Mutational analysis of C-lobe ligands of human serum transferrin: Insights into the mechanism of iron release

Biochemistry

Volumn 44, Issue 22, 2005, Pages 8013-8021

  Mason, Anne B ^a   Halbrooks, Peter J ^a   James, Nicholas G ^a   Connolly, Susan A ^a   Larouche, Julia R ^a   Smith, Valerie C ^b   MacGillivray, Ross T A ^b   Chasteen, N Dennis ^c  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c Univ of New Hampshire   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; CARBONATES; CELLS; CHEMICAL BONDS; CONFORMATIONS; FREE ENERGY; NEGATIVE IONS; PARAMAGNETIC RESONANCE; REACTION KINETICS;

HUMAN SERUM TRANSFERRIN (HTF); MUTATIONS; SYNERGISTIC ANIONS; TYROSINE;

PROTEINS;

ASPARTIC ACID; CARBONIC ACID; FERRITIN; HISTIDINE; LIGAND; OXYGEN; TYROSINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATION; ELECTRON SPIN RESONANCE; FERRITIN BLOOD LEVEL; GENE CONSTRUCT; HUMAN; IRON KINETICS; KINETICS; MEASUREMENT; MUTATION; PH; PRIORITY JOURNAL; ULTRAVIOLET RADIATION;

ANIMALS; BINDING, COMPETITIVE; CELL ADHESION; CELL LINE; CRICETINAE; ELECTRON SPIN RESONANCE SPECTROSCOPY; HELA CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; IRON; KINETICS; LIGANDS; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; RECEPTORS, TRANSFERRIN; RECOMBINANT PROTEINS; SPECTROPHOTOMETRY, ULTRAVIOLET; TRANSFERRIN;

EID: 20144373868     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050015f     Document Type: Article

References (49)

