1H NMR study of the molecular structure and magnetic properties of the active site for the cyanomet complex of O2-avid hemoglobin from the trematode Paramphistomum epiclitum

European Journal of Biochemistry

Volumn 270, Issue 13, 2003, Pages 2707-2720

  Du, Weihong ^a   Xia, Zhicheng ^a   Dewilde, Sylvia ^b   Moens, Luc ^b   La Mar, Gerd N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Dipolar shift; H bonding; Hemoglobin; NMR; Trematode

Indexed keywords

CYANIDE; GLOBIN; HEME; HEMOGLOBIN; HISTIDINE; IMIDAZOLE; LIGAND; METHYL GROUP; OXYGEN; TYROSINE; CYANOMETHEMOGLOBIN; DRUG DERIVATIVE; HELMINTH PROTEIN; METHEMOGLOBIN;

ANISOTROPY; ARTICLE; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; HEMOGLOBIN DETERMINATION; HYDROGEN BOND; MAGNETISM; NONHUMAN; OXYGEN AFFINITY; PARAMPHISTOMUM EPICLITUM; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; TREMATODE; ANIMAL; BINDING SITE; CHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE;

INVERTEBRATA; MAMMALIA; PARAMPHISTOMUM; PARAMPHISTOMUM EPICLITUM; TREMATODA;

ANIMALS; BINDING SITES; HELMINTH PROTEINS; HYDROGEN BONDING; MAGNETICS; METHEMOGLOBIN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXYGEN; PARAMPHISTOMATIDAE;

EID: 0038384007     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03638.x     Document Type: Article

References (56)

