Deamidation and disulfide bridge formation in human calbindin D 28k with effects on calcium binding

Protein Science

Volumn 14, Issue 4, 2005, Pages 968-979

  Vanbelle, Christophe ^a,d   Halgand, Frédéric ^b   Cedervall, Tommy ^a,c   Thulin, Eva ^a   Åkerfeldt, Karin S ^c   Laprévote, Olivier ^b   Linse, Sara ^a  

^a LUND UNIVERSITY   (Sweden)

^b CNRS   (France)

^c HAVERFORD COLLEGE   (United States)

^d INSERM   (France)

Author keywords

Calbindin D28k; Calcium binding; Deamidation; Disulfide bond; ICAT; Mass spectrometry; Post translational modifications

Indexed keywords

ASPARAGINE; ASPARTIC ACID; CALBINDIN; CALCIUM; CYSTEINE; CYTOPLASM PROTEIN; ISOPROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CALCIUM BINDING; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; DEAMINATION; DISULFIDE BOND; ENZYME REGULATION; HUMAN; KINETICS; MASS SPECTROMETRY; MOLECULAR CLONING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; REDUCTION; STOICHIOMETRY; TECHNIQUE; TEMPERATURE DEPENDENCE;

ALKYLATION; AMINO ACID SEQUENCE; ASPARAGINE; ASPARTIC ACID; CALCIUM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CYSTEINE; ELECTROPHORESIS, AGAR GEL; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 15244343344     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041157705     Document Type: Article

References (41)

