Characterization of purified c-type heme-containing peptides and identification of c-type heme-attachment sites in Shewanella oneidenis cytochromes using mass spectrometry

Journal of Proteome Research

Volumn 4, Issue 3, 2005, Pages 846-854

  Yang, Feng ^a   Bogdanov, Bogdan ^a   Strittmatter, Eric F ^a   Vilkov, Andrey N ^a   Gritsenko, Marina ^a   Shi, Liang ^a   Elias, Dwayne A ^a   Ni, Shuisong ^a   Romine, Margaret ^a   Paša Tolić, Ljiljana ^a   Lipton, Mary S ^a   Smith, Richard D ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

c type cytochromes; Charged heme; Fragmentation; Heme loss; Heme containing peptides

Indexed keywords

BACTERIAL PROTEIN; CYTOCHROME C; HEMOPROTEIN; PROTEIN MTRA; PROTEOME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; ION TRAP MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PURIFICATION; SHEWANELLA ONEIDENSIS; TANDEM MASS SPECTROMETRY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CYTOCHROME C GROUP; HEME; MASS SPECTROMETRY; PEPTIDE FRAGMENTS; SHEWANELLA;

SHEWANELLA;

EID: 20844448190     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr0497475     Document Type: Article

References (43)

1. Pettigrew, G. W.; Moore, G. R. Cytochromes c: Biological Aspects; Springer: New York, 1987.
2. Scott, R. A.; Mauk, A. G. Cytochrome c: A Multidisciplinary Approach; University Science Books: Mill Valley, CA, 1995.
3. Einsle, O.; Messerschmidt, A.; Stach, P.; Bourenkov, G. P.; Bartunik, H. D.; Huber, R.; Kroneck, P. M. Structure of cytochrome c nitrite reductase. Nature (London) 1999, 400, 476-480.
4. Igarashi, N.; Moriyama, H.; Fujiwara, T.; Fukumori, Y.; Tanaka, N. The 2.8 A structure of hydroxylamine oxidoreductase from a nitrifying chemoautotrophic bacterium. Nitrosomonas europaea. Nat. Struct. Biol. 1997, 4, 276-284.
5. Martinou, J. C.; Desagher, S.; Antonsson, B. Cytochrome c release from mitochondria: all or nothing. Nat. Cell Biol. 2000, 2, E41-E43.
6. Barker, P. D.; Ferguson, S. J. Still a puzzle: why is haem covalently attached in c-type cytochromes? Structure Fold. Des. 1999, 7, R281-R290.
7. Page, M. D., Sambongi, Y.; Ferguson, S. J. Contrasting routes of c-type cytochrome assembly in mitochondria, chloroplasts and bacteria. Trends Biochem. Sci. 1998, 23, 103-108.
8. Thöny-Meyer, L. Biogenesis of respiratory cytochromes in bacteria. Microbiol. Mol. Biol. Rev. 1997, 61, 337-376.
9. Nealson, K. H.; Saffarini, D. Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu. Rev. Microbiol. 1994, 48, 311-343.
10. Krause, B.; Nealson, K. H. Physiology and enzymology involved in denitrification by Shewanella putrefaciens. Appl. and Environ. Microb. 1997, 63, 2613-2618.
11. Myers, C. R.; Myers, J. M. Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens, MR-1. J. Bacteriol. 1992, 174, 3429-3438.
12. Heidelberg, J. F.; Paulsen, I. T.; Nelson, K. E.; Gaidos, E. J.; Nelson, W. C.; Read, T. D.; Eisen, J. A.; Seshadri, R.; Ward, N.; Methe, B.; Clayton, R. A.; Meyer, T.; Tsapin, A.; Scott, J.; Beanan, M.; Brinkac, L.; Daugherty, S.; DeBoy, R. T.; Dodson, R. J.; Durkin, A. S.; Haft, D. H.; Kolonay, J. F.; Madupu, R.; Peterson, J. D.; Umayam, L. A.; White, O.; Wolf, A. M.; Vamathevan, J.; Weidman, J.; Impraim, M.; Lee, K.; Berry, K.; Lee, C.; Mueller, J.; Khouri, H., Gill, J.; Utterback, T. R.; McDonald, L. A.; Feldblyum, T. V.; Smith, H. O.; Venter, J. C.; Nealson, K. H.; Fraser, C. M. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat. Biotechnol. 2002, 20, 1118-1123.
