Engineering the Assembly of Heme Cofactors in Man-Made Proteins

Solomon, Lee A.; Kodali, Goutham; Moser, Christopher C.; Dutton, P. Leslie

doi:10.1021/ja411845f

Title: Engineering the Assembly of Heme Cofactors in Man-Made Proteins

Authors:

Solomon, Lee A. ^[1]; Kodali, Goutham ^[1]; Moser, Christopher C. ^[1]; Dutton, P. Leslie ^[1]

The Johnson Research Foundation, Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, Pennsylvania 19104, United States

Publication Date:: Thu Feb 13 00:00:00 EST 2014

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1179598

Grant/Contract Number:: FG02-05ER46223

Resource Type:: Published Article

Journal Name:: Journal of the American Chemical Society

Additional Journal Information:: Journal Name: Journal of the American Chemical Society Journal Volume: 136 Journal Issue: 8; Journal ID: ISSN 0002-7863

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

Citation Formats


                    Solomon, Lee A., Kodali, Goutham, Moser, Christopher C., and Dutton, P. Leslie. Engineering the Assembly of Heme Cofactors in Man-Made Proteins.  United States: N. p., 2014. 
Web.  doi:10.1021/ja411845f.

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                    Solomon, Lee A., Kodali, Goutham, Moser, Christopher C., & Dutton, P. Leslie. Engineering the Assembly of Heme Cofactors in Man-Made Proteins.  United States.  https://doi.org/10.1021/ja411845f

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                    Solomon, Lee A., Kodali, Goutham, Moser, Christopher C., and Dutton, P. Leslie. Thu .  
"Engineering the Assembly of Heme Cofactors in Man-Made Proteins".  United States.  https://doi.org/10.1021/ja411845f.

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@article{osti_1179598,

  title        = {Engineering the Assembly of Heme Cofactors in Man-Made Proteins},

  author       = {Solomon, Lee A. and Kodali, Goutham and Moser, Christopher C. and Dutton, P. Leslie},

  abstractNote = {},

  doi          = {10.1021/ja411845f},

  journal      = {Journal of the American Chemical Society},

  number       = 8,

  volume       = 136,

  place        = {United States},

  year         = {Thu Feb 13 00:00:00 EST 2014},

  month        = {Thu Feb 13 00:00:00 EST 2014}

}

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Works referenced in this record:

Constructing a man-made c-type cytochrome maquette in vivo: electron transfer, oxygen transport and conversion to a photoactive light harvesting maquette.
journal, January 2014

Anderson, J. L. Ross; Armstrong, Craig T.; Kodali, Goutham
Chem. Sci., Vol. 5, Issue 2
DOI: 10.1039/C3SC52019F

Kinetics of heme interaction with heme-binding proteins: The effect of heme aggregation state
journal, October 1997

Kuželová, Kateřina; Mrhalová, Marcela; Hrkal, Zbyněk
Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1336, Issue 3
DOI: 10.1016/S0304-4165(97)00062-7

Structural propensities in the heme binding region of apocytochrome b5. II. Heme conjugates
journal, January 2008

Davis, Ronald B.; Lecomte, Juliette T. J.
Biopolymers, Vol. 90, Issue 4
DOI: 10.1002/bip.20995

Peptide Chemistry
book, January 1993

Bodanszky, Miklos
Springer Link
DOI: 10.1007/978-3-642-78206-0

Design and synthesis of multi-haem proteins
journal, March 1994

Robertson, Dan E.; Farid, Ramy S.; Moser, Christopher C.
Nature, Vol. 368, Issue 6470, p. 425-432
DOI: 10.1038/368425a0

Is Apomyoglobin a Molten Globule? Structural Characterization by NMR
journal, November 1996

Eliezer, David; Wright, Peter E.
Journal of Molecular Biology, Vol. 263, Issue 4
DOI: 10.1006/jmbi.1996.0596

Molecular Genetic Identification of a Pathway for Heme Binding to Cytochrome b ₆
journal, December 1997

