Structural insights into the MMACHC-MMADHC protein complex involved in vitamin B12 trafficking

Journal of Biological Chemistry

Volumn 290, Issue 49, 2015, Pages 29167-29177

  Froese, D Sean ^a,b   Kopec, Jolanta ^c   Fitzpatrick, Fiona ^c   Schuller, Marion ^c   McCorvie, Thomas J ^c   Chalk, Rod ^c   Plessl, Tanja ^a   Fettelschoss, Victoria ^a   Fowler, Brian ^a   Baumgartner, Matthias R ^a,b   Yue, Wyatt W ^c  

^a UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYMES; TRACE ELEMENTS; X RAY SCATTERING;

DIFFERENT MECHANISMS; ENZYMATIC ACTIVITIES; INTRACELLULAR PROTEINS; METHIONINE SYNTHASE; METHYLMALONYL-COA MUTASE; PROTEIN-PROTEIN INTERACTIONS; SEQUENCE CONSERVATION; STRUCTURAL INSIGHTS;

PROTEINS;

CBL PROTEIN; CYANOCOBALAMIN; HETERODIMER; NITROREDUCTASE; PROTEIN MMACHC; PROTEIN MMADHC; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHAPERONE; MMACHC PROTEIN, HUMAN; MMADHC PROTEIN, HUMAN; MMADHC PROTEIN, MOUSE; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; MISSENSE MUTATION; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; TRANSPORT KINETICS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; METABOLIC DISORDER; METABOLISM; MOLECULAR GENETICS; MOUSE; MUTATION; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; HUMANS; METABOLIC DISEASES; MICE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NITROREDUCTASES; PHENOTYPE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; VITAMIN B 12;

EID: 84948966489     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.683268     Document Type: Article

References (40)

