Reversible S-nitrosylation in an engineered azurin
Abstract
Here, S-Nitrosothiols are known as reagents for NO storage and transportation and as regulators in many physiological processes. Although the S-nitrosylation catalysed by haem proteins is well known, no direct evidence of S-nitrosylation in copper proteins has been reported. Here, we report reversible insertion of NO into a copper–thiolate bond in an engineered copper centre in Pseudomonas aeruginosa azurin by rational design of the primary coordination sphere and tuning its reduction potential by deleting a hydrogen bond in the secondary coordination sphere. The results not only provide the first direct evidence of S-nitrosylation of Cu(II)-bound cysteine in metalloproteins, but also shed light on the reaction mechanism and structural features responsible for stabilizing the elusive Cu(I)–S(Cys)NO species. The fast, efficient and reversible S-nitrosylation reaction is used to demonstrate its ability to prevent NO inhibition of cytochrome bo3 oxidase activity by competing for NO binding with the native enzyme under physiologically relevant conditions.
- Authors:
-
- Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
- Stanford Univ., Stanford, CA (United States)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Oregon Health & Sciences Univ., Portland, OR (United States)
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1340343
- Report Number(s):
- BNL-112002-2016-JA
Journal ID: ISSN 1755-4330
- Grant/Contract Number:
- SC00112704
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Chemistry
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 7; Journal ID: ISSN 1755-4330
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE
Citation Formats
Tian, Shiliang, Liu, Jing, Cowley, Ryan E., Hosseinzadeh, Parisa, Marshall, Nicholas M., Yu, Yang, Robinson, Howard, Nilges, Mark J., Blackburn, Ninian J., Solomon, Edward I., and Lu, Yi. Reversible S-nitrosylation in an engineered azurin. United States: N. p., 2016.
Web. doi:10.1038/nchem.2489.
Tian, Shiliang, Liu, Jing, Cowley, Ryan E., Hosseinzadeh, Parisa, Marshall, Nicholas M., Yu, Yang, Robinson, Howard, Nilges, Mark J., Blackburn, Ninian J., Solomon, Edward I., & Lu, Yi. Reversible S-nitrosylation in an engineered azurin. United States. https://doi.org/10.1038/nchem.2489
Tian, Shiliang, Liu, Jing, Cowley, Ryan E., Hosseinzadeh, Parisa, Marshall, Nicholas M., Yu, Yang, Robinson, Howard, Nilges, Mark J., Blackburn, Ninian J., Solomon, Edward I., and Lu, Yi. Mon .
"Reversible S-nitrosylation in an engineered azurin". United States. https://doi.org/10.1038/nchem.2489. https://www.osti.gov/servlets/purl/1340343.
@article{osti_1340343,
title = {Reversible S-nitrosylation in an engineered azurin},
author = {Tian, Shiliang and Liu, Jing and Cowley, Ryan E. and Hosseinzadeh, Parisa and Marshall, Nicholas M. and Yu, Yang and Robinson, Howard and Nilges, Mark J. and Blackburn, Ninian J. and Solomon, Edward I. and Lu, Yi},
abstractNote = {Here, S-Nitrosothiols are known as reagents for NO storage and transportation and as regulators in many physiological processes. Although the S-nitrosylation catalysed by haem proteins is well known, no direct evidence of S-nitrosylation in copper proteins has been reported. Here, we report reversible insertion of NO into a copper–thiolate bond in an engineered copper centre in Pseudomonas aeruginosa azurin by rational design of the primary coordination sphere and tuning its reduction potential by deleting a hydrogen bond in the secondary coordination sphere. The results not only provide the first direct evidence of S-nitrosylation of Cu(II)-bound cysteine in metalloproteins, but also shed light on the reaction mechanism and structural features responsible for stabilizing the elusive Cu(I)–S(Cys)NO species. The fast, efficient and reversible S-nitrosylation reaction is used to demonstrate its ability to prevent NO inhibition of cytochrome bo3 oxidase activity by competing for NO binding with the native enzyme under physiologically relevant conditions.},
doi = {10.1038/nchem.2489},
journal = {Nature Chemistry},
number = 7,
volume = 8,
place = {United States},
year = {Mon Apr 25 00:00:00 EDT 2016},
month = {Mon Apr 25 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
CHEMICAL PHYSIOLOGY OF BLOOD FLOW REGULATION BY RED BLOOD CELLS:: The Role of Nitric Oxide and S-Nitrosohemoglobin
journal, March 2005
- Singel, David J.; Stamler, Jonathan S.
