Three toxic gases meet in the mitochondria

Frontiers in Physiology

Volumn 6, Issue Aug, 2015, Pages

  Decréau, Richard A ^a,b   Collman, James P ^b  

^a UNIVERSITÉ BOURGOGNE FRANCHE COMTÉ   (France)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Anticoagulants; Biomimetic functional model; Blood platelets; Cytochrome c oxidase; Electrocatalytic oxygen reduction; Mitochondria; Mitochondrial respiration; Reversible inhibition

Indexed keywords

COPPER COMPLEX; CYTOCHROME C OXIDASE; HEME; HYDROGEN SULFIDE; IMIDAZOLE; IRON; LIGAND; MYOGLOBIN; NITRATE; NITRIC OXIDE; OXYGEN; PEROXYNITRITE; PHENOL; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TETRAZOLE DERIVATIVE; TOXIC GAS; TRIS IMIDAZOLE COPPER COMPLEX; UNCLASSIFIED DRUG;

BLOOD CLOTTING; BODY TEMPERATURE; BREATHING; CATALYSIS; CHEMICAL REACTION; CROSS LINKING; DIFFUSION; ELECTRODE; ENZYME ACTIVE SITE; HIBERNATION; HUMAN; IMMOBILIZATION; MITOCHONDRION; NONHUMAN; PH; REDUCTION; REVIEW; THROMBOCYTE;

EID: 84940842603     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00210     Document Type: Review

References (128)

1. Aguilar, F., Autrup, H., Barlow, S., Castle, L., Crebelli, R., Dekan, W., et al.(2007). Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food. Eur. Food Safe Auth. 455, 1-76. doi: 10.2903/j.efsa.2007.428.
2. Alonso, J.R., Cardellach, F., López, S., Casademont, J., and Miró, O. (2003). Carbon monoxide specifically inhibits cytochrome c oxidase of human mitochondrial respiratory chain. Pharmacol. Toxicol. 93, 142-146. doi: 10.1034/j.1600-0773.2003.930306.x.
3. Anderson, A., Binbrekt, S., and Tang, H.C. (1977). Raman and infrared study of the low temperature phase of solid H2S and D2S. J. Raman Spectrosc. 6, 213-220. doi: 10.1002/jrs.1250060502.
4. Aregheore, E.M., and Agunbiade, O.O. (1991). The toxic effects of cassava manihot esculenta grantz diets on humans: a review. Vet. Hum. Toxicol. 33, 274-275.
5. Babcock, G.T., and Wikström, M. (1992). Oxygen activation and the conservation of energy in cell respiration. Nature 356, 301-309. doi: 10.1038/356301a0.
6. Barile, C.J., Herrmann, P.C., Tyvoll, D.A., Collman, J.P., Decreau, R.A., and Bull, B.S. (2012). Inhibiting platelet-stimulated blood coagulation by inhibition of mitochondrial respiration. Proc. Natl. Acad. Sci. U.S.A. 109, 2539-2543. doi: 10.1073/pnas.1120645109.
7. Beauchamp, R.O. J., Bus, J.S., Popp, J.A., Boreiko, C.J., and Andjelkovich, D.A. (1984). A critical review of the literature on hydrogen-sulfide toxicity. Crit. Rev. Toxicol. 65, 18-25. doi: 10.3109/10408448409029321.
8. Bennett, J.A., Neiswonger, M.A., Wheeler, C.D., Pander, J.E., and McKinney, S.E. (2012). Cyanide-coordinated Fe(III) meso-tetra(4-carboxyphenyl) porphyrin as a possible electrocatalytic material for selective H2S oxidation physical and analytical electrochemistry. J. Electrochem. Soc. 159, F119-F124. doi: 10.1149/2.055205jes.
9. Blackstone, E., Morrison, M., and Roth, M.B. (2005). H2S induces a suspended animation-like state in mice. Science 308, 518. doi: 10.1126/science.1108581.
10. Blackstone, E., and Roth, M.B. (2007). Suspended animation-like state protects mice from lethal hypoxia. Shock 27, 370-372. doi: 10.1097/SHK.0b013e31802e27a0.
11. Bowen, W.J. (1949). The absorption spectra and extinction coefficients of myoglobin. J. Biol. Chem. 179, 235-245.
12. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle-dye binding. Anal. Biochem. 72, 248-254. doi: 10.1016/0003-2697(76)90527-3.
