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Analysis of Heme and Hemoproteins

  • Angela Wilks
Protocol
Part of the Springer Protocols Handbooks book series (SPH)

Abstract

Heme is perhaps the most ubiquitous cofactor found in nature and the most functionally diverse. Hemoproteins are involved in cell respiration (cytochromes), oxygen-binding and transport (hemoglobin and myoglobin), oxidative bio transformations (cytochrome P-450 and peroxidases), and most recently, as sensors in 2-component regulatory systems (guanylate cyclase, FixL, and CooA). The ability of hemoproteins to carry out extremely diverse reactions arises largely from the protein environment in which the heme molecule resides and specifically the nature of the heme-ligands. Other factors that contribute to the reactivity of the heme are intrinsic to the heme itself, including the substituents on the heme periphery and, in some cases, the covalent attachment of the heme to the protein. The structures of the most common heme-ligands and examples of the hemoproteins in which they occur are found in Table 1.
Table 1.

Heme Ligand Structure and Function

Heme coordination

Protein class

Protein function

Cytochrome b5

Electron transfer

 

Cytochrome c (Class II and IV)

 
 

Cytochrome c oxidase

 
 

(contains heme a)

 

Hexacoordinate

  

Soluble cytochrome b562

Electron transfer

 

Cytochrome c (Class I, IIb and IV)

 

Hexacoordinate

  

Hemoglobin, myoglobin

O2-binding

 

Fix IVCooA

O2/CO-binding

 

Soluble guany late cyclase

NO-binding

 

Peroxidases

Oxidoreductase

 

Heme oxygenase

Oxidoreductase

Hexa/Pentacoordinate

  

Catalase

Oxidoreductase

Hexa/Pentacoordinate

  

Cytochrome P450

Oxidoreductases

 

Nitric oxide synthases

 
 

Chloroperoxidase

 

Hexa/Pentacoordinate

  

