ATPase activity associated with the magnesium chelatase H-subunit of the chlorophyll biosynthetic pathway is an artefact

Biochemical Journal

Volumn 400, Issue 3, 2006, Pages 477-484

  Sirijovski, Nick ^a   Olsson, Ulf ^a   Lundqvist, Joakim ^a   Al Karadaghi, Salam ^a   Willows, Robert D ^b   Hansson, Mats ^a  

^a LUND UNIVERSITY   (Sweden)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

ATPases associated with various cellular activities (AAA+); bchH; Chlorophyll; Magnesium chelatase; Protoporphyrin IX; Rhodobacter capsulatus

Indexed keywords

ADENOSINETRIPHOSPHATE; BIOSYNTHESIS; CELLS; CHLOROPHYLL; CHROMATOGRAPHIC ANALYSIS; ESCHERICHIA COLI;

ATPASES ASSOCIATED WITH VARIOUS CELLULAR ACTIVITIES (AAA+); BCHH; MAGNESIUM CHELATASE; PROTOPORPHYRIN IX; RHODOBACTER CAPSULATUS;

ENZYME KINETICS;

ADENOSINE TRIPHOSPHATASE; CHLOROPHYLL; LYASE; MAGNESIUM CHELATASE;

ARTICLE; ARTIFACT; AUTORADIOGRAPHY; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; ESCHERICHIA COLI; GEL FILTRATION CHROMATOGRAPHY; LIGHT EXPOSURE; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; RHODOBACTER CAPSULATUS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ARTIFACTS; BACTERIAL PROTEINS; CHLOROPHYLL; GENE EXPRESSION REGULATION, BACTERIAL; LIGHT; LYASES; PLANTS; PROTEIN SUBUNITS; PROTOPORPHYRINS; RHODOBACTER CAPSULATUS;

ESCHERICHIA COLI; RHODOBACTER CAPSULATUS;

EID: 33845722688     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061103     Document Type: Article

References (49)