13. Brunori, M., Forte, E., Arese, M., Mastronicola, D., Giuffrè, A., and Sarti, P. (2006). Nitric oxide and the respiratory enzyme. Biochim. Biophys. Acta 1757, 1144-1154. doi: 10.1016/j.bbabio.2006.05.011.
14. Burke, J.M., Kincaid, J.R., Peters, S., Gagne, R.R., Collman, J.P., and Spiro, T.G. (1978). Structure-sensitive resonance Raman bands of tetraphenyl and picket fence porphyrin-iron complexes, including an oxyhemoglobin analog. J. Am. Chem. Soc. 100, 6083-6088. doi: 10.1021/ja00487a018.
15. Calhoun, M.W., Hill, J.J., Lemieux, L.J., Ingledew, W.J., Alben, J.O., and Gennis, R.B. (1993). Site-directed mutants of the cytochrome bo ubiquinol oxidase of Escherichia coli: amino acid substitutions for two histidines that are putative CuB ligands. Biochemistry 32, 11524-11529. doi: 10.1021/bi00094a008.
16. Cheng, L., and Richter-Addo, G.B. (2000). "Binding and activation of nitric oxide by metalloporphyrins and heme," in The Porphyrin Handbook, Vol. 4, eds K. M. Kadish, K.M. Smith, and R. Guilard (San Diego, CA: Academic Press), 219-291.
17. Collman, J.P. (1977). Synthetic models for the oxygen-binding hemoproteins. Acc. Chem. Res. 10, 265-272. doi: 10.1021/ar50115a006.
18. Collman, J.P., Boulatov, R., Sunderland, C.J., and Fu, L. (2004a). Functional analogues of cytochrome c oxidase, myoglobin, and hemoglobin. Chem. Rev. 104, 561-588. doi: 10.1021/cr0206059.
19. Collman, J.P., Brauman, J.I., Halbert, T.R., and Suslick, K.S. (1976). Nature of oxygen and carbon monoxide binding to metalloporphyrins and heme proteins. Proc. Natl. Acad. Sci. U.S.A. 73, 3333-3337. doi: 10.1073/pnas.73.10.3333.
20. Collman, J.P., Brauman, J.I., Rose, E., and Suslick, K.S. (1978). Cooperativity in O2 binding to iron porphyrins. Proc. Natl. Acad. Sci. U.S.A. 75, 1052-1055. doi: 10.1073/pnas.75.3.1052.
21. Collman, J.P., Brauman, J.I., and Suslick, K.S. (1975b). Oxygen binding to iron porphyrins. J. Am. Chem. Soc. 97, 7185-7186. doi: 10.1021/ja00857a050.
22. Collman, J.P., Bröring, M., Fu, L., Rapta, M., and Schwenninger, R. (1998). Imidazole acid chlorides: preparation and application in the syntheses of biomimetic heme models. J. Org. Chem. 63, 8084-8085. doi: 10.1021/jo981835j.
23. Collman, J.P., and Decréau, R.A. (2008). Functional models for the active site in the respiratory enzyme cytochrome c oxidase; catalytic reactions with dioxygen. Chem. Commun. 41, 5065-5076. doi: 10.1039/b808070b.
24. Collman, J.P., Decréau, R.A., and Costanzo, S. (2004c). Appending a tris-imidazole ligand with a Tyr(244) mimic on the distal face of bromoacetamidoporphyrin. Org. Lett. 6, 1033-1036. doi: 10.1021/ol049912m.
25. Collman, J.P., Decréau, R.A., Dey, A., and Yang, Y. (2009a). Water may inhibit oxygen binding in hemoprotein models. Proc. Natl. Acad. Sci. U.S.A. 106, 4101-4105. doi: 10.1073/pnas.0900893106.
26. Collman, J.P., Decréau, R.A., Lin, H., Hosseini, A., Yang, Y., Dey, A., et al. (2009c). Role of a distal pocket in the catalytic O2 reduction by cytochrome c oxidase models immobilized on inter-digitated array electrodes. Proc. Natl. Acad. Sci. U.S.A. 106, 7320-7323. doi: 10.1073/pnas.0902285106.
27. Collman, J.P., Decréau, R.A., and Sunderland, C. (2006b). Single-turnover intermolecular reaction between a FeIII-superoxide-CuI cytochrome c oxidase model and exogeneous Tyr244 mimics. Chem. Commun. 37, 3894-3896. doi: 10.1039/b607277a.