Keywords

Heme Oxygenase Ethylene Diamine Tetraacetic Acid Ethylene Diamine Tetraacetic Acid Magnetic Circular Dichroism Urea Buffer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Agalidis, I., E. Jauneau, and F. Reiss-Husson. 1974. Influence of iron deficiency on the cytochromes of Rhodopseudomonas spheroides. Eur. J. Biochem. 47:573–580.PubMedCrossRefGoogle Scholar
  2. 2.
    Aono, S., H. Nakajima, K. Saito, and M. Okada. 1996. A novel heme protein that acts as a carbon monoxide-dependent transcriptional activator in Rhodospirillum rubrum. Biochem. Biophys. Res. Commun. 228:752–756.PubMedCrossRefGoogle Scholar
  3. 3.
    Barnes, H.J., M.P. Arlotto, and M.R. Waterman. 1991. Expression and enzymatic activity of recombinant cytochrome P450 17 alpha-hydroxylase in Escherichia coli. Proc. Natl. Acad. Sci. USA 88:5597–5601.PubMedCrossRefGoogle Scholar
  4. 4.
    Bartsch, R.G. 1971. Cytochromes: bacterial. Methods Enzymol. 23:344–363.Google Scholar
  5. 5.
    Beck von Bodman, S., M.A. Schuler, D.R. Jollie, and S.G. Sligar. 1986. Synthesis, bacterial expression, and mutagenesis of the gene coding for mammalian cytochrome b5. Proc. Natl. Acad. Sci. USA 83:9443–9447}.PubMedCrossRefGoogle Scholar
  6. 6.
    Black, S.M. and P.R. Ortiz de Montellano. 1995. Characterization of rat neuronal nitric oxide synthase expressed in Saccharomyces cerevisiae. DNA Cell Biol. 14:789–794.PubMedCrossRefGoogle Scholar
  7. 7.
    Boyle, R.C., A.L. Tappel, A.A. Tappel, H. Chen, and H.J. Andersen. 1994. Quantitation of heme proteins from mixtures. J. Agric. Food Chem. 42:100–104.CrossRefGoogle Scholar
  8. 8.
    Braun, V., K. Hantke, and W. Koster. 1998. Bacterial iron transport: mechanisms, genetics, and regulation. Met. Ions Biol. Syst. 35:67–145.PubMedGoogle Scholar
  9. 9.
    Champiat, D., A. Roux, O. Lhomme, and G. Nosenzo. 1994. Biochemiluminescence and biomedical applications. Cell Biol. Toxicol. 10:345–351.PubMedCrossRefGoogle Scholar
  10. 10.
    Chance, B. 1954. Spectrophotometry of intracellular respiratory pigments. Science 120:767.PubMedCrossRefGoogle Scholar
  11. 11.
    Charles, I.G., A. Chubb, R. Gill, J. Clare, P.N. Lowe, L.S. Holmes, M. Page, J.G. Keeling, S. Moncada, and V. Rrveros-Moreno. 1993. Cloning and expression of a rat neuronal nitric oxide synthase coding sequence in a baculovirus/insect cell system. Biochem. Biophys. Res. Commun. 196:1481–1489.PubMedCrossRefGoogle Scholar
  12. 12.
    Charles, I.G., C.A. Scorer, M.A. Moro, C. Fernandez, A. Chubb, J. Dawson, N. Foxwell, R.G. Knowles, and S.A. Baylis. 1996. Expression of human nitric oxide synthase isozymes. Methods Enzymol. 268:449–460.PubMedCrossRefGoogle Scholar
  13. 13.
    Chen, H., A.L. Tappel, and R.C. Boyle. 1993. Oxidation of heme proteins as a measure of oxidative damage to liver tissue slices. Free Radic. Biol. Med. 14:509–517.PubMedCrossRefGoogle Scholar
  14. l4.
    Cornejo, J., R.D. Willows, and S.I. Beale. 1998. Phytobilin biosynthesis: cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J. 15:99–107.Google Scholar
  15. 15.
    Dawson, J.H. and D.M. Dooley. 1989. Iron Porphyrins. Part 3, p. 1–135. In A.P.B. Lever and H.B. Gray (Eds.). VCH publishers, New York.Google Scholar
  16. 16.
    Dawson, J.H., S. Kadkhodayan, C. Zhuang, and M. Sono. 1992. On the use of iron octa-alkylporphyrins as models for protoporphyrin IX-containing heme systems in studies employing magnetic circular dichroism spectroscopy. J. Inorg. Biochem. 45:179–192.PubMedCrossRefGoogle Scholar
  17. 17.
    DePillis, G.D., S. Ozaki, J.M. Kuo, D.A. Maltby, and P.R. Ortiz de Montellano. 1997. Autocatalytic processing of heme by lactoperoxidase produces the native protein-bound prosthetic group. J. Biol. Chem. 272:8857–8860.PubMedCrossRefGoogle Scholar
  18. 18.
    Dierks, E.A., Z. Zhang, E.F. Johnson, and P.R. de Montellano. 1998. The catalytic site of cytochrome P4504A11 (CYP4A11) and its L131F mutant. J. Biol. Chem. 273:23055–23061.PubMedCrossRefGoogle Scholar
  19. 19.
    Dorward, D.W. 1993. Detection and quantitation of heme-containing proteins by chemiluminescence. Anal. Biochem. 209:219–223.PubMedCrossRefGoogle Scholar
  20. 20.
    Durante, W., M.H. Kroll, N. Christodoulides, K.J. Peyton, and A.I. Schafer. 1997. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ. Res. 80:557–564.PubMedGoogle Scholar
  21. 21.
