Iron-binding process in the amino- and carboxyl-terminal lobes of ovotransferrin: Quantitative studies utilizing single Fe3+-binding mutants

Biochemistry

Volumn 43, Issue 34, 2004, Pages 11118-11125

  Okamoto, Ikuko ^a   Mizutani, Kimihiko ^a   Hirose, Masaaki ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFERENTIAL SCANNING CALORIMETRY; ELECTROPHORESIS; FREE ENERGY; GELS; IRON; PH EFFECTS; UREA;

IRON BINDING; LIGANDS; MUTANTS; UREA GEL ELECTROPHORESIS;

MUTAGENESIS;

IRON; OVOTRANSFERRIN; PROTEIN Y191F; PROTEIN Y524F; UNCLASSIFIED DRUG; FERRIC ION; IRON BINDING PROTEIN; LIGAND; PEPTIDE FRAGMENT; PHENYLALANINE; TYROSINE;

ABSORPTION SPECTROPHOTOMETRY; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DIFFERENTIAL SCANNING CALORIMETRY; GEL ELECTROPHORESIS; KINETICS; PH; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; BINDING COMPETITION; CHEMICAL MODEL; CHEMISTRY; CHICKEN; GENETICS; METABOLISM; PICHIA; PROTEIN BINDING; PROTEIN DENATURATION; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS;

SIGMOIDEA;

AMINO ACID SEQUENCE; ANIMALS; BINDING, COMPETITIVE; CALORIMETRY, DIFFERENTIAL SCANNING; CHICKENS; CONALBUMIN; FERRIC COMPOUNDS; IRON-BINDING PROTEINS; LIGANDS; MODELS, CHEMICAL; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PHENYLALANINE; PICHIA; PROTEIN BINDING; PROTEIN DENATURATION; THERMODYNAMICS; TYROSINE;

EID: 4644356895     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049147j     Document Type: Article

References (45)