1. Willows, R. D. and Hansson, M. (2003) Mechanism, structure and regulation of magnesium chelatase. In The Porphyrin Handbook II, Vol. 13 (Kadish, K. M., Smith, K. and Guilard, R., eds.), pp. 1-47, Elsevier Science, Amsterdam
2. Fuesler, T. P., Castelfranco, P. A. and Wong, Y. S. (1984) Formation of magnesium-containing chlorophyll precursors from protoporphyrin IX, δ-aminolevulinic acid, and glutamate in isolated, photosynthetically competent, developing chloroplasts. Plant Physiol. 74, 928-933
3. Fuesler, T. P., Wright, L. A. and Castelfranco, P. A. (1981) Properties of magnesium chelatase in greening etioplasts. Plant Physiol. 67, 246-249
4. Castelfranco, P. A., Weinstein, J. D., Schwarcz, S., Pardo, A. D. and Wezelman, B. E. (1979) The magnesium insertion step in chlorophyll biosynthesis. Arch. Biochem. Biophys. 192, 592-598
5. Walker, C. J. and Weinstein, J. D. (1991) In vitro assay of the chlorophyll biosynthetic enzyme magnesium chelatase: resolution of the activity into soluble and membrane bound fractions. Proc. Natl. Acad. Sci. U.S.A. 88, 5789-5793
6. Walker, C. J. and Weinstein, J. D. (1991) Further characterization of the magnesium chelatase in isolated developing cucumber chloroplasts: substrate specificity, regulation, intactes and ATP requirements. Plant Physiol. 95, 1189-1196
7. Walker, C. J. and Weinstein, J. D. (1994) The magnesium-insertion step of chlorophyll biosynthesis is a two-stage reaction. Biochem. J. 299, 277-284
8. Gibson, L. C. D., Willows, R. D., Kannangara, C. G., von Wettstein, D. and Hunter, C. N. (1995) Magnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: reconstitution of activity by combining the products of the bchH, -I, and -D genes expressed in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92, 1941-1944
9. Willows, R. D., Gibson, L. C. D., Kanangara, C. G., Hunter, C. N. and von Wettstein, D. (1996) Three separate proteins constitute the magnesium chelatase of Rhodobacter sphaeroides. Eur. J. Biochem. 235, 438-443
10. Gibson, L. C. D., Jensen, P. E. and Hunter, C. N. (1999) Magnesium chelatase from Rhodobacter sphaeroides: initial characterization of the enzyme using purified subunits and evidence for a Bchl-BchD complex. Biochem. J. 337, 243-251
11. Willows, R. D. and Beale, S. I. (1998) Heterologous expression of the Rhodobacter capsulatus Bchl, -D, and -H genes that encode magnesium chelatase subunits and characterization of the reconstituted enzyme. J. Biol. Chem. 273, 34206-34213
12. Petersen, B. L., Jensen, P. E., Gibson, L. C., Stummann, B. M., Hunter, C. N. and Henningsen, K. W. (1998) Reconstitution of an active magnesium chelatase enzyme complex from the bchl, -D, and -H gene products of the green sulfur bacterium Chlorobium vibrioforme expressed in Escherichia coli. J. Bacteriol. 180, 699-704
13. Jensen, P. E., Gibson, L. C., Henningsen, K. W. and Hunter, C. N. (1996) Expression of the chlI, chlD, and ChlH genes from the cyanobacterium Synechocystis PCC6803 in Escherichia coli and demonstration that the three cognate proteins are required for magnesium-protoporphyrin chelatase activity. J. Biol. Chem. 271, 16662-16667
14. Jensen, P. E., Gibson, L. C. D. and Hunter, C. N. (1998) Determinants of catalytic activity with the use of purified I, D and H subunits of the magnesium protoporphyrin IX chelatase from Synechocystis PCC6803. Biochem. J. 334, 335-344
15. Masuda, T., Inoue, K., Masuda, M., Nagayama, M., Tamaki, A., Ohta, H., Shimada, H. and Takamiya, K.-I. (1999) Magnesium insertion by magnesium chelatase in the biosynthesis of zinc bacteriochlorophyll a in an aerobic acidophilic bacterium Acidiphilum rubrum. J. Biol. Chem. 274, 33594-33600
16. Fodje, M. N., Hansson, A., Hansson, M., Olsen, J. G., Gough, S., Willows, R. D. and Al-Karadaghi, S. (2001) Interplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase. J. Mol. Biol. 311, 111-122
17. Hansson, M. and Kannangara, C. G. (1997) ATPases and phosphate exchange activities in magnesium chelatase subunits of Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. U.S.A. 94, 13351-13356
18. 2+ insertion, and the MgATP-dependent interaction of the ChlI and ChlD subunits. Biochem. J. 339, 127-134
19. Petersen, B. L., Kannangara, C. G. and Henningsen, K. W. (1999) Distribution of ATPase and ATP-to-ADP phosphate exchange activities in magnesium chelatase subunits of Chlorobium vibrioforme and Synechocystis PCC6803. Arch. Microbiol. 171, 146-150