    Dutta, C. and H.L. Henry. 1990. Detection of hemo-protein peroxidase activity on polyvinylidene difluoride membrane. Anal. Biochem. 184:96–99.PubMedCrossRefGoogle Scholar
  22. 22.
    Elkins, C, C.J. Chen, and C.E. Thomas. 1995. Characterization of the hgbA locus encoding a hemoglobin receptor from Haemophilus ducreyi. Infect. Immun. 63:2194–2200.PubMedGoogle Scholar
  23. 23.
    Estabrook, R.W., J. Peterson, J. Barn, and A. Hildebrant. 1972. The spectrophotometric measurement of turbid suspensions of cytochromes associated with drug metabolism, p. 303–350. In C.F. Chignell (Ed.), Methods in Pharmacology. Vol. 2. Appleton-Century-Crofts, New York.Google Scholar
  24. 24.
    Falk, J.E. 1963. Part A. Pyrrole pigments: chemistry and biochemistry of porphyrins and metalloporphyrins, p. 3–33. In M. Florkin and E.H. Stotz (Eds.), Comprehensive Biochemistry, Vol. 9. Elsevier, Amsterdam.Google Scholar
  25. 25.
    Falk, J.E. 1964. Porphyrins and Metalloporphyrins. Elsevier, New York.Google Scholar
  26. 26.
    Fishel, L.A., J.E. Villafranca, J.M. Mauro, and J. Kraut. 1987. Yeast cytochrome c peroxidase: mutagenesis and expression in Escherichia coli show tryptophan-51 is not the radical site in compound I. Biochemistry 26:351–360.PubMedCrossRefGoogle Scholar
  27. 27.
    Fronticelli, C., J.K. O’Donnell, and W.S. Brinigar. 1991. Recombinant human hemoglobin: expression and refolding of beta-globin from Escherichia coli. J. Prot. Chem. 10:495–501.CrossRefGoogle Scholar
  28. 28.
    Gegner, J.A. and F.W. Dahlquist. 1991. Signal transduction in bacteria: CheW forms a reversible complex with the protein kinase CheA. Proc. Natl. Acad Sci. USA 88:750–754.PubMedCrossRefGoogle Scholar
  29. 29.
    George, H.J., D.E. Van Dyk, R.A. Straney, J.M. Trzaskos, and R.A. Copeland. 1996. Expression purification and characterization of recombinant human inducible prostaglandin G/H synthase from baclovirus-infected insect cells. Protein Expr. Purif. 7:19–26.PubMedCrossRefGoogle Scholar
  30. 30.
    Gerber, N.C., C.R. Nishida, and P.R. Ortiz de Montellano. 1997. Characterization of human liver inducible nitric oxide synthase expressed in Escherichia coli. Arch. Biochem. Biophys. 343:249–253.PubMedCrossRefGoogle Scholar
  31. 31.
    Gerber, N.C. and P.R. Ortiz de Montellano. 1995. Neuronal nitric oxide synthase. Expression in Escherichia coli, irreversible inhibition by phenyldiazene, and active site topology. J. Biol. Chem. 270:17791–17796.PubMedCrossRefGoogle Scholar
  32. 32.
    Gilles-Gonzalez, M.A., G. Gonzalez, M.F. Perutz, L. Kiger, M.C. Marden, and C. Poyart. 1994. Heme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation. Biochemistry 33:8067–8073.PubMedCrossRefGoogle Scholar
  33. 33.
    Gonzalez, F.J. and K.R. Korzekwa. 1995. Cytochromes P450 expression systems. Annu. Rev. Pharmacol. Toxicol. 35:369–390.PubMedCrossRefGoogle Scholar
  34. 34.
    Guengerich, F.P. 1983. Oxidation-reduction properties of rat liver cytochromes P-450 and NADPH-cytochrome p-450 reductase related to catalysis in reconstituted systems. Biochemistry 22:2811–2820.PubMedCrossRefGoogle Scholar
  35. 35.
    Guengerich, F.P., N.A. Hosea, A. Parikh, L.C. Bell-Parikh, W.W. Johnson, E.M. Gillam, and T. Shimada. 1998. Twenty years of biochemistry of human P45Os: purification, expression, mechanism, and relevance to drugs. Drug Metab. Dispos. 26:1175–1178.PubMedGoogle Scholar
  36. 36.
    Guengerich, F.P., M.V. Martin, Z. Guo, and Y.J. Chun. 1996. Purification of functional recombinant P450s from bacteria. Methods Enzymol. 272:35–44.PubMedCrossRefGoogle Scholar
  37. 37.
    Halaka, F.G., G.T. Babcock, and J.L. Dye. 1985. The use of principal component analysis to resolve the spectra and kinetics of cytochrome c oxidase reduction by 5, 10-dihydro-5-methyl phenazine. Biophys. J. 48:209–219.PubMedCrossRefGoogle Scholar
  38. 38.
    Halpert, J.R., T.L. Domanski, O. Adali, C.P. Biagini, J. Cosme, E. A. Dierks, E.F. Johnson, J.P. Jones et al. 1998. Structure-function of cytochromes P450 and flavin-containing monooxygenases: implications for drug metabolism. Drug Metab. Dispos. 26:1223–1231.PubMedGoogle Scholar
  39. 39.
    Hartmann, C. and P.R. Ortiz de Montellano. 1992. Baculovirus expression and characterization of catalytically active horseradish peroxidase. Arch. Biochem. Biophys. 297:61–72.PubMedCrossRefGoogle Scholar
  40. 40.
