BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Protection of aquo/hydroxocobalamin from reduced glutathione by a B12 trafficking chaperone

  • Jeong, Jin-Ju (School of Biotechnology, Yeungnam University) ;
  • Ha, Tal-Soo (Department of Biomedical Science, College of Natural Science, Daegu University) ;
  • Kim, Ji-Hoe (School of Biotechnology, Yeungnam University)
  • Received : 2010.12.16
  • Accepted : 2010.12.23
  • Published : 2011.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

We identified a bovine $B_{12}$ trafficking chaperone bCblC in Bos taurus that showed 88% amino acid sequence identity with a human homologue. The protein bCblC was purified from E. coli by over-expression of the encoding gene. bCblC bound cyanocobalamin (CNCbl), methylcobalamin (MeCbl) and adenosylcobalamin (AdoCbl) in the base-off states and eliminated the upper axial ligands forming aquo/hydroxocobalamin ($OH_2$/OHCbl) under aerobic conditions. A transition of $OH_2$/OHCbl was induced upon binding to bCblC. Interestingly, bCblC-bound $OH_2$/OHCbl did not react with reduced glutathione (GSH), while the reaction of free$OH_2$/OHCbl with GSH resulted in the formation of glutathionylcobalamin (GSCbl) and glutathione disulfide (GSSG). Furthermore we found that bCblC eliminates the GSH ligand of GSCbl forming $OH_2$/OHCbl. The results demonstrated that bCblC is a $B_{12}$ trafficking chaperone that binds cobalamins and protects $OH_2$/OHCbl from GSH, which could be oxidized to GSSG by free $OH_2$/OHCbl.

Keywords

References

  1. Banerjee, R. (2006) $B_{12}$ trafficking in mammals: a case forcoenzyme escort service. ACS. Chem. Biol. 1, 149-159. https://doi.org/10.1021/cb6001174
  2. Oh, R. and Brown, D. L. (2003) Vitamin $B_{12}$ deficiency.Am. Fam. Physician. 67, 979-986.
  3. Hodgkin, D. C., Kamper, J., Mackay, M., Pickworth, J.,Trueblood, K. N. and White, J. G. (1956) Structure of vitamin$B_{12}$. Nature 178, 64-66. https://doi.org/10.1038/178064a0
  4. Kolhouse, J. F. and Allen, R. H. (1977) Recognition of twointracellular cobalamin binding proteins and their identificationas methylmalonyl-CoA mutase and methioninesynthetase. Proc. Natl. Acad. Sci. U.S.A. 74, 921-925. https://doi.org/10.1073/pnas.74.3.921
  5. Mellman, I. S., Youngdahl-Turner, P., Willard, H. F. andRosenberg, L. E. (1977) Intracellular binding of radioactivehydroxocobalamin to cobalamin-dependent apoenzymesin rat liver. Proc. Natl. Acad. Sci. U.S.A. 74, 916-920. https://doi.org/10.1073/pnas.74.3.916
  6. Banerjee, R., Gherasim, C. and Padovani, D. (2009) Thetinker, tailor, soldier in intracellular $B_{12}$ trafficking. Curr.Opin. Chem. Biol. 13, 484-491. https://doi.org/10.1016/j.cbpa.2009.07.007
  7. Lerner-Ellis, J. P., Tirone, J. C., Pawelek, P. D., Dore, C.,Atkinson, J. L., Watkins, D., Morel, C. F., Fujiwara, T. M.,Moras, E., Hosack, A. R., Dunbar, G. V., Antonicka, H.,Forgetta, V., Dobson, C. M., Leclerc, D., Gravel, R. A.,Shoubridge, E. A., Coulton, J. W., Lepage, P., Rommens, J.M., Morgan, K. and Rosenblatt, D. S. (2006) Identification ofthe gene responsible for methylmalonic aciduria and homocystinuria,cblC type. Nat. Genet. 38, 93-100. https://doi.org/10.1038/ng1683
  8. Froese, D. S., Zhang, J., Healy, S. and Gravel, R. A. (2009)Mechanism of vitamin $B_{12}-responsiveness$ in cblC methylmalonic aciduria with homocystinuria. Mol. Genet. Metab. 98, 338-343. https://doi.org/10.1016/j.ymgme.2009.07.014
  9. Kim, J., Gherasim, C. and Banerjee, R. (2008) Decyanationof vitamin $B_{12}$ by a trafficking chaperone. Proc. Natl.Acad. Sci. U.S.A. 105, 14551-14554. https://doi.org/10.1073/pnas.0805989105
  10. Kim, J., Hannibal, L., Gherasim, C., Jacobsen, D. W. andBanerjee, R. (2009) A human vitamin $B_{12}$ trafficking proteinuses glutathione transferase activity for processingalkylcobalamins. J. Biol. Chem. 284, 33418-33424. https://doi.org/10.1074/jbc.M109.057877
  11. Brown, K. L. and Hakimi, J. M. (1984) HeteronuclearNMR studies of cobalamins. 3. 31P NMR of aquocobalaminand various organocobalamins. J. Am. Chem. Soc.106, 7894-7899. https://doi.org/10.1021/ja00337a043
  12. Xia, L., Cregan, A. G., Berben, L. A. and Brasch, N. E.(2004) Studies on the formation of glutathionylcobalamin:any free intracellular aquacobalamin is likely to be rapidlyand irreversibly converted to glutathionylcobalamin. Inorg.Chem. 43, 6848-6857. https://doi.org/10.1021/ic040022c
  13. Jacobsen, D., Troxell, L. S. and Brown, K. L. (1984) Catalysisof thiol oxidation by cobalamins and cobinamides:reaction products and kinetics. Biochemistry 23, 2017-2025. https://doi.org/10.1021/bi00304a021
  14. Ballatori, N., Krance, S. M., Notenboom, S., Shi, S., Tieu,K. and Hammond, C. L. (2009) Glutathione dysregulationand the etiology and progression of human diseases. Biol.Chem. 390, 191-214. https://doi.org/10.1515/BC.2009.033
  15. Jones, D. P. (2006) Redefining oxidative stress. Antioxid.Redox. Signal 8, 1865-1879. https://doi.org/10.1089/ars.2006.8.1865
  16. Drennan, C. L., Huang, S., Drummond, J. T., Matthews, R.G. and Lidwig, M. L. (1994) How a protein binds $B_{12}$: a3.0 ${\AA}$ X-ray structure of B12-binding domains of methioninesynthase. Science 266, 1669-1674. https://doi.org/10.1126/science.7992050
  17. Rutsch, F., Gailus, S., Miousse, I. R., Suormala, T., Sagne,C., Toliat, M. R., Nurnberg, G., Wittkampf, T., Buers, I.,Sharifi, A., Stucki, M., Becker, C., Baumgartner, M.,Robenek, H., Marquardt, T., Hohne, W., Gasnier, B.,Rosenblatt, D. S., Fowler, B. and Nurnberg, P. (2009)Identification of a putative lysosomal cobalamin exporteraltered in the cblF defect of vitamin $B_{12}$ metabolism. Nat. Genet. 41, 234-239. https://doi.org/10.1038/ng.294
  18. Stich, T. A., Yamanishi, M., Banerjee, R. and Brunold, T.C. (2005) Spectroscopic evidence for the formation of afour-coordinate $Co^{2+}$ cobalamin species upon binding tothe human ATP: cobalamin adenosyltransferase. J. Am.Chem. Soc. 127, 7660-7661. https://doi.org/10.1021/ja050546r
  19. Yamada, K., Gravel, R. A., Toraya, T. and Matthews, R. G.(2006) Human methionine synthase reductase is a molecularchaperone for human methionine synthase. Proc.Natl. Acad. Sci. U.S.A. 103, 9476-9481. https://doi.org/10.1073/pnas.0603694103
  20. Padovani, D., Labunska, T., Palfey, B. A., Ballou, D. P.and Banerjee, R. (2008) Adenosyltransferase tailors anddelivers coenzyme $B_{12}$. Nat. Chem. Biol. 4, 194-196. https://doi.org/10.1038/nchembio.67
  21. Lexa, D. and Saveant, J. M. (1983) The electrochemistry ofvitamin $B_{12}$. Acc. Chem. Res. 16, 235-243. https://doi.org/10.1021/ar00091a001
  22. Suto, R. K., Brasch, N. E., Anderson, O. P. and Finke, R. G. (2001) Synthesis, characterization, solution stability,and X-ray crystal structure of the thiolatocobalamin gamma-glutamylcysteinylcobalamin, a dipeptide analogue ofglutathionylcobalamin: insights into the enhanced Co-Sbond stability of the natural product glutathionylcobalamin.Inorg. Chem. 40, 2686-2692. https://doi.org/10.1021/ic001365n
  23. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning:a Laboratory Manual, 3rd ed., Cold Spring Harbor LaboratoryPress, Cold Spring Harbor, N.Y, USA.
  24. Babior, B. M. (1975) Cobalamin: biochemistry and pathophysiology.Wiley, New York, USA.
  25. Bradford, M. M. (1976) A rapid and sensitive method forthe quantitation of microgram quantities of protein utilizingthe principle of protein-dye binding. Anal. Biochem.72, 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Cited by

