The chemical and structural bases of heme recognition: Binding interactions of heme with proteins and peptides

Heme Biology: The Secret Life of Heme in Regulating Diverse Biological Processes

Volumn , Issue , 2011, Pages 161-196

  Li, Y ^a   Zhang, Li ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84970943672     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1142/9789814287937_0008     Document Type: Chapter

References (193)

1. Barker PD, Ferguson SJ. 1999. Still a puzzle: Why is haem covalently attached in c-type cytochromes? Structure 7: R281-290.
2. Bowman SE, Bren KL. 2008. The chemistry and biochemistry of heme c: Functional bases for covalent attachment. Nat Prod Rep 25: 1118-1130.
3. Ortiz de Montellano PR. 2008. Mechanism and role of covalent heme binding in the CYP4 family of P450 enzymes and the mammalian peroxidases. Drug Metab Rev 40: 405-426.
4. Zederbauer M, Furtmuller PG, Brogioni S, Jakopitsch C, Smulevich G, Obinger C. 2007. Heme to protein linkages in mammalian peroxidases: Impact on spectroscopic, redox and catalytic properties. Nat Prod Rep 24: 571-584.
5. Tang XD, Xu R, Reynolds MF, Garcia ML, Heinemann SH, Hoshi T. 2003. Haem can bind to and inhibit mammalian calcium-dependent Slol BK channels. Nature 425: 531-535.
6. Hou S, Xu R, Heinemann SH, Hoshi T. 2008. The RCKl high-affinity Ca2+ sensor confers carbon monoxide sensitivity to Slol BK channels. Proc Natl Acad Sci U S A 105: 4039-4043.
7. Zhang L, Hach A. 1999. Molecular mechanism of heme signaling in yeast: The transcriptional activator Hapl serves as the key mediator. Cell Mol Life Sci 56: 415-426.
8. Mense SM, Zhang L. 2006. Heme: A versatile signaling molecule controlling The activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res 16: 681-692.
9. Hou S, Reynolds MF, Horrigan FT, Heinemann SH, Hoshi T. 2006. Reversible binding of heme to proteins in cellular signal transduction. Acc Chem Res 39: 918-924.
10. Kendrew JC, Bodo G, Dintzis HM, Parrish RG, Wyckoff H, Phillips DC. 1958. A three-dimensional model of the myoglobin molecule obtained by X-ray analysis. Nature 181: 662-666.
11. Poulos TL, Li H, Raman CS. 1999. Heme-mediated oxygen activation in biology: Cytochrome c oxidase and nitric oxide synthase. Curr Opin Chem Biol 3: 131-137.
12. Paoli M, Marles-Wright J, Smith A. 2002. Structure-function relationships in heme-proteins. DNA Cell Biol 21: 271-280.
13. Smulevich G, Feis A, Howes BD. 2005. Fifteen years of Raman spectroscopy of engineered heme containing peroxidases: What have we learned? Acc Chem Res 38: 433-440.
14. Anderson JL, Chapman SK. 2005. Ligand probes for heme proteins. Dalton Trans: 13-24.
15. Lombardi A, Nastri F, Pavone V. 2001. Peptide-based heme-protein models. Chem Rev 101: 3165-3189.
16. Collman JP. 1997. Functional analogs of heme protein active sites. Inorganic Chemistry 36: 5145-5155.
17. Collman JP, Boulatov R, Sunderland CJ, Fu L. 2004. Functional analogues of cytochrome c oxidase, myoglobin, and hemoglobin. Chem Rev 104: 561-588.
18. Landfried DA, Vuletich DA, Pond MP, Lecomte JT. 2007. Structural and thermodynamic consequences of b heme binding for monomeric apoglobins and other apoproteins. Gene 398: 12-28.
19. Poulos TL. 2007. The Janus nature of heme. Nat Prod Rep 24: 504-510.
20. Pardee KI, Xu X, Reinking J, Schuetz A, Dong A, Liu S, Zhang R, Tiefenbach J, Lajoie G, Plotnikov AN, Botchkarev A, Krause HM, Edwards A. 2009. The structural basis of gas-responsive transcription by the human nuclear hormone receptor REV-ERBbeta. PLoS Biol 7: e43.
21. Nienhaus K, Nienhaus GU. 2005. Probing heme protein-ligand interactions by UV/visible absorption spectroscopy. Methods Mol Biol 305: 215-242.
22. Spiro TG. 1985. Resonance Raman spectroscopy as a probe of heme protein structure and dynamics. Adv Protein Chem 37: 111-159.
23. Blumberg WE, Peisach J, Wittenberg BA, Wittenberg JB. 1968. The electronic structure of protoheme proteins. I. An electron paramagnetic resonance and optical study of horseradish peroxidase and its derivatives. J Biol Chem 243: 1854-1862.
24. Wittenberg BA, Kampa L, W’ittenberg JB, Blumberg WE, Peisach J. 1968. The electronic structure of protoheme proteins. II. An electron paramagnetic resonance and optical study of cytochrome c peroxidase and its derivatives. J Biol Chem 243: 1863-1870.
25. Simonneaux G, Bondon A. 2005. Mechanism of electron transfer in heme proteins and models: The NMR approach. Chem Rev 105: 2627-2646.
26. Roberts GC. 1996. The other kind of biological NMR studies of enzyme-substrate interactions. Neurochem Res 21: 1117-1124.