    Hawkins, B.K., A. Wilks, L.S. Powers, P.R. Ortiz de Montellano, and J.H. Dawson. 1996. Ligation of the iron in the heme-heme oxygenase complex: X-ray absorption, electronic absorption and magnetic circular dichroism studies. Biochim. Biophys. Acta 1295:165–173.PubMedCrossRefGoogle Scholar
  41. 41.
    Hernan, RA,, H.L. Hui, M.E. Andracki, R.W. Noble, S.G. Sligar, J.A. Walder, and R.Y. Walder. 1992. Human hemoglobin expression in Escherichia coli: importance of optimal codon usage. Biochemistry 31:8619–8628.PubMedCrossRefGoogle Scholar
  42. 42.
    Hernan, RA and S.G. Sligar. 1995. Tetrameric hemoglobin expressed in Escherichia coli. Evidence of heterogeneous subunit assembly. J. Biol. Chem. 270:26257–26264.PubMedCrossRefGoogle Scholar
  43. 43.
    Hernandez, G., A. Wilks, R. Paolesse, K.M. Smith, P.R. Ortiz de Montellano, and G.N. La Mar. 1994. Proton NMR investigation of substrate-bound heme oxygenase: evidence for electronic and steric contributions to stereoselective heme cleavage. Biochemistry 33:6631–6641.PubMedCrossRefGoogle Scholar
  44. 44.
    Hoffman, S.J., D.L. Looker, J.M. Roehrich, P.E. Cozart, S.L. Durfee, J.L. Tedesco, and G.L. Stetler. 1990. Expression of fully functional tetrameric human hemoglobin in Escherichia coli. Proc. Natl. Acad. Sci. USA 87:8521–8525.PubMedCrossRefGoogle Scholar
  45. 45.
    Hofrichter, J., J.H. Sommer, E.R. Herry, and W.A. Eaton. 1983. Nanosecond absorption spectroscopy of hemoglobin. Proc. Natl. Acad. Sci. USA 80:2235–2239.PubMedCrossRefGoogle Scholar
  46. 46.
    Holmans, P.L., M.S. Shet, C.A. Martin-Wixtrom, C.W. Fisher, and R.W. Estabrook. 1994. The high-level expression in Escherichia coli of the membrane-bound form of human and rat cytochrome b5 and studies on their mechanism of function. Arch. Biochem. Biophys. 312:554–565.PubMedCrossRefGoogle Scholar
  47. 47.
    Hui, H.L., J.S. Kavanaugh, M.L. Doyle, A. Wierzba, P.H. Rogers, A. Arnone, J.M. Holt, G.K. Ackers, and R.W. Noble. 1999. Structural and functional properties of human hemoglobins reassembled after synthesis in Escherichia coli. Biochemistry 38:1040–1049.PubMedCrossRefGoogle Scholar
  48. 48.
    Ishikawa, K., M. Sato, and T. Yoshida. 1991. Expression of rat heme oxygenase in Escherichia coli as a catalytically active, full-length form that binds to bacterial membranes. Eur. J. Biochem. 202:161–165.PubMedCrossRefGoogle Scholar
  49. 49.
    Jennings, P.A., M.J. Stone, and P.E. Wright. 1995. Overexpression of myoglobin and assignment of its amide, C alpha and C beta resonances. J. Biomol. NMR. 6:271–276.PubMedCrossRefGoogle Scholar
  50. 50.
    Jones, S., M. Tasab, J.E. Ogden, D.J. Ballance, and M.J. Powell. 1996. Expression of rat neuronal nitric oxide synthase in Saccharomyces cerevisiae. J. Biotechnol. 48:37–41.PubMedCrossRefGoogle Scholar
  51. 51.
    Jung, C., O. Ristau, and H. Rein. 1991. The high-spin/low-spin equilibrium in cytochrome P-450-a new method for determination of the high-spin content. Biochim. Biophys. Acta 1076:130–136.PubMedCrossRefGoogle Scholar
  52. 52.
    Kakuno, T., R.G. Bartsch, K. Nishikawa, and T. Horio. 1981. Redox componenets associated with chromatophores from Rhodospirillum rubrum. J. Biochem. 70:79–94.Google Scholar
  53. 53.
    Kincaid, J., P. Stein, and T.G. Spiro. 1979. Absence of heme-localized strain in T state hemoglobin: insensitivity of heme-imidazole resonance Raman frequencies to quaternary structure. Proc. Natl. Acad. Sci. USA 76:549–552.PubMedCrossRefGoogle Scholar
  54. 54.
    King, M.T. and G. Drews. 1975. The respiratory electron transport system of heterotrophically-grown Rhodopseudomonas palustris. Arch. Microbiol. 102:219–231.PubMedCrossRefGoogle Scholar
  55. 55.
    Kitagawa, T., K. Nagai, and M. Tsubaki. 1979. Assignment of the Fe-Nepsilon (His F8) stretching band in the resonance Raman spectra of deoxy myoglobin. FEBS Lett. 104:376–378.PubMedCrossRefGoogle Scholar
  56. 56.
    Knaff, D.B. and B.B. Buchanan. 1975. Cytochrome b and photosynthetic sulfur bacteria. Biochim. Biophys. Acta. 376:549–560.PubMedCrossRefGoogle Scholar
  57. 57.
    Koenigs, L.L. and W.F. Trager. 1998. Mechanism-based inactivation of cytochrome P450 2B1 by 8-methoxypsoralen and several other furanocoumarins. Biochemistry 37:13184–13193.PubMedCrossRefGoogle Scholar
  58. 58.
    Koenigs, L.L. and W.F. Trager. 1998. Mechanism-based inactivation of P450 2A6 by furanocoumarins. Biochemistry 37:10047–10061.PubMedCrossRefGoogle Scholar