- Annual Review of Physiology, Vol. 67, Issue 1
Activation of the Cardiac Calcium Release Channel (Ryanodine Receptor) by Poly-S-Nitrosylation
journal, January 1998
- Xu, Le; Eu, Jerry P.; Meissner, Gerhard
- Science, Vol. 279, Issue 5348
S-Nitrosylation of β-Arrestin Regulates β-Adrenergic Receptor Trafficking
journal, August 2008
- Ozawa, Kentaro; Whalen, Erin J.; Nelson, Christopher D.
- Molecular Cell, Vol. 31, Issue 3
Regulated Protein Denitrosylation by Cytosolic and Mitochondrial Thioredoxins
journal, May 2008
- Benhar, M.; Forrester, M. T.; Hess, D. T.
- Science, Vol. 320, Issue 5879
Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease
journal, February 2012
- Anand, Puneet; Stamler, Jonathan S.
- Journal of Molecular Medicine, Vol. 90, Issue 3
Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling
journal, December 2012
- Smith, Brian C.; Marletta, Michael A.
- Current Opinion in Chemical Biology, Vol. 16, Issue 5-6
Dinitrosyliron complexes and the mechanism(s) of cellular protein nitrosothiol formation from nitric oxide
journal, March 2009
- Bosworth, C. A.; Toledo, J. C.; Zmijewski, J. W.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 12
The oxyhemoglobin reaction of nitric oxide
journal, August 1999
- Gow, A. J.; Luchsinger, B. P.; Pawloski, J. R.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 16
Reactions of Deoxy-, Oxy-, and Methemoglobin with Nitrogen Monoxide: MECHANISTIC STUDIES OF THE S -NITROSOTHIOL FORMATION UNDER DIFFERENT MIXING CONDITIONS
journal, December 2002
- Herold, Susanna; Röck, Gabriele
- Journal of Biological Chemistry, Vol. 278, Issue 9
Crystallographic Analysis of the Interaction of Nitric Oxide with Quaternary-T Human Hemoglobin † , ‡
journal, January 2004
- Chan, Nei-Li; Kavanaugh, Jeffrey S.; Rogers, Paul H.
- Biochemistry, Vol. 43, Issue 1
Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein
journal, January 2005
- Weichsel, A.; Maes, E. M.; Andersen, J. F.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 3
Superoxide Dismutase Targets NO from GSNO to Cysβ93 of Oxyhemoglobin in Concentrated but Not Dilute Solutions of the Protein
journal, November 2003
- Romeo, Andrea A.; Capobianco, John A.; English, Ann M.
- Journal of the American Chemical Society, Vol. 125, Issue 47
Nitrosothiol Formation Catalyzed by Ceruloplasmin: IMPLICATION FOR CYTOPROTECTIVE MECHANISM IN VIVO
journal, September 1999
- Inoue, Katsuhisa; Akaike, Takaaki; Miyamoto, Yoichi
- Journal of Biological Chemistry, Vol. 274, Issue 38
Ceruloplasmin is a NO oxidase and nitrite synthase that determines endocrine NO homeostasis
journal, August 2006
- Shiva, Sruti; Wang, Xunde; Ringwood, Lorna A.