27. Liu Y, Moenne-Loccoz P, Hildebrand DP, Wilks A, Loehr TM, Mauk AG, Ortiz de Montellano PR. 1999. Replacement of the proximal histidine iron ligand by a cysteine or tyrosine converts heme oxygenase to an oxidase. Biochemistry 38: 3733-3743.
28. Schneider S, Maries-Wright J, Sharp KH, Paoli M. 2007. Diversity and conservation of interactions for binding heme in b-type heme proteins. Nat Prod Rep 24: 621-630.
29. Smith LJ, Kahraman A, Thornton JM. 2010. Heme proteins diversity in structural characteristics, function, and folding. Proteins 78: 2349-2368.
30. Reedy CJ, Elvekrog MM, Gibney BR. 2008. Development of a heme protein structure-electrochemical function database. Nucleic Acids Res 36: D307-313.
31. Tohjo M, Shibata K. 1963. Absorption spectra of hematin complexes with polyhistidine and copoly-(histidine. glutamic acid). Arch Biochem Biophys 103: 401-408.
32. Blauer G. 1964. Spectrophotometric Investigations of the system poly-L-lysine: Ferriheme at pH 10-12. Biochim Biophys Acta 79: 547-562.
33. Zhang L, Guarente L. 1995. Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J 14: 313-320.
34. Huffman DL, Rosenblatt MM, Suslick KS. 1998. Synthetic heme-peptide complexes. J Am Chem Soc 120: 6183-6184.
35. Huffman DL, Suslick KS. 2000. Hydrophobic interactions in metalloporphyrin-peptide complexes. Inorganic Chemistry 39: 5418-5419.
36. Cowley AB, Kennedy ML, Silchenko S, Lukat-Rodgers GS, Rodgers KR, Benson DR. 2006. Insight into heme protein redox potential control and functional aspects of six-coordinate ligand-sensing heme proteins from studies of synthetic heme peptides. Inorganic Chemistry 45: 9985-10001.
37. Lin YW, Yeung N, Gao YG, Miner KD, Tian S, Robinson H, Lu Y. 2010. Roles of glutamates and metal ions in a rationally designed nitric oxide reductase based on myoglobin. Proc Natl Acad Sci USA 107: 8581-8586.
38. Komatsu T, Ohmichi N, Nakagawa A, Zunszain PA, Curry S, Tsuchida E. 2005. CO binding properties of artificial hemoproteins formed by complexing iron protoporphyrin IX with human serum albumin mutants. J Am Chem Soc 127: 15933-15942.
39. Komatsu T, Nakagawa A, Zunszain PA, Curry S, Tsuchida E. 2007. Genetic engineering of the heme pocket in human serum albumin: Modulation of 02 binding of iron protoporphyrin IX by variation of distal amino acids. J Am Chem Soc 129: 11286-11295.
40. Tsuchida E, Sou K, Nakagawa A, Sakai H, Komatsu T, Kobayashi K. 2009. Artificial oxygen carriers, hemoglobin vesicles and albumin-hemes, based on bioconjugate chemistry. Bioconjug Chem 20: 1419-1440.
41. Koder RL, Anderson JL, Solomon LA, Reddy KS, Moser CC, Dutton PL. 2009. Design and engineering of an transport protein. Nature 458: 305-309.
42. Fitzgerald MM, Churchill MJ, McRee DE, Goodin DU. 1994. Small molecule binding to an artificially created cavity at the active site of cytochrome c peroxidase. Biochemistry 33: 3807-3818.
43. Negron C, Fufezan C, Koder RL. 2009. Geometric constraints for porphyrin binding in helical protein binding sites. Proteins 74: 400-416.
44. Suits MD, Jaffer N, Jia Z. 2006. Structure of the Escherichia coli Ol57:H7 heme oxygenase ChuS in complex with heme and enzymatic inactivation by mutation of the heme coordinating residue His-193. J Biol Chem 281: 36776-36782.
45. Schneider S, Sharp KH, Barker PD, Paoli M. 2006. An induced fit conformational change underlies the binding mechanism of the heme transport proteobacteria-protein HemS. J Biol Chem 281: 32606-32610.
46. Hou S, Larsen RW, Boudko D, Riley CW, Karat an E, Zimmer M, Ordal GW, Alam M. 2000. Myoglobin-like aerotaxis transducers in archaea and bacteria. Nature 403: 540-544.
47. Hefti MH, Francoijs KJ, de Vries SC, Dixon R., Vervoort J. 2004. The PAS fold. A redefinition of the PAS domain based upon structural prediction. Eur J Biochem 271: 1198-1208.
48. Gilles-Gonzalez MA, Gonzalez G. 2004. Signal transduction by heme-containing PAS-domain proteins. J Appl Physiol 96: 774-783.
49. Gilles-Gonzalez MA, Gonzalez G. 2005. Heme-based sensors: Defining characteristics, recent developments, and regulatory hypotheses. J Inorg Biochem 99: 1-22.
50. Youn H, Kerby RL, Thorsteinsson MV, Conrad M, Staples CR, Serate J, Beack J, Roberts GP. 2001. The heme pocket afforded by Glyll7 is crucial for proper heme ligation and activity of CooA. J Biol Chem 276: 41603-41610.
51. Lanzilotta WN, Schuller DJ, Thorsteinsson MV, Kerby RL, Roberts GP, Poulos TL. 2000. Structure of the CO sensing transcription activator CooA. Nat Struct Biol 7: 876-880.
52. Leys D, Backers K, Meyer TE, Hagen WR, Cusanovich MA, Van Beeumen JJ. 2000. Crystal structures of an oxygen-binding cytochrome c from Rhodobacter sphaeroides. J Biol Chem 275: 16050-16056.
53. Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK. 2000. The structure of malaria pigment beta-haematin. Nature 404: 307-310.
54. de Villiers KA, Kaschula CH, Egan TJ, Marques HM. 2007. Speciation and structure of ferriprotoporphyrin IX in aqueous solution: Spectroscopic and diffusion measurements demonstrate dimerization, but not mu-oxo dimer formation. J Biol Inorg Chem 12: 101-117.
55. Joyce MG, Girvan HM, Munro AW, Leys D. 2004. A single mutation in cytochrome P450 BM3 induces the conformational rearrangement seen upon substrate binding in the wild-type enzyme. J Biol Chem 279: 23287-23293.
56. Girvan HM, Marshall KR, Lawson RJ, Leys D, Joyce MG, Clarkson J, Smith WE, Cheesman MR, Munro AW. 2004. Flavocytochrome P450 BM3 mutant A264E undergoes substrate-dependent formation of a novel heme iron ligand set. J Biol Chem 279: 23274-23286.
57. Rodrigues ML, Oliveira TF, Pereira IA, Archer M. 2006. X-ray structure of the membrane-bound cytochrome c quinol dehydrogenase NrfH reveals novel haem coordination. EMBO J 25: 5951-5960.
58. Rodrigues ML, Scott KA, Sansom MS, Pereira IA, Archer M. 2008. Quinol oxidation by c-type cytochromes: Structural characterization of the menaquinol binding site of NrfHA. J Mol Biol 381: 341-350.
59. Adachi S, Nagano S, Ishimori K, Watanabe Y, Morishima I, Egawa T, Kitagawa T, Makino R. 1993. Roles of proximal ligand in heme proteins: Replacement of proximal histidine of human myoglobin with cysteine and tyrosine by site-directed mutagenesis as models for P-450, chloroperoxidase. and catalase. Biochemistry 32: 241-252.
60. Kurumbail RG, Stevens AM, Gierse JK, McDonald JJ, Stegeman RA, Pak JY, Gildehaus D, Miyashiro JM, Penning TD, Seibert K, Isakson PC, Stallings WC. 1996. Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 384: 644-648.
61. Luong C, Miller A, Barnett J, Chow J, Ramesha C, Browner MF. 1996. Flexibility of the NSAID binding site in the structure of human cyclooxygenase-2. Nat Struct Biol 3: 927-933.
62. Sugimoto H, Oda S, Otsuki T, Hino T, Yoshida T, Shiro Y. 2006. Crystal structure of human indoleamine 2,3-dioxygenase: Catalytic mechanism of 02 incorporation by a heme-containing dioxygenase. Proc Natl Acad Sci USA 103: 2611-2616.
63. Jensen LM, Sanishvili R, Davidson VL, Wilmot CM. 2010. In crystallo post-translational modification within a MauG/pre-methylamine dehydrogenase complex. Science 327: 1392-1395
64. Goff II, Morgan LO. 1976. Amino acid-substituted iron porphyrins. 2. Thermodynamic studies of ligand binding. Inorganic Chemistry 15: 2069-2076.
65. Barrick D. 1994. Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His Gly. Biochemistry 33: 6546-6554.
66. Barrick D. 1995. Depletion and replacement of protein metal ligands. Curr Opin BiotechnolG: 411-418.
67. Hirst J, Wilcox SK, Ai J, Moenne-Loccoz P, Loehr TM, Goodin DB. 2001. Replacement of the axial histidine ligand with imidazole in cytochrome c peroxidase. 2. Effects on heme coordination and function. Biochemistry 40: 1274-1283.
68. Hirst J, Wilcox SK, Williams PA, Blankenship J, McRee DE, Goodin DB. 2001. Replacement of the axial histidine ligand with imidazole in cytochrome c peroxidase. Effects on structure. Biochemistry 40: 1265-1273.
69. McRee DE, Jensen GM, Fitzgerald MM, Siegel HA, Goodin DB. 1994. Construction of a bisaquo heme enzyme and binding by exogenous ligands. Proc Natl Acad Sci U S A 91: 12847-12851.
70. Barrick D. 2000. Trans-substitution of the proximal hydrogen bond in myoglobin: II. Energetics, functional consequences, and implications for hemoglobin allostery. Proteins 39: 291-308.
71. Barrick D, Dahlquist FW. 2000. TYans-substitution of the proximal hydrogen bond in myoglobin: I. Structural consequences of hydrogen bond deletion. Proteins 39: 278-290.
72. Zhou WP, Zhong WW, Zhang XH, Ding JP, Zhang ZL, Xia ZW. 2009. Comparison of the crystal structure and function to wild-type and His25Ala mutant human heme oxygenase-1. Int J Mol Med 23: 379-387.
73. Roach MP, Ozaki S, Watanabe Y. 2000. Investigations of the myoglobin cavity mutant H93G with unnatural imidazole proximal ligands as a modular peroxide 0-0 bond cleavage model system. Biochemistry 39: 1446-1454.
74. Roach MP, Puspita WJ, W'atanabe Y. 2000. Proximal ligand control of heme iron coordination structure and reactivity with hydrogen peroxide: Investigations of the myoglobin cavity mutant H93G with unnatural oxygen donor proximal ligands. J Inorg Biochem 81: 173-182.
75. Reddi AR, Reedy CJ, Mui S, Gibney BR. 2007. Thermodynamic investigation into the mechanisms of proton-coupled electron transfer events in heme protein maquettes. Biochemistry 46: 291-305.
