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Role of binding site loops in controlling nitric oxide release: structure and kinetics of mutant forms of nitrophorin 4.

Maes EM, Weichsel A, Andersen JF, Shepley D, Montfort WR
Biochemistry 43 6679-90 (2004)
Related entries: 1sxu, 1sxw, 1sxx, 1sy0, 1sy1, 1sy2, 1sy3

Cited: 40 times
EuropePMC logo PMID: 15157102

Abstract

Nitrophorins are ferric heme proteins that transport nitric oxide (NO) from blood-sucking insects to victims. NO binding is tighter at lower pH values, as found in the insect salivary gland, and weaker at the pH of the victim's tissue, facilitating NO release and subsequent vasodilation. Previous structural analyses of nitrophorin 4 (NP4) from Rhodnius prolixus revealed a substantial NO-induced conformational change involving the A-B and G-H loops, which rearrange to desolvate the distal pocket and pack nonpolar residues against the heme-ligated NO. Previous kinetic analyses revealed a slow, biphasic, and pH-dependent NO release, which was proposed to be associated with loop movements. In this study, we created NP4 mutants D30A and D30N (A-B loop), D129A/L130A (G-H loop), and T121V (distal pocket). Eight crystal structures were determined, including complexes with NO, NH(3), and imidazole, to resolutions as high as 1.0 A. The NO-induced conformational change is largely abolished in the loop mutants, but retained in T121V. Kinetic analyses using stopped-flow spectroscopy revealed the pH dependence for NO release is eliminated for D129A/L130A, considerably reduced for D30A and D30N, but retained for T121V. NO association rates were increased 2-5-fold for T121V, but were unchanged in the loop mutants. Taken together, our findings demonstrate that the pH dependency for NO release is linked to loop dynamics and that solvent reorganization is apparently rate-limiting for formation of the initial iron-nitrosyl bond. Interestingly, the multiphasic kinetic behavior of rNPs was not affected by mutations, and its cause remains unclear.

Articles - 1sxy mentioned but not cited (1)

  1. NMR studies of the dynamics of nitrophorin 2 bound to nitric oxide. Muthu D, Berry RE, Zhang H, Walker FA. Biochemistry 52 7910-7925 (2013)


Reviews citing this publication (1)

  1. Iron transitions during activation of allosteric heme proteins in cell signaling. Négrerie M. Metallomics 11 868-893 (2019)

Articles citing this publication (38)

