Asian Journal of Physics  Vol. 31 No 2, 2022, 375-390

Raman capability to study heme proteins
Giulietta Smulevich


Abstract

This short review aims to demonstrate how resonance Raman spectroscopy can be extremely useful in elucidating subtle structural features in heme proteins. In particular, selected examples have been chosen to elucidate how vibrational modes of the heme chromophore provide specific structural information not only on the ligation, oxidation, and spin states, but also on the stability and on the structure-function relationship of enzymes. © Anita Publications. All rights reserved.
Keywords: Resonance Raman, Heme proteins, Marker bands, Propionate, Fe-ligand.


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References

  1. In: Spiro, T G, (Ed.). Biological applications of Raman spectroscopy: Resonance Raman spectra of hemes and metalloproteins, (Wiley, New York). 1988, Vol. 3.
  2. Smulevich G, Mauro J M, Fishel L A, English A, Kraut J, Spiro T G, Heme Pocket Interactions in Cytochrome c Peroxidase Studied by Site-Directed Mutagenesis and Resonance Raman Spectroscopy, Biochemistry, 27(1988)5477-5485.
  3. Smith M. In Vitro Annu Rev Genet, 19(1985)423–462.
  4. Fishel L A, Villafranca J E, Mauro J M, Kraut J, Yeast CCP: Mutagenesis and Expression in Escherichia Coli Show Tryptophan-51 Is Not the Radical Site in Compound I, Biochemistry, 26(1987)351–360.
  5. Smulevich G, Structure-function relationships in peroxidases via resonance Raman spectroscopy and site-directed mutagenesis: cytochrome c peroxidase. In: Clark R J, Hester R E, (Eds), Biomolecular Spectroscopy, Part A, (John Wiley & Sons, New York), 1993, pp 163–193.
  6. Smulevich G, Understanding Heme Cavity Structure of Peroxidases: Comparison of Electronic Absorption and Resonance Raman Spectra with Crystallographic Results, Biospectroscopy, 4(1998)S3–S17.
  7. Smulevich G, Feis A, Howes B D, Fifteen Years of Raman Spectroscopy of Engineered Heme Containing Peroxidases: What Have We Learned?, Acc Chem Res, 38(2005)433–440.
  8. Smulevich G, Feis A, Howes B D, Ivancich A. Structure-Function Relationships Among Heme Peroxidases: New Insights from Electronic Absorption, Resonance Raman, and Multifrequency Electron Paramagnetic Resonance Spectroscopies. In Kadish K M, Smith, K M, Guilard R, (Eds), Handbook of porphyrin science with applications to chemistry, physics, materials science, engineering, biology and medicine, Vol 6, )World Scientific), 2010, pp 367–455.
  9. Smulevich G, Howes B D, Droghetti E, Structural and Functional Properties of Heme-containing Peroxidases: a Resonance Raman Perspective for the Superfamily of Plant, Fungal and Bacterial Peroxidases. In: Raven E, Dunford B, (Eds), Heme peroxidase, (Royal Society of Chemistry, UK), 2015, pp 61–98.
  10. Altose M D, Zheng Y, Dong J, Palfey B A, Carey P R, Comparing protein–ligand interactions in solution and single crystals by Raman spectroscopy, Proc Natl Acad Sci (USA), 98(2001)3006–3011.
  11. Carey P R, Dong J, Following Ligand Binding and Ligand Reactions in Proteins via Raman Crystallography Biochemistry, 43(2004)8885–8893.
  12. Carey P R, Raman crystallography and other biochemical applications of Raman spectroscopy. Annu Rev Phys Chem, 57(2006)527–554.
  13. Smulevich G, Wang Y, Edwards S L, Poulos T L, English A M, Spiro T G, Resonance Raman Spectroscopy of Cytochrome c Peroxidase Single Crystals on a Variable-Temperature Microscope Stage, Biochemistry, 29(1990)2586–2592.
  14. Smulevich G, Wang Y, Mauro J M, Wang J M, Fishel L A, Kraut J, Spiro T G. Single-Crystal Resonance Raman spectroscopy of Site-Directed Mutants of Cytochrome c Peroxidase, Biochemistry, 29(1990)7174–7180.