13. Methe, B. A.; Nelson, K. E.; Eisen, J. A.; Paulsen, I. T.; Nelson, W.; Heidelberg, J. F.; Wu, D.; Wu, M.; Ward, N.; Beanan, M. J.; Dodson, R. J.; Madupu, R.; Brinkac, L. M.; Daugherty, S. C., DeBoy, R. T., Durkin, A. S., Gwinn, M., Kolonay, J. F., Sullivan, S. A.; Haft, D. H.; Selengut, J.; Davidsen, T. M.; Zafar, N.; White, O.; Tran, B.; Romero, C.; Forberger, H. A.; Weidman, J.; Khouri, H.; Feldblyum, T. V.; Utterback, T. R.; Van Aken, S. E.; Lovley, D. R.; Fraser, C. M. Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 2003, 302, 1967-1969.
14. Meyer, T. E.; Tsapin, A. I.; Vandenberghe, I.; de Smet, L.; Frishman, D.; Nealson, K. H.; Cusanovich, M. A.; van Beeumen, J. J. Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 2004, 8, 57-77.
15. Pitts, K. E.; Dobbin, P. S.; Reyes-Ramirez, F.; Thomson, A. J.; Richardson, D. J.; Seward, H. E. Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA: expression in Escherichia coli confers the ability to reduce soluble Fe(III) chelates. J. Biol. Chem. 2003, 278, 27758-27765.
16. Giometti, C. S.; Khare, T., Tollaksen, S. L.; Tsapin, A.; Zhu, W.; Yates, J. R., III.; Nealson, K. H. Analysis of the Shewanella oneidensis proteome by two-dimensional gel electrophoresis under nondenaturing conditions. Proteomics 2003, 3, 777-785.
17. Hunt, D. F.; Alexander, J. E.; McCormack, A. L.; Martino, P. A.; Michel, H.; Shabanowitz, J.; Sherman, N.; Moseley, M. A.; Jorgenson, J. W.; Tomer, K. B. Mass Spectrometric Methods for Protein and Peptide Sequence Analysis. In Techniques in Protein Chemistry II; Villafranca, J. J., Ed.; Academic Press: San Diego, 1991, pp 441-454.
18. Smith, R. D. Advanced Mass Spectrometric Methods for the Rapid and Quantitative Characterization of Proteomes. Comparative and Functional Genomics 2002, 3, 143-150.
19. Romine, M. F.; Elias, D. A.; Monroe, M. E.; Auberry, K. J.; Fang, R.; Fredrickson, J. K.; Anderson, G. A.; Smith, R. D.; Lipton, M. S. Validation of Shewanella oneidensis MR-1 small proteins by AMT tag-based proteome analysis. OMICS 2004, 8, 239-254.
20. Lei, Q. P.; Cui, X. Y.; Kurtz, D. M.; Amster, I. J.; Chernushevich, I. V. Electrospray mass spectrometry studies of non-heme iron-containing proteins. Anal. Chem. 1998, 70, 1838-1846.
21. Yu, X. L.; Wojciechowski, M.; Fenselau, C. Assessment of metals in reconstituted metallothioneins by electrospray mass spectrometry. Anal. Chem. 1993, 65, 1355-1359.
22. Yates, J. R., III.; Eng, J. K.; McCormack, A. L.; Schieltz, D. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 1995, 67, 1426-1436.
23. Wu, Q.; Van Orden S.; Cheng, X. H.; Bakhtiar, R.; Smith, R. D. Characterization of cytochrome c variants with high-resolution FTICR mass spectrometry: Correlation of fragmentation and structure. Anal. Chem. 1995, 67, 2498-2509.
24. McLafferty, F. W.; Guan, Z.; Haupts, U.; Wood, T. D.; Kelleher, N. L. Gaseous conformational structures of cytochrome c. J. Am. Chem. Soc. 1998, 120, 4732-4740.
25. He, F.; Hendrickson, C. L.; Marshall, A. G. Unequivocal determination of metal atom oxidation state in naked heme proteins: Fe(III)Myglobin, Fe(III)Cytochrome c, Fe(III)Cytochrome b5, and Fe(III)Cytochrome b5 L47R. J. Am. Soc. Mass Spectrom. 2000, 11, 120-126.
26. Wells, J. M.; Reid, G. E.; Engel, B. J.; Pan, P.; McLuckey, S. A. Dissociation reactions of gaseous ferro-, ferri-, and apo-cytochrome c ions. J. Am. Soc. Mass Spectrom. 2001, 12, 873-876.
27. Engel, B. J.; Pan, P.; Reid, G. E.; Wells, J. M.; McLuckey, S. A. Charge state dependent fragmentation of gaseous protein ions in a quadrupole ion trap: bovine ferri-, ferro-, and apo-cytochrome c. Int. J. Mass Spectrom. 2002, 219, 171-187.
28. Stone, E.; Gillig, K. J.; Ruotolo, B.; Fuhrer, K.; Gonin, M.; Schultz, A.; Russell, D. H. Surface-induced dissociation on a MALDI-ion mobility-orthogonal time-of-flight mass spectrometer: Sequencing Peptides from an "In-Solution" Protein Digest. Anal. Chem. 2001, 73, 2233-2238.
