Reconstitution of formylglycine-generating enzyme with copper(II) for aldehyde tag conversion

Journal of Biological Chemistry

Volumn 290, Issue 25, 2015, Pages 15730-15745

  Holder, Patrick G ^a   Jones, Lesley C ^a   Drake, Penelope M ^a   Barfield, Robyn M ^a   Bañas, Stefanie ^a   De Hart, Gregory W ^a   Baker, Jeanne ^a   Rabuka, David ^a  

^a CATALENT PHARMA SOLUTIONS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDES; AMINO ACIDS; ANTIBODIES; BIOSYNTHESIS; ENZYMES; MONOCLONAL ANTIBODIES; RECOMBINANT PROTEINS;

BIOCATALYTIC REACTION; BIOTECHNOLOGY APPLICATIONS; COFACTORS; FORMYLGLYCINE-GENERATING ENZYMES; HOMO SAPIENS; STREPTOMYCES COELICOLOR; TAGGED PROTEINS; TURNOVER RATE;

COPPER;

ALDEHYDE; COPPER; CYSTEINE; ENZYME; FORMYLGLYCINE; FORMYLGLYCINE GENERATING ENZYME; GLYCINE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; COENZYME; SULFATASE; SUMF1 PROTEIN, HUMAN;

ARTICLE; BIOCATALYSIS; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME RECONSTITUTION; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; OXIDATION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; RATE CONSTANT; X RAY CRYSTALLOGRAPHY; CHEMISTRY; COENZYME; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; STREPTOMYCES COELICOLOR;

EUKARYOTA; HOMO SAPIENS; PROKARYOTA; STREPTOMYCES COELICOLOR;

BACTERIAL PROTEINS; COENZYMES; COPPER; CYSTEINE; HUMANS; STREPTOMYCES COELICOLOR; SULFATASES;

EID: 84940198874     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.652669     Document Type: Article

References (51)

