Addressing Shewanella oneidensis "cytochromome": The first step towards high-throughput expression of cytochromes c

Protein Expression and Purification

Volumn 62, Issue 1, 2008, Pages 128-137

  Londer, Yuri Y ^a   Giuliani, Sarah E ^a   Peppler, Terese ^a   Collart, Frank R ^a  

^a ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

Cytochrome c; High throughput; Ligation independent cloning; Periplasmic expression; Protein expression; Shewanella oneidensis

Indexed keywords

BACTERIAL PROTEIN; CYTOCHROME C; HYBRID PROTEIN; LIGAND;

ARTICLE; BIOSYNTHESIS; CYTOPLASM; GENETICS; METABOLISM; MOLECULAR CLONING; SHEWANELLA;

BACTERIAL PROTEINS; CLONING, MOLECULAR; CYTOCHROMES C; LIGANDS; PERIPLASM; RECOMBINANT FUSION PROTEINS; SHEWANELLA;

SHEWANELLA ONEIDENSIS;

EID: 52949132999     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2008.06.014     Document Type: Article

References (50)

1. Thöny-Meyer L., Fischer F., Kunzler P., Ritz D., and Hennecke H. Escherichia coli genes required for cytochrome c maturation. J. Bacteriol. 177 (1995) 4321-4326
2. Thöny-Meyer L. Biogenesis of respiratory cytochromes in bacteria. Microbiol. Mol. Biol. Rev. 61 (1997) 337-376
3. Page M.D., Sambongi Y., and Ferguson S.J. Contrasting routes of c-type cytochrome assembly in mitochondria chloroplasts and bacteria. Trends Biochem. Sci. 23 (1998) 103-108
4. Thöny-Meyer L. Haem-polypeptide interactions during cytochrome c maturation. Biochim. Biophys. Acta 1459 (2000) 316-324
5. Kranz R., Lill R., Goldman B., Bonnard G., and Merchant S. Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol. Microbiol. 29 (1998) 383-396
6. Grove J., Tanapongpipat S., Thomas G., Griffiths L., Crooke H., and Cole J. Escherichia coli K-12 genes essential for the synthesis of c-type cytochromes and a third nitrate reductase located in the periplasm. Mol. Microbiol. 19 (1996) 467-481
7. 3 oxidase in Escherichia coli. Biochem. Biophys. Res. Commun. 251 (1998) 744-747
8. Londer Y.Y., Pokkuluri P.R., Erickson J., Orshonsky V., and Schiffer M. Heterologous expression of hexaheme fragments of a multidomain cytochrome from Geobacter sulfurreducens representing a novel class of cytochromes c. Protein Expr. Purif. 39 (2005) 254-260
9. Londer Y.Y., Pokkuluri P.R., Orshonsky V., Orshonsky L., and Schiffer M. Heterologous expression of dodecaheme "Nanowire" Cytochromes c from Geobacter sulfurreducens. Protein Expr. Purif. 47 (2006) 241-248
10. Sanders C., and Lill H. Expression of prokaryotic and eukaryotic cytochromes c in Escherichia coli. Biochim. Biophys. Acta 1459 (2000) 131-138
11. Heidelberg J.F., Paulsen I.T., Nelson K.E., Gaidos E.J., Nelson W.C., et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat. Biotechnol. 20 (2002) 1118-1123
12. Meyer T.E., TsapinI A.I., Vandenberghe I., de Smet L., Frishman D., Nealson K.H., Cusanovich M.A., and van Beeumen J.J. Identification of 42 possible cytochrome C genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 8 (2004) 57-77
13. Myers C.R., and Myers J.M. Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J. Bacteriol. 179 (1997) 1143-1152
14. Beliaev A.S., and Saffarini D.A. Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J. Bacteriol. 180 (1998) 6292-6297
15. Beliaev A.S., Saffarini D.A., McLaughlin J.L., and Hunnicut D. MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol. Microbiol. 39 (2001) 722-730
16. Myers J.M., and Myers C.R. Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl. Environ. Microbiol. 67 (2001) 260-269
17. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. second ed. (1989), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
18. Bothmann H., and Plückthun A. Selection for a periplasmic factor improving phage display and functional periplasmic expression. Nat. Biotechnol. 16 (1998) 376-380
19. Schäfer U., Beck K., and Müller M. Skp, a molecular chaperone of gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J. Biol. Chem. 274 (1999) 24567-24574
20. Mavrangelos C., Thiel M., Adamson P.J., Millard D.J., Nobbs S., Zola H., and Nicholson I.C. Increased yield and activity of soluble single-chain antibody fragments by combining high-level expression and the Skp periplasmic chaperonin. Protein Expr. Purif. 23 (2001) 289-295
21. Bothmann H., and Plückthun A. The periplasmic Escherichia coli peptidylprolyl cis, trans-isomerase FkpA. I. Increased functional expression of antibody fragments with and without cis-proline. J. Biol. Chem. 275 (2000) 17100-17105
22. Arié J.P., Sassoon N., and Betton J.M. Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol. Microbiol. 39 (2001) 199-210
23. Donnelly M.I., Zhou M., Millard C.S., Clancy S., Stols L., Eschenfeldt W.H., Collart F.R., and Joachimiak A. An expression vector tailored for large-scale, high-throughput purification of recombinant proteins. Protein Expr. Purif. 47 (2006) 446-454