  59. 59.
    Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.PubMedCrossRefGoogle Scholar
  60. 60.
    Lee, B.C. 1992. Isolation of an outer membrane he-min-binding protein of Haemophilus influenzae type b. Infect. Immun. 60:810–816.PubMedGoogle Scholar
  61. 61.
    Lindenmayer, A. and R.W. Estabrook. 1958. Low temperature spectral studies on the biosynthesis of cytochromes in bakers yeast. Arch. Biochem. Biophy. 78:66–82.CrossRefGoogle Scholar
  62. 62.
    List, B.M., P. Klatt, E.R. Werner, K. Schmidt, and B. Mayer. 1996. Overexpression of neuronal nitric oxide synthase in insect cells reveals requirement of haem for tetrahydrobiopterin binding. Biochem. J. 315:57–63.PubMedGoogle Scholar
  63. 63.
    Maines, M.D. 1997. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 35:517–554.CrossRefGoogle Scholar
  64. 64.
    Mayer, B., P. Klatt, B.M. List, C. Harteneck, and K. Schmidt. 1996. Large-scale purification of rat brain nitric oxide synthase from baculovirus overexpression system. Methods Enzymol. 268:420–427.PubMedCrossRefGoogle Scholar
  65. 65.
    McMillan, K., D.S. Bredt, D.J. Hirsch, S.H. Snyder, J.E. Clark, and B.S. Masters. 1992. Cloned, expressed rat cerebellar nitric oxide synthase contains stoichiometric amounts of heme, which binds carbon monoxide. Proc. Natl. Acad. Sci. USA 89:11141–11145.PubMedCrossRefGoogle Scholar
  66. 66.
    McMillan, K., J.C. Salerno, and B.S. Masters. 1996. Nitric oxide synthases: analogies to cytochrome P450 monooxygenases and characterization of recombinant rat neuronal nitric oxide synthase hemoprotein. Methods Enzymol. 268:460–472.PubMedCrossRefGoogle Scholar
  67. 67.
    Miller, J.P. and R.E. White. 1994. Photoafnnity labeling of cytochrome P450 2B4: capture of active site heme ligands by a photocarbene. Biochemistry 33:807–817.PubMedCrossRefGoogle Scholar
  68. 68.
    Miyake, Y. and N. Takayama. 1976. Spectral intermediates during the reduction of hepatic microsomal cytochrome P-450. J. Biochem. (Tokyo) 79:1077–1087.Google Scholar
  69. 69.
    Modi, S., M.J. Paine, M.J. Sutdiffe, L.Y. Lian, W.U. Primrose, C.R. Wolf, and G.C. Roberts. 1996. A model for human cytochrome P450 2D6 based on homology modeling and NMR studies of substrate binding. Biochemistry 35:4540–4550.PubMedCrossRefGoogle Scholar
  70. 70.
    Mok, T.C., R.A. Rickard, and F.J. Moss. 1969. The carbon monoxide-reactive haemoproteins of yeast. Biochim. Biophys. Acta 172:438–449.PubMedCrossRefGoogle Scholar
  71. 71.
    Muchmore, D.C., L.P. McIntosh, C.B. Russell, D.E. Anderson, and F.W. Dahlquist. 1989. Expression and nitrogen-15 labeling of proteins for proton and nitrogen-15 nuclear magnetic resonance. Methods Enzymol. 177:44–73.PubMedCrossRefGoogle Scholar
  72. 72.
    Nagai, K. and H.C. Thogersen. 1984. Generation of betaglo-bin by sequence-specific proteolysis of a hybrid protein produced in Escherichia coli. Nature 309:810–812.PubMedCrossRefGoogle Scholar
  73. 73.
    Nakane, M., J.S. Pollock, V. Klinghofer, F. Basha, R.A. Marsden, A. Hokari, T. Ogura, H. Esumi, and G.W. Carter. 1995. Functional expression of three isoforms of human nitric oxide synthase in baculovirus-infected insect cells. Biochem. Biophys. Res. Commun. 206:511–517.PubMedCrossRefGoogle Scholar
  74. 74.
    North, J.A., R. Dietrich, and A.L. Tappel. 1996. Multicomponent analysis of heme protein spectra in biological materials. Anal. Biochem. 233:115–123.PubMedCrossRefGoogle Scholar
  75. 75.
    Ohnishi, T., S. Miura, and Y. Ichikawa. 1993. Photoaffinity labeling of cytochrome P-45011 beta with methyltrienolone as a probe for the substrate binding region. Biochim. Biophys. Acta 1161:257–264.PubMedCrossRefGoogle Scholar
  76. 76.
    Ortiz de Montellano, P.R. 1995. Arylhydrazines as probes of hemoprotein structure and function. Bio-chimie 77:581–593.Google Scholar
  77. 77.
    Ortiz de Montellano, P.R., C. Nishida, I. Rodriguez-Crespo, and N. Gerber. 1998. Nitric oxide synthase structure and electron transfer. Drug Metab. Dispos. 26:1185–1189.PubMedGoogle Scholar
  78. 78.
    Ortiz de Montellano, P.R. and A. Wilks. 2000. Structure and mechanism of heme oxygenase. Adv. Inorg. Chem. 51:359–402.CrossRefGoogle Scholar
  79. 79.