76. Robinson VL, Smith BB, Arnone A. 2003. A pH-dependent aquomet-to-hemichrome transition in crystalline horse methemoglobin. Biochemistry 42: 10113-10125.
77. Caillet-Saguy C, Turano P, Piccioli M, Lukat-Rodgers GS, Czjzek M, Guigliarelli B, Izadi-Pruneyre N, Rodgers KR, Delepierre M, Lecroisey A. 2008. Deciphering the structural role of histidine 83 for heme binding in hemophore HasA. J Biol Chem 283: 5960-5970.
78. Wolff N, Deniau C, Letoffe S, Simenel C, Kumar V, Stojiljkovic I, Wandersman C, Delepierre M, Lecroisey A. 2002. Histidine pK(a) shifts and changes of tautomeric states induced by the binding of gallium-protopor-phyrin IX in the hemophore HasA(SM). Protein Sd 11: 757-765.
79. Ribbing W, Ruterjans II. 1980. Isomeric incorporation of the Haem into monomeric haemoglobins of chironomus thummi thummi. 2. The Bohr effect of the component III explained on a molecular basis and functional differences between the two isomeric structures. Eur J Biochem 108: 89-102.
80. Chatake T, Shibayama N, Park SY, Kurihara K, Tamada T, Tanaka I, Niimura N, Kuroki R, Morimoto Y. 2007. Protonation states of buried histidine residues in human deoxyhemoglobin revealed by neutron crystallography. J Am Chem Soc 129: 14840-14841.
81. Kovalevsky AY, Chatake T, Shibayama N, Park SY, Ishikawa T, Mustyakimov M, Fisher Z, Langan P, Morimoto Y. 2010. Direct determination of protonation states of histidine residues in a 2 A neutron structure of deoxy-human normal adult hemoglobin and implications for the Bohr effect. J Mol Biol 398: 276-291.
82. Mueser TC, Griffith WP, Kovalevsky AY, Guo J, Seaver S, Langan P, Hanson BL. 2010. Hemoglobin redux: Combining neutron and X-ray diffraction with mass spectrometry to analyse the quaternary state of oxidized hemoglobins. Acta Crystallogr D Biol Crystallogr 66: 1249-1256.
83. Fufezan C, Zhang J, Gunner MR. 2008. Ligand preference and orientation in b- and c-type heme-binding proteins. Proteins 73: 690-704.
84. Zaric SD, Popovic DM, Knapp EW. 2001. Factors determining the orientation of axially coordinated imidazoles in heme proteins. Biochemistry 40: 7914-7928.
85. Galstyan AS, Zaric SD, Knapp EW. 2005. Computational studies on imidazole heme conformations. J Biol Inorg Chem 10: 343-354.
86. Sarma S, DiGate RJ, Goodin DB, Miller CJ, Guiles RD. 1997. Effect of axial ligand plane reorientation on electronic and electrochemical properties observed in the A67V mutant of rat cytochrome b5. Biochemistry 36: 5658-5668.
87. Yi L, Morgan JT, Ragsdale SW. 2010. Identification of a thiol/disulfide redox switch in the human BK channel that controls its affinity for heme and CO. J Biol Chem 285: 20117-20127.
88. Allen JW, Barker PD, Daltrop O, Stevens JM, Tomlinson EJ, Sinha N, Sambongi Y, Ferguson SJ. 2005. Why isn’t ‘standard’ heme good enough for c-type and dl-type cytochromes? Dalton Trans 3410-3418.
89. Stevens JM, Daltrop O, Allen JW, Ferguson SJ. 2004. C-type cytochrome formation: Chemical and biological enigmas. Acc Chem Res 37: 999-1007.
90. Ambler RJS. 1991. Sequence variability in bacterial cytochromes c. Biochim Biophys Acta 1058: 42-47.
91. Hartshorne IIS, Kern M, Meyer B, Clarke TA, Karas M, Richardson DJ, Simon J, 2007. A dedicated haem lyase is required for the maturation of a novel bacterial cytochrome c with unconventional covalent haem binding. Mol Microbiol 64: 1049-1060.
92. Hartshorne S, Richardson DJ, Simon J. 2006. Multiple haem lyase genes indicate substrate specificity in cytochrome c biogenesis. Biochem Soc Trans 34: 146-149.
93. Aragao D, FYazao C, Sieker L, Sheldrick GM, LeGall J, Carrondo MA. 2003. Structure of dimeric cytochrome c3 from Desulfovibrio gigas at 1.2 A resolution. Acta Crystallogr D Biol Crystallogr 59: 644-653.
94. Correia IJ, Paquete CM, Coelho A, Almeida CC, Catarino T, Louro RO, Frazao C, Saraiva LM, Carrondo MA, Turner DL, Xavier AV. 2004. Proton-assisted two-electron transfer in natural variants of tetraheme cytochromes from Desulfomicrobium Sp. J Biol Chem 279: 52227-52237.
95. Fulop V, Sam KA, Ferguson SJ, Ginger ML, Allen JW. 2009. Structure of a trypanosomatid mitochondrial cytochrome c with heme attached via only one thioether bond and implications for the substrate recognition requirements of heme lyase. FEBS J 276: 2822-2832.
96. Kranz RG, Richard-Fogal C, Taylor JS, Frawley ER. 2009. Cytochrome c biogenesis: Mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol Mol Biol Rev 73: 510-528.
97. Kooter IM, Moguilevsky N, Bollen A, van der Veen LA, Otto C, Dekker HL, Wever R. 1999. The sulfonium ion linkage in myeloperoxidase. Direct spectroscopic detection by isotopic labeling and effect of mutation. J Biol Chem 274: 26794-26802.
