Extreme differences between Hemoglobins I and II of the Clam Lucina pectinalis in their reactions with nitrite

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 10, 2010, Pages 1988-1995

  Bonaventura, Celia ^a   Henkens, Robert ^a,d   De Jesus Bonilla, Walleska ^b   Lopez Garriga, Juan ^b   Jia, Yiping ^c   Alayash, Abdu I ^b   Siburt, Claire J Parker ^d   Crumbliss, Alvin L ^d  

^a DUKE UNIVERSITY MARINE LABORATORY   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

Adaptations; Dynamics; Heme accessibility; Heme oxidation; Hemoglobin; Nitrite

Indexed keywords

HEME; HEMOGLOBIN DERIVATIVE; HEMOGLOBIN I; HEMOGLOBIN II; NITRITE; OXYGEN; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ARTICLE; CLAM; HYDROGEN BOND; LUCINA PECTINALIS; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; OXYGEN AFFINITY; PRIORITY JOURNAL; THERMODYNAMICS;

ANIMALS; BINDING SITES; BIVALVIA; HEME; HEMOGLOBINS; HUMANS; HYDROGEN BONDING; KINETICS; NITRITES; OXIDATION-REDUCTION; OXYGEN;

BIVALVIA; LUCINA;

EID: 77956060006     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.06.016     Document Type: Article

References (38)