Kuras, Richard; de Vitry, Catherine; Choquet, Yves
Journal of Biological Chemistry, Vol. 272, Issue 51
DOI: 10.1074/jbc.272.51.32427

Chlorophyll Biosynthesis: Recent Advances and Areas of Current Interest
journal, June 1983

Castelfranco, P. A.; Beale, S. I.
Annual Review of Plant Physiology, Vol. 34, Issue 1
DOI: 10.1146/annurev.pp.34.060183.001325

Self-Assembly of Heme A and Heme B in a Designed Four-Helix Bundle: Implications for a Cytochrome c Oxidase Maquette
journal, August 2000

Gibney, Brian R.; Isogai, Yasuhiro; Rabanal, Francesc
Biochemistry, Vol. 39, Issue 36
DOI: 10.1021/bi000925r

Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra
journal, February 1987

Berry, Edward A.; Trumpower, Bernard L.
Analytical Biochemistry, Vol. 161, Issue 1
DOI: 10.1016/0003-2697(87)90643-9

Partition coefficients and their uses
journal, December 1971

Leo, Albert; Hansch, Corwin; Elkins, David
Chemical Reviews, Vol. 71, Issue 6
DOI: 10.1021/cr60274a001

Engineering oxidoreductases: maquette proteins designed from scratch
journal, May 2012

Lichtenstein, Bruce R.; Farid, Tammer A.; Kodali, Goutham
Biochemical Society Transactions, Vol. 40, Issue 3
DOI: 10.1042/BST20120067

Biogenesis of cytochrome c oxidase
journal, December 2005

Khalimonchuk, Oleh; Rödel, Gerhard
Mitochondrion, Vol. 5, Issue 6
DOI: 10.1016/j.mito.2005.08.002

The Solution Structure of Oxidized Escherichia coli Cytochrome b ₅₆₂ ^,
journal, June 1999

Arnesano, Fabio; Banci, Lucia; Bertini, Ivano
Biochemistry, Vol. 38, Issue 27
DOI: 10.1021/bi982785f

Speciation and structure of ferriprotoporphyrin IX in aqueous solution: spectroscopic and diffusion measurements demonstrate dimerization, but not μ-oxo dimer formation
journal, September 2006

de Villiers, Katherine A.; Kaschula, Catherine H.; Egan, Timothy J.
JBIC Journal of Biological Inorganic Chemistry, Vol. 12, Issue 1
DOI: 10.1007/s00775-006-0170-1

Cloning and expression of the gene encoding the soluble cytochrome b562 of Escherichia coli
journal, December 1991

Nikkila, Heli; Gennis, Robert B.; Sligar, Stephen G.
European Journal of Biochemistry, Vol. 202, Issue 2
DOI: 10.1111/j.1432-1033.1991.tb16377.x

Nativelike Structure in Designed Four α-Helix Bundles Driven by Buried Polar Interactions
journal, November 2006

Koder, Ronald L.; Valentine, Kathleen G.; Cerda, Jose
Journal of the American Chemical Society, Vol. 128, Issue 45
DOI: 10.1021/ja064883r

Manipulating Cofactor Binding Thermodynamics in an Artificial Oxygen Transport Protein
journal, November 2011

Zhang, Lei; Anderson, J. L. Ross; Ahmed, Ismail
Biochemistry, Vol. 50, Issue 47
DOI: 10.1021/bi201242a

Hydrophobic Modulation of Heme Properties in Heme Protein Maquettes ^†
journal, September 2001

Gibney, Brian R.; Huang, Steve S.; Skalicky, Jack J.
Biochemistry, Vol. 40, Issue 35
DOI: 10.1021/bi002806h

The Heme Chaperone ApoCcmE Forms a Ternary Complex with CcmI and Apocytochrome c
journal, January 2013

Verissimo, Andreia F.; Mohtar, Mohamad A.; Daldal, Fevzi
Journal of Biological Chemistry, Vol. 288, Issue 9
DOI: 10.1074/jbc.M112.440024

Elementary tetrahelical protein design for diverse oxidoreductase functions
journal, October 2013

