Multiple Step Assembly Of The Transmembrane Cytochrome b6

Journal of Molecular Biology

Volumn 382, Issue 4, 2008, Pages 1057-1065

  Dreher, Carolin ^a   Prodöhl, Alexander ^a   Hielscher, Ruth ^b   Hellwig, Petra ^b   Schneider, Dirk ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITÉ LOUIS PASTEUR   (France)

Author keywords

assembly; cytochrome b6; heme; ligand; membrane protein folding

Indexed keywords

CYTOCHROME B6; HEME; HISTIDINE;

ARTICLE; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SPINACH;

EID: 51249104025     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.07.025     Document Type: Article

References (50)

1. Bowie J.U. Solving the membrane protein folding problem. Nature 438 (2005) 581-589
2. Booth P.J., and Curnow P. Membrane proteins shape up: understanding in vitro folding. Curr. Opin. Struct. Biol. 16 (2006) 480-488
3. Stanley A.M., and Fleming K.G. The process of folding proteins into membranes: challenges and progress. Arch. Biochem. Biophys. 469 (2008) 46-66
4. MacKenzie K.R. Folding and stability of alpha-helical integral membrane proteins. Chem. Rev. 106 (2006) 1931-1977
5. Schneider D., Finger C., Prodöhl A., and Volkmer T. From interactions of single transmembrane helices to folding of -helical membrane proteins: analyzing transmembrane helix-helix interactions in bacteria. Curr. Protein Pept. Sci. 8 (2007) 45-61
6. Popot J.L., and Engelman D.M. Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29 (1990) 4031-4037
7. Engelman D.M., Chen Y., Chin C.N., Curran A.R., Dixon A.M., Dupuy A.D., et al. Membrane protein folding: beyond the two stage model. FEBS Lett. 555 (2003) 122-125
8. Koch H.G., and Schneider D. Assembly and stability of transmembrane cytochromes. Curr. Chem. Biol. 1 (2007) 59-74
9. Robinson C.R., Liu Y., O'Brien R., Sligar S.G., and Sturtevant J.M. A differential scanning calorimetric study of the thermal unfolding of apo- and holo-cytochrome b562. Protein Sci. 7 (1998) 961-965
10. Mukhopadhyay K., and Lecomte J.T. A relationship between heme binding and protein stability in cytochrome b5. Biochemistry 43 (2004) 12227-12236
11. Feng Y.Q., and Sligar S.G. Effect of heme binding on the structure and stability of Escherichia coli apocytochrome b562. Biochemistry 30 (1991) 10150-10155
12. Garcia P., Bruix M., Rico M., Ciofi-Baffoni S., Banci L., Shastry M.R., et al. Effects of heme on the structure of the denatured state and folding kinetics of cytochrome b562. J. Mol. Biol. 346 (2005) 331-344
13. Fisher M.T. Differences in thermal stability between reduced and oxidized cytochrome b562 from Escherichia coli. Biochemistry 30 (1991) 10012-10018
14. Tomlinson E.J., and Ferguson S.J. Conversion of a c type cytochrome to a b type that spontaneously forms in vitro from apo protein and heme: implications for c type cytochrome biogenesis and folding. Proc. Natl Acad. Sci. USA 97 (2000) 5156-5160
15. Robertson D.E., Farid R.S., Moser C.C., Urbauer J.L., Mulholland S.E., Pidikiti R., et al. Design and synthesis of multi-haem proteins. Nature 368 (1994) 425-432
16. Gibney B.R., Isogai Y., Rabanal F., Reddy K.S., Grosset A.M., Moser C.C., and Dutton P.L. Self-assembly of heme A and heme B in a designed four-helix bundle: implications for a cytochrome c oxidase maquette. Biochemistry 39 (2000) 11041-11049
17. Gibney B.R., Rabanal F., Reddy K.S., and Dutton P.L. Effect of four helix bundle topology on heme binding and redox properties. Biochemistry 37 (1998) 4635-4643
18. Discher B.M., Noy D., Strzalka J., Ye S., Moser C.C., Lear J.D., et al. Design of amphiphilic protein maquettes: controlling assembly, membrane insertion, and cofactor interactions. Biochemistry 44 (2005) 12329-12343
19. Ghirlanda G., Osyczka A., Liu W., Antolovich M., Smith K.M., Dutton P.L., et al. De novo design of a D2-symmetrical protein that reproduces the diheme four-helix bundle in cytochrome bc1. J. Am. Chem. Soc. 126 (2004) 8141-8147
20. Shifman J.M., Gibney B.R., Sharp R.E., and Dutton P.L. Heme redox potential control in de novo designed four-alpha-helix bundle proteins. Biochemistry 39 (2000) 14813-14821
21. Prodöhl A., Weber M., Dreher C., and Schneider D. A mutational study of transmembrane helix-helix interactions. Biochimie 89 (2007) 1433-1437
22. Volkmer T., Becker C., Prodöhl A., Finger C., and Schneider D. Assembly of a transmembrane b-type cytochrome is mainly driven by transmembrane helix interactions. Biochim. Biophys. Acta 1758 (2006) 1815-1822
23. Prodöhl A., Volkmer T., Finger C., and Schneider D. Defining the structural basis for assembly of a transmembrane cytochrome. J. Mol. Biol. 350 (2005) 744-756
24. Cramer W.A., Yan J., Zhang H., Kurisu G., and Smith J.L. Structure of the cytochrome b6f complex: new prosthetic groups, Q-space, and the 'hors d'oeuvres hypothesis' for assembly of the complex. Photosynth. Res. 85 (2005) 133-143