28. Collman, J.P., Decréau, R.A., Yan, Y., Yoon, J., and Solomon, E.I. (2007a). Intramolecular single-turnover reaction in a cytochrome c oxidase model bearing a Tyr244 mimic. J. Am. Chem. Soc. 129, 5794-5795. doi: 10.1021/ja0690969.
29. Collman, J.P., Decréau, R.A., and Zhang, C. (2004b). Synthesis of cytochrome c oxidase models bearing a Tyr244 mimic. J. Org. Chem. 69, 3546-3549. doi: 10.1021/jo0499625.
30. Collman, J.P., Devaraj, N.K., and Chidsey, C.E. D. (2004d). "Clicking" functionality onto electrode surfaces. Langmuir 20, 1051-1053. doi: 10.1021/la0362977.
31. Collman, J.P., Devaraj, N.K., Decréau, R.A., Yang, Y., Yan, Y., Ebina, W., et al. (2007b). A Functional mimic of cytochrome c oxidase selectively reduces oxygen by four electrons under rate-limiting electron flux: the role of CuB and Tyr-244. Science 315, 1565-1568. doi: 10.1126/science.1135844.
32. Collman, J.P., Devaraj, N.K., Eberspacher, T.A., and Chidsey, C.E. D. (2006a). Mixed azide-terminated monolayers: a platform for modifying electrode surfaces. Langmuir 22, 2457-2464. doi: 10.1021/la052947q.
33. Collman, J.P., Dey, A., Decréau, R.A., and Yang, Y. (2008a). Model studies of azide binding to functional analogues of CcO. Inorg. Chem. 47, 2916-2918. doi: 10.1021/ic702294n.
34. Collman, J.P., Dey, A., Decreau, R.A., Yang, Y., Hosseini, A., and Solomon, E.I. (2008c). Interaction of nitric oxide with a functional model of cytochrome c oxidase. Proc. Natl. Acad. Sci. U.S.A. 105, 9892-9896. doi: 10.1073/pnas.0804257105.
35. Collman, J.P., Dey, A., Yang, Y., Decréau, R.A., Ohta, T., and Solomon, E.I. (2008d). Intermediates involved in the two electron reduction of NO to N2O by a synthetic functional model of heme containing bacterial NO reductase. J. Am. Chem. Soc. 130, 16498-16499. doi: 10.1021/ja807700n.
36. Collman, J.P., and Fu, L. (1999). Synthetic models for hemoglobin and myoglobin. Acc. Chem. Res. 32, 455-463. doi: 10.1021/ar9603064.
37. Collman, J.P., Fu, L., Herrmann, P.C., and Zhang, X. (1997a). A functional model related to cytochrome c oxidase and its electrocatalytic four-electron reduction of O2. Science 275, 949-951. doi: 10.1126/science.275.5302.949.
38. Collman, J.P., Fu, L., Zingg, A., and Diederich, F. (1997b). Dioxygen and carbon monoxide binding in dendritic iron(II)porphyrins. Chem Commun. 2, 193-194. doi: 10.1039/a607413h.
39. Collman, J.P., Gagne, R.R., Halbert, T.R., Marchon, J.C., and Reed, C.A. (1973). Reversible oxygen adduct formation in ferrous complexes derived from a picket fence porphyrin model for oxy myoglobin. J. Am. Chem. Soc. 95, 7868-7870. doi: 10.1021/ja00804a054.
40. Collman, J.P., Gagne, R.R., and Reed, C.A. (1974). A paramagnetic dioxygen complex of iron II derived from a picket fence porphyrin further models for hemoproteins. J. Am. Chem. Soc. 96, 2629-2631. doi: 10.1021/ja00815a060.
41. Collman, J.P., Gagne, R.R., Reed, C., Halbert, T.R., Lang, G., and Robinson, W.T. (1975a). Picket-fence porphyrins. Synthetic Models for Oxygen Binding Hemoproteins. J. Am. Chem. Soc. 97, 1427-1439. doi: 10.1021/ja00839a026.
42. Collman, J.P., Gosh, S., Dey, A., and Decréau, R.A. (2009d). Using a functional enzyme model to understand the chemistry behind hydrogen sulfide induced hibernation. Proc. Natl. Acad. Sci. U.S.A. 106, 22090-22095. doi: 10.1073/pnas.0904082106.