Farid, Tammer A.; Kodali, Goutham; Solomon, Lee A.
Nature Chemical Biology, Vol. 9, Issue 12
DOI: 10.1038/nchembio.1362

Speciation of Ferriprotoporphyrin IX in Aqueous and Mixed Aqueous Solution Is Controlled by Solvent Identity, pH, and Salt Concentration
journal, August 2009

Asher, Constance; de Villiers, Katherine A.; Egan, Timothy J.
Inorganic Chemistry, Vol. 48, Issue 16
DOI: 10.1021/ic900647y

Fenton chemistry in biology and medicine
journal, January 2007

Prousek, Josef
Pure and Applied Chemistry, Vol. 79, Issue 12
DOI: 10.1351/pac200779122325

Proton and nitrogen-15 NMR resonance assignments and preliminary structural characterization of Escherichia coli apocytochrome b562
journal, August 1991

Feng, Yiqing; Wand, A. Joshua; Sligar, Stephen G.
Biochemistry, Vol. 30, Issue 31
DOI: 10.1021/bi00245a007

Aggregation of ferrihaems. Dimerization and protolytic equilibria of protoferrihaem and deuteroferrihaem in aqueous solution
journal, May 1970

Brown, S. B.; Dean, T. C.; Jones, Peter
Biochemical Journal, Vol. 117, Issue 4
DOI: 10.1042/bj1170733

X-ray Structure of a Maquette Scaffold
journal, February 2003

Huang, Steve S.; Gibney, Brian R.; Stayrook, Steven E.
Journal of Molecular Biology, Vol. 326, Issue 4
DOI: 10.1016/S0022-2836(02)01441-9

Effect of Alkali and Borohydride on Cardiac Cytochrome Oxidase
journal, January 1965

Takemori, Shigeki; King, Tsoo E.
Journal of Biological Chemistry, Vol. 240, Issue 1
DOI: 10.1016/S0021-9258(18)97680-5

Negative activation enthalpies in the kinetics of protein folding.
journal, September 1995

Oliveberg, M.; Tan, Y. J.; Fersht, A. R.
Proceedings of the National Academy of Sciences, Vol. 92, Issue 19
DOI: 10.1073/pnas.92.19.8926

Histidine placement in de novo-designed heme proteins
journal, January 1999

Gibney, Brian R.; Dutton, P. Leslie
Protein Science, Vol. 8, Issue 9
DOI: 10.1110/ps.8.9.1888

Effect of Four Helix Bundle Topology on Heme Binding and Redox Properties ^†
journal, March 1998

Gibney, Brian R.; Rabanal, Francesc; Reddy, Konda S.
Biochemistry, Vol. 37, Issue 13
DOI: 10.1021/bi971856s

Second order kinetics of the reduction of cytochrome c2 by the ubiquinone cytochrome b-c2 oxidoreductase of Rhodopseudomonas sphaeroides.
journal, June 1978

Prince, R. C.; Bashford, C. L.; Takamiya, K. I.
Journal of Biological Chemistry, Vol. 253, Issue 12
DOI: 10.1016/S0021-9258(17)34694-X

Energetics of Heme Binding to Native and Denatured States of Cytochrome b ₅₆₂
journal, December 1997

Robinson, Clifford R.; Liu, Yufeng; Thomson, James A.
Biochemistry, Vol. 36, Issue 51
DOI: 10.1021/bi971470h

Heme models I. solution behavior of a water soluble iron porphyrin
journal, January 1976

Stong, John D.; Hartzell, Charles R.
Bioinorganic Chemistry, Vol. 5, Issue 3
DOI: 10.1016/S0006-3061(00)82020-7

Structure, function and assembly of Photosystem II and its light-harvesting proteins
journal, December 2004

Minagawa, Jun; Takahashi, Yuichiro
Photosynthesis Research, Vol. 82, Issue 3
DOI: 10.1007/s11120-004-2079-2