    Osawa, Y., K. Nakatsuka, M.S. Williams, J.T. Kindt, and M. Nakatsuka. 1996. Reactions of reactive metabolites with hemoproteins-toxicological implications: covalent alteration of hemoproteins. Adv. Exp. Med. Biol. 387:37–45.PubMedGoogle Scholar
  80. 80.
    Otto, B.R., S.J. van Dooren, J.H. Nuijens, J. Luirink, and B. Oudega. 1998. Characterization of a hemoglobin protease secreted by the pathogenic Escherichia coli strain EB1. J. Exp. Med. 188:1091–1103.PubMedCrossRefGoogle Scholar
  81. 81.
    Pollock, W.B., F.I. Rosell, M.B. Twitchett, M.E. Dumont, and A.G. Mauk. 1998. Bacterialexpression of a mitochondrial cytochrome c. Trimethylation of lys72 in yeast iso-1-cytochrome c and the alkaline con-formational transition. Biochemistry 37:6124–6131.PubMedCrossRefGoogle Scholar
  82. 82.
    Poole, R.K., R.I. Scott, and B. Chance. 1980. Low-temperature spectral and kinetic properties of cytochromes in Escherichia coli K-12 grown at lowered oxygen tension. Biochim. Biophys. Acta 591:471–482.PubMedCrossRefGoogle Scholar
  83. 83.
    Poulos, T.L. 1991. Modeling of mammalian P450s on basis of P450cam X-ray structure. Methods Enzymol. 206:11–30.PubMedCrossRefGoogle Scholar
  84. 84.
    Poulos, T.L. 1993. Peroxidases. Curr. Opin. Biotechnol. 4:484–489.CrossRefGoogle Scholar
  85. 85.
    Ramos, L.S., K.R. Beebe, W.P. Karey, M.E. Sanches, B.C. Erickson, B.E. Wilson, B.E. Wangen, and B.R. Kowalski. 1986. Chemometrics. Anal. Chem. 58:294R–515R.CrossRefGoogle Scholar
  86. 86.
    Renaud, J.P., D.R. Davydov, K.P. Heirwegh, D. Mansuy, and G.H. Hui Bon Hoa. 1996. Thermodynamic studies of substrate binding and spin transitions in human cytochrome P-450 3A4 expressed in yeast microsomes. Biochem. J. 319:675–681.PubMedGoogle Scholar
  87. 87.
    Rieske, J.S. 1967. The quantitative determination of mitochondrial hemoproteins. Methods Enzymol. 10:488–493.CrossRefGoogle Scholar
  88. 88.
    Ristau, O., H. Rein, S. Greschner, G.R. Janig, and K. Ruckpaul. 1979. Quantitative analysis of the spin equilibrium of cytochrome P-450 LM2 fraction from rabbit liver microsomes. Acta Biol. Med. Ger. 38:177–185.PubMedGoogle Scholar
  89. 89.
    Rivera, M., C. Barillas-Mury, K.A. Christensen, J.W. Little, M.A. Wells, and F.A. Walker. 1992. Gene synthesis, bacterial expression, and 1H NMR spectroscopic studies of the rat outer mitochondrial membrane cytochrome b5.Biochemistry 31:12233–12240.PubMedCrossRefGoogle Scholar
  90. 90.
    Riveros-Moreno, V., B. Heffernan, B. Torres, A. Chubb, I. Charles, and S. Moncada. 1995. Purification to homogeneity and characterisation of rat brain recombinant nitric oxide synthase. Eur. J. Biochem. 230:52–57.PubMedCrossRefGoogle Scholar
  91. 91.
    Rodgers, K.R. 1999. Heme-based sensors in biological systems [In Process Citation]. Curr. Opin. Chem. Biol. 3:158–167.PubMedCrossRefGoogle Scholar
  92. 92.
    Rodriguez-Crespo, I., N.C. Gerber, and P.R. Ortiz de Montellano. 1996. Endothelial nitric-oxide synthase. Expression in Escherichia coli, spectroscopic characterization, and role of tetrahydrobiopterin in dimer formation. J. Biol. Chem. 271:11462–11467.PubMedCrossRefGoogle Scholar
  93. 93.
    Roman, L.J., E.A. Sheta, P. Martasek, S.S. Gross, Q. Liu, and B.S. Masters. 1995. High-level expression of functional rat neuronal nitric oxide synthase in Escherichia coli. Proc. Natl. Acad. Sci. USA 92:8428–8432.PubMedCrossRefGoogle Scholar
  94. 94.
    Sari, M.A., S. Booker, M. Jaouen, S. Vadon, J.I. Boucher, D. Pompon, and D. Mansuy. 1996. Expression in yeast and purification of functional macrophage nitric oxide synthase. Evidence for cysteine-194 as iron proximal ligand. Biochemistry 35:7204–7213.PubMedCrossRefGoogle Scholar
  95. 95.
    Sarma, S., R.J. DiGate, D.L. Banville, and R.D. Guiles. 1996. 1H, 13C and 15N NMR assignments and secondary structure of the paramagnetic form of rat cytochrome b5. J. Biomol. NMR 8:171–183.PubMedCrossRefGoogle Scholar
  96. 96.
    Schmidt, M.L. and J.Q. Trojanowski. 1986. Enzymatic detection of native and derivatized horseradish peroxidase in sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 755:371–375.CrossRefGoogle Scholar
  97. 97.
    Schuller, D.J., A. Wilks, P.R. Ortiz de Montellano, and T.L. Poulos. 1999. Crystal structure of human heme oxygenase-1. Nat. Struct. Biol. 6:860–867.PubMedCrossRefGoogle Scholar
  98. 98.