  1. Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein. Weichsel A, Maes EM, Andersen JF, Valenzuela JG, Shokhireva TKh, Walker FA, Montfort WR. Proc Natl Acad Sci U S A 102 594-599 (2005)
  2. Crystal structures of the nitrite and nitric oxide complexes of horse heart myoglobin. Copeland DM, Soares AS, West AH, Richter-Addo GB. J Inorg Biochem 100 1413-1425 (2006)
  3. pH-Dependent conformational changes in proteins and their effect on experimental pK(a)s: the case of Nitrophorin 4. Di Russo NV, Estrin DA, Martí MA, Roitberg AE. PLoS Comput Biol 8 e1002761 (2012)
  4. Assignment of the ferriheme resonances of the low-spin complexes of nitrophorins 1 and 4 by (1)H and (13)C NMR spectroscopy: comparison to structural data obtained from X-ray crystallography. Shokhireva TKh, Weichsel A, Smith KM, Berry RE, Shokhirev NV, Balfour CA, Zhang H, Montfort WR, Walker FA. Inorg Chem 46 2041-2056 (2007)
  5. Ultrafast dynamics of diatomic ligand binding to nitrophorin 4. Benabbas A, Ye X, Kubo M, Zhang Z, Maes EM, Montfort WR, Champion PM. J Am Chem Soc 132 2811-2820 (2010)
  6. Effect of the N-terminus on heme cavity structure, ligand equilibrium, rate constants, and reduction potentials of nitrophorin 2 from Rhodnius prolixus. Berry RE, Shokhireva TKh, Filippov I, Shokhirev MN, Zhang H, Walker FA. Biochemistry 46 6830-6843 (2007)
  7. Allostery in recombinant soluble guanylyl cyclase from Manduca sexta. Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A, Montfort WR. J Biol Chem 283 20968-20977 (2008)
  8. pH-dependent mechanism of nitric oxide release in nitrophorins 2 and 4. Swails JM, Meng Y, Walker FA, Marti MA, Estrin DA, Roitberg AE. J Phys Chem B 113 1192-1201 (2009)
  9. Spectroscopic and functional characterization of nitrophorin 7 from the blood-feeding insect Rhodnius prolixus reveals an important role of its isoform-specific N-terminus for proper protein function. Knipp M, Yang F, Berry RE, Zhang H, Shokhirev MN, Walker FA. Biochemistry 46 13254-13268 (2007)
  10. The structure and NO binding properties of the nitrophorin-like heme-binding protein from Arabidopsis thaliana gene locus At1g79260.1. Bianchetti CM, Blouin GC, Bitto E, Olson JS, Phillips GN. Proteins 78 917-931 (2010)
  11. 1H and 13C NMR spectroscopic studies of the ferriheme resonances of three low-spin complexes of wild-type nitrophorin 2 and nitrophorin 2(V24E) as a function of pH. Yang F, Knipp M, Shokhireva TK, Berry RE, Zhang H, Walker FA. J Biol Inorg Chem 14 1077-1095 (2009)
  12. Effect of mutation of carboxyl side-chain amino acids near the heme on the midpoint potentials and ligand binding constants of nitrophorin 2 and its NO, histamine, and imidazole complexes. Berry RE, Shokhirev MN, Ho AY, Yang F, Shokhireva TK, Zhang H, Weichsel A, Montfort WR, Walker FA. J Am Chem Soc 131 2313-2327 (2009)
  13. Assignment of the ferriheme resonances of high- and low-spin forms of the symmetrical hemin-reconstituted nitrophorins 1-4 by 1H and 13C NMR spectroscopy: the dynamics of heme ruffling deformations. Shokhireva TK, Shokhirev NV, Berry RE, Zhang H, Walker FA. J Biol Inorg Chem 13 941-959 (2008)
  14. Assignment of the ferriheme resonances of the high-spin forms of nitrophorins 1 and 4 by 1H NMR spectroscopy: comparison to structural data obtained from X-ray crystallography. Shokhireva TKh, Smith KM, Berry RE, Shokhirev NV, Balfour CA, Zhang H, Walker FA. Inorg Chem 46 170-178 (2007)
  15. Protonation state of Asp30 exerts crucial influence over surface loop rearrangements responsible for NO release in nitrophorin 4. Menyhárd DK, Keserü GM. FEBS Lett 579 5392-5398 (2005)
  16. Role of the NC-loop in catalytic activity and stability in lipase from Fervidobacterium changbaicum. Li B, Yang G, Wu L, Feng Y. PLoS One 7 e46881 (2012)
  17. Replacement of the axial histidine heme ligand with cysteine in nitrophorin 1: spectroscopic and crystallographic characterization. Vetter SW, Terentis AC, Osborne RL, Dawson JH, Goodin DB. J Biol Inorg Chem 14 179-191 (2009)
  18. Binding of YC-1 or BAY 41-2272 to soluble guanylyl cyclase induces a geminate phase in CO photolysis. Hu X, Feng C, Hazzard JT, Tollin G, Montfort WR. J Am Chem Soc 130 15748-15749 (2008)