- Nature Chemical Biology, Vol. 2, Issue 9
Mechanism of S -Nitrosothiol Formation and Degradation Mediated by Copper Ions
journal, October 1999
- Stubauer, Gottfried; Giuffrè, Alessandro; Sarti, Paolo
- Journal of Biological Chemistry, Vol. 274, Issue 40
Cellular copper management—a draft user's guide
journal, March 2010
- Bertini, Ivano; Cavallaro, Gabriele; McGreevy, Kathleen S.
- Coordination Chemistry Reviews, Vol. 254, Issue 5-6
The mechanism of nitric oxide formation from S-nitrosothiols (thionitrites)
journal, January 1996
- Williams, D. Lyn H.
- Chemical Communications, Issue 10
The Chemistry of S-Nitrosothiols
journal, October 1999
- Williams, D. Lyn H.
- Accounts of Chemical Research, Vol. 32, Issue 10
The reaction of nitric oxide with ceruloplasmin
journal, April 1973
- Wever, R.; Van Leeuwen, F. X. R.; Van Gelder, B. F.
- Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 302, Issue 2
The interaction of nitric oxide with ascorbate oxidase
journal, October 1975
- van Leeuwen, F. X. R.; Wever, R.; van Gelder, B. F.
- Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 403, Issue 2
The reaction of nitric oxide with copper proteins and the photodissociation of copper-NO complexes
journal, November 1987
- Gorren, A. C. F.; de Boer, E.; Wever, R.
- Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 916, Issue 1
Ligand Binding and Protein Dynamics in Cupredoxins
journal, September 1995
- Ehrenstein, David; Filiaci, Mattia; Scharf, Birgit
- Biochemistry, Vol. 34, Issue 38
What is the real physiological NO concentration in vivo?
journal, September 2009
- Hall, Catherine N.; Garthwaite, John
- Nitric Oxide, Vol. 21, Issue 2
Type-zero copper proteins
journal, November 2009
- Lancaster, Kyle M.; George, Serena DeBeer; Yokoyama, Keiko
- Nature Chemistry, Vol. 1, Issue 9
Outer-Sphere Contributions to the Electronic Structure of Type Zero Copper Proteins
journal, April 2012
- Lancaster, Kyle M.; Zaballa, María-Eugenia; Sproules, Stephen
- Journal of the American Chemical Society, Vol. 134, Issue 19
Copper-sulfenate complex from oxidation of a cavity mutant of Pseudomonas aeruginosa azurin
journal, January 2014
- Sieracki, N. A.; Tian, S.; Hadt, R. G.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 3
Understanding copper-thiolate containing electron transfer centers by incorporation of unnatural amino acids and the CuA center into the type 1 copper protein azurin
journal, January 2013
- Wilson, Tiffany D.; Yu, Yang; Lu, Yi
- Coordination Chemistry Reviews, Vol. 257, Issue 1
Redesigning the Blue Copper Azurin into a Redox-Active Mononuclear Nonheme Iron Protein: Preparation and Study of Fe(II)-M121E Azurin
journal, August 2014
- Liu, Jing; Meier, Katlyn K.; Tian, Shiliang
- Journal of the American Chemical Society, Vol. 136, Issue 35
Nitrosocyanin, a Red Cupredoxin-like Protein from Nitrosomonas europaea †
journal, February 2002
- Arciero, David M.; Pierce, Brad S.; Hendrich, Michael P.
- Biochemistry, Vol. 41, Issue 6
Complete Genome Sequence of the Ammonia-Oxidizing Bacterium and Obligate Chemolithoautotroph Nitrosomonas europaea
journal, May 2003
- Chain, P.; Lamerdin, J.; Larimer, F.
