N-terminal acetylation and protonation of individual hemoglobin subunits: Position-dependent effects on tetramer strength and cooperativity

Protein Science

Volumn 14, Issue 6, 2005, Pages 1458-1471

  Ashiuchi, Makoto ^a   Yagami, Takeshi ^a   Willey, Ronald J ^b   Padovan, Julio C ^c   Chait, Brian T ^c   Popowicz, Anthony ^c   Manning, Lois R ^a   Manning, James M ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b Northeastern University   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Acetylation; Hemoglobin; Protein protonation; Subunit interfaces; Tetramer disassembly; Tetramer stability

Indexed keywords

ALANINE; CARBON; DIMER; GLOBULAR PROTEIN; HEMOGLOBIN; LIGAND; NITROGEN; OXYGEN; PROTEIN SUBUNIT; SERINE; TETRAMER;

ACETYLATION; ALLOSTERISM; ARTICLE; CIRCULAR DICHROISM; CONFORMATION; DISSOCIATION CONSTANT; HUMAN; MASS SPECTROMETRY; OXYGEN AFFINITY; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTON TRANSPORT; SUBSTITUTION REACTION;

ACETYLATION; ALANINE; AMINO ACID SUBSTITUTION; HEMOGLOBIN A; HUMANS; OXYGEN; PROTEIN STRUCTURE, QUATERNARY; PROTONS; SERINE;

EID: 22444438012     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041267405     Document Type: Article

References (37)

