Abstract

The functionality of active centers in proteins is governed by the secondary and higher structure of proteins which often lead to structures in the active center that are different from the structures found in protein-free models of the active center. To elucidate this structure–function relationship, it is therefore necessary to investigate both the protein structure and the local structure of the active center. In this work, we investigate the application of hetero (resonance) Raman two-dimensional correlation spectroscopy (2D-COS) to this problem. By employing a combination of near-infrared-Fourier transform-Raman- and vis-resonance Raman spectroscopy, we could show that this combination of techniques is able to directly probe the structure–function relationship of proteins. We were able to correlate the transition of the heme center in cytochrome c from low to high spin with changes in the secondary structure with the above mentioned two spectroscopic in situ techniques and without sample preparation. Thereby, we were able to reveal that the combination of a spectroscopic method to selectively observe the active center with a technique that monitors the whole system offers a promising toolkit to investigate the structure–function relationship of proteins with photoactive centers in general.

© 2021 The Author(s)

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2021 (1)

E.F. Pettersen, T.D. Goddard, C.C. Huang, et al. “UCSF ChimeraX: Structure Visualization for Researchers, Educators, and Developers”. Protein Sci. 2021, 30(1): 70–82.

2020 (2)

H. Wu, Y. Wei, R. Yang, et al. “Analysis of Chalk in Rice by Two-Dimensional Correlation Spectroscopy”. J. Mol. Struct. 2020, 1218: 128471.

J. Hniopek, M. Schmitt, J. Popp, et al. “PC 2D-COS: A Principal Component Base Approach to Two-Dimensional Correlation Spectroscopy”. Appl. Spectros. 2020, 74(4): 460–472.

2019 (1)

R. Geitner, R. Fritzsch, J. Popp, et al. “Corr2D: Implementation of Two-Dimensional Correlation Analysis in R”. J. Stat. Softw. 2019, 90(1): 1–33.

2018 (2)

L. Milazzo, L. Tognaccini, B.D. Howes, et al. “Probing the Non-Native States of Cytochrome C with Resonance Raman Spectroscopy: A Tool for Investigating the Structure–Function Relationship”. J. Raman Spectrosc. 2018, 49(6): 1041–1055.

Y. Wu, L. Zhang, Y.M. Jung, et al. “Two-Dimensional Correlation Spectroscopy in Protein Science, a Summary for Past 20 Years”. Spectrochim. Acta, Part A. 2018, 189: 291–299.

2016 (1)

R. Yang, R. Liu, G. Dong, et al. “Two-Dimensional Hetero-Spectral Mid-Infrared and Near-Infrared Correlation Spectroscopy for Discrimination Adulterated Milk”. Spectrochim. Acta, Part A. 2016, 157: 50–54.

2015 (1)

J.G. Kleingardner, K.L. Bren. “Biological Significance and Applications of Heme C Proteins and Peptides”. Acc. Chem. Res. 2015, 48(7): 1845–1852.

2013 (2)

A. Rygula, K. Majzner, K.M. Marzec, et al. “Raman Spectroscopy of Proteins: A Review”. J. Raman. Spectrosc. 2013, 44(8): 1061–1076.

R.L. Baldwin, G.D. Rose. “Molten Globules, Entropy-Driven Conformational Change and Protein Folding”. Curr. Opin. Struct. Biol. 2013, 23(1): 4–10.

2010 (1)

H. Fabian, Z. Yu, Y. Wange, et al. “Generalized 2D and Time-resolved FTIR Studies of Protein Unfolding Events”. J. Mol. Struct. 2010, 974(1): 203–209.

2008 (3)

M. Morháč, V. Matoušek. “Peak Clipping Algorithms for Background Estimation in Spectroscopic Data”. Appl. Spectrosc. 2008, 62(1): 91–106.

J.D. Marth. “A Unified Vision of the Building Blocks of Life”. Nat. Cell. Biol. 2008, 10(9): 1015–1015.

N. Mirkin, J. Jaconcic, V. Stojanoff, et al. “High Resolution X-Ray Crystallographic Structure of Bovine Heart Cytochrome C and its Application to the Design of an Electron Transfer Biosensor”. Proteins: Struct., Funct., Bioinf. 2008, 70(1): 83–92.