    Seo, H.G., J. Fujii, H. Soejima, N. Niikawa, and N. Taniguchi. 1995. Heme requirement for production of active endothelial nitric oxide synthase in baculovirus-infected insect cells. Biochem. Biophys. Res. Commun. 208:10–18.PubMedCrossRefGoogle Scholar
  99. 99.
    Shelver, D., M.V. Thorsteinsson, R.L. Kerby, S.Y. Chung, G.P. Roberts, M.F. Reynolds, R.B. Parks, and J.N. Burstyn. 1999. Identification of two important heme site residues (cysteine 75 and histidine 77) in CooA, the CO-sensing transcription factor of Rhodospirillum rubrum. Biochemistry 38:2669–2678.PubMedCrossRefGoogle Scholar
  100. 100.
    Shen, T.J., N.T. Ho, V. Simplaceanu, M. Zou, B.N. Green, M.F. Tam, and C. Ho. 1993. Production of unmodified human adult hemoglobin in Escherichia coli. Proc. Natl. Acad. Sci. USA 90:8108–8112.PubMedCrossRefGoogle Scholar
  101. l01.
    Shioi, Y., K. Takamiya, and M. Nishimura. 1972. Studies on energy and electron transfer systems in green photosynthetic bacterium Chloropseudomonas ethylica strain 2K. I. Isolation and characterization of cytochromes from Chloropseudomonas ethylica strain 2K. J. Biochem. (Tokyo) 71:285–294.Google Scholar
  102. 102.
    Shrager, R.I. and R.W. Hendler. 1982. Titration of individual components in a mixture with resolution of difference spectra, pK’s and redox transitions. Anal. Chem. 54:1147–1152.CrossRefGoogle Scholar
  103. 103.
    Shu, F., V. Ramakrishnan, and B.P. Schoenborn. 1996. High-level expression and deuteration of sperm whale myoglobin. A study of its solvent structure by X-ray and neutron diffraction methods. Basic Life Sci. 64:309–323.PubMedGoogle Scholar
  104. 104.
    Smith, A.T., N. Santama, S. Dacey, M. Edwards, R.C. Bray, R.N. Thorneley, and J.F. Burke. 1990. Expression of a synthetic gene for horseradish peroxidase C in Escherichia coli and folding and activation of the recombinant enzyme with Ca2+ and heme. J. Biol. Chem. 265:13335–13343.PubMedGoogle Scholar
  105. 105.
    Smulevich, G., J.M. Mauro, L.A. Fishel, A.M. English, J. Kraut, and T.G. Spiro. 1988. Heme pocket interactions in cytochrome c peroxidase studied by site-directed mutagenesis and resonance Raman spectroscopy. Biochemistry 27:5477–5485.PubMedCrossRefGoogle Scholar
  106. 106.
    Smulevich, G., M.A. Miller, J. Kraut, and T.G. Spiro. 1991. Conformational change and histidine control of heme chemistry in cytochrome c peroxidase: resonance Raman evidence from Leu-52 and Gly-181 mutants of cytochrome c peroxidase. Biochemistry 30:9546–9558.PubMedCrossRefGoogle Scholar
  107. 107.
    Spiro, T.G. 1978. Resonance Raman spectra of hemoproteins. Methods Enzymol. 54:233–249.PubMedCrossRefGoogle Scholar
  108. 108.
    Spiro, T.G. 1985. Resonance Raman spectroscopy as a probe of heme protein structure and dynamics. Adv. Prot. Chem. 37:111–159.CrossRefGoogle Scholar
  109. 109.
    Spiro, T.G. and R.S. Czernuszewicz. 1995. Resonance Raman spectroscopy of metalloproteins. Methods Enzymol. 246:416–460.PubMedCrossRefGoogle Scholar
  110. 110.
    Springer, B.A. and S.G. Sligar. 1987. High-level expression of sperm whale myoglobin in Escherichia coli. Proc. Natl. Acad. Sci. USA 84:8961–8965.PubMedCrossRefGoogle Scholar
  111. 111.
    Sun, J., A. Wilks, P.R. Ortiz de Montellano, and T.M. Loehr. 1993. Resonance Raman and EPR spectroscopic studies on heme-heme oxygenase complexes. Biochemistry 32:14151–14157.PubMedCrossRefGoogle Scholar
  112. 112.
    Tamburini, P.P., G.G. Gibson, W.L. Backes, S.G. Sligar, and J.B. Schenkman. 1984. Reduction kinetics of purified rat liver cytochrome P-450. Evidence for a sequential reaction mechanism dependent on the hemoprotein spin state. Biochemistry 23:4526–4533.PubMedCrossRefGoogle Scholar
  113. 113.
    Taylor, K.L., D.J. Uhlinger, and J.M. Kinkade, Jr. 1992. Expression of recombinant myeloperoxidase using a baculovirus expression system. Biochem. Biophys. Res. Commun. 187:1572–1578.PubMedCrossRefGoogle Scholar
  114. 114.
    Teale, F.W.J. 1959. Cleavage of the haem-protein link by acid methyl ethyl ketone. Biochim. Biophy. Acta. 35:543.CrossRefGoogle Scholar
  115. 115.
    Teraoka, J. and T. Kitagawa. 1981. Structural implication of the heme-linked ionization of horseradish peroxidase probed by the Fe-histidine stretching Raman line. J. Biol. Chem. 256:3969–3977.PubMedGoogle Scholar
  116. 116.
    Thomas, P.E., D. Ryan, and W. Levin. 1976. An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 75:168–176.PubMedCrossRefGoogle Scholar
  117. 117.