1. Aisen, P., and Listowsky, I. (1980) Iron transport and storage proteins, Annu. Rev. Biochem. 49, 357-393.
2. Baker, H. M., Anderson, B. F., and Baker, E. N. (2003) Dealing with iron: common structural principles in proteins that transport iron and heme, Proc. Natl. Acad. Sci. U.S.A. 100, 3579-3583.
3. Arnold, R. R., Cole, M. F., and McGhee, J. R. (1977) A bactericidal effect for human lactoferrin, Science 197, 263-265.
4. He, J., and Furmanski, P. (1995) Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA, Nature 373, 721-724.
5. Thibodeau, S. N., Lee, D. C., and Palmiter, R. D. (1978) Identical precursors for serum transferrin and egg white conalbumin, J. Biol. Chem. 255, 3771-3774.
6. Guha Thakurta, P., Choudhury, D., Dasgupta, R., and Dattagupta, J. K. (2003) Structure of diferric hen serum transferrin at 2.8 Å resolution, Acta Crystallogr., Sect. D: Biol. Crystallogr. 59, 1773-1781.
7. Kurokawa, H., Mikami, B., and Hirose, M. (1995) Crystal structure of diferric hen ovotransferrin at 2.4 Å resolution, J. Mol. Biol. 254, 196-207.
8. Dewan, J. C., Mikami, B., Hirose, M., and Sacchettini, J. C. (1993) Structural evidence for a pH-sensitive dilysine trigger in the hen ovotransferrin N-lobe: implications for transferrin iron release, Biochemistry 32, 11963-11968.
9. MacGillivray, R. T., Moore, S. A., Chen, J., Anderson, B. F., Baker, H., Luo, Y., Bewley, M., Smith, C. A., Murphy, M. E., Wang, Y., Mason, A. B., Woodworth, R. C., Brayer, G. D., and Baker, E. N. (1998) Two high-resolution crystal structures of the recombinant N-lobe of human transferrin reveal a structural change implicated in iron release, Biochemistry 37, 7919-7928.
10. Brown-Mason, A., and Woodworth, R. C. (1984) Physiological levels of binding and iron donation by complementary half-molecules of ovotransferrin to transferrin receptors of chick reticulocytes, J. Biol. Chem. 259, 1866-1873.
11. Mason, A. B., Brown, S. A., and Church, W. R. (1987) Monoclonal antibodies to either domain of ovotransferrin block binding to transferrin receptors on chick reticulocytes, J. Biol. Chem. 262, 9011-9015.
12. Mason, A. B., Woodworth, R. C., Oliver, R. W., Green, B. N., Lin, L. N., Brandts, J. F., Savage, K. J., Tam, B. M., and MacGillivray, R. T. (1996) Association of the two lobes of ovotransferrin is a prerequisite for receptor recognition. Studies with recombinant ovotransferrins, Biochem. J. 319, 361-368.
13. Dautry-Varsat, A., Ciechanover, A., and Lodish, H. F. (1983) pH and the recycling of transferrin during receptor-mediated endocytosis, Proc. Natl. Acad. Sci. U.S.A. 80, 2258-2262.
14. Klausner, R. D., Ashwell, G., van Renswoude, J., Harford, J. B., and Bridges, K. R. (1983) Binding of apotransferrin to K562 cells: explanation of the transferrin cycle, Proc. Natl. Acad. Sci. U.S.A. 80, 2263-2266.
15. Rawas, A., Muirhead, H., and Williams, J. (1996) Structure of diferric duck ovotransferrin at 2.35 angstrom resolution, Acta Crystallogr., Sect. D: Biol. Crystallogr. 52, 631-640.
16. Mizutani, K., Mikami, B., and Hirose, M. (2001) Domain closure mechanism in transferrins: new viewpoints about the hinge structure and motion as deduced from high-resolution crystal structures of ovotransferrin N-lobe, J. Mol. Biol. 309, 937-947.
17. Rawas, A., Muirhead, H., and Williams, J. (1997) Structure of apo duck ovotransferrin: The structures of the N and C lobes are in the open form, Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 464-468.
18. Kurokawa, H., Dewan, J. C., Mikami, B., Sacchettini, J. C., and Hirose, M. (1999) Crystal structure of hen apo-ovotransferrin. Both lobes adopt an open conformation upon loss of iron, J. Biol. Chem. 274, 28445-28452.
19. Mizutani, K., Yamashita, H., Mikami, B., and Hirose, M. (2000) Crystal structure at 1.9 Å resolution of the apoovotransferrin N-lobe bound by sulfate anions: implications for the domain opening and iron release mechanism, Biochemistry 39, 3258-3265.
20. 2- binding site and its implications for the kinetic pathway, J. Biol. Chem. 276, 35940-35946.
21. Hirose, M. (2000) The structural mechanism for iron uptake and release by transferrins, Biosci., Biotechnol., Biochem. 64, 1328-1336.
22. Young, S. P., Bomford, A., and Williams, R. (1984) The effect of the iron saturation of transferrin on its binding and uptake by rabbit reticulocytes, Biochem. J. 219, 505-510.
23. Williams, J., Evans, R. W., and Moreton, K. (1978) The iron-binding properties of hen ovotransferrin, Biochem. J. 173, 533-539.