2006 (2)

P. Fromme, H. Yu, Y.S. DeRuyter, et al. “Structure of Photosystems I and II”. C. R. Chimie. 2006, 9(2): 188–200.

Y. Wang, W. Gao, I. Noda, et al. “A Modified Mean Normalization Method to Reduce the Effect of Peak Overlap in Two-dimensional Correlation Spectroscopy”. J. Mol. Struct. 2006, 799(1): 128–133.

2002 (1)

M. Paoli, J. Marles-Wright, A. Smith. “Structure–Function Relationships in Heme-Proteins”. DNA Cell Biol. 2002, 21(4): 271–280.

2000 (2)

Y.M. Jung, B. Czarnik-Matusewicz, Y. Ozaki. “Two-Dimensional Infrared, Two-Dimensional Raman, and Two-Dimensional Infrared and Raman Heterospectral Correlation Studies of Secondary Structure of β-Lactoglobulin in Buffer Solutions”. J. Phys. Chem. B. 2000, 104(32): 7812–7817.

I. Noda, A.E. Dowrey, C. Marcott, et al. “Generalized Two-Dimensional Correlation Spectroscopy”. Appl. Spectrosc. 2000, 54(7): 236A–248A.

1999 (1)

S.U. Sane, S.M. Cramer, T.M. Przybycien. “A Holistic Approach to Protein Secondary Structure Characterization Using Amide I Band Raman Spectroscopy”. Anal. Biochem. 1999, 269(2): 255–272.

1996 (1)

Z. Ahmad, S. Yadav, F. Ahmad, et al. “Effects of Salts of Alkali Earth Metals and Calcium Chloride on the Stability of Cytochrome C and Myoglobin”. Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1996, 1294(1): 63–71.

1995 (1)

T. Jordan, J.C. Eads, T.G. Spiro. “Secondary and Tertiary Structure of the A-State of Cytochrome C from Resonance Raman Spectroscopy”. Protein Sci. 1995, 4(4): 716–728.

1993 (1)

I. Noda. “Generalized Two-Dimensional Correlation Method Applicable to Infrared, Raman, and other Types of Spectroscopy”. Appl. Spectrosc. 1993, 47(9): 1329–1336.

1991 (1)

Y. Wang, R. Purrello, T. Jordan, et al. “UVRR Spectroscopy of the Peptide Bond. 1. Amide S, a Nonhelical Structure Marker, is a CαH Bending Mode”. J. Am. Chem. Soc. 1991, 113(17): 6359–6368.

1983 (1)

M. Ohgushi, A. Wada. “Molten-Globule State’: A Compact Form of Globular Proteins with Mobile Side-chains”. FEBS Lett. 1983, 164(1): 21–24.

1981 (1)

J.P. Harrington. “The Denatured States of Cytochrome C”. Biochim. Biophys. Acta, Protein Struct. 1981, 671(1): 85–92.

1979 (1)

T.G. Spiro, J.D. Stong, P. Stein. “Porphyrin Core Expansion and Doming in Heme Proteins. New Evidence from Resonance Raman Spectra of Six-Coordinate High-Spin Iron(III) Hemes”. J. Am. Chem. Soc. 1979, 101(10): 2648–2655.

1978 (2)

P.R. Carey. “Resonance Raman Spectroscopy in Biochemistry and Biology”. Q. Rev. Biophys. 1978, 11(3): 309–370.

J.F. Nagle, H.J. Morowitz. “Molecular Mechanisms for Proton Transport in Membranes”. Proc. Natl. Acad. Sci. USA. 1978, 75(1): 298–302.

1977 (1)

D.P. Strommen, K. Nakamoto. “Resonance Raman Spectroscopy”. J. Chem. Educ. 1977, 54: 474.

1974 (1)

T.G. Spiro, T.C. Strekas. “Resonance Raman Spectra of Heme Proteins. Effects of Oxidation and Spin State”. J. Am. Chem. Soc. 1974, 96(2): 338–345.

1970 (1)

E. Antonini, M. Brunori. “Hemoglobin”. Annu. Rev. Biochem. 1970, 39(1): 977–1042.

1965 (1)

D.W. Urry. “Protein-Heme Interactions in Heme-proteins: Cytochrome C”. Proc. Natl. Acad. Sci. USA. 1965, 54(2): 640–648.

Ahmad, F.

Z. Ahmad, S. Yadav, F. Ahmad, et al. “Effects of Salts of Alkali Earth Metals and Calcium Chloride on the Stability of Cytochrome C and Myoglobin”. Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1996, 1294(1): 63–71.

Ahmad, Z.