- Journal of Bacteriology, Vol. 185, Issue 9
Spectroscopic and Density Functional Studies of the Red Copper Site in Nitrosocyanin: Role of the Protein in Determining Active Site Geometric and Electronic Structure
journal, February 2005
- Basumallick, Lipika; Sarangi, Ritimukta; DeBeer George, Serena
- Journal of the American Chemical Society, Vol. 127, Issue 10
Dali server: conservation mapping in 3D
journal, May 2010
- Holm, Liisa; Rosenstr�m, P�ivi
- Nucleic Acids Research, Vol. 38, Issue suppl_2
Copper coordination in blue proteins
journal, October 2000
- Gray, Harry B.; Malmström, Bo G.; Williams, R. J. P.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 5, Issue 5
Crystal Structure of a Novel Red Copper Protein from Nitrosomonas europaea † , ‡
journal, May 2001
- Lieberman, Raquel L.; Arciero, David M.; Hooper, Alan B.
- Biochemistry, Vol. 40, Issue 19
Rack-induced metal binding vs. flexibility: Met121His azurin crystal structures at different pH
journal, March 1998
- Messerschmidt, A.; Prade, L.; Kroes, S. J.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 7
Reduction potentials and their pH dependence in site-directed-mutant forms of azurin from Pseudomonas aeruginosa
journal, March 1993
- Pascher, Torbjorn; Karlsson, B. Goran; Nordling, Margareta
- European Journal of Biochemistry, Vol. 212, Issue 2
Rationally tuning the reduction potential of a single cupredoxin beyond the natural range
journal, November 2009
- Marshall, Nicholas M.; Garner, Dewain K.; Wilson, Tiffany D.
- Nature, Vol. 462, Issue 7269
Design of a single protein that spans the entire 2-V range of physiological redox potentials
journal, December 2015
- Hosseinzadeh, Parisa; Marshall, Nicholas M.; Chacón, Kelly N.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 2
The Role of Hydrogen Bonding at the Active Site of a Cupredoxin: The Phe114Pro Azurin Variant † , ‡
journal, July 2006
- Yanagisawa, Sachiko; Banfield, Mark J.; Dennison, Christopher
- Biochemistry, Vol. 45, Issue 29
Spectroscopic Methods in Bioinorganic Chemistry: Blue to Green to Red Copper Sites
journal, October 2006
- Solomon, Edward I.
- Inorganic Chemistry, Vol. 45, Issue 20
Nitric Oxide and Cytochrome c Oxidase: Mechanisms of Inhibition and NO Degradation
journal, July 2000
- Sarti, Paolo; Giuffré, Alessandro; Forte, Elena
- Biochemical and Biophysical Research Communications, Vol. 274, Issue 1
Effect of Superoxide Dismutase on the Stability ofS-Nitrosothiols
journal, January 1999
- Jourd'heuil, David; Laroux, F. Stephen; Miles, Allen M.
- Archives of Biochemistry and Biophysics, Vol. 361, Issue 2
Copper(I) Nitrosyls from Reaction of Copper(II) Thiolates with S -Nitrosothiols: Mechanism of NO Release from RSNOs at Cu
journal, October 2013
- Zhang, Shiyu; Çelebi-Ölçüm, Nihan; Melzer, Marie M.
- Journal of the American Chemical Society, Vol. 135, Issue 45
Spontaneous Catalytic Generation of Nitric Oxide from S -Nitrosothiols at the Surface of Polymer Films Doped with Lipophilic Copper(II) Complex
journal, August 2003
- Oh, Bong Kyun; Meyerhoff, Mark E.
- Journal of the American Chemical Society, Vol. 125, Issue 32
Theoretical Evidence that Cu I Complexation Promotes Degradation of S -Nitrosothiols
journal, December 2002
- Toubin, Céline; Yeung, David Y. -H.; English, Ann M.
- Journal of the American Chemical Society, Vol. 124, Issue 50
Influence of Cu + on the RS−NO Bond Dissociation Energy of S-Nitrosothiols
journal, February 2005
- Baciu, Cristina; Cho, Kyung-Bin; Gauld, James W.