1. Dierks, T., Schmidt, B., and von Figura, K. (1997) Conversion of cysteine to formylglycine: a protein modification in the endoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 94, 11963-11968
2. Dierks, T., Lecca, M. R., Schlotterhose, P., Schmidt, B., and von Figura, K. (1999) Sequence determinants directing conversion of cysteine to formylglycine in eukaryotic sulfatases. EMBO J. 18, 2084-2091
3. Landgrebe, J., Dierks, T., Schmidt, B., and von Figura, K. (2003) The human SUMF1 gene, required for posttranslational sulfatase modification, defines a new gene family which is conserved from pro- to eukaryotes. Gene 316, 47-56
4. von Figura, K., Schmidt, B., Selmer, T., and Dierks, T. (1998) A novel protein modification generating an aldehyde group in sulfatases: its role in catalysis and disease. BioEssays 20, 505-510
5. Dierks, T., Schmidt, B., Borissenko, L. V., Peng, J., Preusser, A., Mariappan, M., and von Figura, K. (2003) Multiple sulfatase deficiency is caused by mutations in the gene encoding the human Cα-formylglycine generating enzyme. Cell 113, 435-444
6. Roeser, D., Preusser-Kunze, A., Schmidt, B., Gasow, K., Wittmann, J. G., Dierks, T., von Figura, K., and Rudolph, M. G. (2006) A general binding mechanism for all human sulfatases by the formylglycine-generating enzyme. Proc. Natl. Acad. Sci. U.S.A. 103, 81-86
7. Preusser-Kunze, A., Mariappan, M., Schmidt, B., Gande, S. L., Mutenda, K., Wenzel, D., von Figura, K., and Dierks, T. (2005) Molecular characterization of the human Cα-formylglycine-generating enzyme. J. Biol. Chem. 280, 14900-14910
8. Dierks, T., Dickmanns, A., Preusser-Kunze, A., Schmidt, B., Mariappan, M., von Figura, K., Ficner, R., and Rudolph, M. G. (2005) Molecular basis for multiple sulfatase deficiency and mechanism for formylglycine generation of the human formylglycine-generating enzyme. Cell 121, 541-552
9. Carlson, B. L., Ballister, E. R., Skordalakes, E., King, D. S., Breidenbach, M. A., Gilmore, S. A., Berger, J. M., and Bertozzi, C. R. (2008) Function and structure of a prokaryotic formylglycine-generating enzyme. J. Biol. Chem. 283, 20117-20125
10. Wu, P., Shui, W., Carlson, B. L., Hu, N., Rabuka, D., Lee, J., and Bertozzi, C. R. (2009) Site-specific chemical modification of recombinant proteins produced in mammalian cells by using the genetically encoded aldehyde tag. Proc. Natl. Acad. Sci. U.S.A. 106, 3000-3005
11. Rabuka, D., Rush, J. S., deHart, G. W., Wu, P., and Bertozzi, C. R. (2012) Site-specific chemical protein conjugation using genetically encoded aldehyde tags. Nat. Protoc. 7, 1052-1067
12. Appel, M. J., and Bertozzi, C. R. (2015) Formylglycine, a post-translationally generated residue with unique catalytic capabilities and biotechnology applications. ACS Chem. Biol. 10, 72-84
13. Lang, K., and Chin, J. W. (2014) Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins. Chem. Rev. 114, 4764-4806
14. Patterson, D. M., Nazarova, L. A., and Prescher, J. A. (2014) Finding the right (bioorthogonal) chemistry. ACS Chem. Biol. 9, 592-605
15. Zhou, Q., Stefano, J. E., Manning, C., Kyazike, J., Chen, B., Gianolio, D. A., Park, A., Busch, M., Bird, J., Zheng, X., Simonds-Mannes, H., Kim, J., Gregory, R. C., Miller, R. J., Brondyk, W. H., Dhal, P. K., and Pan, C. Q. (2014) Site-specific antibody-drug conjugation through glycoengineering. Bioconjug. Chem. 25, 510-520
16. Agarwal, P., van der Weijden, J., Sletten, E. M., Rabuka, D., and Bertozzi, C. R. (2013) A Pictet-Spengler ligation for protein chemical modification. Proc. Natl. Acad. Sci. U.S.A. 110, 46-51
17. Agarwal, P., Kudirka, R., Albers, A. E., Barfield, R. M., de Hart, G. W., Drake, P. M., Jones, L. C., and Rabuka, D. (2013) Hydrazino-Pictet-Spengler ligation as a biocompatible method for the generation of stable protein conjugates. Bioconjug. Chem. 24, 846-851
18. Sasaki, T., Kodama, K., Suzuki, H., Fukuzawa, S., and Tachibana, K. (2008) N-terminal labeling of proteins by the Pictet-Spengler reaction. Bioorg. Med. Chem. Lett. 18, 4550-4553
19. Kudirka, R., Barfield, R. M., McFarland, J., Albers, A. E., de Hart, G. W., Drake, P. M., Holder, P. G., Banas, S., Jones, L. C., Garofalo, A. W., and Rabuka, D. (2015) Generating site-specifically modified proteins via a versatile and stable nucleophilic carbon ligation. Chem. Biol. 22, 293-298
20. Roeser, D., Dickmanns, A., Gasow, K., and Rudolph, M. G. (2005) De novo calcium/sulfur SAD phasing of the human formylglycine-generating enzyme using in-house data. Acta Crystallogr. D Biol. Crystallogr. 61, 1057-1066
21. Roeser, D., Schmidt, B., Preusser-Kunze, A., and Rudolph, M. G. (2007) Probing the oxygen-binding site of the human formylglycine-generating enzyme using halide ions. Acta Crystallogr. D Biol. Crystallogr. 63, 621-627
22. Mariappan, M., Gande, S. L., Radhakrishnan, K., Schmidt, B., Dierks, T., and von Figura, K. (2008) The non-catalytic N-terminal extension of formylglycine-generating enzyme is required for its biological activity and retention in the endoplasmic reticulum. J. Biol. Chem. 283, 11556-11564
23. Solomon, E. I., Heppner, D. E., Johnston, E. M., Ginsbach, J. W., Cirera, J., Qayyum, M., Kieber-Emmons, M. T., Kjaergaard, C. H., Hadt, R. G., and Tian, L. (2014) Copper active sites in biology. Chem. Rev. 114, 3659-3853