1. Watkins, D., and Rosenblatt, D. S. (2014) Inherited disorders of folate and cobalamin transport and metabolism. in The Online Metabolic and Molecular Bases of Inherited Disease (Valle, D., Beaudet, A. L., Vogelstein, B., Kinzler, K. W., Antonarakis, S. E., Ballabio, A., Gibson, M., and Mitchell, G., eds), McGraw-Hill, New York
2. Froese, D. S., and Gravel, R. A. (2010) Genetic disorders of vitamin B metabolism: eight complementation groups-eight genes. Expert Rev. Mol. Med. 12, e37
3. Gherasim, C., Lofgren, M., and Banerjee, R. (2013) Navigating the B12 road: assimilation, delivery, and disorders of cobalamin. J. Biol. Chem. 288, 13186-13193
4. Baumgartner, M. R. (2013) Vitamin-responsive disorders: cobalamin, folate, biotin, vitamins B1 and E. Handb. Clin. Neurol. 113, 1799-1810
5. Harding, C. O., Arnold, G., Barness, L. A., Wolff, J. A., and Rosenblatt, D. S. (1997) Functional methionine synthase deficiency due to cblG disorder: a report of two patients and a review. Am. J. Med. Genet. 71, 384-390
6. Hörster, F., Baumgartner, M. R., Viardot, C., Suormala, T., Burgard, P., Fowler, B., Hoffmann, G. F., Garbade, S. F., Kölker, S., and Baumgartner, E. R. (2007) Long-term outcome in methylmalonic acidurias is influenced by the underlying defect (mut0, mut, cblA, cblB). Pediatr. Res. 62, 225-230
7. Fowler, B., Leonard, J. V., and Baumgartner, M. R. (2008) Causes of and diagnostic approach to methylmalonic acidurias. J. Inherit. Metab. Dis. 31, 350-360
8. Lerner-Ellis, J. P., Anastasio, N., Liu, J., Coelho, D., Suormala, T., Stucki, M., Loewy, A. D., Gurd, S., Grundberg, E., Morel, C. F., Watkins, D., Baumgartner, M. R., Pastinen, T., Rosenblatt, D. S., and Fowler, B. (2009) Spectrum of mutations in MMACHC, allelic expression, and evidence for genotype-phenotype correlations. Hum. Mutat. 30, 1072-1081
9. Suormala, T., Baumgartner, M. R., Coelho, D., Zavadakova, P., Kozich, V., Koch, H. G., Berghaüser, M., Wraith, J. E., Burlina, A., Sewell, A., Herwig, J., and Fowler, B. (2004) The cblD defect causes either isolated or combined deficiency of methylcobalamin and adenosylcobalamin synthesis. J. Biol. Chem. 279, 42742-42749
10. Coelho, D., Suormala, T., Stucki, M., Lerner-Ellis, J. P., Rosenblatt, D. S., Newbold, R. F., Baumgartner, M. R., and Fowler, B. (2008) Gene identification for the cblD defect of vitamin B12 metabolism. N. Engl. J. Med. 358, 1454-1464
11. Stucki, M., Coelho, D., Suormala, T., Burda, P., Fowler, B., and Baumgartner, M. R. (2012) Molecular mechanisms leading to three different phenotypes in the cblD defect of intracellular cobalamin metabolism. Hum. Mol. Genet. 21, 1410-1418
12. Jusufi, J., Suormala, T., Burda, P., Fowler, B., Froese, D. S., and Baumgartner, M. R. (2014) Characterization of functional domains of the cblD (MMADHC) gene product. J. Inherit. Metab. Dis. 37, 841-849
13. Deme, J. C., Miousse, I. R., Plesa, M., Kim, J. C., Hancock, M. A., Mah, W., Rosenblatt, D. S., and Coulton, J. W. (2012) Structural features of recombinant MMADHC isoforms and their interactions with MMACHC, proteins of mammalian vitamin B12 metabolism. Mol. Genet. Metab. 107, 352-362
14. Gherasim, C., Hannibal, L., Rajagopalan, D., Jacobsen, D. W., and Banerjee, R. (2013) The C-terminal domain of CblD interacts with CblC and influences intracellular cobalamin partitioning. Biochimie 95, 1023-1032
15. Plesa, M., Kim, J., Paquette, S. G., Gagnon, H., Ng-Thow-Hing, C., Gibbs, B. F., Hancock, M. A., Rosenblatt, D. S., and Coulton, J. W. (2011) Interaction between MMACHC and MMADHC, two human proteins participating in intracellular vitamin B12 metabolism. Mol. Genet. Metab. 102, 139-148
16. Froese, D. S., Krojer, T., Wu, X., Shrestha, R., Kiyani, W., von Delft, F., Gravel, R. A., Oppermann, U., and Yue, W. W. (2012) Structure of MMACHC reveals an arginine-rich pocket and a domain-swapped dimer for its B12 processing function. Biochemistry 51, 5083-5090
17. Koutmos, M., Gherasim, C., Smith, J. L., and Banerjee, R. (2011) Structural basis of multifunctionality in a vitamin B12-processing enzyme. J. Biol. Chem. 286, 29780-29787
18. Froese, D. S., Zhang, J., Healy, S., and Gravel, R. A. (2009) Mechanism of vitamin B12-responsiveness in cblC methylmalonic aciduria with homocystinuria. Mol. Genet. Metab. 98, 338-343
19. Kim, J., Gherasim, C., and Banerjee, R. (2008) Decyanation of vitamin B12 by a trafficking chaperone. Proc. Natl. Acad. Sci. U.S.A. 105, 14551-14554