98. Guallar V, Olsen B. 2006. The role of the heme propionates in heme biochemistry. J Inorg Biochem 100: 755-760.
99. Munakata H, Sun JY, Yoshida K, Nakatani T, Honda E, Hayakawa S, Furuyama K, Hayashi N. 2004. Role of the heme regulatory motif in the heme-mediated inhibition of mitochondrial import of 5-aminolevulinate synthase. J Biochem 136: 233-238.
100. Dailey TA, Woodruff JH, Dailey HA. 2005. Examination of mitochondrial protein targeting of haem synthetic enzymes: In vivo identification of three functional haem-responsive motifs in 5-aminolaevulinate synthase. Biochem J 386: 381-386.
101. Goodfellow BJ, Dias JS, Ferreira GC, Henklein P, Wray V, Macedo AL. 2001. The solution structure and heme binding of the presequence of murine 5-aminolevulinate synthase. FEBS Lett 505: 325-331.
102. Astner I, Schulze JO, van den Heuvel J, Jahn D, Schubert WD, Heinz DW. 2005. Crystal structure of 5-aminolevulinate synthase, the first enzyme of heme biosynthesis, and its link to XLSA in humans. EMBO J 24: 3166-3177.
103. Hunter GA, Ferreira GC, 2009. 5-aminolevulinate synthase: catalysis of the first step of heme biosynthesis. Cell Mol Biol (Noisy-le-grand) 55: 102-110.
104. Wu N, Yin L, Hanniman EA, Joshi S, Lazar MA. 2009. Negative feedback maintenance of heme homeostasis by its receptor, Rev-erbalpha. Genes Dev 23: 2201-2209.
105. Siegert SW, Holt RJ. 2008. Physicochemical properties, pharmacokinetics, and pharmacodynamics of intravenous hematin: A literature review. Adv Ther 25: 842-857.
106. Zunszain PA, Ghuman J, Komatsu T, Tsuchida E, Curry S. 2003. Crystal structural analysis of human serum albumin complexed with hemin and fatty acid. BMC Struct Biol 3: 6.
107. Wardell M, Wang Z, Ho JX, Robert J, Ruker F, Ruble J, Carter DC. 2002. The atomic structure of human methemalbumin at 1.9 A. Biochem Biophys Res Commun 291: 813-819.
108. Paoli M, Anderson BF, Baker HM, Morgan WT, Smith A, Baker EN. 1999. Crystal structure of hemopexin reveals a novel high-affinity heme site formed between two beta-propeller domains. Nat Struct Biol 6: 926-931.
109. Fanali G, De Sanctis G, Gioia M, Coletta M, Ascenzi P, Fasano M. 2009. Reversible two-step unfolding of heme-human serum albumin: A MH-NMR relaxometric and circular dichroism study. J Biol Inorg Chem 14: 209-217.
110. Wallace AC, Laskowski RA, Thornton JM. 1995. LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8: 127-134.
111. Muller-Eberhard U. 1988. Hemopexin. Methods Enzymol 163: 536-565.
112. Shipulina N, Smith A, Morgan WT. 2000. Heme binding by hemopexin: Evidence for multiple modes of binding and functional implications. J Protein Chem 19: 239-248.
113. Shipulina NV, Smith A, Morgan WT. 2001. Effects of reduction and ligation of heme iron on the thermal stability of heme-hemopexin complexes. J Protein Chem 20: 145-154.
114. Baker HM, Anderson BF, Baker EN. 2003. Dealing with iron: Common structural principles in proteins that transport iron and heme. Proc Natl Acad Sci U S A 100: 3579-3583.
115. Resell FI, Mauk MR, Mauk AG, 2005. pH- and metal ion-linked stability of the hemopexin-heme complex. Biochemistry 44: 1872-1879.
116. Wolff N, Izadi-Pruneyre N, Couprie J, Habeck M, Linge J, Rieping W, Wandersman C, Nilges M, Delepierre M, Lecroisey A. 2008. Comparative analysis of structural and dynamic properties of the loaded and unloaded hemophore HasA: Functional implications. J Mol Biol 376: 517-525.
117. Czjzek M, Letoffe S, Wandersman C, Delepierre M, Lecroisey A, Izadi-Pruneyre N. 2007. The crystal structure of the secreted dimeric form of the hemophore HasA reveals a domain swapping with an exchanged heme ligand. J Mol Biol 365: 1176-1186.
118. Brill AS, Williams RJ. 1961. The absorption spectra, magnetic moments and the binding of iron in some haemoproteins. Biochem J 78: 246-253.
119. Peisach J, Blumberg WE, Ogawa S, Rachmilewitz EA, Oltzik R. 1971. The effects of protein conformation on the heme symmetry in high spin ferric heme proteins as studied by electron paramagnetic resonance. J Biol Chem 246: 3342-3355.
120. Peisach J, Blumberg WE, Wittenberg BA, Wittenberg JB. 1968. The electronic structure of protoheme proteins. 3. Configuration of the heme and its ligands. J Biol Chem 243: 1871-1880.
121. Scott RA, Lukehart CM. 2007. Applications of physical methods to inorganic and bioinorganic chemistry. Wiley-Interscience.
122. Tezcan FA, Winkler JR, Gray HB. 1998. Effects of ligation and folding on reduction potentials of heme proteins. J Am Chem Soc 120: 13383-13388.