Regulation of the Heme A Biosynthetic Pathway
journal, January 2009

Wang, Zhihong; Wang, Yuxin; Hegg, Eric L.
Journal of Biological Chemistry, Vol. 284, Issue 2
DOI: 10.1074/jbc.M804167200

Effect of heme binding on the structure and stability of Escherichia coli apocytochrome b562
journal, October 1991

Feng, Yiqing; Sligar, Stephen G.
Biochemistry, Vol. 30, Issue 42
DOI: 10.1021/bi00106a011

A New Method of Solvation Analysis: Applications to Quinones
journal, May 1990

Keske, Jonathan M.; Bruce, J. Malcolm; Dutton, P. Leslie
Zeitschrift für Naturforschung C, Vol. 45, Issue 5
DOI: 10.1515/znc-1990-0520

Proof of Principle in a De novo Designed Protein Maquette: An Allosterically Regulated, Charge-Activated Conformational Switch in a Tetra-α-Helix Bundle ^†
journal, May 2001

Grosset, Anne M.; Gibney, Brian R.; Rabanal, Francesc
Biochemistry, Vol. 40, Issue 18
DOI: 10.1021/bi002504f

Speeding molecular recognition by using the folding funnel: The fly-casting mechanism
journal, July 2000

Shoemaker, B. A.; Portman, J. J.; Wolynes, P. G.
Proceedings of the National Academy of Sciences, Vol. 97, Issue 16
DOI: 10.1073/pnas.160259697

The histidine of the c-type cytochrome CXXCH haem-binding motif is essential for haem attachment by the Escherichia coli cytochrome c maturation (Ccm) apparatus
journal, July 2005

Allen, James W. A.; Leach, Nicholas; Ferguson, Stuart J.
Biochemical Journal, Vol. 389, Issue 2
DOI: 10.1042/BJ20041894

Covalent cofactor attachment to proteins: cytochrome c biogenesis
journal, August 2005

Stevens, J. M.; Uchida, T.; Daltrop, O.
Biochemical Society Transactions, Vol. 33, Issue 4
DOI: 10.1042/BST0330792

The assembly and organisation of photosynthetic membranes in Rhodobacter sphaeroides
journal, January 2005

Hunter, C. Neil; Tucker, Jamey D.; Niederman, Robert A.
Photochemical & Photobiological Sciences, Vol. 4, Issue 12
DOI: 10.1039/b506099k

Role of Heme in the Unfolding and Assembly of Myoglobin
journal, June 2010

Culbertson, David S.; Olson, John S.
Biochemistry, Vol. 49, Issue 29
DOI: 10.1021/bi1006942

Design and engineering of an O₂ transport protein
journal, March 2009

Koder, Ronald L.; Anderson, J. L. Ross; Solomon, Lee A.
Nature, Vol. 458, Issue 7236, p. 305-309
DOI: 10.1038/nature07841

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Title: Engineering the Assembly of Heme Cofactors in Man-Made Proteins

Citation Formats

Constructing a man-made c-type cytochrome maquette in vivo: electron transfer, oxygen transport and conversion to a photoactive light harvesting maquette. journal, January 2014

Kinetics of heme interaction with heme-binding proteins: The effect of heme aggregation state journal, October 1997

Structural propensities in the heme binding region of apocytochrome b5. II. Heme conjugates journal, January 2008

Peptide Chemistry book, January 1993

Design and synthesis of multi-haem proteins journal, March 1994

Is Apomyoglobin a Molten Globule? Structural Characterization by NMR journal, November 1996

Molecular Genetic Identification of a Pathway for Heme Binding to Cytochrome b 6 journal, December 1997

Chlorophyll Biosynthesis: Recent Advances and Areas of Current Interest journal, June 1983

Self-Assembly of Heme A and Heme B in a Designed Four-Helix Bundle: Implications for a Cytochrome c Oxidase Maquette journal, August 2000

Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra journal, February 1987

Partition coefficients and their uses journal, December 1971

Engineering oxidoreductases: maquette proteins designed from scratch journal, May 2012