20. + hexamer. J. Struct. Biol. 146, 227-233
21. + ring. Biochemistry 42, 6912-6920
22. Vale, R. D. (2000) AAA proteins: Lords of the ring. J. Cell Biol. 150, F13-F19
23. + superfamily ATPases: common structure - diverse function. Genes Cells 6, 575-597
24. +: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43
25. Lake, V., Olsson, U., Willows, R. D. and Hansson, M. (2004) ATPase activity of magnesium chelatase subunit I is required to maintain subunit D in vivo. Eur. J. Biochem. 271, 2182-2188
26. + hexamers. Proc. Natl. Acad. Sci. U.S.A. 99, 13944-13949
27. Petersen, B. L., Kannangara, C. G. and Henningsen, K. W. (1998) ATPase and phosphate exchange activities in Mg-chelatase subunits of Chlorobium and Synechocystis. Photosynth. Mech. Eff. Proc. Int. Congr. 11th 4, 3241-3244
28. Papenbrock, J., Gräfe, S., Kruse, E., Hanel, F. and Grimm, B. (1997) Mg-chelatase of tobacco: identification of a Chl D cDNA sequence encoding a third subunit, analysis of the interaction of the three subunits with the yeast two-hybrid system, and reconstitution of the enzyme activity by co-expression of recombinant CHL D, CHL H and CHL I, Plant J. 12, 981-990
29. Jensen, P. E., Reid, J. D. and Hunter, C. N. (2000) Modification of cysteine residues in the ChlI and ChlH subunits of magnesium chelatase results in enzyme inactivation. Biochem. J. 352, 435-441
30. Karger, G. A., Reid, J. D. and Hunter, C. N. (2001) Characterization of the binding of deuteroporphyrin IX to the magnesium chelatase H subunit and spectroscopic properties of the complex. Biochemistry 40, 9291-9299
31. Smirnov, I. P., Zhu, X., Taylor, T., Huang, Y., Ross, P., Papayanopoulos, I. A., Martin, S. A. and Pappin, D. J. (2004) Suppression of α-cyano-4-hydroxycinnamic acid matrix clusters and reduction of chemical noise in MALDI-TDF mass spectrometry. Anal. Chem. 76, 2958-2965
32. Perkins, D. N., Pappin, D. J., Creasay, D. M. and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
33. Fling, S. P. and Gregerson, D. S. (1986) Peptide and protein molecular weight determination by electrophoresis using a high-molarity Tris buffer system without urea. Anal. Biochem. 155, 83-88
34. Schägger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379
35. Neuhoff, V., Arold, N., Taube, D. and Ehrhardt, W. (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9, 255-262
36. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680
37. Gattiker, A., Gasteiger, E. and Bairoch, A. (2002) ScanProsite: a reference implementation of a PROSITE scanning tool. Appl. Bioinformatics 1, 107-108
38. Walker, J. E., Saraste, M., Runswick, M. J. and Gay, N. J. (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951
39. Möller, W. and Amons, R. (1985) Phosphate-binding sequences in nucleotide-binding proteins. FEBS Lett. 186, 1-7
40. Saraste, M., Sibbald, P. R. and Wittinghofer, A. (1990) The P-loop: a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 15, 430-434
41. Koonin, E. V. (1993) A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif. J. Mol. Biol. 229, 1165-1174
42. Dever, T. E., Glynias, M. J. and Merrick, W. C. (1987) GTP-binding domain: three consensus sequence elements with distinct spacing. Proc. Natl. Acad. Sci. U.S.A. 84, 1814-1818
43. Willows, R. D., Lake, V., Roberts, T. H. and Beale, S. I. (2003) Inactivation of Mg chelatase during transition from anaerobic to aerobic growth in Rhodobacter capsulatus. J. Bacteriol. 185, 3249-3258
44. Hoskins, J. R., Singh, S. K., Maurizi, M. R. and Wickner, S. (2000) Protein binding and unfolding by the chaperone ClpA and degradation by the protease ClpAP. Proc. Natl. Acad. Sci. U.S.A. 97, 8892-8897
45. Olsson, U., Sirijovski, N. and Hansson, M. (2004) Characterization of eight barley xantha-f mutants deficient in magnesium chelatase. Plant Physiol. Biochem. 42, 557-564
46. Hanson, P. I., Roth, R., Morisaki, H., Jahn, R. and Heuser, J. E. (1997) Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90, 523-535
47. Rouiller, I., DeLaBarre, B., May, A. P., Weis, W. I., Brunger, A. T., Milligan, R. A. and Wilson-Kubalek, E. M. (2002) Conformational changes of the multifunction p97 AAA ATPase during its ATPase cycle. Nat. Struct. Biol. 9, 950-957
48. Song, H. K., Hartmann, C., Ramachandran, R., Bochtler, M., Behrendt, R., Moroder, L. and Huber, R. (2000) Mutational studies on HslU and its docking mode with HslV. Proc. Natl. Acad. Sci. U.S.A. 97, 14103-14108
49. 54. Proc. Natl. Acad. Sci. U.S.A. 100, 2278-2283