29. Winger, B. E.; Hofstadler, S. A.; Bruce, J. E.; Udseth, H. R.; Smith, R. D. High-resolution accurate mass measurements of biomolecules using a new electrospray ionization ion cyclotron resonance mass spectrometer. J. Am. Soc. Mass Spectrom. 1993, 4, 566-577.
30. Vilkov, A. N.; Paša-Tolić, L.; Bogdanov, B.; Ahn S., Prior, D. C.; Anderson, G. A.; Masselon, C.; Moore, R. J.; Smith, R. D. Multistage external pre-selection of ions for increased sensitivity of LC-FTICR MS/MS. Proc. 51st ASMS Conf. Mass Spectrometry and Allied Topics, 2003, Montreal, Canada.
31. Vilkov, A. N.; Bogdanov, B.; Paša-Tolić; Prior, D. C.; Anderson, G. A.; Masselon, C.; Moore, R. J.; Smith, R. D. Tailored noise waveform/collision-induced dissociation of ions stored in a linear ion trap combined with liquid chromatography/Fourier transform ion cyclotron resonance mass spectrometry. Rapid Comm. Mass Spectrom. 2004, 18, 2682-2690.
32. Guan, S. H.; Marshall, A. G. Stored waveform inverse Fourier transform (SWIFT) ion excitation in trapped-ion mass spectrometry: Theory and applications. Int. J. Mass Spectrom. (and Ion Processes) 1996, 158, 5-37.
33. Shi, L.; Lin, J.-T.; Markillie, L. M.; Squier, T. C.; Hooker, B. S. Overexpression of multi-heme c-type cytochromes. BioTechniques 2005, 38, 297-299.
34. Harkewicz, R.; Belov, M. E.; Anderson, D. A.; Paša-Tolić, L.; Masselon, C. D.; Prior, D. C.; Udseth, H. R.; Smith, R. D. ESI-FTICR mass spectrometry employing data-dependent external ion selection and accumulation. J. Am. Soc. Mass Spectrom. 2002, 13, 144-154.
35. Shen, Y.; Zhao, R.; Belov, M. E.; Conrads, T. P.; Anderson, G. A.; Tang, K.; Paša-Tolić, L.; Veenstra, T. D.; Lipton, M. S.; Smith, R. D. Packed capillary reversed-phase liquid chromatography with high-performance electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry for proteomics. Anal. Chem. 2001, 73, 1766-1775.
36. Shen, Y.; Tolić, N.; Masselon, C.; Paša-Tolić, L.; Camp, D. G., II.; Lipton, M. S.; Anderson, G. A.; Smith, R. D. Nanoscale proteomics. Anal. Bioanal. Chem. 2004, 378, 1037-1045.
37. Horn, D. M.; Zubarev, R. A.; McLafferty, F. W. Automated reduction and interpretation of high-resolution electrospray mass spectra of large molecules. J. Am. Soc. Mass Spectrom. 2000, 11, 320-332.
38. Johnson, K. A.; Verhagen, M. F. J. M.; Brereton, P. S.; Adams, M. W. W.; Amster, I. J. Probing the stoichiometry and oxidation states of metal centers in iron-sulfur proteins using electrospray FTICR mass spectrometry. Anal. Chem. 2000, 72, 1410-1418.
39. Bruce, J. E.; Anderson, G. A.; Brands, M. D. Obtaining more accurate FTICR mass measurements without internal standards using multiply charged ions. J. Am. Soc. Mass Spectrom. 2000, 11, 416-421.
40. Strittmatter, E. F.; Camp, D. G., II.; Paša-Tolić, L.; Anderson, G. A.; Kangas, L. J.; Smith, R. D. PARALLAX: High throughput software tools for the detection of modified, mutated and nonspecifically cleaved proteins in Conference of the Am. Soc. Mass Spectrom. 2002, Orlando, FL.
41. Washburn, M. P.; Wolters, D.; Yates, J. R. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nature Biotech. 2001, 19, 242-247.
42. Smith, R. D.; Loo, J. A.; Loo, R. R. O.; Busman, M.; Udseth H. R. Principles and practice of electrospray ionization-mass spectrometry for large polypeptides and proteins. Mass Spectrom. Rev. 1991, 10, 359-451.
43. Senko, M. W.; Beu, S. C.; McLafferty, F. W. Determination of monoisotopic masses and ion populations for large biomolecules from resolved isotopic distributions. J. Am. Soc. Mass Spectrom. 1995, 6, 229-233.