20. Hannibal, L., Kim, J., Brasch, N. E., Wang, S., Rosenblatt, D. S., Banerjee, R., and Jacobsen, D. W. (2009) Processing of alkylcobalamins in mammalian cells: A role for the MMACHC (cblC) gene product. Mol. Genet. Metab. 97, 260-266
21. Froese, D. S., Healy, S., McDonald, M., Kochan, G., Oppermann, U., Niesen, F. H., and Gravel, R. A. (2010) Thermolability of mutant MMACHC protein in the vitamin B12-responsive cblC disorder. Mol. Genet. Metab. 100, 29-36
22. Sheldrick, G. M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485
23. Cowtan, K. (2006) The Buccaneer software for automated model building. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011
24. Terwilliger, T. C., Adams, P. D., Read, R. J., McCoy, A. J., Moriarty, N. W., Grosse-Kunstleve, R. W., Afonine, P. V., Zwart, P. H., and Hung, L. W. (2009) Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr. D Biol. Crystallogr. 65, 582-601
25. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
26. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
27. Foerster, S., Apostol, L., and Bras, W. (2010) Scatter: software for the analysis of nano- and mesoscale small-angle scattering. J. Appl. Crystallogr. 43, 639-646
28. Petoukhov, M. V., Franke, D., Shkumatov, A. V., Tria, G., Kikhney, A. G., Gajda, M., Gorba, C., Mertens, H. D., Konarev, P. V., and Svergun, D. I. (2012) New developments in the program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350
29. Niesen, F. H., Berglund, H., and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2, 2212-2221
30. Kim, J., Hannibal, L., Gherasim, C., Jacobsen, D. W., and Banerjee, R. (2009) A human vitamin B12 trafficking protein uses glutathione transferase activity for processing alkylcobalamins. J. Biol. Chem. 284, 33418-33424
31. Li, Z., Gherasim, C., Lesniak, N. A., and Banerjee, R. (2014) Glutathionedependent one-electron transfer reactions catalyzed by a B12 trafficking protein. J. Biol. Chem. 289, 16487-16497
32. Gherasim, C., Ruetz, M., Li, Z., Hudolin, S., and Banerjee, R. (2015) Pathogenic mutations differentially affect the catalytic activities of the human B12-processing chaperone CblC and increase futile redox cycling. J. Biol. Chem. 290, 11393-11402
33. McWilliam, H., Li, W., Uludag, M., Squizzato, S., Park, Y. M., Buso, N., Cowley, A. P., and Lopez, R. (2013) Analysis Tool Web Services from the EMBL-EBI. Nucleic Acids Res. 41, W597-W600
34. Mertens, H. D., and Svergun, D. I. (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J. Struct. Biol. 172, 128-141
35. Pierce, B. G., Wiehe, K., Hwang, H., Kim, B. H., Vreven, T., and Weng, Z. (2014) ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers. Bioinformatics 30, 1771-1773
36. Wassenaar, T., van Dijk, M., Loureiro-Ferreira, N., van der Schot, G., de Vries, S., Schmitz, C., van der Zwan, J., Boelens, R., Giachetti, A., Ferella, L., Rosato, A., Bertini, I., Herrmann, T., Jonker, H. A., Bagaria, A., Jaravine, V., Güntert, P., Schwalbe, H., Vranken, W., Doreleijers, J., Vriend, G., Vuister, G., Franke, D., Kikhney, A., Svergun, D., Fogh, R., Ionides, J., Laue, E., Spronk, C., Jurks?a, S., Verlato, M., Badoer, S., Dal Pra, S., Mazzucato, M., Frizziero, E., and Bonvin, A. J. J. (2012) WeNMR: structural biology on the grid. J. Grid Computing 10, 743-767
37. Mah, W., Deme, J. C., Watkins, D., Fung, S., Janer, A., Shoubridge, E. A., Rosenblatt, D. S., and Coulton, J. W. (2013) Subcellular location of MMACHC and MMADHC, two human proteins central to intracellular vitamin B12 metabolism. Mol. Genet. Metab. 108, 112-118
38. Fofou-Caillierez, M. B., Mrabet, N. T., Chéry, C., Dreumont, N., Flayac, J., Pupavac, M., Paoli, J., Alberto, J. M., Coelho, D., Camadro, J. M., Feillet, F., Watkins, D., Fowler, B., Rosenblatt, D. S., and Guéant, J. L. (2013) Interaction between methionine synthase isoforms and MMACHC: characterization in cblG-variant, cblG and cblC inherited causes of megaloblastic anaemia. Hum. Mol. Genet. 22, 4591-4601
39. Franke, D., and Svergun, D. I. (2009) DAMMIF, a program for rapid abinitio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346
40. Yamada, K., Gherasim, C., Banerjee, R., and Koutmos, M. (2015) Structure of human B12 trafficking protein Cb1D reveals molecular mimicry and identifies a new subfamily of nitro-FMN reductases. J. Biol. Chem. 290, 29155-29166