1. Aisen, P., Enns, C., and Wessling-Resnick, M. (2001) Chemistry and biology of eukaryotic iron metabolism, Int. J. Biochem. Cell Biol. 33, 940-959.
2. Baker, E. N., Baker, H. M., and Kidd, R. D. (2002) Lactoferrin and transferrin: Functional variations on a common structural framework, Biochem. Cell Biol. 80, 27-34.
3. Zuccola, H. J. (1993) The crystal structure of monoferric human serum transferrin, Ph.D. Thesis, Georgia Institute of Technology, Atlanta, GA.
4. Hall, D. R., Hadden, J. M., Leonard, G. A., Bailey, S., Neu, M., Winn, M., and Lindley, P. F. (2002) The crystal and molecular structures of diferric porcine and rabbit serum transferrins at resolutions of 2.15 and 2.60 Å, respectively, Acta Crystallogr., Sect. D: Biol. Crystallogr. 58, 70-80.
5. 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.
6. Zak, O., and Aisen, P. (2003) Iron release from transferrin, its C-lobe, and their complexes with transferrin receptor: Presence of N-lobe accelerates release from C-lobe at endosomal pH, Biochemistry 42, 12330-12334.
7. He, Q.-Y., and Mason, A. B. (2002) Molecular aspects of release of iron from transferrins, in Molecular and Cellular Iron Transport (Templeton, D. M., Ed.) pp 95-123, Marcel Dekker, New York.
8. Jeffrey, P. D., Bewley, M. C., MacGillivray, R. T. A., Mason, A. B., Woodworth, R. C., and Baker, E. N. (1998) Ligand-induced conformational change in transferrins: crystal structure of the open form of the N-terminal half-molecule of human transferrin, Biochemistry 37, 13978-13986.
9. MacGillivray, R. T. A., Moore, S. A., Chen, J., Anderson, B. F., Baker, H., Luo, Y. G., 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. He, Q.-Y., Mason, A. B., Woodworth, R. C., Tam, B. M., MacGillivray, R. T. A., 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.
11. Mason, A. B., Tam, B. M., Woodworth, R. C., Oliver, R. W. A., Green, B. N., Lin, L.-N., Brandts, J. F., Savage, K. J., Lineback, J. A., and MacGillivray, R. T. A. (1997) Receptor recognition sites reside in both lobes of human serum transferrin, Biochem. J. 326, 77-85.
12. Zak, O., and Aisen, P. (2002) A new method for obtaining human transferrin C-lobe in the native conformation: Preparation and properties, Biochemistry 41, 1647-1653.
13. Mason, A. B., He, Q. Y., Halbrooks, P. J., Everse, S. J., Gumerov, D. R., Kaltashov, I. A., Smith, V. C., Hewitt, J., and MacGillivray, R. T. A. (2002) Differential effect of a His tag at the N- and C-termini: Functional studies with recombinant human serum transferrin, Biochemistry 41, 9448-9454.
14. Gumerov, D. R., Mason, A. B., and Kaltashov, I. A. (2003) Interlobe communication in human serum transferrin: Metal binding and conformational dynamics investigated by electrospray ionization mass spectrometry, Biochemistry 42, 5421-5428.
15. Princiotto, J. V., and Zapolski, E. J. (1975) Difference between the two iron-binding sites of transferrin, J. Biol. Chem. 253, 1930-1937.
16. Cannon, J. C., and Chasteen, N. D. (1975) Nonequivalence of the metal binding sites in vanadyl-labeled human serum transferrin, Biochemistry 14, 4573-4577.
17. Lestas, A. N. (1976) The effect of pH upon human transferrin: selective labelling of the two iron-binding sites, Br. J. Haematol. 32, 341-350.
18. Baldwin, D. A., and DeSousa, D. M. R. (1981) The effect of salts on the kinetics of iron release from N-terminal and C-terminal monoferric transferrins. Biochem. Biophys. Res. Commun. 99, 1101-1107.
19. Marques, H. M., Watson, D. L., and Egan, T. J. (1991) Kinetics of iron removal from human serum monoferric transferrins by citrate, Inorg. Chem. 30, 3758-3762.
20. Halbrooks, P. J., He, Q. Y., Briggs, S. K., Everse, S. J., Smith, V. C., MacGillivray, R. T. A., and Mason, A. B. (2003) Investigation of the mechanism of iron release from the C-lobe of human serum transferrin: Mutational analysis of the role of a pH sensitive triad, Biochemistry 42, 3701-3707.
21. Mason, A. B., Miller, M. K., Funk, W. D., Banfield, D. K., Savage, K. J., Oliver, R. W. A., Green, B. N., MacGillivray, R. T. A., and Woodworth, R. C. (1993) Expression of glycosylated and nonglycosylated human transferrin in mammalian cells. Characterization of the recombinant proteins with comparison to three commercially available transferrins, Biochemistry 32, 5472-5479.
22. Mason, A. B., Halbrooks, P. J., Larouche, J. R., Briggs, S. K., Moffett, M. L., Ramsey, J. E., Connolly, S. A., Smith, V. C., and MacGillivray, R. T. A. (2004) Expression, purification, and characterization of authentic monoferric and apo-human serum transferrins, Protein Expression Purif. 36, 318-326.