  15. Smulevich G, Spiro T G, Single-crystal micro-Raman spectroscopy, Methods Enzymol, 226(1993)397–408.
  16. Zhu L, Sage T, Champion P M. Quantitative Structural comparison of heme protein crystal and solutions using resonance Raman spectroscopy, Biochemistry, 32(1993)11181–11185.
  17. Smulevich G, Solution, and crystal phase resonance Raman spectroscopy: Valuable tools to unveil the structure and function of heme proteins, J Porphyrins Phthalocyanines, 22(2019)1–10.
  18. Spiro, T G, Strekas T C, Resonance Raman Spectra of Hemoglobin and Cytochrome c: Inverse Polarization and Vibronic Scattering, Proc Natl Acad Sci (USA), 69(1972)2622–2626.
  19. Spiro T G, Resonance Raman spectroscopic studies of heme proteins,Biochim Biophys Acta, 416(1975)169–189.
  20. Spiro T G, Stein P, Resonance effects in vibrational scattering from complex molecules, Annu Rev Phys Chem, 28(1977)501–521.
  21. Burke J M, Kincaid J R, Peters R R, Gagne R R, Collman JP, Spiro T G, Structure-sensitive resonance Raman bands of tetraphenyl and “picket fence” porphyrin-iron complexes, including an oxyhemoglobin analog,J Am Chem Soc, 100(1978)6083–6088.
  22. Burke J M, Kincaid J R, Spiro T G, Resonance Raman spectra and vibrational modes of iron(III) tetraphenylporphine µ-oxo dimer. Evidence for phenyl interaction and lack of dimer splitting, J Am Chem Soc, 100(1978)6077–6083.
  23. Spiro T G, The Resonance Raman Spectroscopy of Metalloporphyrins and Heme Proteins. In: Lever A B P, Gray H B, (Eds), Iron Porphyrins, (Addison-Wesley, Reading, Mass.) 1982, part 2, pp 89–159.
  24. Spiro T G, Czernuszewicz R S, Li X-Y, Metalloporphyrin structure and dynamics from resonance Raman spectroscopy, Coord Chem Rev, 100(1990)514–571.
  25. Li X Y, Czernuszewlcz R S, Kincaid J R, Spiro, T G, Conststent porphyrm force field. 3. Out-of-plane modes in the resonance Raman spectra of planar and ruffled nickel octaethylporphyrin, J Am Chem Soc, 111(1989)7012–7023.
  26. Li X Y, Czernuszewicz R S, Kincaid J R, Stem P, Spiro T G, Consistent porphyrin force field. 2. Nickel octaethylporphyrm skeletal and substituent mode assignments from 15N, Meso-d4, and methylene-d16 Raman and Infrared isotope shifts, J Phys Chem, 94(1990)47–61.
  27. Czernuszewicz R S, Li X Y, Spiro T G, Nickel octaethylporphyrin ruffling dynamics from resonance Raman spectroscopy, J Am Chem Soc, 111(1989)7024–7031.
  28. Czernuszewicz R S, Macor K A, Li X Y, Kincaid J R, Spiro T G Resonance Raman spectroscopy reveals alu, vs a2u character and pseudo Jahn-Teller distortion in radical cations of NIII, CuII, and ClFeIII octaethyl-and tetraphenylporphyrns Am Chem. Soc, 111(1989)3860–3869.
  29. Abe M, Kitagawa T, Kyogoku Y, Resonance Raman spectra of octaethylporphyrinato-Ni(II) and meso-deuterated and 15N substituted derivatives. II. A normal coordinate analysis, J Chem Phys, 69(1978)4526–4534.
  30. Jentzen W, Simpson M C, Hobbs J D, Song X, Ema T, Nelson N Y, Medforth C J, Smith K M, Veyrat M, Maxxanti M, Ramasseul R, Marchon J C, Takeuchi T, Goddard W A, Shelnutt J A, Ruffling in a Series of Nickel(II) meso-Tetrasubstituted Porphyrins as a Model for the Conserved Ruffling of the Heme of Cytochromes c, J Am Chem Soc, 117(1995)11085–11097.