  1. Glutathione and Vitamin B12 Cooperate in Stabilization of a B12 Trafficking Chaperone Protein vol.31, pp.2, 2012, https://doi.org/10.1007/s10930-011-9385-2
  2. C-terminal truncation of a bovine B12trafficking chaperone enhances the sensitivity of the glutathione-regulated thermostability vol.46, pp.3, 2013, https://doi.org/10.5483/BMBRep.2013.46.3.158
  3. Glutathione metabolism in cobalamin deficiency type C (cblC) vol.37, pp.1, 2014, https://doi.org/10.1007/s10545-013-9605-3
  4. Processing of glutathionylcobalamin by a bovine B12 trafficking chaperone bCblC involved in intracellular B12 metabolism vol.443, pp.1, 2014, https://doi.org/10.1016/j.bbrc.2013.11.075
  5. Glutathione increases the binding affinity of a bovine B12 trafficking chaperone bCblC for vitamin B12 vol.412, pp.2, 2011, https://doi.org/10.1016/j.bbrc.2011.07.103
  6. Glutathione-dependent One-electron Transfer Reactions Catalyzed by a B12Trafficking Protein vol.289, pp.23, 2014, https://doi.org/10.1074/jbc.M114.567339
  7. Identification of anti-adipogenic proteins in adult bovine serum suppressing 3T3-L1 preadipocyte differentiation vol.46, pp.12, 2013, https://doi.org/10.5483/BMBRep.2013.46.12.082
  8. Destabilization of a bovine B12 trafficking chaperone protein by oxidized form of glutathione vol.420, pp.3, 2012, https://doi.org/10.1016/j.bbrc.2012.03.031
  9. Pathogenic Mutations Differentially Affect the Catalytic Activities of the Human B12-processing Chaperone CblC and Increase Futile Redox Cycling vol.290, pp.18, 2015, https://doi.org/10.1074/jbc.M115.637132