Effect of the N-terminus on heme cavity structure, ligand equilibrium, rate constants, and reduction potentials of nitrophorin 2 from Rhodnius prolixus

Biochemistry

Volumn 46, Issue 23, 2007, Pages 6830-6843

  Berry, Robert E ^a   Shokhireva, Tatiana Kh ^a   Filippov, Igor ^a   Shokhirev, Maxim N ^a   Zhang, Hongjun ^a   Walker, F Ann ^a  

^a University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYANIDE COMPLEXES; REDUCTION POTENTIALS; RHODNIUS PROLIXUS; TERMINAL AMINO ACID;

CHEMICAL SHIFT; LIGANDS; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHASE EQUILIBRIA; RATE CONSTANTS; REDUCTION;

PROTEINS;

1 METHYLIMIDAZOLE; ALANINE; AMINO ACID; CYANIDE; HEME; HEMIN; HISTAMINE; IMIDAZOLE; INSECT PROTEIN; LIGAND; METHIONINE; MUTANT PROTEIN; NITROPHORIN 2; OXYGEN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; ESCHERICHIA COLI; ISOMER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REDUCTION; RHODNIUS; RHODNIUS PROLIXUS;

AMINO ACID SEQUENCE; ANIMALS; HEME; HEMEPROTEINS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RHODNIUS; SALIVARY PROTEINS;

RHODNIUS PROLIXUS;

EID: 34250177977     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7002263     Document Type: Article

References (52)