123. Mao J, Hauser K, Gunner MR. 2003. How cytochromes with different folds control heme redox potentials. Biochemistry 42: 9829-9840.
124. Stellwagen E. 1978. Haem exposure as the determinate of oxidation-reduction potential of haem proteins. Nature 275: 73-74.
125. Maes EM, Roberts SA, Weichsel A, Montfort WR. 2005. Ultrahigh resolution structures of nitrophorin 4: Heme distortion in ferrous CO and NO complexes. Biochemistry 44: 12690-12699.
126. Olea C, Kuriyan J, Marietta MA. Modulating heme redox potential through protein-induced porphyrin distortion. J Am Chem Soc 132: 12794-12795.
127. Olea C, Boon EM, Pellicena P, Kuriyan J, Marietta MA. 2008. Probing the function of heme distortion in the H-NOX family. ACS Chem Biol 3: 703-710.
128. Chen Z, Ost TW, Schelvis JP. 2004. Phe393 mutants of cytochrome P450 BM3 with modified heme redox potentials have altered heme vinyl and propionate conformations. Biochemistry 43: 1798-1808.
129. Reid LS, Mauk MR, Mauk AG. 1984. Role of heme propionate groups in cytochrome b5 electron transfer. J Am Chem Soc 106: 2182-2185.
130. Das DK, Medhi OK. 1998. The role of heme propionate in controlling the redox potential of heme: Square wave voltammetry of protoporphyrinato IX iron (III) in aqueous surfactant micelles. J Inorg Biochem 70: 83-90.
131. Bowman SE, Bren KL. 2010. Variation and analysis of second-sphere interactions and axial histidinate character in c-type cytochromes. Inorg Chem 49: 7890-7897.
132. Cho HY, Cho HJ, Kim YM, Oh JI, Kang BS. 2009. Structural insight into the heme-based redox sensing by DosS from Mycobacterium tuberculosis. J Biol Chem 284: 13057-13067.
133. Badyal SK, Metcalfe CL, Basran J, Efimov I, Moody PC, Raven EL. 2008. Iron oxidation state modulates active site structure in a heme peroxidase. Biochemistry 47: 1403-4409.
134. Carlsson GH, Nicholls P, Svistunenko D, Berglund GI, Hajdu J. 2005. Complexes of horseradish peroxidase with formate, acetate, and carbon monoxide. Biochemistry 44: 635-642.
135. Hirotsu S, Chu GC, Unno M, Lee DS, Yoshida T, Park SY, Shiro Y, Ikeda-Saito M. 2004. The crystal structures of the ferric and ferrous forms of the heme complex of HmuO, a heme oxygenase of Corynebacterium diphtheriae. J Biol Chem 279: 11937-11947.
136. Sugishima M, Sakamoto H, Noguchi M, Fukuyama K. 2003. Crystal structures of ferrous and CO-, CN(-)-, and NO-bound forms of rat heme oxygenase-1 (HO-1) in complex with heme: Structural implications for discrimination between CO and 02 in HO-1. Biochemistry 42: 9898-9905.
137. Lad L, Wang J, Li II, Friedman J, Bhaskar B, Ortiz de Montellano PR, Poulos TL. 2003. Crystal structures of the ferric, ferrous, and ferrous-NO forms of the Aspl40Ala mutant of human heme oxygenase-1: Catalytic implications. J Mol Biol 330: 527-538.
138. Geremia S, Garau G, Vaccari L, Sgarra R, Viezzoli MS, Calligaris M, Randaccio L. 2002. Cleavage of the iron-methionine bond in c-type cytochromes: Crystal structure of oxidized and reduced cytochrome c(2) from Rhodopseudomonas palustris and its ammonia complex. Protein Sci 11: 6-17.
139. Andreoletti P, Pernoud A, Sainz G, Gouet P, Jouve HM. 2003. Structural studies of Proteus mirabilis catalase in its ground state, oxidized state and in complex with formic acid. Acta Crystallogr D Biol Crystallogr 59: 2163-2168.
140. Berghuis AM, Brayer GI. 1992. Oxidation state-dependent conformational changes in cytochrome c. J Mol Biol 223: 959-976.
141. Norager S, Legrand P, Pieulle L, Hatchikian C, Roth M. 1999. Crystal structure of the oxidised and reduced acidic cytochrome c3 from Desulfovibrio africanus. J Mol Biol 290: 881-902.
142. Ishikawa H, Kato M, Hori H, Ishimori K, Kirisako T, Tokunaga F, Iwai K. 2005. Involvement of heme regulatory motif in heme-mediated ubiquitination and degradation of IRP2. Mol Cell 19: 171-181.
143. Dycke C, Bougault C, Gaillard J, Andrieu JP, Pantopoulos K, Moulis JM. 2007. Human iron regulatory protein 2 is easily cleaved in its specific domain: Consequences for the haem binding properties of the protein. Biochem J 408: 429-439.
144. Gong W, Hao B, Mansy SS, Gonzalez G, Gilles-Gonzalez MA, Chan MK. 1998. Structure of a biological oxygen sensor: A new mechanism for heme-driven signal transduction. Proc Natl Acad Sci USA 95: 15177-15182.
145. Miyatake H, Mukai M, Park SY, Adachi S, Tamura K, Nakamura H, Nakamura K, Tsuchiya T, Iizuka T, Shiro Y. 2000. Sensory mechanism of oxygen sensor FixL from Rhizobium meliloti: Crystallographic. mutagenesis and resonance Raman spectroscopic studies. J Mol Biol 301: 415-431.