24. Nakazato, K., Yamamura, T., and Satake, K. (1988) Different stability of N- and C-domain of diferric ovotransferrin in urea and application to the determination of iron distribution between the two domains, J. Biochem. (Tokyo) 103, 823-828.
25. Lin, L. N., Mason, A. B., Woodworth, R. C., and Brandts, J. F. (1994) Calorimetric studies of serum transferrin and ovotransferrin. Estimates of domain interactions, and study of the kinetic complexities of ferric ion binding, Biochemistry 33, 1881-1888.
26. Kretchmar, S. A., and Raymond, K. N. (1986) Biphasic kinetics and temperature-dependence of iron removal from transferrin by 3,4-licams, J. Am. Chem. Soc. 108, 6212-6218.
27. Bali, P. K., and Harris, W. R. (1989) Cooperativity and heterogeneity between the 2 binding-sites of diferric transferrin during iron removal by pyrophosphate, J. Am. Chem. Soc. 111, 4457-4461.
28. Bali, P. K., Harris, W. R., and Nessettollefson, D. (1991) Kinetics of iron removal from monoferric and cobalt-labeled monoferric human serum transferrin by nitrilotris(methylenephosphonic acid) and nitrilotriacetic acid, Inorg. Chem. 30, 502-508.
29. Muralidhara, B. K., and Hirose, M. (2000) Anion-mediated iron release from transferrins. The kinetic and mechanistic model for N-lobe of ovotransferrin, J. Biol. Chem. 275, 12463-12469.
30. Mazurier, J., and Spik, G. (1980) Comparative study of the iron-binding properties of human transferrins, Biochim. Biophys. Acta 629, 399-408.
31. Ward, P. P., Zhou, X., and Conneely, O. M. (1996) Cooperative interactions between the amino- and carboxyl-terminal lobes contribute to the unique iron-binding stability of lactoferrin, J. Biol. Chem. 271, 12790-12794.
32. Mizutani, K., Okamoto, I., Fujita, K., Yamamoto, K., and Hirose, M. (2004) Structural and functional characterization of ovotransferrin produced by Pichia pastoris, Biosci., Biotechnol., Biochem. 68, 376-383.
33. Evans, R. W., and Williams, J. (1980) The electrophoresis of transferrins in urea/polyacrylamide gels, Biochem. J. 189, 541-546.
34. Mizutani, K., Yamashita, H., Kurokawa, H., Mikami, B., and Hirose, M. (1999) Alternative structural state of transferrin. The crystallographic analysis of iron-loaded but domain-opened ovotransferrin N-lobe, J. Biol. Chem. 274, 10190-10194.
35. Donovan, J. W., Beardslee, R. A., and Ross, K. D. (1976) Formation of monoferric ovotransferrins in the presence of chelates, Biochem. J. 153, 631-639.
36. Faber, H. R., Bland, T., Day, C. L., Norris, G. E., Tweedie, J. W., and Baker, E. N. (1996) Altered domain closure and iron binding in transferrins: the crystal structure of the Asp60Ser mutant of the amino-terminal half-molecule of human lactoferrin, J. Mol. Biol. 256, 352-363.
37. Nicholson, H., Anderson, B. F., Bland, T., Shewry, S. C., Tweedie, J. W., and Baker, E. N. (1997) Mutagenesis of the histidine ligand in human lactoferrin: iron binding properties and crystal structure of the histidine-253→methionine mutant, Biochemistry 36, 341-346.
38. MacGillivray, R. T., Bewley, M. C., Smith, C. A., He, Q. Y., Mason, A. B., Woodworth, R. C., and Baker, E. N. (2000) Mutation of the iron ligand His 249 to Glu in the N-lobe of human transferrin abolishes the dilysine "trigger" but does not significantly affect iron release, Biochemistry 39, 1211-1216.
39. Baker, H. M., Mason, A. B., He, Q. Y., MacGillivray, R. T., and Baker, E. N. (2001) Ligand variation in the transferrin family: the crystal structure of the H249Q mutant of the human transferrin N-lobe as a model for iron binding in insect transferrins, Biochemistry 40, 11670-11675.
40. He, Q. Y., Mason, A. B., Woodworth, R. C., Tam, B. M., MacGillivray, R. T., Grady, J. K., and Chasteen, N. D. (1997) Inequivalence of the two tyrosine ligands in the N-lobe of human serum transferrin, Biochemistry 36, 14853-14860.
41. 3+ binding pathway of camel lactoferrin at 2.7 Å resolution, J. Biol. Chem. 276, 36817-36823.
42. Nagaoka, M. H., and Maitani, T. (2000) Differed preferential iron-binding lobe in human transferrin depending on the presence of bicarbonate detected by HPLC/high-resolution inductively coupled plasma mass spectrometry, Biochim. Biophys. Acta 1523, 182-188.
43. Ikeda, H., Nabuchi, Y., Nakazato, K., Tanaka, Y., and Satake, K. (1985) Preparation and characterization of trypsin-nicked ovotransferrin, FEBS Lett. 182, 305-309.
44. Oe, H., Doi, E., and Hirose, M. (1988) Amino-terminal and carboxyl-terminal half-molecules of ovotransferrin: preparation by a novel procedure and their interactions, J. Biochem. (Tokyo) 103, 1066-1072.
45. Williams, J., and Moreton, K. (1988) The dimerization of half-molecule fragments of transferrin, Biochem. J. 251, 849-855.