43. Collman, J.P., Gosh, S., Dey, A., Decréau, R.A., and Yang, Y. (2009b). Catalytic oxidation of cytochrome c by O2 using a synthetic functional model of cytochrome c oxidase. J. Am. Chem. Soc. 131, 5034-5035. doi: 10.1021/ja9001579.
44. Collman, J.P., Herrmann, P.C., Boitrel, B., Zhang, X., Eberspacher, T.A., Fu, L., et al. (1994). Synthetic analog for the oxygen binding site in cytochrome c oxidase. J. Am. Chem. Soc. 116, 9783-9784. doi: 10.1021/ja00100a067.
45. Collman, J.P., Herrmann, P.C., Tyvoll, D.A., Decreau, R.A., Bull, B.S., and Barile, C.J. (2011). Reducing Platelet Activation, Aggregation and Platelet-Stimulated Thrombosis or Blood Coagulation by Reducing Mitochondrial Respiration. US Patent; USPTO Application: 20110301180: Stanford, CA.
46. Collman, J.P., Sunderland, C.J., Berg, K.E., Vance, M.A., and Solomon, E.I. (2003). Spectroscopic evidence for a heme-superoxide/Cu(I) intermediate in a functional model of cytochrome c oxidase. J. Am. Chem. Soc. 125, 6648-6649. doi: 10.1021/ja034382v.
47. Collman, J.P., Sunderland, C.J., and Boulatov, R. (2002). Biomimetic studies of terminal oxidases: trisimidazole picket metalloporphyrins. Inorg. Chem. 41, 2282-2291. doi: 10.1021/ic011191p.
48. Collman, J.P., Yang, Y., Dey, A., Decréau, R.A., Ghosh, S., Otah, T., et al. (2008b). A functional nitric oxide reductase model. Proc. Natl. Acad. Sci. U.S.A. 105, 15660-15665. doi: 10.1073/pnas.0808606105.
49. Cooper, C.E., and Brown, G.C. (2008). The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J. Bionenerg. Biomembr. 40, 533-539. doi: 10.1007/s10863-008-9166-6.
50. Decreau, R.A., Collman, J.P., and Hosseini, A. (2010). Electrochemical applications. How click chemistry brought biomimetic models to the next level: electrocatalysis under controlled rate of electron transfer. Chem. Soc. Rev. 39, 1291-1301. doi: 10.1039/b901972n.
51. Decréau, R.A., Collman, J.P., Yang, Y., Yan, Y., and Devaraj, N.K. (2007). Syntheses of hemoprotein models that can be covalently attached onto electrode surfaces by click chemistry. J. Org. Chem. 72, 2794-2802. doi: 10.1021/jo062349w.
52. Degli Esposti, M. (1998). Inhibitors of NADH-ubiquinone reductase: an overview. Biochim. Biophys. Acta 1364, 222-235. doi: 10.1016/S0005-2728(98)00029-2.
53. Devaraj, N.K., Decreau, R.A., Ebina, W., Collman, J.P., and Chidsey, C.E. D. (2006). Rate of interfacial electron transfer through the 1,2,3-triazole linkage. J. Phys. Chem. B 110, 15955-15962. doi: 10.1021/jp057416p.
54. Dorman, D.C., Moulin, F.J., McManus, B.E., Mahle, K.C., James, R.A., and Struve, M.F. (2002). Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol. Sci. 65, 18-25. doi: 10.1093/toxsci/65.1.18.
55. Enemark, J.H., and Feltham, R.D. (1974). Principles of structure, bonding, and reactivity for metal nitrosyl complexes. Coord. Chem. Rev. 13, 339-406. doi: 10.1016/S0010-8545(00)80259-3.
56. Ferguson-Miller, S., and Babcock, G.T. (1996). Heme/copper terminal oxidases. Chem. Rev. 96, 2889-2907. doi: 10.1021/cr950051s.
57. Ford, P.C., and Lorkovic, I.M. (2002). Mechanistic aspects of the reactions of nitric oxide with transition-metal complexes. Chem. Rev. 102, 993-1017. doi: 10.1021/cr0000271.
58. Ghafourifar, P., and Richter, C. (1997). Nitric oxide synthase activity in mitochondria. FEBS Lett. 418, 291-296. doi: 10.1016/S0014-5793(97)01397-5.
59. Giulivi, C., Poderoso, J.J., and Boveris, A. (1998). Production of nitric oxide by mitochondria. J. Biol. Chem. 273, 11038-11043. doi: 10.1074/jbc.273.18.11038.
