones, Kevin C.; Tokmakoff, Andrei Phys. Chem. Chem. Phys., Vol. 12, Issue 14 https://doi.org/10.1039/B923515A	journal	January 2010
T HE F AST P ROTEIN F OLDING P ROBLEM Gruebele, M. Annual Review of Physical Chemistry, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.physchem.50.1.485	journal	October 1999
Effect of Environmental Factors on the Kinetics of Insulin Fibril Formation: Elucidation of the Molecular Mechanism ^† Nielsen, Liza; Khurana, Ritu; Coats, Alisa Biochemistry, Vol. 40, Issue 20 https://doi.org/10.1021/bi002555c	journal	May 2001
Transient 2D IR spectroscopy of ubiquitin unfolding dynamics Chung, H. S.; Ganim, Z.; Jones, K. C. Proceedings of the National Academy of Sciences, Vol. 104, Issue 36 https://doi.org/10.1073/pnas.0700959104	journal	June 2007
Ferritin Assembly Revisited: A Time-Resolved Small-Angle X-ray Scattering Study Sato, Daisuke; Ohtomo, Hideaki; Yamada, Yoshiteru Biochemistry, Vol. 55, Issue 2 https://doi.org/10.1021/acs.biochem.5b01152	journal	January 2016
Stimulation of Insulin Fibrillation by Urea-induced Intermediates Ahmad, Atta; Millett, Ian S.; Doniach, Sebastian Journal of Biological Chemistry, Vol. 279, Issue 15 https://doi.org/10.1074/jbc.M313134200	journal	January 2004
Partially Folded Intermediates in Insulin Fibrillation ^† Ahmad, Atta; Millett, Ian S.; Doniach, Sebastian Biochemistry, Vol. 42, Issue 39 https://doi.org/10.1021/bi034868o	journal	October 2003
Monitoring and Inhibition of Insulin Fibrillation by a Small Organic Fluorogen with Aggregation-Induced Emission Characteristics Hong, Yuning; Meng, Luming; Chen, Sijie Journal of the American Chemical Society, Vol. 134, Issue 3 https://doi.org/10.1021/ja208720a	journal	January 2012
Unifying features in protein-folding mechanisms Gianni, S.; Guydosh, N. R.; Khan, F. Proceedings of the National Academy of Sciences, Vol. 100, Issue 23 https://doi.org/10.1073/pnas.1835776100	journal	October 2003
Laser Temperature Jump Induced Protein Refolding ^† Gruebele, Martin; Sabelko, Jobiah; Ballew, Richard Accounts of Chemical Research, Vol. 31, Issue 11 https://doi.org/10.1021/ar970083x	journal	November 1998
Direct Observation of Cooperative Protein Structural Dynamics of Homodimeric Hemoglobin from 100 ps to 10 ms with Pump–Probe X-ray Solution Scattering Kim, Kyung Hwan; Muniyappan, Srinivasan; Oang, Key Young Journal of the American Chemical Society, Vol. 134, Issue 16 https://doi.org/10.1021/ja210856v	journal	April 2012

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