Biogenesis of cytochrome c oxidase journal, December 2005

The Solution Structure of Oxidized Escherichia coli Cytochrome b 562 , journal, June 1999

Speciation and structure of ferriprotoporphyrin IX in aqueous solution: spectroscopic and diffusion measurements demonstrate dimerization, but not μ-oxo dimer formation journal, September 2006

Cloning and expression of the gene encoding the soluble cytochrome b562 of Escherichia coli journal, December 1991

Nativelike Structure in Designed Four α-Helix Bundles Driven by Buried Polar Interactions journal, November 2006

Manipulating Cofactor Binding Thermodynamics in an Artificial Oxygen Transport Protein journal, November 2011

Hydrophobic Modulation of Heme Properties in Heme Protein Maquettes † journal, September 2001

The Heme Chaperone ApoCcmE Forms a Ternary Complex with CcmI and Apocytochrome c journal, January 2013

Elementary tetrahelical protein design for diverse oxidoreductase functions journal, October 2013

Speciation of Ferriprotoporphyrin IX in Aqueous and Mixed Aqueous Solution Is Controlled by Solvent Identity, pH, and Salt Concentration journal, August 2009

Fenton chemistry in biology and medicine journal, January 2007

Proton and nitrogen-15 NMR resonance assignments and preliminary structural characterization of Escherichia coli apocytochrome b562 journal, August 1991

Aggregation of ferrihaems. Dimerization and protolytic equilibria of protoferrihaem and deuteroferrihaem in aqueous solution journal, May 1970

X-ray Structure of a Maquette Scaffold journal, February 2003

Effect of Alkali and Borohydride on Cardiac Cytochrome Oxidase journal, January 1965

Negative activation enthalpies in the kinetics of protein folding. journal, September 1995

Histidine placement in de novo-designed heme proteins journal, January 1999

Effect of Four Helix Bundle Topology on Heme Binding and Redox Properties † journal, March 1998

Second order kinetics of the reduction of cytochrome c2 by the ubiquinone cytochrome b-c2 oxidoreductase of Rhodopseudomonas sphaeroides. journal, June 1978

Energetics of Heme Binding to Native and Denatured States of Cytochrome b 562 journal, December 1997

Heme models I. solution behavior of a water soluble iron porphyrin journal, January 1976

Structure, function and assembly of Photosystem II and its light-harvesting proteins journal, December 2004

Regulation of the Heme A Biosynthetic Pathway journal, January 2009

Effect of heme binding on the structure and stability of Escherichia coli apocytochrome b562 journal, October 1991

A New Method of Solvation Analysis: Applications to Quinones journal, May 1990

Proof of Principle in a De novo Designed Protein Maquette: An Allosterically Regulated, Charge-Activated Conformational Switch in a Tetra-α-Helix Bundle † journal, May 2001

Speeding molecular recognition by using the folding funnel: The fly-casting mechanism journal, July 2000

The histidine of the c-type cytochrome CXXCH haem-binding motif is essential for haem attachment by the Escherichia coli cytochrome c maturation (Ccm) apparatus journal, July 2005

Covalent cofactor attachment to proteins: cytochrome c biogenesis journal, August 2005

The assembly and organisation of photosynthetic membranes in Rhodobacter sphaeroides journal, January 2005

Role of Heme in the Unfolding and Assembly of Myoglobin journal, June 2010

Design and engineering of an O2 transport protein journal, March 2009

Constructing a man-made c-type cytochrome maquette in vivo: electron transfer, oxygen transport and conversion to a photoactive light harvesting maquette.
journal, January 2014

Kinetics of heme interaction with heme-binding proteins: The effect of heme aggregation state
journal, October 1997

Structural propensities in the heme binding region of apocytochrome b5. II. Heme conjugates
journal, January 2008

Peptide Chemistry
book, January 1993

Design and synthesis of multi-haem proteins
journal, March 1994

Is Apomyoglobin a Molten Globule? Structural Characterization by NMR
journal, November 1996