60. Gross, E.G., and Featherstone, R.M. (1946). Studies with tetrazole derivatives; some pharmacologic properties of 1,5-disubstituted tetrazoles. J. Pharmacol. Exp. Ther. 87, 299-305.
61. Harmoning, D.M. (2009). Clinical Hematology and Fundamentas of Hemostasis, 5th Edn. Philadelphia: FA Davis.
62. Hartle, M.D., Sommer, S.K., Dietrich, S.R., and Pluth, M.D. (2014). Chemically reversible reactions of hydrogen sulfide with metal phthalocyanines. Inorg. Chem. 53, 7800-7802. doi: 10.1021/ic500664c.
63. Heldmaier, G., Ortmann, S., and Elvert, R. (2004). Natural hypometabolism during hibernation and daily torpor in mammals. Respir. Physiol. Neurobiol. 141, 317-329. doi: 10.1016/j.resp.2004.03.014.
64. Hill, B.C., Brittain, T., Eglinton, D.G., Gadsby, P.M., Greenwood, C., Nicholls, P., et al. (1984). Low-spin ferric forms of cytochrome-a3 in mixed-ligand and partially reduced cyanide-bound derivatives of cytochrome c oxidase. Biochem. J. 224, 591-600.
65. Hillman, R., Ault, K., Leporrier, M., and Rinder, H. (2005). Hematology in Clinical Practice, 4th Edn. Columbus, OH: McGraw-Hill.
66. Hosseini, A., Barile, C.J., Devadoss, A., Eberspacher, T.A., Decreau, R.A., and Collman, J.P. (2011). Hybrid bilayer membrane: a platform to study the role of proton flux on the efficiency of oxygen reduction by a molecular electrocatalyst. J. Am. Chem. Soc. 133, 11100-11102. doi: 10.1021/ja204418j.
67. Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. (1995). Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660-669. doi: 10.1038/376660a0.
68. Jobe, S.M., Wilson, K.M., Leo, L., Raimondi, A., Molkentin, J.D., Lentz, S.R., et al. (2008). Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood 111, 1257-1265. doi: 10.1182/blood-2007-05-092684.
69. Johnson, D., and Lardy, H. (1967). Isolation of liver or kidney mitochondria. Methods Enzymol. 10, 94-96. doi: 10.1016/0076-6879(67)10018-9.
70. Khan, A.A., Schuler, M.M., Prior, M.G., Yong, S., Coppock, R.W., Florence, L.Z., et al. (1990). Effects of hydrogen-sulfide exposure on lung mitochondrial respiratory-chain enzymes in rats. Toxicol. Appl. Pharmacol. 103, 482-490. doi: 10.1016/0041-008X(90)90321-K.
71. Kieber-Emmons, M.T., Qayyum, M.F., Li, Y., Halime, Z., Hodgson, K.O., Hedman, B., et al. (2012). Spectroscopic elucidation of a new heme/copper dioxygen structure type: implications for O-O bond rupture in cytochrome c oxidase. Angew. Chem. Int. Ed. 51, 168-172. doi: 10.1002/anie.201104080.
72. Kojima, N., and Palmer, G. (1983). Further characterization of the potentiometric behavior of cytochrome oxidase cytochrome a stays low spin during oxidation and reduction. J. Biol. Chem. 258, 14908-14913.
73. Kolb, H.C., Finn, M.G., and Sharpless, K.B. (2001). Click chemistry: diverse chemical function from a few good reactions. Angew. Chem. Int. Ed. 40, 2004-2021. doi: 10.1002/1521-3773(20010601)40:11<2004::AID-ANIE2004>3.0.CO;2-5.
74. Koppenol, W.H., Kissner, R., and Beckman, J.S. (1996). Syntheses of peroxynitrite: to go with the flow or on solid grounds? Methods Enzymol. 269, 296-302. doi: 10.1016/S0076-6879(96)69030-2.
75. Kuehn, C.G., and Taube, H. (1976). Ammineruthenium complexes of hydrogen sulfide and related sulfur ligands. J. Am. Chem. Soc. 98, 689-702. doi: 10.1021/ja00419a010.
76. Lee, C.C. (2008). Is human hibernation possible? Annu. Rev. Med. 59, 177-186. doi: 10.1146/annurev.med.59.061506.110403.