Z. Ahmad, S. Yadav, F. Ahmad, et al. “Effects of Salts of Alkali Earth Metals and Calcium Chloride on the Stability of Cytochrome C and Myoglobin”. Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1996, 1294(1): 63–71.

Antonini, E.

E. Antonini, M. Brunori. “Hemoglobin”. Annu. Rev. Biochem. 1970, 39(1): 977–1042.

Baldwin, R.L.

R.L. Baldwin, G.D. Rose. “Molten Globules, Entropy-Driven Conformational Change and Protein Folding”. Curr. Opin. Struct. Biol. 2013, 23(1): 4–10.

Bren, K.L.

J.G. Kleingardner, K.L. Bren. “Biological Significance and Applications of Heme C Proteins and Peptides”. Acc. Chem. Res. 2015, 48(7): 1845–1852.

Brunori, M.

E. Antonini, M. Brunori. “Hemoglobin”. Annu. Rev. Biochem. 1970, 39(1): 977–1042.

Carey, P.R.

P.R. Carey. “Resonance Raman Spectroscopy in Biochemistry and Biology”. Q. Rev. Biophys. 1978, 11(3): 309–370.

Cramer, S.M.

S.U. Sane, S.M. Cramer, T.M. Przybycien. “A Holistic Approach to Protein Secondary Structure Characterization Using Amide I Band Raman Spectroscopy”. Anal. Biochem. 1999, 269(2): 255–272.

Czarnik-Matusewicz, B.

Y.M. Jung, B. Czarnik-Matusewicz, Y. Ozaki. “Two-Dimensional Infrared, Two-Dimensional Raman, and Two-Dimensional Infrared and Raman Heterospectral Correlation Studies of Secondary Structure of β-Lactoglobulin in Buffer Solutions”. J. Phys. Chem. B. 2000, 104(32): 7812–7817.

DeRuyter, Y.S.

P. Fromme, H. Yu, Y.S. DeRuyter, et al. “Structure of Photosystems I and II”. C. R. Chimie. 2006, 9(2): 188–200.

Dong, G.

R. Yang, R. Liu, G. Dong, et al. “Two-Dimensional Hetero-Spectral Mid-Infrared and Near-Infrared Correlation Spectroscopy for Discrimination Adulterated Milk”. Spectrochim. Acta, Part A. 2016, 157: 50–54.

Dowrey, A.E.

I. Noda, A.E. Dowrey, C. Marcott, et al. “Generalized Two-Dimensional Correlation Spectroscopy”. Appl. Spectrosc. 2000, 54(7): 236A–248A.

Eads, J.C.

T. Jordan, J.C. Eads, T.G. Spiro. “Secondary and Tertiary Structure of the A-State of Cytochrome C from Resonance Raman Spectroscopy”. Protein Sci. 1995, 4(4): 716–728.

Fabian, H.

H. Fabian, Z. Yu, Y. Wange, et al. “Generalized 2D and Time-resolved FTIR Studies of Protein Unfolding Events”. J. Mol. Struct. 2010, 974(1): 203–209.

Fritzsch, R.

R. Geitner, R. Fritzsch, J. Popp, et al. “Corr2D: Implementation of Two-Dimensional Correlation Analysis in R”. J. Stat. Softw. 2019, 90(1): 1–33.

Fromme, P.

P. Fromme, H. Yu, Y.S. DeRuyter, et al. “Structure of Photosystems I and II”. C. R. Chimie. 2006, 9(2): 188–200.

Gao, W.

Y. Wang, W. Gao, I. Noda, et al. “A Modified Mean Normalization Method to Reduce the Effect of Peak Overlap in Two-dimensional Correlation Spectroscopy”. J. Mol. Struct. 2006, 799(1): 128–133.

Geitner, R.

R. Geitner, R. Fritzsch, J. Popp, et al. “Corr2D: Implementation of Two-Dimensional Correlation Analysis in R”. J. Stat. Softw. 2019, 90(1): 1–33.

Goddard, T.D.

E.F. Pettersen, T.D. Goddard, C.C. Huang, et al. “UCSF ChimeraX: Structure Visualization for Researchers, Educators, and Developers”. Protein Sci. 2021, 30(1): 70–82.

Harrington, J.P.

J.P. Harrington. “The Denatured States of Cytochrome C”. Biochim. Biophys. Acta, Protein Struct. 1981, 671(1): 85–92.

Hniopek, J.