1. Antonini, E. & Brunori, M. (1971) Hemoglobin and Myoglobin and Their Reactions with Ligands. Elsevier, North-Holland Publishing, Amsterdam, the Netherlands.
2. Dickerson, R.E. & Geis, I. (1983) Hemoglobin: Structure, Function, Evolution and Pathology. Benjamin-Cummings, Menlo Park, CA, USA.
3. Mukai, M., Savard, P.-Y., Ouellet, H., Guertin, M. & Yeh, S.-R. (2002) Unique ligand-protein interactions in a new truncated hemoglobin from Mycobacterium tuberculosis. Biochemistry 41, 3897-3905.
4. Pesce, A., Couture, M., Dewilde, S., Guertin, M., Yamauchi, K., Ascenzi, P., Moens, L. & Bolognesi, M. (2000) A novel two-over-two α-helical sandwich fold is characteristic of the truncated hemoglobin family. EMBO J. 19, 2424-2434.
5. 2 diffusion to the heme. EMBO J. 20, 3902-3909.
6. Springer, B.A., Sligar, S.G., Olson, J.S. & Phillips, G.N. (1994) Mechanisms of ligand recognition in myoglobin. Chem. Rev. 94, 699-714.
7. Dene, H., Goodman, M. & Romero-Herrera, A.E. (1980) The Amino Acid Sequence (Elephas maximus) Myoglobin and the Phylogen of Proboscidea. Proc. Royal Soc. London B207, 111-127.
8. Zhao, X., Vyas, K., Nguyen, B.D., Rajarathnam, K., La Mar., G.N., Li, T., Phillips, G.N.J., Eich, R.F., Olson, J.S., Ling, J. & Bocian, D.F. (1995) A double mutant of sperm whale myoglobin mimics the structure and function of elephant myoglobin. J. Biol. Chem. 270, 20763-20774.
9. Bisig, D.A., Di Iorio, E.E., Diederichs, K., Winterhalter, K.H. & Piontek, K. (1995) Crystal structure of asian elephant (Elephas maximus) cyano-metmyoglobin at 1.78-Å resolution. J. Biol. Chem. 270, 20754-20762.
10. Bolognesi, M., Coda, A., Frigero, F., Gatti, G., Ascenzi, P. & Brunori, M. (1989) Aplysia limacina myoglobin - crystallographic analysis at 1.6Å resolution. J. Mol. Biol. 205, 529-544.
11. De Baere, I., Perutz, M.F., Kiger, L., Marden, M.C. & Poyart, C. (1994) Formation of two hydrogen bonds from the globin to the heme-linked oxygen molecule in Ascaris hemoglobin. Proc. Natl Acad. Sci. USA 91, 1594-1597.
12. Yang, J., Kloek, A., Goldberg, D.E. & Mathews, F.S. (1995) The structure of Ascaris hemoglobin domain I at 2.2 angstrom resolution - molecular features of oxygen avidity. Proc. Natl Acad. Sci. USA 92, 4224-4228.
13. Kapp, O., Moens, L., Vanfleteren, J., Trotman, C., Suzuki, T. & Vinogradov, S. (1995) Alignment of 7-00 globin sequences - extent of amino-acid substitution and its correlation with variation in volume. Protein Sci. 4, 2179-2190.
14. Rashid, A.K., Van Hauwaert, M.L., Haque, M., Siddiqi, A.H., Lasters, I., De Mayer, M., Griffon, N., Marden, M.C., De Wilde, S., Clauwaert, J., Vinogradov, S.N. & Moens, L. (1997) Trematode myoglobins, functional molecules with a distal tyrosine. J. Biol. Chem. 272, 2992-2999.
15. Rashid, A.K. & Weber, R.E. (1999) Functional differentiation in trematode hemoglobin isoforms. Eur. J. Biochem. 260, 717-725.
16. Pesce, A., Dewilde, S., Kiger, L., Milani, M., Ascenzi, P., Marden, M.C., Hauwaert, M.-L.V., Vanfleteren, J., Moens, L. & Bolognesi, M. (2001) Very High Resolution Structure of a Trematode Hemoglobin Displaying a TyrB10-TyrE7 Heme Distal Residue Pair and High Oxygen Affinity. J. Mol. Biol. 309, 1153-1164.
17. Milani, M., Pesce, A., Dewilde, S., Ascenzi, P., Moens, L. & Bolognesi, M. (2002) Structural plasticity in the eight-helix fold of a trematode haemoglobin. Acta Crystallogr. D-Biol Cryst. D58, 1-4.
18. Cutruzzola, F., Allocatelli, C.T., Brancaccio, A. & Brunori, M. (1996) Aplysia limacina myoglobin cDNA cloning - an alternative mechanism of oxygen stabilization as studied by active-site mutagenesis. Biochem. J. 314, 83-90.
19. Parkhurst, L.J., Sima, P. & Goss, D.J. (1980) Kinetics of oxygen and carbon monoxide binding to the hemoglobins of Glycera dibranchiata. Biochemistry 19, 2688-2692.
20. Goldberg, D.E. (1995) The enigmatic oxygen-avid hemoglobin of Ascaris. Bioessays. 17, 177-182.
21. Rizzi, M., Wittenberg, J.G., Coda, A., Fasano, M., Ascenzi, P. & Bolognesi, M. (1994) Structure of the sulfide-reactive hemoglobin from the clam Lucina pectinata. Crystallographic analysis at 1.5 Å resolution. J. Mol. Biol. 244, 86-89.
22. Zhang, W., Cutruzzolá, F., Travaglini Allocatelli, C., Brunori, M. & La Mar., G.N. (1997) A myoglobin mutant designed to mimic the oxygen-avid Ascaris suum hemoglobin: elucidation of the distal hydrogen bonding network by solution NMR. Biophys. J. 73, 1019-1030.
23. 1H NMR structure of the heme cavity in the oxygen-avid myoglobin from the trematode Paramphistonum epiclitum. J. Biol. Chem. 275, 3000-3006.
24. 1H NMR probe for hydrogen bonding of distal residues to bound ligands in heme proteins: isotope effect on heme electronic structure of myoglobin. J. Am. Chem. Soc. 109, 7219-7220.
25. Thanabal, V., de Ropp, J.S. & La Mar., G.N. (1988) Proton NMR characterization of the catalytically relevant proximal and distal hydrogen-bonding networks in ligated resting state horse-radish peroxidase. J. Am. Chem. Soc. 110, 3027-3035.
26. 1H NMR structure of the heme cavity in the low-affinity state for the allosteric monomeric cyano-met hemoglobins from Chironomus thummi thummi. Comparison to the crystal structure. Eur. J. Biochem. 237, 841-853.
27. Yamamoto, Y. (1998) H-1-NMR investigation of the influence of the heme orientation on functional properties of myoglobin. Biochim. Biophys. Acta. 1388, 349-362.