24. Tipton, K. F., Armstrong, R. N., Bakker, B. M., Bairoch, A., Cornish-Bowden, A., Halling, P. J., Hofmeyr, J.-H., Leyh, T. S., Kettner, C., Raushel, F. M., Rohwer, J., Schomburg, D., and Steinbeck, C. (2014) Standards for reporting enzyme data: the STRENDA consortium: what it aims to do and why it should be helpful. Perspect. Sci. 1, 131-137
25. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., and MacCoss, M. J. (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968
26. Carrico, I. S., Carlson, B. L., and Bertozzi, C. R. (2007) Introducing genetically encoded aldehydes into proteins. Nat. Chem. Biol. 3, 321-322
27. Bleck, G. T. (2006) An alternative method for the rapid generation of stable, high-expressing mammalian cell lines. BioProcess. J. 5, 36-42
28. Peng, H., Cheng, Y., Dai, C., King, A. L., Predmore, B. L., Lefer, D. J., and Wang, B. (2011) A fluorescent probe for fast and quantitative detection of hydrogen sulfide in blood. Angew. Chem. Int. Ed. 50, 9672-9675
29. Montoya, L. A., and Pluth, M. D. (2012) Selective turn-on fluorescent probes for imaging hydrogen sulfide in living cells. Chem. Commun. 48, 4767-4769
30. Boeker, E. A. (1984) Integrated rate equations for enzyme-catalysed first-order and second-order reactions. Biochem. J. 223, 15-22
31. Boeker, E. A. (1985) Integrated rate equations for irreversible enzyme-catalysed first-order and second-order reactions. Biochem. J. 226, 29-35
32. Mariappan, M., Radhakrishnan, K., Dierks, T., Schmidt, B., and von Figura, K. (2008) ERp44 mediates a thiol-independent retention of formylglycine-generating enzyme in the endoplasmic reticulum. J. Biol. Chem. 283, 6375-6383
33. Ennemann, E. C., Radhakrishnan, K., Mariappan, M., Wachs, M., Pringle, T. H., Schmidt, B., and Dierks, T. (2013) Proprotein convertases process and thereby inactivate formylglycine-generating enzyme. J. Biol. Chem. 288, 5828-5839
34. Saaranen, M. J., Karala, A.-R., Lappi, A.-K., and Ruddock, L. W. (2010) The role of dehydroascorbate in disulfide bond formation. Antioxid. Redox Signal. 12, 15-25
35. Capozzi, G., and Modena, G. (1974) Oxidation of thiols. in The Thiol Group (Patai, S., ed) pp. 785-839 John Wiley & Sons, Ltd., Chichester, UK
36. McGuirl, M. A., Brown, D. E., and Dooley, D. M. (1997) Cyanide as a copper-directed inhibitor of amine oxidases: implications for the mechanism of amine oxidation. J. Biol. Inorg. Chem. 2, 336-342
37. Whittaker, M. M., and Whittaker, J. W. (1993) Ligand interactions with galactose oxidase: mechanistic insights. Biophys. J. 64, 762-772
38. Blackburn, N. J., Collison, D., Sutton, J., and Mabbs, F. E. (1984) Kinetic and e.p.r. studies of cyanide and azide binding to the copper sites of dopamine (3,4-dihydroxyphenethylamine) β-mono-oxygenase. Biochem. J. 220, 447-454
39. Kishishita, S., Okajima, T., Kim, M., Yamaguchi, H., Hirota, S., Suzuki, S., Kuroda, S., Tanizawa, K., and Mure, M. (2003) Role of copper ion in bacterial copper amine oxidase: spectroscopic and crystallographic studies of metal-substituted enzymes. J. Am. Chem. Soc. 125, 1041-1055
40. Sun, M. M., Beam, K. S., Cerveny, C. G., Hamblett, K. J., Blackmore, R. S., Torgov, M. Y., Handley, F. G., Ihle, N. C., Senter, P. D., and Alley, S. C. (2005) Reduction-alkylation strategies for the modification of specific monoclonal antibody disulfides. Bioconjug. Chem. 16, 1282-1290
41. Szajewski, R. P., and Whitesides, G. M. (1980) Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione. J. Am. Chem. Soc. 102, 2011-2026
42. Klinman, J. P. (2006) The copper-enzyme family of dopamine β-monooxygenase and peptidylglycine α-hydroxylating monooxygenase: resolving the chemical pathway for substrate hydroxylation. J. Biol. Chem. 281, 3013-3016
43. Bertolotti-Ciarlet, A., Wang, W., Lownes, R., Pristatsky, P., Fang, Y., McKelvey, T., Li, Y., Li, Y., Drummond, J., Prueksaritanont, T., and Vlasak, J. (2009) Impact of methionine oxidation on the binding of human IgG1 to FcRn and Fcγ receptors. Mol. Immunol. 46, 1878-1882
44. Wang, W., Vlasak, J., Li, Y., Pristatsky, P., Fang, Y., Pittman, T., Roman, J., Wang, Y., Prueksaritanont, T., and Ionescu, R. (2011) Impact of methionine oxidation in human IgG1 Fc on serum half-life of monoclonal antibodies. Mol. Immunol. 48, 860-866
45. Farver, O., and Pecht, I. (2011) Electron transfer in blue copper proteins. Coord. Chem. Rev. 255, 757-773
46. Gande, S. L., Mariappan, M., Schmidt, B., Pringle, T. H., von Figura, K., and Dierks, T. (2008) Paralog of the formylglycine-generating enzyme-retention in the endoplasmic reticulum by canonical and noncanonical signals: ER retention by noncanonical retention signals. FEBS J. 275, 1118-1130
47. Ito, N., Phillips, S. E., Stevens, C., Ogel, Z. B., McPherson, M. J., Keen, J. N., Yadav, K. D., and Knowles, P. F. (1991) Novel thioether bond revealed by a 1.7-Å crystal structure of galactose oxidase. Nature 350, 87-90
48. Finney, J., Moon, H.-J., Ronnebaum, T., Lantz, M., and Mure, M. (2014) Human copper-dependent amine oxidases. Arch. Biochem. Biophys. 546, 19-32
49. Weinberg, D. R., Gagliardi, C. J., Hull, J. F., Murphy, C. F., Kent, C. A., Westlake, B. C., Paul, A., Ess, D. H., McCafferty, D. G., and Meyer, T. J. (2012) Proton-coupled electron transfer. Chem. Rev. 112, 4016-4093
50. Hammes-Schiffer, S. (2012) Proton-coupled electron transfer: classification scheme and guide to theoretical methods. Energy Environ. Sci. 5, 7696-7703
51. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy server. in The Proteomics Protocols Handbook (Walker, J. M., ed) pp. 571-607, Humana Press, Totowa, NJ