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The distal pocket histidine residue in horse heart myoglobin directs the O-binding mode of nitrite to the heme iron.

Yi J, Heinecke J, Tan H, Ford PC, Richter-Addo GB
J Am Chem Soc 131 18119-28 (2009)
Related entries: 3hen, 3heo, 3hep

Cited: 51 times
EuropePMC logo PMID: 19924902

Abstract

It is now well-established that mammalian heme proteins are reactive with various nitrogen oxide species and that these reactions may play significant roles in mammalian physiology. For example, the ferrous heme protein myoglobin (Mb) has been shown to reduce nitrite (NO(2)(-)) to nitric oxide (NO) under hypoxic conditions. We demonstrate here that the distal pocket histidine residue (His64) of horse heart metMb(III) (i.e., ferric Mb(III)) has marked effects on the mode of nitrite ion coordination to the iron center. X-ray crystal structures were determined for the mutant proteins metMb(III) H64V (2.0 A resolution) and its nitrite ion adduct metMb(III) H64V-nitrite (1.95 A resolution), and metMb(III) H64V/V67R (1.9 A resolution) and its nitrite ion adduct metMb(III) H64V/V67R-nitrite (2.0 A resolution). These are compared to the known structures of wild-type (wt) hh metMb(III) and its nitrite ion adduct hh metMb(III)-nitrite, which binds NO(2)(-) via an O-atom in a trans-FeONO configuration. Unlike wt metMb(III), no axial H(2)O is evident in either of the metMb(III) mutant structures. In the ferric H64V-nitrite structure, replacement of the distal His residue with Val alters the binding mode of nitrite from the nitrito (O-binding) form in the wild-type protein to a weakly bound nitro (N-binding) form. Reintroducing a H-bonding residue in the H64V/V67R double mutant restores the O-binding mode of nitrite. We have also examined the effects of these mutations on reactivities of the metMb(III)s with cysteine as a reducing agent and of the (ferrous) Mb(II)s with nitrite ion under anaerobic conditions. The Mb(II)s were generated by reduction of the Mb(III) precursors in a second-order reaction with cysteine, the rate constants for this step following the order H64V/V67R > H64V >> wt. The rate constants for the oxidation of the Mb(II)s by nitrite (giving NO as the other product) follow the order wt > H64V/V67R >> H64V and suggest a significant role of the distal pocket H-bonding residue in nitrite reduction.

Articles - 3hc9 mentioned but not cited (3)

  1. The distal pocket histidine residue in horse heart myoglobin directs the O-binding mode of nitrite to the heme iron. Yi J, Heinecke J, Tan H, Ford PC, Richter-Addo GB. J Am Chem Soc 131 18119-18128 (2009)
  2. Factors correlating with significant differences between X-ray structures of myoglobin. Rashin AA, Domagalski MJ, Zimmermann MT, Minor W, Chruszcz M, Jernigan RL. Acta Crystallogr D Biol Crystallogr 70 481-491 (2014)
  3. Water stabilizes an alternate turn conformation in horse heart myoglobin. Bronstein A, Marx A. Sci Rep 13 6094 (2023)


Reviews citing this publication (5)

  1. Small molecule signaling agents: the integrated chemistry and biochemistry of nitrogen oxides, oxides of carbon, dioxygen, hydrogen sulfide, and their derived species. Fukuto JM, Carrington SJ, Tantillo DJ, Harrison JG, Ignarro LJ, Freeman BA, Chen A, Wink DA. Chem Res Toxicol 25 769-793 (2012)
  2. Nitrite and nitrate chemical biology and signalling. DeMartino AW, Kim-Shapiro DB, Patel RP, Gladwin MT. Br J Pharmacol 176 228-245 (2019)
  3. Myoglobin functions in the heart. Hendgen-Cotta UB, Kelm M, Rassaf T. Free Radic Biol Med 73 252-259 (2014)
  4. Nitrite and nitrite reductases: from molecular mechanisms to significance in human health and disease. Castiglione N, Rinaldo S, Giardina G, Stelitano V, Cutruzzolà F. Antioxid Redox Signal 17 684-716 (2012)
  5. Small ligand-globin interactions: reviewing lessons derived from computer simulation. Capece L, Boechi L, Perissinotti LL, Arroyo-Mañez P, Bikiel DE, Smulevich G, Marti MA, Estrin DA. Biochim Biophys Acta 1834 1722-1738 (2013)