23. Mason, A. B., He, Q.-Y., Adams, T. E., Gumerov, D. R., Kaltashov, I. A., Nguyen, V., and MacGillivray, R. T. A. (2001) Expression, purification, and characterization of recombinant nonglycosylated human serum transferrin containing a C-terminal hexahistidine tag, Protein Expression Purif. 23, 142-150.
24. He, Q. Y., Mason, A. B., Nguyen, V., MacGillivray, R. T. A., and Woodworth, R. C. (2000) The chloride effect is related to anion binding in determining the rate of iron release from the human transferrin N-lobe, Biochem. J. 350, 909-915.
25. Mason, A. B., He, Q.-Y., Tam, B. M., MacGillivray, R. T. A., and Woodworth, R. C. (1998) Mutagenesis of the aspartic acid ligands in human serum transferrin: lobe-lobe interaction and conformation as revealed by antibody, receptor-binding and iron-release studies, Biochem. J. 330, 35-40.
26. McFarlane, A. S. (1963) In vivo behavior of I131-fibrinogen, J. Clin. Invest. 42, 346-361.
27. Aisen, P. (2004) Transferrin receptor 1, Int. J. Biochem. Cell Biol. 36, 2137-2143.
28. Bali, P. K., and Harris, W. R. (1989) Cooperativity and heterogeneity between the two binding sites of diferric transferrin during iron removal by pyrophosphate, J. Am. Chem. Soc. 111, 4457-4461.
29. Bali, P. K., Harris, W. R., and Nesset-Tollefson, 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.
30. 13C-methionine-labeled human transferrin, Biochemistry 35, 7635-7642.
31. 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.
32. Kurokawa, H., Mikami, B., and Hirose, M. (1994) Crucial role of intralobe peptide-peptide interactions in the uptake and release of iron by ovotransferrin, J. Biol. Chem. 269, 6671-6676.
33. Lin, L., Mason, A. B., Woodworth, R. C., and Brandts, J. F. (1991) Calorimetric studies of the binding of ferric ions to ovotransferrin and interactions between binding sites, Biochemistry 30, 11660-11669.
34. Mason, A. B., Woodworth, R. C., Oliver, R. W. A., Green, B. N., Lin, L.-N., Brandts, J. F., Savage, K. J., Tam, B. M., and MacGillivray, R. T. A. (1996) Association of the two lobes of ovotransferrin is a prerequisite for receptor recognition. Studies with recombinant ovotransferrins., Biochem. J. 319, 361-368.
35. 3+-binding mutants, Biochemistry 43, 11118-11125.
36. Day, C. L., Stowell, K. M., Baker, E. N., and Tweedie, J. W. (1992) Studies of the N-terminal half of human lactoferrin produced from the cloned cDNA demonstrate that interlobe interactions modulate iron release. J. Biol. Chem. 267, 13857-13862.
37. 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.
38. 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.
39. Grossmann, J. G., Mason, A. B., Woodworth, R. C., Neu, M., Lindley, P. F., and Hasnain, S. S. (1993) Asp ligand provides the trigger for closure of transferrin molecules. Direct evidence from X-ray scattering studies of site-specific mutants of the N-terminal half-molecule of human transferrin, J. Mol. Biol. 231, 554-558.
40. 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.
41. Cheng, Y., Zak, O., Aisen, P., Harrison, S. C., and Walz, T. (2004) Structure of the human transferrin receptor-transferrin complex, Cell 116, 565-576.
42. Giannetti, A. M., Snow, P. M., Zak, O., and Bjorkman, P. J. (2003) Mechanism for multiple ligand recognition by the human transferrin receptor, PLoS Biol. 1, 341-350.
43. Bali, P. K., Zak, O., and Aisen, P. (1991) A new role for the transferrin receptor in the release of iron from transferrin, Biochemistry 30, 324-328.
44. Spik, G., Coddeville, B., and Montreuil, J. (1988) Comparative study of the primary structures of sero-, lacto- and ovotransferrin glycans from different species, Biochimie 70, 1459-1469.
45. 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.
46. He, Q.-Y., Mason, A. B., Tam, B. M., MacGillivray, R. T. A., and Woodworth, R. C. (1999) Dual role of Lys206-Lys296 interaction in human transferrin N-lobe: Iron-release trigger and anion-binding site, Biochemistry 38, 9704-9711.
47. Woodworth, R. C., Mason, A. B., Funk, W. D., and MacGillivray, R. T. A. (1991) Expression and initial characterization of five site-directed mutants of the N-Terminal half-molecule of human transferrin, Biochemistry 30, 10824-10829.
48. He, Q.-Y., Mason, A. B., Pakdaman, R., Chasteen, N. D., Dixon, B. L., Tam, B. M., Nguyen, V., MacGillivray, R. T. A., and Woodworth, R. C. (2000) Mutations at the histidine 249 ligand profoundly alter the spectral and iron-binding properties of human serum transferrin N-lobe. Biochemistry 39, 1205-1210.
49. DeLano, W. L. (2002) The PyMOL Molecular Graphics System (http://www.pymol.org).