J. Hniopek, M. Schmitt, J. Popp, et al. “PC 2D-COS: A Principal Component Base Approach to Two-Dimensional Correlation Spectroscopy”. Appl. Spectros. 2020, 74(4): 460–472.

Howes, B.D.

L. Milazzo, L. Tognaccini, B.D. Howes, et al. “Probing the Non-Native States of Cytochrome C with Resonance Raman Spectroscopy: A Tool for Investigating the Structure–Function Relationship”. J. Raman Spectrosc. 2018, 49(6): 1041–1055.

Huang, C.C.

E.F. Pettersen, T.D. Goddard, C.C. Huang, et al. “UCSF ChimeraX: Structure Visualization for Researchers, Educators, and Developers”. Protein Sci. 2021, 30(1): 70–82.

Jaconcic, J.

N. Mirkin, J. Jaconcic, V. Stojanoff, et al. “High Resolution X-Ray Crystallographic Structure of Bovine Heart Cytochrome C and its Application to the Design of an Electron Transfer Biosensor”. Proteins: Struct., Funct., Bioinf. 2008, 70(1): 83–92.

Jordan, T.

T. Jordan, J.C. Eads, T.G. Spiro. “Secondary and Tertiary Structure of the A-State of Cytochrome C from Resonance Raman Spectroscopy”. Protein Sci. 1995, 4(4): 716–728.

Y. Wang, R. Purrello, T. Jordan, et al. “UVRR Spectroscopy of the Peptide Bond. 1. Amide S, a Nonhelical Structure Marker, is a CαH Bending Mode”. J. Am. Chem. Soc. 1991, 113(17): 6359–6368.

Jung, Y.M.

Y. Wu, L. Zhang, Y.M. Jung, et al. “Two-Dimensional Correlation Spectroscopy in Protein Science, a Summary for Past 20 Years”. Spectrochim. Acta, Part A. 2018, 189: 291–299.

Y.M. Jung, B. Czarnik-Matusewicz, Y. Ozaki. “Two-Dimensional Infrared, Two-Dimensional Raman, and Two-Dimensional Infrared and Raman Heterospectral Correlation Studies of Secondary Structure of β-Lactoglobulin in Buffer Solutions”. J. Phys. Chem. B. 2000, 104(32): 7812–7817.

Kleingardner, J.G.

J.G. Kleingardner, K.L. Bren. “Biological Significance and Applications of Heme C Proteins and Peptides”. Acc. Chem. Res. 2015, 48(7): 1845–1852.

Liu, R.

R. Yang, R. Liu, G. Dong, et al. “Two-Dimensional Hetero-Spectral Mid-Infrared and Near-Infrared Correlation Spectroscopy for Discrimination Adulterated Milk”. Spectrochim. Acta, Part A. 2016, 157: 50–54.

Majzner, K.

A. Rygula, K. Majzner, K.M. Marzec, et al. “Raman Spectroscopy of Proteins: A Review”. J. Raman. Spectrosc. 2013, 44(8): 1061–1076.

Marcott, C.

I. Noda, A.E. Dowrey, C. Marcott, et al. “Generalized Two-Dimensional Correlation Spectroscopy”. Appl. Spectrosc. 2000, 54(7): 236A–248A.

Marles-Wright, J.

M. Paoli, J. Marles-Wright, A. Smith. “Structure–Function Relationships in Heme-Proteins”. DNA Cell Biol. 2002, 21(4): 271–280.

Marth, J.D.

J.D. Marth. “A Unified Vision of the Building Blocks of Life”. Nat. Cell. Biol. 2008, 10(9): 1015–1015.

Marzec, K.M.

A. Rygula, K. Majzner, K.M. Marzec, et al. “Raman Spectroscopy of Proteins: A Review”. J. Raman. Spectrosc. 2013, 44(8): 1061–1076.

Matoušek, V.

M. Morháč, V. Matoušek. “Peak Clipping Algorithms for Background Estimation in Spectroscopic Data”. Appl. Spectrosc. 2008, 62(1): 91–106.

Milazzo, L.

L. Milazzo, L. Tognaccini, B.D. Howes, et al. “Probing the Non-Native States of Cytochrome C with Resonance Raman Spectroscopy: A Tool for Investigating the Structure–Function Relationship”. J. Raman Spectrosc. 2018, 49(6): 1041–1055.

Mirkin, N.