24. Skerra A., Pfitzinger I., and Plückthun A. The functional expression of antibody Fv fragments in Escherichia coli: improved vectors and a generally applicable purification technique. Biotechnology (New York) 9 (1991) 273-278
25. 7 from Geobacter sulfurreducens in Escherichia coli. Biochim. Biophys. Acta 1554 (2002) 202-211
26. Nielsen H., Engelbrecht J., Brunak S., and von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10 (1997) 1-6
27. Bendtsen J.D., Nielsen H., von Heijne G., and Brunak S. Improved prediction of signal peptides: SignalP 3. 0. J. Mol. Biol. 340 (2004) 783-795
28. Juncker A.S., Willenbrock H., von Heijne G., Nielsen H., Brunak S., and Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12 (2003) 1652-1662
29. Tusnády G.E., and Simon I. The HMMTOP transmembrane topology prediction server. Bioinformatics 17 (2001) 849-850
30. Hirokawa T., Boon-Chieng S., and Mitaku S. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14 (1998) 378-379
31. Krogh A., Larsson B., von Heijne G., and Sonnhammer E.L.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305 (2001) 567-580
32. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
33. Stols L., Gu M., Dieckman L., Raffen R., Collart F.R., and Donnelly M.I. A new vector for high-throughput ligation-independent cloning encoding a tobacco etch virus protease cleavage site. Protein Expr. Purif. 25 (2002) 8-15
34. Yoon J.R., Laible P.D., Gu M., Scott H.N., and Collart F.R. Express primer tool for high-throughput gene cloning and expression. Biotechniques 33 (2002) 1328-1333
35. Dieckman L., Gu M., Stols L., Donnelly M.I., and Collart F.R. High throughput methods for gene cloning and expression. Protein Expr. Purif. 25 (2002) 1-7
36. Hoover D.M., and Lubkowski J. DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res. 30 (2002) e43
37. Wu G., Wolf J.B., Ibrahim A.F., Vadasz S., Gunasinghe M., and Freeland S.J. Simplified gene synthesis: a one-step approach to PCR-based gene construction. J. Biotechnol. 124 (2006) 496-503
38. Feissner R., Xiang Y., and Kranz R.G. Chemiluminescent-based methods to detect subpicomole levels of c-type cytochromes. Anal. Biochem. 315 (2003) 90-94
39. Londer Y.Y., Dementieva I.S., D'Ausilio C.A., Pokkuluri P.R., and Schiffer M. Characterization of a c-type heme-containing PAS sensor domain from Geobacter sulfurreducens representing a novel family of periplasmic sensors in Geobacteraceae and other bacteria. FEMS Microbiol. Lett. 258 (2006) 173-181
40. Brigé A., Cole J.A., Hagen W.R., Guisez Y., and Van Beeumen J.J. Overproduction, purification and novel redox properties of the dihaem cytochrome c, NapB, from Haemophilus influenzae. Biochem. J. 356 (2001) 851-858
41. Pokkuluri P.R., Pessanha M., Londer Y.Y., Wood S.J., Duke N.E.C., Wilton R., Catarino T., Salgueiro C.A., and Schiffer M. Structures and solution properties of two novel periplasmic sensor domains with c-type heme from chemotaxis proteins of Geobacter sulfurreducens: implications for signal transduction. J. Mol. Biol. 377 (2008) 1498-1517
42. Keiler K.C., and Sauer R.T. Sequence determinants of C-terminal substrate recognition by the Tsp protease. J. Biol. Chem. 271 (1996) 2589-2593
43. 7-type three-heme cytochrome domain from a multidomain cytochrome c polymer. Protein Sci. 13 (2004) 1684-1692
44. Morgado L., Bruix M., Londer Y.Y., Pokkuluri P.R., Schiffer M., and Salgueiro C.A. Redox-linked conformational changes of a multiheme cytochrome from Geobacter sulfurreducens. Biochem. Biophys. Res. Commun. 360 (2007) 194-198
45. Kapust R.B., and Waugh D.S. Controlled intracellular processing of fusion proteins by TEV protease. Protein Expr. Purif. 19 (2000) 312-318
46. Braun M., and Thöny-Meyer L. Biosynthesis of artificial microperoxidases by exploiting the secretion and cytochrome c maturation apparatuses of Escherichia coli. Proc. Natl. Acad. Sci. USA 101 (2004) 12830-12835
47. Braun M., Rubio I.G., and Thöny-Meyer L. A heme tag for in vivo synthesis of artificial cytochromes. Appl. Microbiol. Biotechnol. 67 (2005) 234-239
48. Enguita F.J., Pohl E., Turner D.L., Santos H., and Carrondo M.A. Structural evidence for a proton transfer pathway coupled with haem reduction of cytochrome c" from Methylophilus methylotrophus. J. Biol. Inorg. Chem. 11 (2006) 189-196
49. Hamill S.J., Meekhof A.E., and Clarke J. The effect of boundary selection on the stability and folding of the third fibronectin type III domain from human tenascin. Biochemistry 37 (1998) 8071-8079
50. Malawski G.A., Hillig R.C., Monteclaro F., Eberspaecher U., Schmitz A.A., Crusius K., Huber M., Egner U., Donner P., and Müller-Tiemann B. Identifying protein construct variants with increased crystallization propensity-a case study. Protein Sci. 15 (2006) 2718-2728