1. Allfrey, V.G., Faulkner, R., and Mirsky, A.E. 1964. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. 51: 786-794.
2. Atha, D.H. and Riggs, A. 1976. Tetramer-dimer dissociation in hemoglobin and the Bohr effect. J. Biol. Chem. 251: 5537-5543.
3. Beavis, R.C. and Chait, B.T. 1996. Matrix-assisted laser desorption ionization mass-spectrometry of proteins. Methods Enzymol. 270: 519-551.
4. Bradshaw, R.A., Brickey, W.W., and Walker, K.W. 1998. N-terminal processing: The methionine aminopeptidase and N-acetyl transferase families. Trends Biochem. Sci. 23: 263-267.
5. Bunn, H.F. and Briehl, R.W. 1970. The interaction of 2,3- diphosphoglycerate with various human hemoglobins. J. Clin. Invest. 49: 1088-1094.
6. S1P requires Nat B-mediated acetylation to inhibit carboxypeptidase Y and to regulate the protein kinase A pathway. J. Biol. Chem. 279: 38532-38543.
7. Chu, A.H. and Ackers, G.K. 1981. Mutual effects of protons, NaCl and oxygen on the dimer-tetramer assembly of human hemoglobin. The dimer Bohr effect. J. Biol. Chem. 256: 1199-1205.
8. Dumoulin, A., Manning, L.R., Jenkins, W.T.,Winslow, R.M., and Manning, J.M. 1997. Exchange of subunit interfaces between recombinant adult and fetal hemoglobins. Evidence for a functional inter-relationship among regions of the tetramer. J. Biol. Chem. 272: 31326-31332.
9. Dumoulin, A., Padovan, J.C., Manning, L.R., Popowicz, A., Winslow, R.M., Chait, B.T., and Manning, J.M. 1998. The N-terminal sequence affects distant helix interactions in hemoglobin. Implications for mutant proteins from studies on recombinant hemoglobin felix. J. Biol. Chem. 273: 35032-35038.
10. K values for the α-amino groups of human hemoglobin. J. Biol. Chem. 250: 4398-4404.
11. 2) assembled in complex transgenic-knockout mice. Blood 97: 1099-1105.
12. Huehns, E.R., Flynn, F.V., Butler, E.A., and Beaven, G.H. 1961. Two new hemoglobin variants in a very young human embryo. Nature 189: 496-497.
13. Kalkum, M., Llyon, G.J., and Chait, B.T. 2003. Detection of secreted peptides by using hypothesis-driven multistage mass spectrometry. Proc. Natl. Acad. Sci. 100: 2795-2800.
14. Kilmartin, J.V., Hewitt, J.A., and Wootton, J.F. 1975. Alteration of functional properties associated with the change in quaternary structure in unliganded hemoglobin. J. Mol. Biol. 93: 203-218.
15. Kouzarides, T. 2000. Acetylation: A regulatory modification to viral phosphorylation? EMBO J. 19: 1176-1179.
16. Krutchinsky, A.N., Zhang, W., and Chait, B.T. 2000. Rapidly switchable matrix-assisted laser desorption/ionization and electrospray quadrupole-time-of-flight mass spectrometry for protein identification. J. Am. Soc. Mass. Spectrom. 11: 493-504.
17. Li, X., Himanen, J.-P., Martin de Llano, J.J., Padovan, J.C., Chait, B.T., and Manning, J.M. 1999. Mutational analysis of sickle haemoglobin (Hb) gelation. Biotechnol. Appl. Biochem. 29: 165-184.
18. 2-terminal residues. Methods Enzymol. 76: 159-167.
19. Manning, L.R. and Manning, J.M. 2001. The acetylation state of human fetal hemoglobin modulates the strength of its subunit interactions: Long-range effects and implications for histone interactions in the nucleosome. Biochemistry 40: 1635-1639.
20. Manning, L.R., Jenkins, W.T., Hess, J.R., Vandegriff, K., Winslow, R.M., and Manning, J.M. 1996. Subunit dissociations in natural and recombinant hemoglobins. Protein Sci. 5: 775-781.
21. Manning, L.R., Dumoulin, A., Jenkins, W.T., Winslow, R.M., and Manning, J.M. 1999. Determining subunit dissociation constants in natural and recombinant proteins. Methods Enzymol. 306: 113-129.
22. Martin de Llano, J.J. and Manning, J.M. 1994. Properties of a recombinant human hemoglobin double mutant: Sickle hemoglobin with Leu-88(β) at the primary aggregation site substituted by Ala. Protein Sci. 3: 1206-1212.
23. Martin de Llano, J.J., Schneewind, O., Stetler, G.L., and Manning, J.M. 1993. Recombinant human sickle hemoglobin expressed in yeast. Proc. Natl. Acad. Sci. 90: 918-922.
24. -. 1994. Purification and characterization of recombinant human sickle hemoglobin expressed in yeast. Methods Enzymol. 231: 390-403.
25. Meister, A. 1965. Biochemistry of the amino acids, 2nd ed., Vol. I, p. 28. Academic Press, New York.
26. Perutz, M. 1989. Mechanisms of cooperativity and allosteric regulation in proteins. Q. Rev. Biophys. 22: 139-237.
27. Polevoda, B. and Sherman, F. 2003. N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J. Mol. Biol. 325: 595-622.
28. Randhawa, Z.I., Jones, R.T., and Lie-Injo, L. 1984. Human hemoglobin Portland-2. J. Biol. Chem. 259: 7325-7330.
29. Rollema, H.S., Gros, G., and Bauer, C. 1980. pH changes accompanying the association of isolated α and β chains of human hemoglobins. J. Biol. Chem. 255: 2756-2760.
30. Root, R.W. 1931. The respiratory function of the blood of marine fishes. Biol. Bull. Mar. Biol. Lab. Woods Hole 61: 427-456.
31. Shaanan, B. 1983. Structure of human oxyhemoglobin at 2.1 Å resolution. J. Mol. Biol. 171: 31-59.
32. Sheff, D.R. and Rubenstein, P.A. 1992. Amino-terminal processing of actions mutagenized at the Cys-1 residue. J. Biol. Chem. 267: 2671-2678.
33. Tsunasawa, S. and Sakiyama, F. 1984. Amino-terminal acetylation of proteins: An overview. Methods Enzymol. 106: 165-170.
34. Urbancikova, M. and Hitchcock-De Gregori, S.E. 1994. Requirement of amino-terminal modification for striated muscle α-tropomyosin function. J. Biol. Chem. 269: 24310-24315.
35. Wagenbach, M., O'Rourke, K., Vitez, L., Wieczorek, A., Horrman, S., Durfee, S., Tedesco, J., and Stetler, G. 1991. Synthesis of wild-type and mutant human hemoglobins in Saccharomyces ceravisae. Biotechnology 9: 57-61.
36. Yagami, T., Ballard, B.T., Padovan, J.C., Chait, B.T., Popowicz, A.M., and Manning, J.M. 2002. N-terminal contributions of the γ-subunit of fetal hemoglobins to its tetramer strength: Remote effects at subunit contacts. Protein Sci. 11: 27-35.
37. Yan, S.C., Grinnell, B.W., and Wold, F. 1989. Post-translational modifications of proteins: Some problems left to solve. Trends Biochem. Sci. 14: 264-268.