146. Key J, Srajer V, Pahl R, Moffat K. 2007. Time-resolved crystallographic studies of the heme domain of the oxygen sensor FixL: Structural dynamics of ligand rebinding and their relation to signal transduction. Biochemistry 46: 4706-4715.
147. Ayers RA, Moffat K. 2008. Changes in quaternary structure in the signaling mechanisms of PAS domains. Biochemistry 47: 12078-12086.
148. Kurokawa H, Lee DS, Watanabe M, Sagami I, Mikami B, Raman CS, Shimizu T. 2004. A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor. J Biol Chem 279: 20186-20193.
149. Park H, Suquet C, Satterlee JD, Kang C. 2004. Insights into signal transduction involving PAS domain oxygen-sensing heme proteins from the X-ray crystal structure of Escherichia coli Dos heme domain (Ec DosH). Biochemistry 43: 2738-2746.
150. Tanaka A, Shimizu T. 2008. Ligand binding to the Fe(III)-protoporphyrin IX complex of phosphodiesterase from Escherichia coli (Ec DOS) markedly enhances catalysis of cyclic di-GMP: Roles of \let95, Arg97. and Phell3 of the putative heme distal side in catalytic regulation and ligand binding. Biochemistry 47: 13438-13446.
151. Ito S, Igarashi J, Shimizu T. 2009. The FG loop of a heme-based gas sensor enzyme. Ec DOS, functions in heme binding, autoxidation and catalysis. J Inorg Biochem 103: 1380-1385.
152. Ito S, Araki Y, Tanaka A, Igarashi J, Wada T, Shimizu T. 2009. Role of Phell3 at the distal side of the heme domain of an oxygen-sensor (Ec DOS) in the characterization of the heme environment. J Inorg Biochem 103: 989-996.
153. Sasakura Y, Yoshimura-Suzuki T, Kurokawa H, Shimizu T. 2006. Structure-function relationships of Ec DOS, a heme-regulated phosphodiesterase from Escherichia coli. -4cc Chem Res 39: 37-43.
154. Gilles-Gonzalez MA, Caceres AI, Sousa EH, Tomchick DR, Brautigam C, Gonzalez C, Machius M. 2006. A proximal arginine R206 participates in switching of the Bradyrhizobium japonicum FixL oxygen sensor. J Mol Biol 360: 80-89.
155. Zhang W, Olson JS, Phillips GN. 2005. Biophysical and kinetic characterization of HemAT, an aerotaxis receptor from Bacillus subtilis. Biophys J 88: 2801-2814.
156. Zhang W, Phillips GN. 2003. Structure of the oxygen sensor in Bacillus subtilis: Signal transduction of chemotaxis by control of symmetry. Structure 11: 1097-1110.
157. Pinakoulaki E, Yoshimura H, Daskalakis V, Yoshioka S, Aono S, Varotsis C. 2006. Two ligand-binding sites in the 02-sensing signal transducer HemAT: Implications for ligand recognition/discrimination and signaling. Proc Natl Acad Sci U S A 103: 14796-14801.
158. Roberts GP, Kerby RL, Youn H, Conrad M. 2005. CooA, a paradigm for gas sensing regulatory proteins. J Inorg Biochem 99: 280-292.
159. Roberts GP, Thorsteinsson MV, Kerby RL, Lanzilotta WN, Poulos T. 2001. CooA: A heme-containing regulatory protein that serves as a specific sensor of both carbon monoxide and redox state. Prog Nucleic Acid Res Mol Biol 67: 35-63.
160. Thorsteinsson MV, Kerby RL, Conrad M, Youn H, Staples CR, Lanzilotta WN, Poulos TJ, Serate J, Roberts GP. 2000. Characterization of variants altered at the N-terminal proline, a novel heme-axial ligand in CooA, the CO-sensing transcriptional activator. J Biol Chem 275: 39332-39338.
161. Borjigin M, Li H, Lanz ND, Kerby RL, Roberts GP, Poulos TL. 2007. Structure-based hypothesis on the activation of the CO-sensing transcription factor CooA. Acta Crystallogr D Biol Crystallogr 63: 282-287.
162. Komori H, Inagaki S, Yoshioka S, Aono S, Higuchi Y. 2007. Crystal structure of CO-sensing transcription activator CooA bound to exogenous ligand imidazole. J Mol Biol 367: 864-871.
163. Zhang T, Rubtsov IV, Nakajima H, Aono S, Yoshihara K. 2006. Effect of mutation on the dissociation and recombination dynamics of CO in transcriptional regulator CooA: A picosecond infrared transient absorption study. Biochemistry 45: 9246-9253.
164. Derbyshire ER, Marietta MA. 2009. Biochemistry of soluble guanylate cyclase. Handb Exp Pharmacok 17-31.
165. Boon EM, Marietta MA. 2005. Ligand discrimination in soluble guanylate cyclase and the II-NOX family of heme sensor proteins. Curr Opin Chem Biol 9: 441-446.
166. Cary SP, Winger JA, Derbyshire ER, Marietta MA. 2006. Nitric oxide signaling: no longer simply on or off. Trends Biochem Sci 31: 231-239.
167. Wingpr JA, Derbyshire ER, Lamers MH, Marietta MA, Kuriyan J. 2008. The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase. BMC Struct Biol 8: 42.
168. Ma X, Beuve A, van den Akker F. 2010. Crystal structure of the signaling helix coiled-coil domain of the betal subunit of the soluble guanylyl cyclase. BMC Struct Biol 10: 2.
169. Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS. 2004. Femtomolar sensitivity of a NO sensor from clostridium botulinum. Science 306: 1550-1553.
170. Pellicena P, Karow DS, Boon EM, Marietta MA, Kuriyan J. 2004. Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases. Proc Natl Acad Sd USA 101: 12854-12859.
171. Martin F, Baskaran P, Ma X, Dunten PW, Schaefer M, Stasch JP, Beuve A, van den Akker F. 2010. Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase. J Biol Chem 285: 22651-22657.
172. Russwurm M, Koesling D. 2004. Guanylyl cyclase: NO hits its target. Biochem Soc Symp: 51-63.
173. Lawson DM, Stevenson CE, Andrew CR, George SJ, Eady RR. 2003. A two-faced molecule offers NO explanation: The proximal binding of nitric oxide to haem. Biochem Soc Trans 31: 553-557.
174. Poulos TL. 2006. Soluble guanylate cyclase. Curr Opin Struct Biol 16: 736-743.
175. Ma X, Sayed N, Beuve A, van den Akker F. 2007. NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism. EMBO J 26: 578-588.
176. Spiro T. 2008. A twist on heme signaling. ACS Chem Biol 3: 673-675.
177. Zhang H, Lu M, Zhang Y, Li Z. 2008. Primary response of the sGC heme binding domain to the cleavage of the Fe-His bond. Bioinformation 2: 296-300.
178. Capece L, Estrin DA, Marti MA. 2008. Dynamical characterization of the heme NO oxygen binding (HNOX) domain. Insight into soluble guanylate cyclase allosteric transition. Biochemistry 47: 9416-9427.
179. Taoka S, Lepore BW, Kabil O, Ojha S, Ringe D, Banerjee R. 2002. Human cystathionine beta-synthase is a heme sensor protein. Evidence that the redox sensor is heme and not the vicinal cysteines in the CXXC motif seen in the crystal structure of the truncated enzyme. Biochemistry 41: 10454-10461.
180. Banerjee R, Zou CG. 2005. Redox regulation and reaction mechanism of human cystathionine-beta-synthase: A PLP-dependent hemesensor protein. Arch Biochem Biophys 433: 144-156.
181. Singh S, Madzelan P, Stasser J, Weeks CL, Becker D, Spiro TG, Penner-Hahn J, Banerjee R. 2009. Modulation of the heme electronic structure and cystathionine beta-synthase activity by second coordination sphere ligands: The role of heme ligand switching in redox regulation. J Inorg Biochem 103: 689-697.
182. Giardina G, Rinaldo S, Johnson KA, Di Matteo A, Brunori M, Cutruzzola F. 2008. NO sensing in Pseudomonas aeruginosa: Structure of the transcriptional regulator DNR. J Mol Biol 378: 1002-1015.
183. Desai KK, Miller BG. 2010. L-glyceraldehyde 3-phosphate reductase from Escherichia coli is a heme binding protein. Bioorg Chem 38: 37-41.
184. Hou S, Heinemann SH, Hoshi T. 2009. Modulation of BKCa channel gating by endogenous signaling molecules. Physiology (Bethesda) 24: 26-35.
185. Horrigan FT, Heinemann SH, Hoshi T. 2005. Heme regulates allosteric activation of the Slol BK channel. J Gen Physiol 126: 7-21.
186. Raghuram S, Stayrook KR, Huang P, Rogers PM, Nosie AK, McClure DB, Burris LL, Khorasanizadeh S, Burris TP, Rastinejad F. 2007. Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. Nat Struct Mol Biol 14: 1207-1213.
187. Yin L, Wu N, Curtin JC, Qatanani M, Szwergold NR, Reid RA, Waitt GM, Parks J, Pearce KH, Wisely GB, Lazar MA. 2007. Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science 318: 1786-1789.
188. Rogers PM, Ying L, Burris TP. 2008. Relationship between circadian oscillations of Rev-erbalpha expression and intracellular levels of its ligand, heme. Biochem Biophys Res Commun 368: 955-958.
189. Burris TP. 2008. Nuclear hormone receptors for heme: REV-ERBalpha and REV-ERBbeta are ligand-regulated components of the mammalian clock. Mol Endocrinol 22: 1509-1520.
190. Kumar N, Solt LA, Wang Y, Rogers PM, Bhattacharyya G, Kamenecka TM, Stayrook KR, Crumbley C, Floyd ZE, Gimble JM, Griffin PR, Burris TP. 2010. Regulation of adipogenesis by natural and synthetic REV-ERB ligands. Endocrinology 151: 3015-3025.
191. Woo EJ, Jeong DG, Lim MY, Jun Kim S, Kim KJ, Yoon SM, Park BC, Ryu SE. 2007. Structural insight into the constitutive repression function of the nuclear receptor Rev-erbbeta. J Mol Biol 373: 735-744.
192. Phelan CA, Gampe RT, Lambert MH, Parks DJ, Montana V, Bynum J, Broderick TM, Hu X, Williams SP, Nolte RT, Lazar MA. 2010. Structure of Rev-erbalpha bound to N-CoR reveals a unique mechanism of nuclear receptor-co-repressor interaction. Nat Struct Mol Biol 17: 808-814.
193. Marvin KA, Reinking JL, Lee AJ, Pardee K, Krause HM, Burstyn JN. 2009. Nuclear receptors homo sapiens Rev-erbbeta and Drosophila melanogaster E75 are thiolate-ligated heme proteins which undergo redox-mediated ligand switching and bind CO and NO. Biochemistry 48: 7056-7071.