  31. Jentzen W, Song X Z, Shelnutt J A, Structural Characterization of Synthetic and Protein-Bound Porphyrins in Terms of the Lowest-Frequency Normal Coordinates of the Macrocycle, J Phys Chem B, 101(1997)1684–1699.
  32. Wang J, Mauro J M, Edwards S L, Oatly S J, Fishel L A, Ashford V A, Xuong N, Kraut J, X-ray structures of recombinant yeast cytochrome c peroxidase and three heme-cleft mutants prepared by site-directed mutagenesis. Biochemistry, 29(1990)7160–7173.
  33. Spiro T G, Smulevich G, Su C, Probing Protein Structure and Dynamics with Resonance Raman Spectroscopy: Cytochrome c Peroxidase and HemoglobinBiochemistry, 29(1990)4497–4508.
  34. Maltempo M M, Moss T H, Cusanovich M A, Magnetic studies on the changes in the iron environment in Chromatium ferricytochrome c, Biochim Biophys Acta, 342(1974)290–305.
  35. Fujii S, Yoshimura T, Kamada H, Yamaguchi K, Suzuki S, Shidara S, Takakuwa S, Electron paramagnetic resonance studies of ferric cytochrome c’ from photosynthetic bacteria, Biochim Biophys Acta, 1251(1995)161–169.
  36. Indiani C, Feis A, Howes B D, Marzocchi M P, Smulevich G, Benzohydroxamic Acid-Peroxidase Complexes: Spectroscopic Characterization of a Novel Heme Spin Species, J Am Chem Soc, 122(2000)7368–7376.
  37. Droghetti E, Nicoletti FP, Bonamore A, Sciamanna N, Boffi A, Feis A, Smulevich G, The optical spectra of fluoride complexes can effectively probe H-bonding interactions in the distal cavity of heme proteins, J Inorg Biochem, 105(2011)1338–1343.
  38. Kerr E A, Yu N T. Vibrational modes of coordinated CO, CN and NO. In Spiro T G (Ed), Biological Applications of Raman Spectroscopy, Vol 3, (John Wiley and Sons, Inc. New York), 1988, pp 39–95.
  39. Kitagawa T, The heme protein structure and the iron histidine stretching mode. In Spiro T G (Ed), Biological Applications of Raman Spectroscopy: Resonance Raman Spectra of Hemes and Metalloproteins, (John Wiley and Sons, Inc. New York), 1988, pp 97–131.
  40. Stein P, Mitchell M, Spiro T G, Hydrogen-bond and deprotonation effects on the resonance Raman iron-imidazole mode in deoxyhemoglobin models: implications for hemoglobin cooperativity, J Am Chem Soc, 102(1980)7795–7797.
  41. Teraoka J, Kitagawa T. Resonance Raman study of the heme-linked ionization in reduced horseradish peroxidase. Biochem Biophys Res Comm, 93(1980)694–700.
  42. Egawa T, Yeh S R, Structural and functional properties of hemoglobins from unicellular organisms as revealed by resonance Raman spectroscopy, J Inorg Biochem, 99(2005)72–96.
  43. Lu C, Egawa T, Mukai M, Poole R K, Yeh S R. Hemoglobins from Mycobacterium tuberculosis and Campylobacter jejuni: A Comparative Study with Resonance Raman Spectroscopy. In Poole R K (Ed), Methods in Enzymology, (Academic Press, New York), Vol 437, 2008, pp 256–286.
  44. Howes B D, Boechi L, Boffi A, Estrin D A, Smulevich G, Bridging Theory and Experiment to Address Structural Properties of Truncated Haemoglobins: Insights from Thermobifida fusca HbO, Adv Microb Physiol, 67(2015)85–126.
  45. Liu Y, Kincaid J R, Resonance Raman studies of gas sensing heme proteins, J Raman Spectrosc. 52(2021)2516-2535.
  46. Spiro T G, Wasbotten I H, CO as a vibrational probe of heme protein active sites, J Inorg Biochem, 99(2005)34–44.
  47. Phillips G N (Jr), Teodoro M L, Li T, Smith B, Olson J S, Bound CO is a molecular probe of electrostatic potential in the distal pocket of myoglobin, J Phys Chem B, 103(1999)8817–8829.