25. Widger W.R., Cramer W.A., Herrmann R.G., and Trebst A. Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b6-f complex: position of the cytochrome b hemes in the membrane. Proc. Natl Acad. Sci. USA 81 (1984) 674-678
26. Kurisu G., Zhang H., Smith J.L., and Cramer W.A. Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302 (2003) 1009-1014
27. Stroebel D., Choquet Y., Popot J.L., and Picot D. An atypical haem in the cytochrome b(6)f complex. Nature 426 (2003) 413-418
28. Yamashita E., Zhang H., and Cramer W.A. Structure of the cytochrome b6f complex: quinone analogue inhibitors as ligands of heme cn. J. Mol. Biol. 370 (2007) 39-52
29. Dreher C., Prodöhl A., Weber M., and Schneider D. Heme binding properties of heterologously expressed spinach cytochrome b(6): Implications for transmembrane b-type cytochrome formation. FEBS Lett. 581 (2007) 2647-2651
30. Prodöhl A., Dreher C., Hielscher R., Hellwig P., and Schneider D. Heterologous expression and in vitro assembly of the transmembrane cytochrome b6. Protein Expr. Purif. 56 (2007) 279-285
31. de Vitry C., Desbois A., Redeker V., Zito F., and Wollman F.A. Biochemical and spectroscopic characterization of the covalent binding of heme to cytochrome b6. Biochemistry 43 (2004) 3956-3968
32. Thomas P.E., Ryan D., and Levin W. An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 75 (1976) 168-176
33. Kuras R., de Vitry C., Choquet Y., Girard-Bascou J., Culler D., Buschlen S., et al. Molecular genetic identification of a pathway for heme binding to cytochrome b6. J. Biol. Chem. 272 (1997) 32427-32435
34. L components of the bc1 complex from Rhodobacter sphaeroides by site-directed mutagenesis. Biochemistry 30 (1991) 6747-6754
35. Kramer D.M., and Crofts A.R. Re-examination of the properties and function of the b cytochromes of the thylakoid cytochrome bf complex. Biochim. Biophys. Acta 1184 (1994) 193-201
36. Kroliczewski J., Hombek-Urban K., and Szczepaniak A. Integration of the thylakoid membrane protein cytochrome b6 in the cytoplasmic membrane of Escherichia coli. Biochemistry 44 (2005) 7570-7576
37. Barrick D. Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His-93 → Gly. Biochemistry 33 (1994) 6546-6554
38. Decatur S.M., DePillis G.D., and Boxer S.G. Modulation of protein function by exogenous ligands in protein cavities: CO binding to a myoglobin cavity mutant containing unnatural proximal ligands. Biochemistry 35 (1996) 3925-3932
39. Pond A.E., Roach M.P., Thomas M.R., Boxer S.G., and Dawson J.H. The H93G myoglobin cavity mutant as a versatile template for modeling heme proteins: ferrous, ferric, and ferryl mixed-ligand complexes with imidazole in the cavity. Inorg. Chem. 39 (2000) 6061-6066
40. Roach M.P., Ozaki S., and Watanabe Y. Investigations of the myoglobin cavity mutant H93G with unnatural imidazole proximal ligands as a modular peroxide O-O bond cleavage model system. Biochemistry 39 (2000) 1446-1454
41. McRee D.E., Jensen G.M., Fitzgerald M.M., Siegel H.A., and Goodin D.B. Construction of a bisaquo heme enzyme and binding by exogenous ligands. Proc. Natl Acad. Sci. USA 91 (1994) 12847-12851
42. Newmyer S.L., and Ortiz de Montellano P.R. Horseradish peroxidase His-42 → Ala, His-42 → Val, and Phe-41 → Ala mutants. Histidine catalysis and control of substrate access to the heme iron. J. Biol. Chem. 270 (1995) 19430-19438
43. Newmyer S.L., Sun J., Loehr T.M., and Ortiz de Montellano P.R. Rescue of the horseradish peroxidase His-170 → Ala mutant activity by imidazole: importance of proximal ligand tethering. Biochemistry 35 (1996) 12788-12795
44. Sun J., Wilks A., Ortiz de Montellano P.R., and Loehr T.M. Resonance Raman and EPR spectroscopic studies on heme-heme oxygenase complexes. Biochemistry 32 (1993) 14151-14157
45. Kamiya N., Okimoto Y., Ding Z., Ohtomo H., Shimizu M., Kitayama A., et al. How does heme axial ligand deletion affect the structure and the function of cytochrome b(562)?. Protein Eng. 14 (2001) 415-419
46. Maklashina E., Rothery R.A., Weiner J.H., and Cecchini G. Retention of heme in axial ligand mutants of succinate-ubiquinone xxidoreductase (complex II) from Escherichia coli. J. Biol. Chem. 276 (2001) 18968-18976
47. Nakamura Y., Kaneko T., Sato S., Mimuro M., Miyashita H., Tsuchiya T., et al. Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res. 10 (2003) 181-201
48. Booth P.J., Flitsch S.L., Stern L.J., Greenhalgh D.A., Kim P.S., and Khorana H.G. Intermediates in the folding of the membrane protein bacteriorhodopsin. Nature Struct. Biol. 2 (1995) 139-143
49. Moss D., Nabedryk E., Breton J., and Mantele W. Redox-linked conformational changes in proteins detected by a combination of infrared spectroscopy and protein electrochemistry. Evaluation of the technique with cytochrome c. Eur. J. Biochem. 187 (1990) 565-572
50. Hellwig P., Behr J., Ostermeier C., Richter O.M., Pfitzner U., Odenwald A., et al. Involvement of glutamic acid 278 in the redox reaction of the cytochrome c oxidase from Paracoccus denitrificans investigated by FTIR spectroscopy. Biochemistry 37 (1998) 7390-7399