N. Mirkin, J. Jaconcic, V. Stojanoff, et al. “High Resolution X-Ray Crystallographic Structure of Bovine Heart Cytochrome C and its Application to the Design of an Electron Transfer Biosensor”. Proteins: Struct., Funct., Bioinf. 2008, 70(1): 83–92.

Morhác, M.

M. Morháč, V. Matoušek. “Peak Clipping Algorithms for Background Estimation in Spectroscopic Data”. Appl. Spectrosc. 2008, 62(1): 91–106.

Morowitz, H.J.

J.F. Nagle, H.J. Morowitz. “Molecular Mechanisms for Proton Transport in Membranes”. Proc. Natl. Acad. Sci. USA. 1978, 75(1): 298–302.

Nagle, J.F.

J.F. Nagle, H.J. Morowitz. “Molecular Mechanisms for Proton Transport in Membranes”. Proc. Natl. Acad. Sci. USA. 1978, 75(1): 298–302.

Nakamoto, K.

D.P. Strommen, K. Nakamoto. “Resonance Raman Spectroscopy”. J. Chem. Educ. 1977, 54: 474.

Noda, I.

Y. Wang, W. Gao, I. Noda, et al. “A Modified Mean Normalization Method to Reduce the Effect of Peak Overlap in Two-dimensional Correlation Spectroscopy”. J. Mol. Struct. 2006, 799(1): 128–133.

I. Noda, A.E. Dowrey, C. Marcott, et al. “Generalized Two-Dimensional Correlation Spectroscopy”. Appl. Spectrosc. 2000, 54(7): 236A–248A.

I. Noda. “Generalized Two-Dimensional Correlation Method Applicable to Infrared, Raman, and other Types of Spectroscopy”. Appl. Spectrosc. 1993, 47(9): 1329–1336.

Ohgushi, M.

M. Ohgushi, A. Wada. “Molten-Globule State’: A Compact Form of Globular Proteins with Mobile Side-chains”. FEBS Lett. 1983, 164(1): 21–24.

Ozaki, Y.

Y.M. Jung, B. Czarnik-Matusewicz, Y. Ozaki. “Two-Dimensional Infrared, Two-Dimensional Raman, and Two-Dimensional Infrared and Raman Heterospectral Correlation Studies of Secondary Structure of β-Lactoglobulin in Buffer Solutions”. J. Phys. Chem. B. 2000, 104(32): 7812–7817.

Paoli, M.

M. Paoli, J. Marles-Wright, A. Smith. “Structure–Function Relationships in Heme-Proteins”. DNA Cell Biol. 2002, 21(4): 271–280.

Pettersen, E.F.

E.F. Pettersen, T.D. Goddard, C.C. Huang, et al. “UCSF ChimeraX: Structure Visualization for Researchers, Educators, and Developers”. Protein Sci. 2021, 30(1): 70–82.

Popp, J.

J. Hniopek, M. Schmitt, J. Popp, et al. “PC 2D-COS: A Principal Component Base Approach to Two-Dimensional Correlation Spectroscopy”. Appl. Spectros. 2020, 74(4): 460–472.

R. Geitner, R. Fritzsch, J. Popp, et al. “Corr2D: Implementation of Two-Dimensional Correlation Analysis in R”. J. Stat. Softw. 2019, 90(1): 1–33.

Przybycien, T.M.

S.U. Sane, S.M. Cramer, T.M. Przybycien. “A Holistic Approach to Protein Secondary Structure Characterization Using Amide I Band Raman Spectroscopy”. Anal. Biochem. 1999, 269(2): 255–272.

Purrello, R.

Y. Wang, R. Purrello, T. Jordan, et al. “UVRR Spectroscopy of the Peptide Bond. 1. Amide S, a Nonhelical Structure Marker, is a CαH Bending Mode”. J. Am. Chem. Soc. 1991, 113(17): 6359–6368.

Rose, G.D.

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Supplementary Material (2)

NameDescription
Supplement 1       sj-pdf-1-asp-10.1177_00037028211028916 - Supplemental material for Probing Protein Secondary Structure Influence on Active Centers with Hetero Two-Dimensional Correlation (Resonance) Raman Spectroscopy: A Demonstration on Cytochrome C
Supplement 2       sj-pdf-2-asp-10.1177_00037028211028916 - Supplemental material for Probing Protein Secondary Structure Influence on Active Centers with Hetero Two-Dimensional Correlation (Resonance) Raman Spectroscopy: A Demonstration on Cytochrome C

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