  48. Droghetti E, Nicoletti F P, Bonamore A, Boechi L, Arroyo-Mañez P, Estrin D A, Boffi A, Smulevich G, Feis A , Hemepocket structural properties of a bacterial truncated hemoglobin from Thermobifida fusca, Biochemistry, 49(2010)10394−10402.
  49. Feis A, Howes BD, Milazzo L, Smulevich G, Structural determinants of ligand binding in truncated hemoglobins: Resonance Raman spectroscopy of the native states and their carbon monoxide and hydroxide complexes. Biopolymers, 109(2018)e23114; doi.org/10.1002/bip.23114.
  50. Hou S B, Larsen R W, Boudko D, Riley C W, Karatan E, Zimmer M, Ordal G W, Alam M, Myoglobin-like aerotaxis transducers in Archaea and Bacteria, Nature, 403(2000)540–544.
  51. Hou S B, Freitas T, Larsen R W, Piatibratov M, Sivozhelezov V, Yamamoto A, Meleshkevitch E A, Zimmer M, Ordal G W, Alam M, Globin-coupled sensors: A class of heme-containing sensors in Archaea and Bacteria, Proc Natl Acad Sci (U S A), 98(2001)9353–9358.
  52. Zhang W, Phillips G N, Structure of the oxygen sensor in Bacillus subtilis: signal transduction of chemotaxis by control of symmetry, Structure, 11(2003)1097–1110.
  53. Ohta T, Yoshimura H, Yoshioka S, Aono S, Kitagawa T, Oxygen-sensing mechanism of HemAT from Bacillus subtilis: a resonance Raman Spectroscopy study, J Am Chem Soc, 126(2004)15000–15001.
  54. Chen Z, Ost T W B, Schelvis P M, Phe393 mutants of cytochrome P450 BM3 with modified heme redox potentials have altered heme vinyl and propionate conformations, Biochemistry 43(2004)1798–1808.
  55. Guallar V, Olsen B, The role of the heme propionates in heme biochemistry, J Inorg Chem, 100(2006)755–760.
  56. Harada K, Makino M, Sugimoto H, Hirota S, Matsuo T, Shiro Y, Hisaeda Y, Hayashi T, Structure and Ligand Binding Properties of Myoglobins Reconstituted with Monodepropionated Heme: Functional Role of Each Heme Propionate Side Chain, Biochemistry 46(2007)9406–9416.
  57. Hu S, Smith K M, Spiro T G, Assignment of protoheme resonance Raman spectrum by heme labeling in myoglobin. J Am Chem Soc, 118(1996)12638–12646.
  58. Gottfried D S, Peterson E S, Sheikh A G, Wang J, Friedman J M, Evidence for Damped Hemoglobin Dynamics in a Room Temperature Trehalose Glass, J Phys Chem, 100(1996)12034–12042.
  59. Evans S V, Brayer G D, High-resolution study of the three-dimensional structure of horse heart metmyoglobin, J Mol Biol, 213(1990)885–897.
  60. Peterson E, Friedman J M, Chien  E Y, Sligar S G, Functional implications of the proximal hydrogen-bonding network in myoglobin: a resonance Raman and kinetic study of Leu89, Ser92, His97, and F-helix swap mutants, Biochemistry, 37(1998)2301–2319.
  61. Gao T, El-Mashtoly S F, Pal B, Hayashi T, Harada K, Kitagawa T, Pathway of information transmission from heme to protein upon ligand binding/dissociation in myoglobin revealed by UV resonance Raman spectroscopy, J Biol Chem, 81(2006)24637–24646.
  62. Cerda J F, Silfa E, Lopez-Garrig J, Unusual Rocking Freedom of the Heme in the Hydrogen Sulfide-Binding Hemoglobin from Lucina pectinata, J Am Chem Soc, 120(1998)9312–9317.