1. Ribeiro, J. M. C. Hazzard, J. M. H., Nussenzveig, R., Champagne, D., and Walker, F. A. (1993) Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect, Science 260, 539-541.
2. Champagne, D. E., Nussenzveig, R. H., and Ribeiro, J. M. C. (1995) Purification, partial characterization, and cloning of nitric oxide-carrying heme proteins (nitrophorins) from salivary glands of the blood-sucking insect Rhodnius prolixus, J. Biol. Chem. 270, 8691-8695.
3. Walker, F. A., Ribeiro, J. M. C., and Montfort, W. R. (1999) Novel NO-Liberating Heme Proteins from the Saliva of Blood-Sucking Insects, in Metal Ions in Biological Systems, Vol. 36, Interrelations between Free Radicals and Metal Ions in Life Processes (Sigel, H., and Sigel, A., Eds.) pp 619-661, Marcel Dekker, New York.
4. Walker, F. A., and Montfort, W. R. (2001) Nitric Oxide-Releasing Heme Proteins from the Saliva of the Blood-Sucking Insect Rhodnius prolixus, in Advances in Inorganic Chemistry (Mauk, A. G., and Sykes, A. G., Eds.) Vol. 51, Chapter 5. pp 295-358. Academic Press, San Diego, CA.
5. 6 complex, J. lnorg. Biochem. 99, 216-236.
6. Moreira, M. F., Coelho, H. S., Zingali, R. B., Oliveira, P. L., and Masuda, H. (2003) Changes in salivary nitrophorin profile during the life cycle of the blood-sucking bug Rhodnius prolixus, Insect Biochem. Mol. Biol. 33, 23-28.
7. Andersen, J. F., Guddena, N., Francischetti, I. M. B., Valenzuela, J. G., and Ribeiro, J. M. C. (2005) Recognition of anionic-phospholipid membranes by an antihemostatic protein from a blood-feeding insect, Biochemistry 43, 6987-6994.
8. Valenzuela, J. G., Walker, F. A., and Ribeiro, J. M. C. (1995) A salivary nitrophorin (nitric-oxide-canying hemoprotein) in the bedbug Cimex lectularius, J. Exp. Biol. 198, 1519-1526.
9. Weichsel, A., Maes, E. M., Andersen, J. F., Valenzuela, J. G., Shokhireva, T. Kh., Walker, F. A., and Montfort, W. R. (2005) Heme-assisted nitrosothiolation of a proximal thiol in a nitric oxide transport protein, Proc. Natl. Acad. Sci. U.S.A. 102, 594-599.
10. Ribeiro, J. M. C. and Nussenzveig, R. H. (1993) Nitric oxide synthase activity from a hematophagous insect salivary gland, FEBS Lett. 330, 165-168.
11. Nussenzveig, R. H., Bentley, D. L., and Ribeiro, J. M. C. (1995) Ultrastructural localization of the salivary diaphorase of Rhodnius prolixus, J. Exp. Biol. 198, 1093-1098.
12. Yuda, M., Hirai, M., Miura, K., Matsumura, H., Ando, K., and Chinzei, Y. (1996) cDNA cloning, expression and characterization of nitric-oxide synthase from the salivary glands of the blood-sucking insect Rhodnius prolixus, Eur. J. Biochem. 242, 807-812.
13. Ribeiro, J. M. C. and Walker, F. A. (1994) High affinity histamine-binding and antihistaminic activity of the salivary nitric oxide-carrying heme protein (nitrophorin) of Rhodnius prolixus, J. Exp. Med. 180, 2251-2257.
14. Ding, X. D., Weichsel, A., Andersen, J. F., Shokhireva, T. Kh., Balfour, C., Pierik, A. J., Averill, B. A., Montfort, W. R., and Walker, F. A. (1999) Nitric oxide binding to the ferri- and ferroheme states of nitrophorin 1, a reversible NO-binding heme protein from the saliva of a blood-sucking insect, Rhodnius prolixus, J. Am. Chem. Soc. 121, 128-138.
15. Maes, E. M., Walker, F. A., Montfort, W. R., and Czernuszewicz, R. S. (2001) A resonance Raman spectroscopic study of nitrophorin 1, a nitric oxide-binding heme protein from the saliva of the blood-sucking insect Rhodnius prolixus, and its NO and cyanide adducts, J. Am. Chem. Soc. 123, 11664-11672.
16. Andersen, J. F., Ding, X. D., Balfour, C., Champagne, D. E., Walker, F. A., and Montfort, W. R. (2000) Kinetics and equilibria in ligand binding by nitrophorins 1-4: evidence for stabilization of a NO-feniheme complex through a ligand-induced conformational trap, Biochemists 39, 10118-10131.
17. Shokhireva, T. Kh., Berry, R. E., Uno, E., Balfour, C. A., Zhang, H., and Walker, F. A. (2003) Electrochemical and NMR spectroscopic studies of single and double distal pocket mutants L122-132V of nitrophorin 2: the effect of altering distal cavity size on stability, structure and dynamics of axial ligand complexes, Proc. Natl. Acad. Sci. U.S.A. 100, 3778-3783.
18. Berry, R. E., Ding, X. D., Shokhireva, T. Kh., Weichsel, A., Montfort, W. R., and Walker, F. A. (2004) Axial ligand complexes of nitrophorins. Electrochemistry, binding constants and structures of the imidazole and 4-iodopyrazole complexes, J. Biol. lnorg. Chem. 9, 135-144.
19. 13C NMR spectroscopy: an explanation of the order of heme methyl resonances in high-spin ferriheme proteins, Biochemistry 42, 679-693.
20. 13C NMR spectroscopy: comparison to structural data obtained from X-ray crystallography, lnorg. Chem. 46, 170-178.
21. 13C NMR spectroscopy: comparison to structural data obtained from X-ray crystallography, lnorg. Chem. 46, 2041-2056.
22. Astashkin, A. V., Raitsimring, A. M., and Walker, F. A. (1999) Two- and four-pulse ESEEM studies of the heme binding center of a low-spin ferriheme protein: the importance of a multi-frequency approach, Chem. Phys. Lett. 306, 9-17.
23. Wegner, P., Benda, R., Schünemann, V., Trautwein, A. X., Berry, R. E., Balfour, C. A., Wert, D., and Walker, F. A. (2002) How a blood sucking insect gets its meal: the ferriheme proteins nitrophorin 2 and 4 studied by Mössbauer spectroscopy, Hyperfine Interact. C5, 253-256.