28. Emerson, S.D. & La Mar., G.N. (1990) NMR determination of the orientation of the magnetic susceptibility tensor in cyano metmyoglobin: a new probe of steric tilt of bound ligand. Biochemistry 29, 1556-1566.
29. Nguyen, B.D., Xia, Z., Yeh, D.C., Vyas, K., Deaguero, H. & La Mar., G. (1999) Solution NMR determination of the anisotropy and orientation of the paramagnetic susceptibility tensor as a function of temperature for metmyoglobin cyanide; implications for the population of excited electronic states. J. Am. Chem. Soc. 121, 208-217.
30. La Mar., G.N., Satterlee, J.D. & de Ropp, J.S. (1999) NMR of hemoproteins. The Porphyrins Handbook (Kadish, K.M., Guilard, R. & Smith, K.M., eds), pp. 185-298. Academic Press, San Diego, USA.
31. Bertini, I. & Luchinat, C. (1996) NMR of paramagnetic substances. Coord. Chem. Rev. 150, 1-296.
32. La Mar., G.N. & de Ropp, J.S. (1993) NMR methodology for paramagnetic proteins. Biol. Magn. Reson. 18, 1-79.
33. Lecomte, J.T.J., La Mar., G.N., Smit, J.D.G., Winterhalter, K.H., Smith, K.M., Langry, K.C. & Leung, H.-K. (1987) Structural and electronic properties of the liver fluke hemoglobin heme cavity by nuclear magnetic resonance: isotope labeling. J. Mol. Biol. 197, 101-110.
34. Peyton, D.H., La Mar., G.N., Pande, U., Ascoli, F., Smith, K.M., Pandey, R.K., Parish, D.W., Bolognesi, M. & Brunori, M. (1989) Proton nuclear magnetic resonance study of the molecular and electronic structure of the heme cavity in Aplysia cyanometmyoglobin. Biochemistry 28, 4880-4887.
35. Shokhirev, N.V. & Walker, F.A. (1998) The effect of axial ligand plane orientation on the contact and pseudocontact shifts of low-spin ferriheme proteins. J. Biol. Inorg. Chem. 3, 581-594.
36. 1H NMR study. Biochemistry 37, 6979-6990.
37. 1H NMR Investigation of the distal hydrogen bonding network and ligand tilt in the cyanomet complex of oxygen-avid Ascaris hemoglobin. J. Biol. Chem. 274, 31819-31826.
38. 1H NMR study of the active site of Aplysia limacina cyanomet myoglobin mutant Val (E7) His/Thr (E10) Arg designed to mimic the sperm whale myoglobin pocket, influence of distal hydrogen-bonding and N-terminus acetylation on the heme electronic and molecular structure. J. Biol. Chem. 275, 742-751.
39. Gupta, R.K. (1976) Dynamic range problem in fourier transform nmr. modified weft pulse sequence. J. Magn. Reson. 24, 461-465.
40. Plateau, P. & Gueron, M. (1982) Exchangeable proton NMR without base-line distortions using new strong-pulse sequences. J. Am. Chem. Soc. 104, 7310-7311.
41. Thanabal, V., de Ropp, J.S. & La Mar, G.N. (1987) Identification of the catalytically important amino acid residues resonances in ferric low-spin horseradish peroxidase using nuclear overhauser effect measurements. J. Am. Chem. Soc. 109, 7516-7525.
42. Jeener, J., Meier, B.H., Bachmann, P. & Ernst, R.R. (1979) Investigation of exchange processes by two dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553.
43. 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110, 7870-7872.
44. Williams, G., Clayden, N.J., Moore, G.R. & Williams, R.J.P. (1985) Comparison of the solution and crystal structures of mitochondrial cytochrome c. Analysis of paramagnetic shifts in the nuclear magnetic resonance spectrum of ferricytochrome c. J. Mol. Biol. 183, 447-460.
45. 1H NMR parameters of the common amino acid residues measured in aqueous solutions of the linear tetrapeptides H-Gly-Gly-X-L-Ala-OH. Biopolymers 18, 285-297.
46. Wishart, D.S., Sykes, B.D. & Richards, F.M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222, 311-333.
47. Cross, K.J. & Wright, P.E. (1985) Calibration of ring-current models for the heme ring. J. Magn. Reson. 64, 220-231.
48. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids. Wiley & Sons, New York, USA.
49. 1h nmr resonance assignment of hyperfine-shifted residues in the active site of a paramagnetic protein: application to Aplysia cyanometmyoglobin. J. Biomol. NMR 2, 597-618.
50. Jeffrey, G.A. (1997) An Introduction to Hydrogen Bonding. Oxford University Press, New York, USA.
51. 1H NMR study of the electronic and molecular structure of the heme cavity in horseradish peroxidase. Complete heme resonance assignments based on saturation transfer and nuclear Overhauser effects. J. Am. Chem. Soc. 109, 265-272.
52. Kuriyan, J., Wilz, S., Karplus, M. & Petsko, G.A. (1986) X-ray structure and refinement of carbon-monoxy (Fe-II)-myoglobin at 1.5 Å resolution. J. Mol. Biol. 192, 133-154.
53. 1H NMR resonance assignment and dynamic analysis of phenylalanine cd1 in a low-spin ferric complex of sperm whale myoglobin. J. Am. Chem. Soc. 110, 4176-4182.
54. Vyas, K. & Rajarathnam, K., Yu, L.P., Emerson, S.D. & La Mar, G.N. (1993) 1H NMR investigation of the heme cavity of elephant (E7 GLN) metMbCN: evidence for a B-helix phenylalanine interaction with bound ligand. J. Biol. Chem. 268, 14826-14835.
55. Lecomte, J.T.J., Smit, J.D.G., Winterhalter, K.H. & La Mar, G.N. (1989) Structural and electronic properties of the liver fluke heme cavity by nuclear magnetic resonance and optical spectroscopy. J. Mol. Biol. 209, 235-247.
56. Tuchschmid, P.E., Kuntz, P.A. & Wilson, K.J. (1978) Isolation and characterization of hemoglobin from Lanceolate fluke Dicrocoelium dendriticum. Eur. J. Biochem. 88, 387-394.