- The Journal of Physical Chemistry B, Vol. 109, Issue 4
Nitric Oxide Donors: Chemical Activities and Biological Applications
journal, April 2002
- Wang, Peng George; Xian, Ming; Tang, Xiaoping
- Chemical Reviews, Vol. 102, Issue 4
Nitric Oxide and Cytochrome c Oxidase: Mechanisms of Inhibition and NO Degradation
journal, July 2000
- Sarti, Paolo; Giuffré, Alessandro; Forte, Elena
- Biochemical and Biophysical Research Communications, Vol. 274, Issue 1
Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease
journal, February 2012
- Anand, Puneet; Stamler, Jonathan S.
- Journal of Molecular Medicine, Vol. 90, Issue 3
The reaction of nitric oxide with ceruloplasmin
journal, April 1973
- Wever, R.; Van Leeuwen, F. X. R.; Van Gelder, B. F.
- Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 302, Issue 2
S-Nitrosylation of β-Arrestin Regulates β-Adrenergic Receptor Trafficking
journal, August 2008
- Ozawa, Kentaro; Whalen, Erin J.; Nelson, Christopher D.
- Molecular Cell, Vol. 31, Issue 3
What is the real physiological NO concentration in vivo?
journal, September 2009
- Hall, Catherine N.; Garthwaite, John
- Nitric Oxide, Vol. 21, Issue 2
Crystal Structure of a Novel Red Copper Protein from Nitrosomonas europaea † , ‡
journal, May 2001
- Lieberman, Raquel L.; Arciero, David M.; Hooper, Alan B.
- Biochemistry, Vol. 40, Issue 19
Nitrosocyanin, a Red Cupredoxin-like Protein from Nitrosomonas europaea †
journal, February 2002
- Arciero, David M.; Pierce, Brad S.; Hendrich, Michael P.
- Biochemistry, Vol. 41, Issue 6
Crystallographic Analysis of the Interaction of Nitric Oxide with Quaternary-T Human Hemoglobin † , ‡
journal, January 2004
- Chan, Nei-Li; Kavanaugh, Jeffrey S.; Rogers, Paul H.
- Biochemistry, Vol. 43, Issue 1
The Role of Hydrogen Bonding at the Active Site of a Cupredoxin: The Phe114Pro Azurin Variant † , ‡
journal, July 2006
- Yanagisawa, Sachiko; Banfield, Mark J.; Dennison, Christopher
- Biochemistry, Vol. 45, Issue 29
Nitric Oxide Donors: Chemical Activities and Biological Applications
journal, April 2002
- Wang, Peng George; Xian, Ming; Tang, Xiaoping
- Chemical Reviews, Vol. 102, Issue 4
Spectroscopic Methods in Bioinorganic Chemistry: Blue to Green to Red Copper Sites
journal, October 2006
- Solomon, Edward I.
- Inorganic Chemistry, Vol. 45, Issue 20
Theoretical Evidence that Cu I Complexation Promotes Degradation of S -Nitrosothiols
journal, December 2002
- Toubin, Céline; Yeung, David Y. -H.; English, Ann M.
- Journal of the American Chemical Society, Vol. 124, Issue 50
Superoxide Dismutase Targets NO from GSNO to Cysβ93 of Oxyhemoglobin in Concentrated but Not Dilute Solutions of the Protein
journal, November 2003
- Romeo, Andrea A.; Capobianco, John A.; English, Ann M.
- Journal of the American Chemical Society, Vol. 125, Issue 47
Spectroscopic and Density Functional Studies of the Red Copper Site in Nitrosocyanin: Role of the Protein in Determining Active Site Geometric and Electronic Structure
journal, February 2005
- Basumallick, Lipika; Sarangi, Ritimukta; DeBeer George, Serena
- Journal of the American Chemical Society, Vol. 127, Issue 10
Outer-Sphere Contributions to the Electronic Structure of Type Zero Copper Proteins
journal, April 2012
- Lancaster, Kyle M.; Zaballa, María-Eugenia; Sproules, Stephen
- Journal of the American Chemical Society, Vol. 134, Issue 19
Copper(I) Nitrosyls from Reaction of Copper(II) Thiolates with S -Nitrosothiols: Mechanism of NO Release from RSNOs at Cu
journal, October 2013
- Zhang, Shiyu; Çelebi-Ölçüm, Nihan; Melzer, Marie M.