24. Andersen, J. F., Champagne, D. E., Weichsel, A., Ribeiro, J. M. C., Balfour, C. A., Dress, V., and Montfort, W. R. (1997) Nitric-oxide binding and crystallization of recombinant nitrophorin 1, a nitric oxide transport protein from the blood-sucking bug Rhodnius prolixus, Biochemists 36, 4423-4428.
25. Weichsel, A., Andersen, J. F., Champagne, D. E., Walker, F. A., and Montfort, W. R. (1998) Crystal structures of a nitric oxide transport protein from a blood-sucking insect, Nature Struct. Biol. 5, 304-309.
26. Andersen, J. F., and Montfort, W. R. (2000) The crystal structure of nitrophorin 2, a trifunctional antihemostatic protein from the saliva of Rhodnius prolixus, J. Biol. Chem. 275, 30496-30503.
27. Andersen, J. F., Weichsel, A., Balfour, C. A. Champagne, D. E., and Montfort, W. R. (1998) The crystal structure of nitrophorin 4 at 1.5 Å resolution: transport of nitric oxide by a lipocalin-based heme protein, Structure 6, 1315-1327.
28. Weichsel, A., Andersen, J. F., Roberts, S. A., and Montfort, W. R. (2000) Nitric oxide binding to nitrophorin 4 induces complete distal pocket burial, Nature Struct. Biol. 7, 551-554.
29. Roberts, S. A., Weichsel, A., Qiu, Y., Shelnutt, J. A., Walker, F. A., and Montfort, W. R. (2001) Ligand-induced heme ruffling and bent NO geometry in ultra-high-resolution structures of nitrophorin 4, Biochemists 40, 11327-11337.
30. Maes, E. M., Weichsel, A., Andersen, J. F., Shepley, D., and Montfort, W. R. (2004) Role of binding site loops in controlling nitric oxide release: structure and kinetics of mutant forms of nitrophorin 4, Biochemistry 43, 6679-6690.
31. Kondrashov, D. A., Roberts, S. A., Weichsel, A., and Montfort, W. R. (2004) Protein functional cycle reviewed at atomic resolution: conformational change and mobility in nitrophorin 4 as a function of pH and NO binding, Biochemists 43, 13637-13647.
32. Maes, E. M., Roberts, S. A., Weichsel, A., and Montfort, W. R. (2005) Ultrahigh resolution structures of nitrophorin 4: heme distortion in fenous CO and NO complexes, Biochemists 44, 12690-12699.
33. Montfort, W. R., Weichsel, A., and Andersen, J. F. (2000) Nitrophorins and related antihemostatic lipocalins from Rhodnius prolixus and other blood-sucking arthropods, Biochim. Biophys. Acta 1482, 110-118.
34. Dickerson, R. E., and Geis, I. (1983) Hemoglobin: Structure, Function, Evolution, and Pathology, Benjamin/Cummings, Menlo Park, CA.
35. Pesce, A., Dewilde, S., Nardini, M., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., and Bolognesi, M. (2003) Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity, Structure 11, 1087-1095.
36. Vallone, B., Nienhaus, K., Brunori, M., and Nienhaus, G. U. (2004) The structure of murine neuroglobin: novel pathways for ligand migration and binding, Proteins: Struct., Funct., Bioinf. 56, 85-94.
37. Vallone, B., Nienhaus, K., Matthes, A., Brunori, M., and Nienhaus, G. U. (2004) The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand affinity, Proc. Natl. Acad. Sci. U.S.A. 101, 17351-17356.
38. de Sanctis, D., Dewilde, S., Pesce, A., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., and Bolognesi, M. (2004) Crystal structure of cytoglobin: the fourth globin type discovered in man displays heme hexa-coordination, J. Mol. Biol. 336, 917-927.
39. Stryer, L. (1995) Biochemistry, 4th ed., p 329. W. H. Freeman, New York.
40. 562 by redetermining the primary structure and using molecular graphics, J. Mol. Biol. 148, 427-448.
41. 562, Biochemistry 38, 8657-8670.
42. Finzel, B. C., Weber, P. C. Hardman, K. D., and Salemme, F. R. (1985) Structure of ferricytochrome c′ from Rhodospirillum molischianum at 1.67 Å resolution, J. Mol. Biol. 186, 627-643.
43. Xie, Y., Lashuel, H. A., Miroy, J. G., Dikler, S., and Kelly, J. W. (1998) Recombinant human retinol-binding protein refolding, native disulfide formation, and characterization, Protein Expression Purif. 14, 31-37.
44. Yamaguchi, H., and Harada, A. (2002) Supramolecular formation of antibodies with viologen dimers: utilization for amplification of methyl viologen detection signals in surface plasmon resonance sensor, Biomacromolecules 3, 1163-1169.
45. Segel, I. H. (1975) Enzyme Kinetics, p 73. Wiley-Interscience, New York.
46. BM3. Evidence that NADP(H) binding controls redox potentials of the flavin cofactors, Biochemistry 39, 12699-12707.
47. Zhang, X., Cardosa, L., Broderick, M., Fein, H., and Davies, I. R. (2000) Novel calibration method for nitric oxide microsensors by stoichiometrical generation of nitric oxide from SNAP, Electroanalysis 12, 425-428.
48. Hoshino, M., Maeda, M., Konishi, R., Seki, H., and Ford, P. C. (1996) Photochemistry of NO adducts of water-soluble iron(III) porphyrin and ferrihemoproteins studied by nanosecond laser photolysis, J. Am. Chem. Soc. 118, 5702-5707.
49. Shokhirev N. V., and Walker, F. A. (2001) Shift Patterns, http://www.shokhirev.com/nikolai/programs/prgsciedu.html.
50. Shokhirev, N. V., and Walker, F. A. (1998) The effect of axial ligand plane orientation on the contact and pseudocontact shifts of low-spin ferriheme proteins, J. Biol, lnorg. Chem. 3, 581-594.
51. 5, J. Am. Chem. Soc. 110, 6234-6240.
52. Ambrus, A., Friedrich, K., and Somogyi, A. (2006) Oligomerization of nitrophorins, Anal. Biochem. 352, 286-295.