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  10. Nitrosyl Myoglobins and Their Nitrite Precursors: Crystal Structural and Quantum Mechanics and Molecular Mechanics Theoretical Investigations of Preferred Fe -NO Ligand Orientations in Myoglobin Distal Pockets. Wang B, Shi Y, Tejero J, Powell SM, Thomas LM, Gladwin MT, Shiva S, Zhang Y, Richter-Addo GB. Biochemistry 57 4788-4802 (2018)
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  12. Endogenous Hemoprotein-Dependent Signaling Pathways of Nitric Oxide and Nitrite. Dent MR, DeMartino AW, Tejero J, Gladwin MT. Inorg Chem 60 15918-15940 (2021)
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  14. Resonance Raman detection of the myoglobin nitrito heme Fe-O-N=O/2-nitrovinyl species: implications for helix E-helix F interactions. Lambrou A, Pinakoulaki E. Phys Chem Chem Phys 17 3841-3849 (2015)
  15. Evaluating the capacity to generate and preserve nitric oxide bioactivity in highly purified earthworm erythrocruorin: a giant polymeric hemoglobin with potential blood substitute properties. Roche CJ, Talwar A, Palmer AF, Cabrales P, Gerfen G, Friedman JM. J Biol Chem 290 99-117 (2015)
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  17. Nitric oxide generation from heme/copper assembly mediated nitrite reductase activity. Hematian S, Siegler MA, Karlin KD. J Biol Inorg Chem 19 515-528 (2014)
  18. The structure of a ferrous heme-nitro species in the binuclear heme a3/CuB center of ba3-cytochrome c oxidase as determined by resonance Raman spectroscopy. Loullis A, Noor MR, Soulimane T, Pinakoulaki E. Chem Commun (Camb) 51 286-289 (2015)
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  20. NMR-guided directed evolution. Bhattacharya S, Margheritis EG, Takahashi K, Kulesha A, D'Souza A, Kim I, Yoon JH, Tame JRH, Volkov AN, Makhlynets OV, Korendovych IV. Nature 610 389-393 (2022)
  21. Unique Tyr-heme double cross-links in F43Y/T67R myoglobin: an artificial enzyme with a peroxidase activity comparable to that of native peroxidases. Liu C, Yuan H, Liao F, Wei CW, Du KJ, Gao SQ, Tan X, Lin YW. Chem Commun (Camb) 55 6610-6613 (2019)
  22. Complexes of ferriheme nitrophorin 4 with low-molecular weight thiol(ate)s occurring in blood plasma. He C, Nishikawa K, Erdem ÖF, Reijerse E, Ogata H, Lubitz W, Knipp M. J Inorg Biochem 122 38-48 (2013)
  23. Residues in the Distal Heme Pocket of Arabidopsis Non-Symbiotic Hemoglobins: Implication for Nitrite Reductase Activity. Kumar N, Astegno A, Chen J, Giorgetti A, Dominici P. Int J Mol Sci 17 E640 (2016)
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  25. Spin Crossover in Nitrito-Myoglobin as Revealed by Resonance Raman Spectroscopy. Lambrou A, Ioannou A, Pinakoulaki E. Chemistry 22 12176-12180 (2016)
  26. Combining selection valve and mixing chamber for nanoflow gradient generation: Toward developing a liquid chromatography cartridge coupled with mass spectrometer for protein and peptide analysis. Chen A, Lu JJ, Gu C, Zhang M, Lynch KB, Liu S. Anal Chim Acta 887 230-236 (2015)
  27. Elucidation of the heme active site electronic structure affecting the unprecedented nitrite dismutase activity of the ferriheme b proteins, the nitrophorins. He C, Ogata H, Lubitz W. Chem Sci 7 5332-5340 (2016)
  28. Influence of the heme distal pocket on nitrite binding orientation and reactivity in Sperm Whale myoglobin. Tse W, Whitmore N, Cheesman MR, Watmough NJ. Biochem J 478 927-942 (2021)
  29. Insertion of an H-bonding residue into the distal pocket of the ferriheme protein nitrophorin 4: effect on nitrite-iron coordination and nitrite disproportionation. He C, Ogata H, Knipp M. Chem Biodivers 9 1761-1775 (2012)
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  31. Regulation of nitrite reductase and lipid binding properties of cytoglobin by surface and distal histidine mutations. Kaliszuk SJ, Morgan NI, Ayers TN, Sparacino-Watkins CE, DeMartino AW, Bocian K, Ragireddy V, Tong Q, Tejero J. Nitric Oxide 125-126 12-22 (2022)
  32. High-performance liquid chromatographic cartridge with gradient elution capability coupled with UV absorbance detector and mass spectrometer for peptide and protein analysis. Lynch KB, Chen A, Yang Y, Lu JJ, Liu S. J Sep Sci 40 2752-2758 (2017)
  33. Intracellular imaging of metmyoglobin and oxygen using new dual purpose probe EYFP-Myoglobin-mCherry. Penjweini R, Roarke B, Alspaugh G, Link KA, Andreoni A, Mori MP, Hwang PM, Sackett DL, Knutson JR. J Biophotonics 15 e202100166 (2022)
  34. Nitrite reductase activity of heme and copper bound Aβ peptides. Nath AK, Ghosh C, Roy M, Seal M, Ghosh Dey S. Dalton Trans 48 7451-7461 (2019)
  35. Probing nitrite coordination in horseradish peroxidase by resonance Raman spectroscopy: Detection of two binding sites. Ioannou A, Pinakoulaki E. J Inorg Biochem 169 79-85 (2017)
  36. Coupling of helix E-F motion with the O-nitrito and 2-nitrovinyl coordination in myoglobin. Ioannou A, Lambrou A, Daskalakis V, Pinakoulaki E. Biophys Chem 221 10-16 (2017)
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  39. Peroxidase from proso millet exhibits endonuclease-like activity. Cui X, Wang T, Wang W, Wang H, Wang Z. Acta Biochim Biophys Sin (Shanghai) 51 688-696 (2019)
  40. Distinctive structural properties of THB11, a pentacoordinate Chlamydomonas reinhardtii truncated hemoglobin with N- and C-terminal extensions. Huwald D, Duda S, Gasper R, Olieric V, Hofmann E, Hemschemeier A. J Biol Inorg Chem 25 267-283 (2020)
  41. Engineering neuroglobin nitrite reductase activity based on myoglobin models. Williams MD, Ragireddy V, Dent MR, Tejero J. Biochem Biophys Rep 36 101560 (2023)
  42. Interactions of metronidazole and chloramphenicol with myoglobin: Crystal structure of a Mb-acetamide product. Powell SM, Prather KY, Nguyen N, Thomas LM, Richter-Addo GB. J Porphyr Phthalocyanines 27 1142-1147 (2023)
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