Crystal structure of the unactivated ribulose 1, 5-bisphosphate carboxylase/oxygenase complexed with a transition state analog, 2-carboxy-D-arabinitol 1, 5-bisphosphate
Kam Y.J. Zhang
Molecular Biology Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90024-1570
Search for more papers by this authorDuilio Cascio
Molecular Biology Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90024-1570
Search for more papers by this authorCorresponding Author
David Eisenberg
Molecular Biology Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90024-1570
Molecular Biology Institute, University of California, Los Angeles, 405 Hilgard Avenue, Los Angeles, California 90024-1570Search for more papers by this authorKam Y.J. Zhang
Molecular Biology Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90024-1570
Search for more papers by this authorDuilio Cascio
Molecular Biology Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90024-1570
Search for more papers by this authorCorresponding Author
David Eisenberg
Molecular Biology Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90024-1570
Molecular Biology Institute, University of California, Los Angeles, 405 Hilgard Avenue, Los Angeles, California 90024-1570Search for more papers by this authorAbstract
The crystal structure of unactivated ribulose 1, 5-bisphosphate carboxylase/oxygenase from Nicotiana tabacum complexed with a transition state analog, 2-carboxy-D-arabinitol 1, 5-bisphosphate, was determined to 2.7 Å resolution by X-ray crystallography. The transition state analog binds at the active site in an extended conformation. As compared to the binding of the same analog in the activated enzyme, the analog binds in a reverse orientation. The active site Lys 201 is within hydrogen bonding distance of the carboxyl oxygen of the analog. Loop 6 (residues 330-339) remains open and flexible upon binding of the analog in the unactivated enzyme, in contrast to the closed and ordered loop 6 in the activated enzyme complex. The transition state analog is exposed to solvent due to the open conformation of loop 6.
References
- Alber T, Banner DW, Bloomer AC, Petsko GA, Phillips D, Rivers PS, Wilson IA. 1981. On the three-dimensional structure and catalytic mechanism of triose phosphate isomerase. Philos Trans R Soc Lond B 293: 159–171.
- Andersson I, Knight S, Schneider G, Lindqvist Y, Lundqvist T, Bränékn CI, Lorimer G. 1989. Crystal structure of the active site of ribulosebisphosphate carboxylase. Nature 337: 229–234.
- Andrews TJ, Lorimer GH. 1987. Rubisco: Structure, mechanisms, and prospects for improvement. In: MD Hatch, NK Boardman, eds. The biochemistry of plants, vol 10. Orlando, Florida: Academic Press. pp 131–218.
- Baker TS, Suh SW, Eisenberg D. 1977. Structure of ribulose-1,5-bisphosphate carboxylase-oxygenase: Form III crystals. Proc Natl Acad Sci USA 74: 1037–1041.
- Brändén CI, Lindqvist Y, Schneider G. 1991. Protein engineering of rubisco. Acta Crystallogr B 47: 824–835.
- Brünger AT. 1990. X-PLOR version 2.1: A system for crystallography and NMR. New Haven, Connecticut: Yale University.
- Brünger AT, Kuriyan J, Karplus M. 1987. Crystallographic R factor refinement by molecular dynamics. Science 235: 458–460.
- Chan PH, Singh KSS, Wildman SG. 1972. Crystalline fraction I protein: Preparation in large yield. Science 176: 1145–1146.
- Chapman MS. Smith WW, Suh SW, Cascio D, Howard A, Hamlin R, Xuong NH, Eisenberg D. 1986. Structural studies of rubisco from tobacco. Philos Trans R Soc Lond B 313: 367–378.
- Chapman MS, Suh SW, Cascio D, Smith WW, Eisenberg D. 1987. Slidinglayer conformational change limited by the quaternary structure of plant rubisco. Nature 329: 354–356.
- Chapman MS, Suh SW, Curmi PMG, Cascio D, Smith WW, Eisenberg D. 1988. Tertiary structure of plant rubisco: Domains and their contacts. Science 241: 71–74.
- Curmi PMG, Cascio D, Sweet RM, Eisenberg D, Schreuder H. 1992. Crystal structure of the unactivated form of ribulose-1,5-bisphpsphate carboxylase/oxygenase (rubisco) from tobacco refined at 2.0 A resolution. J Biol Chem 267: 16980–16989.
- Ellis RJ. 1979. The most abundant protein in the world. Trends Biochem Sci 4: 241–244.
- Estelle M, Hanks J, McIntosh L, Somerville C. 1985. Site-specific Mutagenesis of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 260: 9523–9526.
- Jones TA. 1985. Interactive computer graphics: FRODO. Methods Enzymol 115: 157–171.
- Kabsch W. 1978. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr A 32: 922–923.
- Lorimer GH. 1981. Ribulosebisphosphate carboxylase: Amino acid sequence of a peptide bearing the activator carbon dioxide. Biochemistry 20: 1236–1240.
- Lorimer GH, Badger MR. Andrews TJ. 1976. The activation of ribulose 1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry 15: 529–536.
- Lorimer GH, Hartman FC. 1988. Evidence supporting lysine 166 of Rhodospirillum rubrum ribulosebisphosphate carboxylase as the essential base which initiates catalysis. J Biol Chem 263: 6468–6471.
- Lundqvist T, Schneider G. 1988. Crystal structure of the binary complex of ribulose-1,5-bisphosphate carboxylase/oxygenase and its product, 3-phospho-D-glycerate. J Biol Chem 263: 3643–3646.
- Lundqvist T, Schneider G. 1989. Crystal structure of the complex of ribulose-1,5-bisphosphate carboxylase/oxygenase and a transition state analogue, 2-carboxy-D-arabinitol 1,5-bisphosphate. J Biol Chem 264: 7078–7083.
- Paulsen JM, Lane MD. 1966. Spinach ribulose diphosphate carboxylase. I. Purification and properties of the enzyme. Biochemistry 5: 2350–2357.
- Pierce J, Andrews TJ, Lorimer GH. 1986. Reaction intermediate partitioning by ribulose-bisphosphate carboxylase with differing substrate specificities. J Biol Chem 261: 10248–10256.
- Pierce J, Tolbert NE, Barker R. 1980. Interaction of ribulose-bisphosphate carboxylase/oxygenase with transition state analogues. Biochemistry 19: 934–942.
- Ray WJ Jr., Bolin JT, Puvathingal JM, Minor W, Liu Y, Muchmore SW. 1991. Removal of salt from a salt-induced protein crystal without crosslinking. Preliminary examination of “desalted” crystals of phosphoglucomutase by X-ray crystallography at low temperature. Biochemistry 30: 6866–6875.
- Schneider G, Lindqvist Y, Branden CI, Lorimer G. 1986. Three-dimensional structure of ribulose-1,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum at 2.9 Å resolution. EMBO J 5: 3409–3415.
- Schreuder HA, Groendijk H, van der Laan JM, Wierenga RK. 1988. The transfer of protein crystals from their original mother liquor to a solution with a completely different precipitant. J Appl Crystallogr 21: 426–429.
- Schreuder HA, Knight S, Curmi PMG, Andersson I, Cascio D, Sweet RM, Brändén CI, Eisenberg D. 1993. Crystal structure of activated tobacco rubisco complexed with the reaction-intermediate analogue 2-carboxy-arabinitol 1,5-bisphosphate. Protein Sci 2: 1136–1146.
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