77. Levich, V.G. (1962). Physiochemical Hydrodynamics. Englewood Cliffs, NJ: Prentice-Hall.
78. Liu, J.G., Naruta, Y., and Tani, F. (2005). A functional model of the cytochrome c oxidase active site: unique conversion of a heme-mu-peroxo-Cu-II intermediate into heme-superoxo/Cu-I. Angew. Chem. Int. Ed. 44, 1836-1840. doi: 10.1002/anie.200462582.
79. Lowicka, E., and Beltowski, J. (2007). Hydrogen sulfide (H2S) - the third gas for interest for pharmacologists. Pharmacol. Rep. 59, 4-24.
80. Ludwig, B., Bender, E., Arnold, S., Hüttemann, M., Lee, I., and Kadenbach, B. (2001). Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chembiochem. 2, 392-403. doi: 10.1002/1439-7633(20010601)2:6<392::AID-CBIC392>3.0.CO;2-N.
81. Ma, Y., Su, H., Kuang, X., Li, X., Zhang, T., and Tang, B. (2014). Heterogeneous nano metal-organic framework fluorescence probe for highly selective and sensitive detection of hydrogen sulfide in living cells. Anal. Chem. 86, 11459-11463. doi: 10.1021/ac503622n.
82. MacMillan, F., Kannt, A., Behr, J., Prisner, T., and Michel, H. (1999). Direct evidence for a tyrosine radical in the reaction of cytochrome c oxidase with hydrogen peroxide. Biochemistry 38, 9179-9184. doi: 10.1021/bi9911987.
83. Makino, R., Matsuda, H., Obayashi, E., Shiro, Y., Iizuka, T., and Hori, H. (1999). EPR characterization of axial bond in metal center of native and cobalt-substituted guanylate cyclase. J. Biol. Chem. 274, 7714-7723. doi: 10.1074/jbc.274.12.7714.
84. Masters, B.S., Kamin, H., Gibson, Q.H., and Williams, C.H., Jr. (1965). Studies on the mechanism of microsomal triphosphopyridine nucleotide-cytochrome c reductase. J. Biol. Chem. 240, 915-920.
85. McCleverty, J.A. (2004). Chemistry of nitric oxide relevant to biology. Chem. Rev. 104, 403-418. doi: 10.1021/cr020623q.
86. Miljkovic, J.L., Kenkel, I., Ivanovic-Burmazovic, I., and Filipovic, M.R. (2013). Generation of HNO and HSNO from nitrite by heme-iron-catalyzed metabolism with H2S, Angew. Chem. Int. Ed. 52, 12061-12064. doi: 10.1002/anie.201305669.
87. Miner, K.D., Mukherjee, A., and Gao, Y.-G. (2012). A designed functional metalloenzyme that reduces O2 to H2O with over one thousand turnovers. Angew. Chem. Int. Ed. 51, 5589-5592. doi: 10.1002/anie.201201981.
88. Mizojiri, K., Norikura, R., Takashima, A., Tanaka, H., Yoshimori, T., Inazawa, K., et al. (1987). Disposition of moxalactam and N-methyltetrazolethiol in rats and monkeys. Antimicrob. Agents Chemother. 31, 1169-1176. doi: 10.1128/AAC.31.8.1169.
89. Momenteau, M., and Reeds, C. (1994). Synthetic heme-dioxygen complexes. Chem. Rev. 94, 659-698. doi: 10.1021/cr00027a006.
90. Muladige, D.C. (1994). Binding and Activation of small molecules by Ruthenium Complexes Containing a Chelated Aminophosphine Ligand. Ph. D. thesis, University of British Colombia, Vancouver, Canada.
91. Nicholls, P., and Kim, J.K. (1982). Sulfide as an inhibitor and electron-donor for the cytochrome c oxidase system. Can. J. Biochem. 60, 613-623. doi: 10.1139/o82-076.
92. O'Neal, C., Sargent, E., and Bagdon, W. (1978). Acute toxicologic evaluation of 4-methylthiazole. J. Am. Coll. Toxicol. 1, 182-183.
93. Otterbein, L.E., Soares, M.P., Yamashita, K., and Bach, F.H. (2003). Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24, 449-455. doi: 10.1016/S1471-4906(03)00181-9.
94. Palmieri, F., and Klingenberg, M. (1967). Inhibition of respiration under the control of azide uptake by mitochondria. Eur. J. Biochem. 1, 439-446. doi: 10.1111/j.1432-1033.1967.tb00093.x.
95. Pappas, J.M., Westengard, J.C., and Bull, B.S. (1994). Population variability in the effect of aspirin on platelet function. Implications for clinical trials and therapy. Arch. Pathol. Lab. Med. 118, 801-804.