  63. Rizzi M, Wittenberg J B, Coda A, Fasno M, Ascenzi P, Bolognesi M, Structure of the sulfide-reactive
    hemoglobin from the clam Lucina pectinata: a Crystallographic analysis at 1.5 Å resolution, J Mol Biol, 244(1994)86–89.
  64. De Simone G, di Masi A, Vita G M, Polticelli F, Pesce A, Nardini M, Bolognesi M, Ciaccio C, ColettaM, Samuela Turilli E, Fasano M, Tognaccini L, Smulevich G, Abbruzzetti S, Viappiani C, Bruno S, Ascenzi P, Mycobacterial and human nitrobindins: Structure and function, Antioxid Redox Signal, 33(2020)229–246.
  65. Bianchetti C M, Bingman C A, Phillips G N (Jr), Structure of the C-terminal heme-binding domain of THAP domain containing protein 4 from Homo sapiens, Proteins, 79(2011)1337–1341.
  66. Dailey T A,Boynton T O,Albetel A N,Gerdes S,Johnson M K,Dailey H A,Discovery and Characterization of HemQ: an essential heme biosynthetic pathway component, J Biol Chem, 285(2010)25978– 25986.
  67. Dailey H A,Gerdes S,Dailey T A,Burch J S,Phillips J D,Noncanonical coproporphyrin-dependent bacterial heme biosynthesis pathway that does not use protoporphyrin, Proc Natl Acad. Sci (U S A), 112(2015)2210–
  68. Celis A I,Streit B R, Moraski G C, Kant R, Lash T D, Lukat-Rodgers G S, Rodgers K R, DuBois J L,Unusual Peroxide-Dependent, Heme-Transforming Reaction Catalyzed by HemQ,Biochemistry, 54(2015)4022– 4032.
  69. Celis, A I, Gauss G H, Streit B R, Shisler K, Moraski G C, Rodgers K R, Lukat-Rodgers G S, Peters J W, DuBois J L,Structure-based mechanism for oxidative decarboxylation reactions mediated by amino acids and heme propionates in coproheme decarboxylase (HemQ). J Am Chem Soc, 139(2017)1900–1911.
  70. Streit B R, Celis A I, Shisler K, Rodgers K R, Lukat-Rodgers G S, DuBois J L,Reactions of Ferrous Coproheme Decarboxylase (HemQ) with O2 and H2O2 Yield Ferric Heme b. Biochemistry, 56(2017)189–201.
  71. Hofbauer S, Mlynek G, Milazzo L, Puhringer D, Maresch D, Schaffner I, Furtmüller P G, Smulevich G, Djinovic-Carugo K, Obinger C,Hydrogen peroxide-mediated conversion of coproheme to heme b by HemQ-lessons from the first crystal structure and kinetic studies,FEBS J, 283(2016)4386– 4401.
  72. Milazzo L, Hofbauer S, Howes B D, Gabler T, Furtmüller P G, Obinger C, Smulevich G, Insights into the Active Site of Coproheme Decarboxylase from Listeria monocytogenes, Biochemistry, 57(2018)2044–2057.
  73. Milazzo L, Gabler T, Pfanzagl V, Michlits H, Furtmüller P G, Obinger C, Hofbauer S, Smulevich G, The hydrogen bonding network of coproheme in coproheme decarboxylase from Listeria monocytogenes: effect on structure and catalysis, J Inorg Chem, 195(2019)61–70.
  74. Milazzo L, Gabler T, Pühringer D, Jandova Z, Maresch D, Michlits H, Pfanzagl V, Djinović-Carugo K, Oostenbrink C, Furtmüller P G, Obinger C, Smulevich G, Hofbauer S, Redox Cofactor Rotates during Its Stepwise Decarboxylation: Molecular Mechanism of Conversion of Coproheme to Heme b, ACS Catal, 9(2019)6766–6782.
  75. Sebastiani F, Michlits H, Lier B, Becucci M, Furtmüller P G, Oostenbrink C, Obinger C, Hofbauer S, Smulevich G,Reaction intermediate rotation during the decarboxylation of coproheme to heme b in diphtheriae, Biophy J, 120(2021)3600-3614.

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