    Tschirret-Guth, R.A., K.F. Medzihradszky, and P.R. Ortiz de Montellano. 1998. Specific azidophenyl-diazene hemoprotein active site probes. Cross-linking of the heme to His-64 in myoglobin. J. Am. Chem. Soc. 120:7404–7410.CrossRefGoogle Scholar
  118. 118.
    Tschirret-Guth, R.A., K.F. Medzihradszky, and P.R. Ortiz de Montellano. 1999. Trifluoromethyl-diazirinylphenyldiazenes: new hemeprotein active-site probes. J. Amer. Chem. Soc. 121:4731–4737.CrossRefGoogle Scholar
  119. 119.
    Tschirret-Guth, R.A. and P.R. Ortiz de Motellano. 1998. Synthesis of photoaffinity probes for heme-containing proteins. J. Org. Chem. 63:9711–9715.CrossRefGoogle Scholar
  120. 120.
    Tsutsui, K. 1986. Affinity chromatography of heme-binding proteins: synthesis of hemin-agarose. Methods Enzymol. 123:331–338.PubMedCrossRefGoogle Scholar
  121. 121.
    Tsutsui, K. and G.C. Mueller. 1982. A protein with multiple heme-binding sites from rabbit serum. J. Biol. Chem. 257:3925–3931.PubMedGoogle Scholar
  122. 122.
    Varadarajan, R., A. Szabo, and S.G. Boxer. 1985. Cloning, expression in Escherichia coll, and reconstitution of human myoglobin. Proc. Natl. Acad. Sci. USA 52:5681–5684.CrossRefGoogle Scholar
  123. 123.
    Vickery, L.E. 1978. Spin states of heme proteins by magnetic circular dichroism. Methods Enzymol. 54:284–302.PubMedCrossRefGoogle Scholar
  124. 124.
    von Wachenfeldt, C., T.H. Richardson, J. Cosme, and E.F. Johnson. 1997. Microsomal P450 2C3 is expressed as a soluble dimer in Escherichia coli following modification of its N-terminus. Arch. Biochem. Biophys. 339:107–114.CrossRefGoogle Scholar
  125. 125.
    Vuletich, J.L. and Y. Osawa. 1998. Chemiluminescence assay for oxidatively modified myoglobin. Anal. Biochem. 265:375–380.PubMedCrossRefGoogle Scholar
  126. 126.
    Wilks, A., S.M. Black, W.L. Miller, and P.R. Ortiz de Montellano. 1995. Expression and characterization of truncated human heme oxygenase (hHO-1) and a fusion protein of hHO-1 with human cytochrome P450 reductase. Biochemistry 34:4421–4427.PubMedCrossRefGoogle Scholar
  127. 127.
    Wilks, A. and P.R. Ortiz de Montellano. 1992. Intramolecular translocation of the protein radical formed in the reaction of recombinant sperm whale myoglobin with H2O2. J. Biol. Chem. 267:8827–8833.PubMedGoogle Scholar
  128. 128.
    Wilks, A. and P.R. Ortiz de Montellano. 1993. Rat liver heme oxygenase. High level expression of a truncated soluble form and nature of the meso-hydroxy-lating species. J. Biol. Chem. 268:22357–22362.PubMedGoogle Scholar
  129. 129.
    Wilks, A. and M.P. Schmitt. 1998. Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle. J. Biol. Chem. 273:837–841.PubMedCrossRefGoogle Scholar
  130. 130.
    Wilks, A., J. Torpey, and P.R. Ortiz de Montellano. 1994. Heme oxygenase (HO-1). Evidence for electrophilic oxygen addition to the porphyrin ring in the formation of alpha-meso-hydroxyheme. J. Biol. Chem. 269:29553–29556.PubMedGoogle Scholar
  131. 131.
    Wu, C., J. Zhang, H. Abu-Soud, D.K. Ghosh, and D.J. Stuehr. 1996. High-level expression of mouse inducible nitric oxide synthase in Escherichia coli requires coexpression with calmodulin. Biochem. Biophys. Res. Commun. 222:439–444.PubMedCrossRefGoogle Scholar
  132. 132.
    Yoshida, T., K. Ishikawa, and M. Sato. 1991. Degradation of heme by a soluble peptide of heme oxygenase obtained from rat liver microsomes by mild trypsinization. Eur. J. Biochem. 199:729–733.PubMedCrossRefGoogle Scholar
  133. 133.
    Yoshida, T. and G. Kikuchi. 1978. Purification and properties of heme oxygenase from pig spleen microsomes. J. Biol. Chem. 253:4224–4229.PubMedGoogle Scholar
  134. 134.
    Yun, C.H., G.J. Hammons, G. Jones, M.V. Martin, N.E. Hopkins, W.L. Alworth, and F.P. Guengerich. 1992. Modification of cytochrome P450 1A2 enzymes by the mechanism-based inactivator 2-ethynylnaphthalene and the photoaffinity label 4-azidobiphenyl. Biochemistry 31:10556–10563.PubMedCrossRefGoogle Scholar
  135. 135.
    Zabel, U., M. Weeger, M. La, and H.H. Schmidt. 1998. Human soluble guanylate cyclase: functional expression and revised isoenzyme family. Biochem. J. 335:51–57.PubMedGoogle Scholar

Copyright information

© Humana Press, Totowa, NJ 2002

Authors and Affiliations

  • Angela Wilks
    • 1
  1. 1.University of MarylandBaltimoreUSA

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