Molecular Genetic Identification of a Pathway for Heme Binding to Cytochrome b ₆
journal, December 1997

Chlorophyll Biosynthesis: Recent Advances and Areas of Current Interest
journal, June 1983

Self-Assembly of Heme A and Heme B in a Designed Four-Helix Bundle: Implications for a Cytochrome c Oxidase Maquette
journal, August 2000

Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra
journal, February 1987

Partition coefficients and their uses
journal, December 1971

Engineering oxidoreductases: maquette proteins designed from scratch
journal, May 2012

Biogenesis of cytochrome c oxidase
journal, December 2005

The Solution Structure of Oxidized Escherichia coli Cytochrome b ₅₆₂ ^,
journal, June 1999

Speciation and structure of ferriprotoporphyrin IX in aqueous solution: spectroscopic and diffusion measurements demonstrate dimerization, but not μ-oxo dimer formation
journal, September 2006

Cloning and expression of the gene encoding the soluble cytochrome b562 of Escherichia coli
journal, December 1991

Nativelike Structure in Designed Four α-Helix Bundles Driven by Buried Polar Interactions
journal, November 2006

Manipulating Cofactor Binding Thermodynamics in an Artificial Oxygen Transport Protein
journal, November 2011

Hydrophobic Modulation of Heme Properties in Heme Protein Maquettes ^†
journal, September 2001

The Heme Chaperone ApoCcmE Forms a Ternary Complex with CcmI and Apocytochrome c
journal, January 2013

Elementary tetrahelical protein design for diverse oxidoreductase functions
journal, October 2013

Speciation of Ferriprotoporphyrin IX in Aqueous and Mixed Aqueous Solution Is Controlled by Solvent Identity, pH, and Salt Concentration
journal, August 2009

Fenton chemistry in biology and medicine
journal, January 2007

Proton and nitrogen-15 NMR resonance assignments and preliminary structural characterization of Escherichia coli apocytochrome b562
journal, August 1991

Aggregation of ferrihaems. Dimerization and protolytic equilibria of protoferrihaem and deuteroferrihaem in aqueous solution
journal, May 1970

X-ray Structure of a Maquette Scaffold
journal, February 2003

Effect of Alkali and Borohydride on Cardiac Cytochrome Oxidase
journal, January 1965

Negative activation enthalpies in the kinetics of protein folding.
journal, September 1995

Histidine placement in de novo-designed heme proteins
journal, January 1999

Effect of Four Helix Bundle Topology on Heme Binding and Redox Properties ^†
journal, March 1998

Second order kinetics of the reduction of cytochrome c2 by the ubiquinone cytochrome b-c2 oxidoreductase of Rhodopseudomonas sphaeroides.
journal, June 1978

Energetics of Heme Binding to Native and Denatured States of Cytochrome b ₅₆₂
journal, December 1997

Heme models I. solution behavior of a water soluble iron porphyrin
journal, January 1976

Structure, function and assembly of Photosystem II and its light-harvesting proteins
journal, December 2004

Regulation of the Heme A Biosynthetic Pathway
journal, January 2009

Effect of heme binding on the structure and stability of Escherichia coli apocytochrome b562
journal, October 1991

A New Method of Solvation Analysis: Applications to Quinones
journal, May 1990

Proof of Principle in a De novo Designed Protein Maquette: An Allosterically Regulated, Charge-Activated Conformational Switch in a Tetra-α-Helix Bundle ^†
journal, May 2001

Speeding molecular recognition by using the folding funnel: The fly-casting mechanism
journal, July 2000

The histidine of the c-type cytochrome CXXCH haem-binding motif is essential for haem attachment by the Escherichia coli cytochrome c maturation (Ccm) apparatus
journal, July 2005

Covalent cofactor attachment to proteins: cytochrome c biogenesis
journal, August 2005

The assembly and organisation of photosynthetic membranes in Rhodobacter sphaeroides
journal, January 2005

Role of Heme in the Unfolding and Assembly of Myoglobin
journal, June 2010

Design and engineering of an O₂ transport protein
journal, March 2009