  19. Oligomerization of nitrophorins. Ambrus A, Friedrich K, Somogyi A. Anal Biochem 352 286-295 (2006)
  20. Guanidine-ferroheme coordination in the mutant protein nitrophorin 4(L130R). He C, Fuchs MR, Ogata H, Knipp M. Angew Chem Int Ed Engl 51 4470-4473 (2012)
  21. Kinetics and computational studies of ligand migration in nitrophorin 7 and its Δ1-3 mutant. Oliveira A, Allegri A, Bidon-Chanal A, Knipp M, Roitberg AE, Abbruzzetti S, Viappiani C, Luque FJ. Biochim Biophys Acta 1834 1711-1721 (2013)
  22. pH-dependent picosecond structural dynamics in the distal pocket of nitrophorin 4 investigated by 2D IR spectroscopy. Cheng M, Brookes JF, Montfort WR, Khalil M. J Phys Chem B 117 15804-15811 (2013)
  23. Apo-nitrophorin 4 at atomic resolution. Amoia AM, Montfort WR. Protein Sci 16 2076-2081 (2007)
  24. Nuclear inelastic scattering and Mössbauer spectroscopy as local probes for ligand binding modes and electronic properties in proteins: vibrational behavior of a ferriheme center inside a β-barrel protein. Moeser B, Janoschka A, Wolny JA, Paulsen H, Filippov I, Berry RE, Zhang H, Chumakov AI, Walker FA, Schünemann V. J Am Chem Soc 134 4216-4228 (2012)
  25. NMR studies of nitrophorin distal pocket side chain effects on the heme orientation and seating of NP2 as compared to NP1. Shokhireva TK, Berry RE, Zhang H, Shokhirev NV, Walker FA. J Inorg Biochem 105 1238-1257 (2011)
  26. Protein dynamics of a beta-sheet protein. Schmidt M, Achterhold K, Prusakov V, Parak FG. Eur Biophys J 38 687-700 (2009)
  27. Structure and dynamics of the membrane attaching nitric oxide transporter nitrophorin 7. Knipp M, Ogata H, Soavi G, Cerullo G, Allegri A, Abbruzzetti S, Bruno S, Viappiani C, Bidon-Chanal A, Luque FJ. F1000Res 4 45 (2015)
  28. Assignment of Ferriheme Resonances for High- and Low-Spin Forms of Nitrophorin 3 by H and C NMR Spectroscopy and Comparison to Nitrophorin 2: Heme Pocket Structural Similarities and Differences. Shokhireva TK, Berry RE, Zhang H, Shokhirev NV, Walker FA. Inorganica Chim Acta 361 925-940 (2008)
  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)
  30. Native N-terminus nitrophorin 2 from the kissing bug: similarities to and differences from NP2(D1A). Berry RE, Muthu D, Shokhireva TK, Garrett SA, Zhang H, Walker FA. Chem Biodivers 9 1739-1755 (2012)
  31. Preparation of nitrophorin 7(Δ1-3) from Rhodnius prolixus without start-methionine using recombinant expression in Escherichia coli. Risse C, Taing JJ, Knipp M. Anal Biochem 451 28-30 (2014)
  32. Assignment of the 1H NMR resonances of protein residues in close proximity to the heme of the nitrophorins: similarities and differences among the four proteins from the saliva of the adult blood-sucking insect Rhodnius prolixus. Shokhireva TK, Walker FA. J Biol Inorg Chem 17 911-926 (2012)
  33. NO Scavenging through Reductive Nitrosylation of Ferric Mycobacterium tuberculosis and Homo sapiens Nitrobindins. De Simone G, di Masi A, Ciaccio C, Coletta M, Ascenzi P. Int J Mol Sci 21 E9395 (2020)
  34. Dimerization of nitrophorin 4 at low pH and comparison to the K1A mutant of nitrophorin 1. Berry RE, Yang F, Shokhireva TK, Amoia AM, Garrett SA, Goren AM, Korte SR, Zhang H, Weichsel A, Montfort WR, Walker FA. Biochemistry 54 208-220 (2015)
  35. Electrostatic Tuning of the Ligand Binding Mechanism by Glu27 in Nitrophorin 7. Abbruzzetti S, Allegri A, Bidon-Chanal A, Ogata H, Soavi G, Cerullo G, Bruno S, Montali C, Luque FJ, Viappiani C. Sci Rep 8 10855 (2018)
  36. NMR studies of the dynamics of high-spin nitrophorins: comparative studies of NP4 and NP2 at close to physiological pH. Berry RE, Muthu D, Yang F, Walker FA. Biochemistry 54 221-239 (2015)
  37. NMR investigations of nitrophorin 2 belt side chain effects on heme orientation and seating of native N-terminus NP2 and NP2(D1A). Berry RE, Muthu D, Shokhireva TK, Garrett SA, Goren AM, Zhang H, Walker FA. J Biol Inorg Chem 19 577-593 (2014)
  38. Nitric oxide delivery and heme-assisted S-nitrosation by the bedbug nitrophorin. Badgandi HB, Weichsel A, Montfort WR. J Inorg Biochem 246 112263 (2023)


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