- Journal of the American Chemical Society, Vol. 135, Issue 45
Redesigning the Blue Copper Azurin into a Redox-Active Mononuclear Nonheme Iron Protein: Preparation and Study of Fe(II)-M121E Azurin
journal, August 2014
- Liu, Jing; Meier, Katlyn K.; Tian, Shiliang
- Journal of the American Chemical Society, Vol. 136, Issue 35
Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein
journal, January 2005
- Weichsel, A.; Maes, E. M.; Andersen, J. F.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 3
Copper-sulfenate complex from oxidation of a cavity mutant of Pseudomonas aeruginosa azurin
journal, January 2014
- Sieracki, N. A.; Tian, S.; Hadt, R. G.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 3
A single protein redox ruler
journal, December 2015
- Bains, Rajneesh K.; Warren, Jeffrey J.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 2
Rack-induced metal binding vs. flexibility: Met121His azurin crystal structures at different pH
journal, March 1998
- Messerschmidt, A.; Prade, L.; Kroes, S. J.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 7
Physiological reactions of nitric oxide and hemoglobin: A radical rethink
journal, August 1999
- Gross, Steven S.; Lane, Paul
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 18
Involvement of Glycosylphosphatidylinositol-linked Ceruloplasmin in the Copper/Zinc-Nitric Oxide-dependent Degradation of Glypican-1 Heparan Sulfate in Rat C6 Glioma Cells
journal, January 2004
- Mani, Katrin; Cheng, Fang; Havsmark, Birgitta
- Journal of Biological Chemistry, Vol. 279, Issue 13
S -Nitrosylation-induced Conformational Change in Blackfin Tuna Myoglobin
journal, May 2007
- Schreiter, Eric R.; Rodríguez, María M.; Weichsel, Andrzej
- Journal of Biological Chemistry, Vol. 282, Issue 27
Dali server: conservation mapping in 3D
journal, May 2010
- Holm, Liisa; Rosenstr�m, P�ivi
- Nucleic Acids Research, Vol. 38, Issue suppl_2
Reduction potentials and their pH dependence in site-directed-mutant forms of azurin from Pseudomonas aeruginosa
journal, March 1993
- Pascher, Torbjorn; Karlsson, B. Goran; Nordling, Margareta
- European Journal of Biochemistry, Vol. 212, Issue 2
Activation of the Cardiac Calcium Release Channel (Ryanodine Receptor) by Poly-S-Nitrosylation
journal, January 1998
- Xu, Le; Eu, Jerry P.; Meissner, Gerhard
- Science, Vol. 279, Issue 5348
Lessons from the Genome of a Lithoautotroph: Making Biomass from Almost Nothing
journal, May 2003
- Ramos, Juan-Luis
- Journal of Bacteriology, Vol. 185, Issue 9
Physiologic and Proteomic Evidence for a Role of Nitric Oxide in Biofilm Formation by Nitrosomonas europaea and Other Ammonia Oxidizers
journal, April 2004
- Schmidt, I.; Steenbakkers, P. J. M.; op den Camp, H. J. M.
- Journal of Bacteriology, Vol. 186, Issue 9
CHEMICAL PHYSIOLOGY OF BLOOD FLOW REGULATION BY RED BLOOD CELLS:: The Role of Nitric Oxide and S-Nitrosohemoglobin
journal, March 2005
- Singel, David J.; Stamler, Jonathan S.
- Annual Review of Physiology, Vol. 67, Issue 1
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- Liu, Chang; Yu, Yingjie; Chen, Daquan
- Nanoscale Advances, Vol. 1, Issue 7
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- Bertoldo, Jean B.; Rodrigues, Tiago; Dunsmore, Lavinia
- Chem, Vol. 3, Issue 4