1. Airaksinen, M.S., Eilers, J., Garaschuk, O., Thoenen, H., Konnerth, A., and Meyer, M. 1997. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc. Natl. Acad. Sci. 94: 1488-1493.
2. Åkerfeldt, K.S., Coyne, A.N., Wilk, R.R., Thulin, E., and Linse, S. 1996. Ca2+-binding stoichiometry of calbindin D28k as assessed by spectroscopic analyses of synthetic peptide fragments. Biochemistry 35: 3662-3669.
3. Andre, I. and Linse, S. 2002. Measurement of Ca2+-binding constants of proteins and presentation of the CaLigator software. Anal. Biochem. 305: 195-205.
4. Andressen, C., Blumcke, I., and Celio, M.R. 1993. Calcium-binding proteins: Selective markers of nerve cells. Cell Tissue Res. 271: 181-208.
5. Arentz-Hansen, H., Korner, R., Molberg, O., Quarsten, H., Vader, W., Kooy, Y.M., Lundin, K.E., Koning, F., Roepstorff, P., Sollid, L.M., et al. 2000. The intestinal T cell response to α-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J. Exp. Med. 191: 603-612.
6. Bellido, T., Huening, M., Raval-Pandya, M., Manolagas, S.C., and Christakos, S. 2000. Calbindin-D28k is expressed in osteoblastic cells and suppresses their apoptosis by inhibiting caspase-3 activity. J. Biol. Chem. 275: 26328-26332.
7. Berggård, T., Silow, M., Thulin, E., and Linse, S. 2000a. Ca(2+)- and H(+)-dependent conformational changes of calbindin D(28k). Biochemistry 39: 6864-6873.
8. Berggård, T., Thulin, E., Åkerfeldt, K.S., and Linse, S. 2000b. Fragment complementation of calbindin D28k. Protein Sci. 9: 2094-2108.
9. Berggård, T., Miron, S., Önnerfjord, P., Thulin, E., Åkerfeldt, K.S., Enghild, J.J., Akke, M., and Linse, S. 2002a. Calbindin D28k exhibits properties characteristic of a Ca2+ sensor. J. Biol. Chem. 277: 16662-16672.
10. Berggård, T., Szczepankiewicz, O., Thulin, E., and Linse, S. 2002b. myo-Inositol monophosphatase is an activated target of calbindin D28k. J. Biol. Chem. 9: 9.
11. Berson, S.A. and Yalow, R.S. 1966. Deamidation of insulin during storage in frozen state. Diabetes 15: 875-879.
12. Bischoff, R. and Kolbe, H.V. 1994. Deamidation of asparagine and glutamine residues in proteins and peptides: Structural determinants and analytical methodology. J. Chromatogr. B Biomed. Appl. 662: 261-278.
13. Bornstein, P. 1970. Structure of α-1-CB8, a large cyanogen bromide produced fragment from the α-1 chain of rat collagen. The nature of a hydroxylamine-sensitive bond and composition of tryptic peptides. Biochemistry 9: 2408-2421.
14. Bornstein, P. and Balian, G. 1970. The specific nonenzymatic cleavage of bovine ribonuclease with hydroxylamine. J. Biol. Chem. 245: 4854-4856.
15. Cedervall, T., Berggård, T., Borek, V., Thulin, E., Linse, S., and Åkerfeldt, KS. 2005. Redox sensitive cystein residues in calbindin D28k are structurally and functionally important. Biochemistry 44: 684-693.
16. Chazin, W.J., Kordel, J., Thulin, E., Hofmann, T., Drakenberg, T., and Forsen, S. 1989. Identification of an isoaspartyl linkage formed upon deamidation of bovine calbindin D9k and structural characterization by 2D 1H NMR. Biochemistry 28: 8646-8653.
17. Christakos, S., Gabrielides, C., and Rhoten, W.B. 1989. Vitamin D-dependent calcium binding proteins: Chemistry, distribution, functional considerations, and molecular biology. Endocr. Rev. 10: 3-26.
18. Drakenberg, T., Fernlund, P., Roepstorff, P., and Stenflo, J. 1983. beta-Hydroxyaspartic acid in vitamin K-dependent protein C. Proc. Natl. Acad. Sci. 80: 1802-1806.
19. Geiger, T. and Clarke, S. 1987. Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J. Biol. Chem. 262: 785-794.
20. Gygi, S.P., Rist, B., Gerber, S.A., Turecek, F., Gelb, M.H., and Aebersold, R. 1999. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17: 994-999.
21. Helgstrand, M., Vanbelle, C., Thulin, E., Linse, S., and Akke, M. 2004. Sequential 1H, 15N and 13C NMR assignment of human calbindin D28k. J. Biomol. NMR 28: 305-306.
22. Johansson, B.G. 1972. Agarose gel electrophoresis. Scand. J. Clin. Lab. Invest. Suppl. 124: 7-19.
23. Johnson, K.L., Veenstra, T.D., Londowski, J.M., Tomlinson, A.J., Kumar, R., and Naylor, S. 1999. On-line sample clean-up and chromatography coupled with electrospray ionization mass spectrometry to characterize the primary sequence and disulfide bond content of recombinant calcium binding proteins. Biomed. Chromatogr. 13: 37-45.
24. Kretsinger, R.H. and Nockolds, C.E. 1973. Carp muscle calcium-binding protein. II. Structure determination and general description. J. Biol. Chem. 248: 3313-3326.
25. Lerm, M., Pop, M., Fritz, G., Aktories, K., and Schmidt, G. 2002. Proteasomal degradation of cytotoxic necrotizing factor 1-activated rac. Infect. Immun. 70: 4053-4058.
26. Linse, S. 2002. Calcium binding to proteins studied via competition with chromophoric chelators. Methods Mol. Biol. 173: 15-24.
27. Luthra, M. and Balasubramanian, D. 1993. Nonenzymatic glycation alters protein structure and stability. A study of two eye lens crystalline. J. Biol. Chem. 268: 18119-18127.
28. Lutz, W., Frank, E.M., Craig, T.A., Thompson, R., Venters, R.A., Kojetin, D., Cavanagh, J., and Kumar, R. 2003. Calbindin D28K interacts with Ran-binding protein M: Identification of interacting domains by NMR spectroscopy. Biochem. Biophys. Res. Commun. 303: 1186-1192.
29. McLachlin, D.T. and Chait, B.T. 2001. Analysis of phosphorylated proteins and peptides by mass spectrometry. Curr. Opin. Chem. Biol. 5: 591-602.
30. Molberg, O., McAdam, S.N., Korner, R., Quarsten, H., Kristiansen, C., Madsen, L., Fugger, L., Scott, H., Noren, O., Roepstorff, P., et al. 1998. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat. Med. 4: 713-717.
31. Ozaki, Y., Mizuno, A., Itoh, K., and Iriyama, K. 1987. Inter- and intramolecular disulfide bond formation and related structural changes in the lens proteins. A Raman spectroscopic study in vivo of lens aging. J. Biol. Chem. 262: 15545-15551.
32. Patel, K. and Borchardt, R.T. 1990. Chemical pathways of peptide degradation. II. Kinetics of deamidation of an asparaginyl residue in a model hexapeptide. Pharm. Res. 7: 703-711.
33. Reissner, K.J. and Aswad, D.W. 2003. Deamidation and isoaspartate formation in proteins: Unwanted alterations or surreptitious signals? Cell Mol. Life Sci. 60: 1281-1295.
34. Robinson, N.E., Robinson, A.B., and Merrifield, R.B. 2001. Mass spectrometric evaluation of synthetic peptides as primary structure models for peptide and protein deamidation. J. Pept. Res. 57: 483-493.
35. Sen, A.C. and Chakrabarti, B. 1990. Effect of acetylation by aspirin on the thermodynamic stability of lens crystallins. Exp. Eye Res. 51: 701-709.
36. Stenflo, J., Fernlund, P., Egan, W., and Roepstorff, P. 1974. Vitamin K dependent modifications of glutamic acid residues in prothrombin. Proc. Natl. Acad. Sci. 71: 2730-2733.
37. Studier, F.W. and Moffatt, B.A. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189: 113-130.
38. Tao, L., Murphy, M.E., and English, A.M. 2002. S-nitrosation of Ca(2+)-loaded and Ca(2+)-free recombinant calbindin D(28K) from human brain. Biochemistry 41: 6185-6192.
39. Thulin, E. and Linse, S. 1999. Expression and purification of human calbindin D28k. Protein Expr. Purif. 15: 265-270.
40. Tyler-Cross, R. and Schirch, V. 1991. Effects of amino acid sequence, buffers, and ionic strength on the rate and mechanism of deamidation of asparagine residues in small peptides. J. Biol. Chem. 266: 22549-22556.
41. Wright, H.T. 1991. Sequence and structure determinants of the nonenzymatic deamidation of asparagine and glutamine residues in proteins. Protein Eng. 4: 283-294.