1. Keszler A., Piknova B., Schechter A.N., Hogg N. The reaction between nitrite and oxyhemoglobin: a mechanistic study. J. Biol. Chem. 2008, 283:9615-9622.
2. Kosaka H., Imaizumi K., Tyuma I. Mechanism of autocatalytic oxidation of oxyhemoglobin by nitrite. An intermediate detected by electron spin resonance. Biochim. Biophys. Acta 1982, 702:237-241.
3. Kosaka H., Tyuma I. Production of superoxide anion by N, N-bis(2-hydroxyethyl)-iminotris(hydroxymethyl)methane buffer during oxidation of oxyhemoglobin by nitrite and effect of inositol hexaphosphate on the oxidation. Biochim. Biophys. Acta 1982, 709:187-193.
4. Doyle M.P., Pickering R.A., Dykstra R.L., Nelson C.L., Boyer R.F. Involvement of peroxide and superoxide in the oxidation of hemoglobin by nitrite. Biochem. Biophys. Res. Commun. 1982, 105:127-132.
5. Lissi E. Autocatalytic oxidation of hemoglobin by nitrite: a possible mechanism. Free Radic. Biol. Med. 1988, 24:1535-1536.
6. Brooks J. Action of nitrite on hemoglobin in the absence of oxygen. Proc. R. Soc. Med. 1937, 123:368-382.
7. Doyle M.P., Pickering R.A., DeWeert T.M., Hoekstra J.W., Pater D. Kinetics and mechanism of the oxidation of human deoxyhemoglobin by nitrites. J. Biol. Chem. 1981, 256:12393-12398.
8. Gladwin M.T., Schechter A.N., Kim-Shapiro D.B., Patel R.P., Hogg N., Shiva S., Cannon R.O., Kelm M., Wink D.A., Espey M.G., Oldfield E.H., Pluta R.M., Freeman B.A., Lancaster J.R., Feelisch M., Lundberg J.O. The emerging biology of the nitrite anion. Nat. Chem. Biol. 2005, 1:308-314.
9. Crawford J.T., Scott I.T., Huang Z., Shiva S., Chacko B., Schechter A.N., Darley-Usmar V., Kerby J., Lang J., Kraus D., Ho C., Gladwin M.T., Patel R. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 2006, 107:566-574.
10. Cosby K., Partovi K.S., Crawford J.H., Patel R.P., Reiter C.D., Martyr S., Yang B.K., Waclawiw M.A., Zalos G., Xu X., Huang K.T., Shields H., Kim-Shapiro D.B., Schechter A.N., Cannon R.O., Gladwin M.T. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat. Med. 2003, 9:1498-1505.
11. Angelo M., Singel D.J., Stamler J.S. An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc. Natl Acad. Sci. 2006, 103:8366-8371.
12. van Faassen E.E., Bahrami S., Feelisch M., Hogg N., Kelm M., Kim-Shapiro D.B., Kozlov A.V., Li H., Lundberg J.O., Mason R., Nohl H., Rassaf T., Samouilov A., Slama-Schwok A., Shiva S., Vanin A.F., Weitzberg E., Zweier J., Gladwin M.T. Nitrite as regulator of hypoxic signaling in mammalian physiology. Med. Res. Rev. 2009, 29:683-741.
13. Nagababu E., Ramasamy S., Abernethy D.R., Rifkind J.M. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J. Biol. Chem. 2003, 278:46349-46356.
14. Salgado M.T., Nagababu E., Rifkind J.M. Quantification of intermediates formed during the reduction of nitrite by deoxyhemoglobin. J. Biol. Chem. 2009, 284:12710-12718.
15. Bonaventura C., Henkens R., Alayash A.I., Crumbliss A.L. Allosteric effects on oxidative and nitrosative reactions of cell-free hemoglobins. IUBMB Life 2007, 59:498-506.
16. Bonaventura C., Henkens R., Weaver K.D., Alayash A.I., Crumbliss A.L. Chapter 9. Protein Reviews Volume 9 2008, Springer, Verlag. M. Bolognesi, G. di Prisco, C. Verde (Eds.).
17. Kraus D.W., Wittenberg J.B. Hemoglobins of the Lucina pectinata/bacteria symbiosis. I. Molecular properties, kinetics and equilibria of reactions with ligands. J. Biol. Chem. 1990, 265:16043-16053.
18. Gavira J.A., Camara-Artigas A., De Jesús-Bonilla W., López-Garriga J., Lewis A., Pietri R., Yeh S.-R., Cadilla C.L., García-Ruiz J.M. Structure and ligand selection of hemoglobin II from Lucina pectinata. J. Biol. Chem. 2008, 283:9414-9423.
19. Rizzi M., Wittenberg J., Coda A., Ascenzi P., Bolognesi M. Structural bases for sulfide recognition in Lucina pectinata hemoglobin. J. Mol. Biol. 1996, 258:1-5.
20. Pietri R., Granell L., Cruz A., De Jesús-Bonilla W., Lewis A., Leon R., Cadilla C.L., López-Garriga J. Tyrosine B10 and heme-ligand interactions of Lucina pectinata hemoglobin II: control of heme reactivity. Biochim. Biophys. Acta 2005, 1747:195-203.
21. De Jesús-Bonilla W., Jia Y., Alayash A.I., López-Garriga J. The heme pocket geometry of Lucina pectinata hemoglobin II restricts nitric oxide and peroxide entry: model of ligand control for the design of a stable oxygen carrier. Biochemistry 2007, 46:10451-10460.
22. Kiese M. Methemoglobinemias: A Comprehensive Treatise 1974, CRC Press Inc., Cleveland.
23. Stewart V. Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol. Rev. 1988, 52:190-232.
24. Hentschel U., Hand S.C., Felbeck H. The contribution of nitrate respiration to the energy budget of the symbiont-containing clam Lucinoma aequizonata: a calorimetric study. J. Exp. Biol. 1996, 199:427-433.
25. Bonaventura C., Ferruzzi G., Tesh S., Stevens R.D. Effects of s-nitrosation on oxygen binding by normal and sickle cell hemoglobin. J. Biol. Chem. 1999, 274:24742-24748.
26. Pietri R., Lewis A., Leon R.G., Casabona G., Kiger L., Yeh S., Fernandez-Alberti S., Marden M.C., Cadilla C.L., Lopez-Garriga J. Factors Controlling the Reactivity of Hydrogen Sulfide with Hemeproteins. Biochemistry 2009, 48:4881-4894.
27. Leon R.G., Munier-Lehmann H., Barzu O., Baudin-Creuza V., Pietri R., López-Garriga J., Cadilla C.L. High-level production of recombinant sulfide-reactive hemoglobin I from Lucina pectinata in Escherichia coli. Protein Expr. Purif. 2004, 38:184-195.
28. Riggs A.F., Wolbach R.A. Sulfhydryl groups and the structure of hemoglobin. J. Gen. Physiol. 1956, 39:585-605.
29. Faulkner K.M., Bonaventura C., Crumbliss A.L. A spectroelectrochemical method for evaluating factors which regulate the redox potential of hemoglobins. Inorg. Chim. Acta 1994, 226:187-194.
30. Taboy C.H., Bonaventura C., Crumbliss A.L. Anaerobic oxidations of myoglobin and hemoglobin by spectroelectrochemistry. Methods in enzymology: redox cell biology and genetics Part B Volume 353 2002, 187-209. Academic Press, New York. C.K. Sen, L. Packer (Eds.).
31. Fago A., Crumbliss A.L., Peterson J., Pearce J.L., Bonaventura C. The case of the missing NO-hemoglobin: spectral changes suggestive of heme redox reactions reflect changes in NO-heme geometry. Proc. Natl Acad. Sci. 2003, 100:12087-12092.
32. Taboy C.H., Faulkner K.M., Kraiter D., Bonaventura C., Crumbliss A.L. Concentration-dependent effects of anions on the anaerobic oxidation of hemoglobin and myoglobin. J. Biol. Chem. 2000, 275:39048-39054.
33. Weber R.E., Vinogradov S.N. Non-vertebrate hemoglobins: functions and molecular adaptations. Physiol. Rev. 2001, 81:596-628.
34. Doyle M.P., Lepoire D.M., Pickering R.A. Oxidation of hemoglobin and myoglobin by alkyl nitrites: inhibition by oxygen. J. Biol. Chem. 1981, 256:12399-12404.
35. Gow A.J., Payson A.P., Bonaventura J. Invertebrate hemoglobins and nitric oxide: how heme pocket structure controls reactivity. J. Inorg. Biochem. 2005, 99:903-911.
36. Crawford M.J., Goldberg D.E. Role for the salmonella flavohemoglobin in protection from nitric oxide. J. Biol. Chem. 1998, 273:12543-12547.
37. Roche C.J., Dantsker D., Samuni U., Friedman J.M. Nitrite reductase activity of sol-gel-encapsulated deoxyhemoglobin: influence of quaternary and tertiary structure. J. Biol. Chem. 2006, 281:38757-38768.
38. Rogers M.S., Brocknor B., Cashon R.E., Alayash A.I. Effects of polymerization on the oxygen carrying and redox properties of diaspirin cross-linked hemoglobin. Biochim. Biophys. Acta 1995, 1248:135-142.