96. Pavlik, J.W., Noll, B.C., Oliver, A.G., Schulz, C.E., and Scheidt, W.R. (2010). Hydrosulfide (HS-) coordination in iron porphyrinates. Inorg. Chem. 49, 1017-1026. doi: 10.1021/ic901853p.
97. Pearce, L.L., Bominaar, E.L., Hill, B.C., and Peterson, J. (2003). Reversal of cyanide inhibition of cytochrome c oxidase by the auxillary substrate nitric oxide: an endogenous antidote to cyanide poisening? J. Biol. Chem. 278, 52139-52145. doi: 10.1074/jbc.M310359200.
98. Pearce, L.L., Kanai, A.J., Birder, L.A., Pitt, B.R., and Peterson, J. (2002). The catabolic fate of nitric oxide: the nitric oxide oxidase and peroxynitrite reductase activities of cytochrome oxidase. J. Biol. Chem. 277, 13556-13562. doi: 10.1074/jbc.m109838200.
99. Pearce, L.L., Lopez Manzano, E., Martinez-Bosch, S., and Peterson, J. (2008). Antagonism of nitric oxide toward the inhibition of cytochrome c oxidase by carbon monoxide and cyanide. Chem. Res. Toxicol. 21, 2073-2081. doi: 10.1021/tx800140y.
100. Petersen, L. (1977). The effect of inhibitors on the oxygen kinetics of cytochrome c oxidase. Biochim. Biophys. Acta 460, 299-307. doi: 10.1016/0005-2728(77)90216-X.
101. Proshlyakov, D.A., Pressler, M.A., and Babcock, G.T. (1998). Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase. Proc. Natl. Acad. Sci. U.S.A. 95, 8020-8025. doi: 10.1073/pnas.95.14.8020.
102. Proshlyakov, D.A., Pressler, M.A., DeMaso, C., Leykam, J.F., DeWitt, D.L., and Babcock, G.T. (2000). Oxygen activation and reduction in respiration: involvement of redox-active tyrosine 244. Science 290, 1588-1591. doi: 10.1126/science.290.5496.1588.
103. Remenyi, G., Szasz, R., Friese, P., and Dale, G.L. (2005). Role of mitochondrial permeability transition pore in coated-platelet formation. Arterioscler. Thromb. Vasc. Biol. 25, 467-471. doi: 10.1161/01.ATV. 0000152726.49229.bf.
104. Salganicoff, L., and Fukami, M.H. (1972). Energy metabolism of blood platelets. I. Isolation and properties of platelet mitochondria. Arch. Biochem. Biophys. 153, 726-735. doi: 10.1016/0003-9861(72)90391-8.
105. Sellman, D., Lechner, P., Knoch, F., and Moll, M. (1991). Proof of strong S-H- S bridges in [Ru(SH2)(PPh,)('S4')] THF, the first H2S complex characterized by X-Ray crystallography. Angew. Chem. Int. Ed. 30, 552-553. doi: 10.1002/anie.199105521.
106. Sengupta, K., Chatterjee, S., Samanta, S., and Dey, A. (2013). Direct observation of intermediates formed during steady-state electrocatalytic O2 reduction by iron porphyrins. Proc. Natl. Acad. Sci. U.S.A. 110, 8431-8436. doi: 10.1073/pnas.1300808110.
107. Sipos, I., Tretter, L., and Adam-Vizi, V. (2003). Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals. J. Neurochem. 84, 112-118. doi: 10.1046/j.1471-4159.2003.01513.x.
108. Stamler, J.S., Singel, D.J., and Loscalzo, J. (1992). Biochemistry of nitric-oxide and its redox-activated forms. Science 258, 1898-1902. doi: 10.1126/science.1281928.
109. Standbury, D.M. (1989). Reduction potentials involving inorganic free radicals in aqueous solution. Adv. Inorg. Chem. 33, 69-138.
110. Stevens, T.H., Bocian, D.F., and Chan, S.I. (1979). EPR studies of 15NO-ferrocytochrome a3 in cytochrome c oxidase. FEBS Lett. 97, 314-316. doi: 10.1016/0014-5793(79)80110-6.
111. Szabó, C. (2007). Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 6, 917-935. doi: 10.1038/nrd2425.
112. Tan, A.M., Xie, C.L., Qu, S.S., Ping, K., and Yu, G. (1996). Microcalorimetric study of mitochondria isolated from fish liver tissue. J. Biochem. Biophys. Methods 31, 189-193. doi: 10.1016/0165-022X(95)00034-O.
113. Toninello, A., Salvi, M., and Colombo, L. (2000). The membrane permeability transition in liver mitochondria of the great green goby Zosterisessor ophiocephalus (Pallas). J. Exp. Biol. 203, 3425-3434.
114. Tornøe, C.W., Christensen, C., and Meldal, M. (2002). Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 67, 3057-3064. doi: 10.1021/jo011148j.
115. Uno, T., Mogi, T., Tsubaki, M., Nishimura, Y., and Anraku, Y. (1994). Resonance Raman and Fourier transform infrared studies on the subunit I histidine mutants of the cytochrome bo complex in Escherichia coli. Molecular structure of redox metal centers. J. Biol. Chem. 269, 11912-11920.
116. Vanbuuren, K.J. H., Nicholls, P., and Van Gelder, V. (1972). Biochemical and biophysical studies on cytochrome aa3: VI, Reaction of cyanide with oxidized and reduced enzyme. Biochim. Biophys. Acta 256, 258-260. doi: 10.1016/0005-2728(72)90057-6.
117. Varotsis, C., Woodruff, W.H., and Babcock, G.T. (1990). Direct detection of a dioxygen adduct of cytochrome a3 in the mixed-valence cytochrome-oxidase dioxygen reaction. J. Biol. Chem. 265, 11131-11136.
118. Vaska, A. (1976). Dioxygen-metal complexes: toward a unified view. Acc. Chem. Res. 9, 175-183. doi: 10.1021/ar50101a002.
119. Volpato, G.P., Searles, R., Yu, B., Scherrer-Crosbie, M., Bloch, K.D., Ichinose, F., et al. (2008). Inhaled hydrogen sufide - A rapidly reversible inhibitor of cardiac and metabolic function in the mouse. Anestaesiology 108, 659-668. doi: 10.1097/ALN.0b013e318167af0d.
120. Wainio, W.W., and Greenlees, J. (1960). Complexes of cytochrome c oxidase with cyanide and carbon monoxide. Arch. Biochem. Biophys. 90, 18-21. doi: 10.1016/0003-9861(60)90605-6.
121. Walter, M.A., Spiro, T.G., Suslick, K.S., and Collman, J.P. (1980). Resonance Raman spectra of (dioxygen)(porphyrinato)(hinderedimidazole)iron(II) complexes. Implications for hemoglobin cooperativity. J. Am. Chem. Soc. 102, 6857-6858. doi: 10.1021/ja00542a037.
122. Wang, R. (2002). Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 16, 1792-1798. doi: 10.1096/fj.02-0211hyp.
123. Weinstein, R.B., and Somero, G.N. (1998). Effects of temperature on mitochondrial function in the Antartic fish Trematomus bernacchii. J. Comp. Physiol. B 168, 190-196. doi: 10.1007/s003600050136.
124. Westcott, B.L., and Enemark, J.M. (1999). "Transition metal nitrosyls," in Inorganic Electronic Structure and Spectroscopy, eds A. B. P. Lever and E. I. Solomon (New York; Chichester; Weinheim; Brisbane; Singapore; Toronto: Wiley), 403-450.
125. Wilson, S.A., Kroll, T., Decreau, R.A., Hocking, R.K., Lundberg, M., Hedman, B., et al. (2013). Iron L-Edge X-ray absorption spectroscopy of oxy-picket fence porphyrin: experimental insight into Fe-O2 bonding. J. Am. Chem. Soc. 135, 1124-1136. doi: 10.1021/ja3103583.
126. Yonetani, T., Yamamoto, H., Erman, J.E., Leigh, J.S. Jr., and Reed, G.H. (1972). Electromagnetic properties of hemoproteins: V, Optical and electron-paramagnetic resonance characteristics of nitric-oxide derivatives of metalloporphyrin-apohemoprotein complexes. J. Biol. Chem. 247, 2447-2455.
127. Yoshikawa, S., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., Yamashita, E., Inoue, N., et al. (1998). Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280, 1723-1729.
128. Yoshimura, T. (1991). 5-Coordinated and 6-coordinated nitrosyl iron(II) complexes of tetrakis (para-substituted phenyl) porphyrins: substituent effect on the EPR parameters and the NO stretching frequencies. Bull. Chem. Soc. Jpn. 64, 2819-2828. doi: 10.1246/bcsj.64.2819.