Structure and mechanism of the Rubisco-assembly chaperone Raf1

Nature Structural and Molecular Biology

Volumn 22, Issue 9, 2015, Pages 720-728

  Hauser, Thomas ^a   Bhat, Javaid Y ^a   Milicic, Goran ^a   Wendler, Petra ^b   Hartl, F Ulrich ^a   Bracher, Andreas ^a   Hayer Hartl, Manajit ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DIMER; HOLOENZYME; RIBULOSEBISPHOSPHATE CARBOXYLASE; RUBISCO ACCUMULATION FACTOR 1; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; RAF1 PROTEIN, ARABIDOPSIS;

ALPHA HELIX; ARABIDOPSIS THALIANA; ARTICLE; BETA SHEET; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME MECHANISM; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; SYNECHOCOCCUS ELONGATUS; ARABIDOPSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOLECULAR WEIGHT; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SYNECHOCOCCUS; X RAY CRYSTALLOGRAPHY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR WEIGHT; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SYNECHOCOCCUS;

EID: 84941023123     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3062     Document Type: Article

References (72)

1. Andersson, I. & Backlund, A. Structure and function of Rubisco. Plant Physiol. Biochem. 46, 275-291 (2008).
2. Hartman, F.C. & Harpel, M.R. Structure, function, regulation, and assembly of D-ribulose-1, 5-bisphosphate carboxylase/oxygenase. Annu. Rev. Biochem. 63, 197-234 (1994).
3. Ellis, R.J. Biochemistry: tackling unintelligent design. Nature 463, 164-165 (2010).
4. Sharkey, T.D. Estimating the rate of photorespiration. Physiol. Plant. 73, 147-152 (1988).
5. Portis, A.R. & Parry, M.A.J. Discoveries in Rubisco (ribulose 1, 5-bisphosphate carboxylase/oxygenase): a historical perspective. Photosynth. Res. 94, 121-143 (2007).
6. Peterhansel, C., Niessen, M. & Kebeish, R.M. Metabolic engineering towards the enhancement of photosynthesis. Photochem. Photobiol. 84, 1317-1323 (2008).
7. Maurino, V.G. & Peterhansel, C. Photorespiration: current status and approaches for metabolic engineering. Curr. Opin. Plant Biol. 13, 249-256 (2010).
8. 2-sequestering enzyme, Rubisco. Plant Physiol. 155, 27-35 (2011).
9. Parry, M.A.J. et al. Rubisco activity and regulation as targets for crop improvement. J. Exp. Bot. 64, 717-730 (2013).
10. Lin, M.T., Occhialini, A., Andralojc, P.J., Parry, M.A. & Hanson, M.R. A faster Rubisco with potential to increase photosynthesis in crops. Nature 513, 547-550 (2014).
11. Durão, P. et al. Opposing effects of folding and assembly chaperones on evolvability of Rubisco. Nat. Chem. Biol. 11, 148-155 (2015).
12. Cleland, W.W., Andrews, T.J., Gutteridge, S., Hartman, F.C. & Lorimer, G.H. Mechanism of Rubisco: the carbamate as general base. Chem. Rev. 98, 549-562 (1998).
13. Andersson, I. Catalysis and regulation in Rubisco. J. Exp. Bot. 59, 1555-1568 (2008).
14. Liu, C. et al. Coupled chaperone action in folding and assembly of hexadecameric Rubisco. Nature 463, 197-202 (2010).
15. Vitlin Gruber, A., Nisemblat, S., Azem, A. & Weiss, C. The complexity of chloroplast chaperonins. Trends Plant Sci. 18, 688-694 (2013).
16. Saschenbrecker, S. et al. Structure and function of RbcX, an assembly chaperone for hexadecameric Rubisco. Cell 129, 1189-1200 (2007).
17. van der Vies, S.M., Bradley, D. & Gatenby, A.A. Assembly of cyanobacterial and higher plant ribulose bisphosphate carboxylase subunits into functional homologous and heterologous enzyme molecules in Escherichia coli. EMBO J. 5, 2439-2444 (1986).
18. Andrews, T.J. Catalysis by cyanobacterial ribulose-bisphosphate carboxylase large subunits in the complete absence of small subunits. J. Biol. Chem. 263, 12213-12219 (1988).
19. Goloubinoff, P., Gatenby, A.A. & Lorimer, G.H. GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature 337, 44-47 (1989).
20. Li, L.-A. & Tabita, F.R. Maximum activity of recombinant ribulose 1, 5-bisphosphate carboxylase/oxygenase of Anabaena sp. strain CA requires the product of the rbcx gene. J. Bacteriol. 179, 3793-3796 (1997).
21. Onizuka, T. et al. The rbcX gene product promotes the production and assembly of ribulose-1, 5-bisphosphate carboxylase/oxygenase of Synechococcus sp. PCC7002 in Escherichia coli. Plant Cell Physiol. 45, 1390-1395 (2004).
22. Bracher, A., Starling-Windhof, A., Hartl, F.U. & Hayer-Hartl, M. Crystal structure of a chaperone-bound assembly intermediate of form I Rubisco. Nat. Struct. Mol. Biol. 18, 875-880 (2011).
23. Emlyn-Jones, D., Woodger, F.J., Price, G.D. & Whitney, S.M. RbcX can function as a Rubisco chaperonin, but is non-essential in Synechococcus PCC7942. Plant Cell Physiol. 47, 1630-1640 (2006).
24. Feiz, L. et al. Ribulose-1, 5-bis-phosphate carboxylase/oxygenase accumulation factor1 is required for holoenzyme assembly in maize. Plant Cell 24, 3435-3446 (2012).
25. Kolesinski, P., Belusiak, I., Czarnocki-Cieciura, M. & Szczepaniak, A. Rubisco accumulation factor 1 from Thermosynechococcus elongatus participates in the fnal stages of ribulose-1, 5-bisphosphate carboxylase/oxygenase assembly in Escherichia coli cells and in vitro. FEBS J. 281, 3920-3932 (2014).
26. Whitney, S.M., Birch, R., Kelso, C., Beck, J.L. & Kapralov, M.V. Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone. Proc. Natl. Acad. Sci. USA 112, 3564-3569 (2015).
27. Leitner, A. et al. The molecular architecture of the eukaryotic chaperonin TRiC/CCT. Structure 20, 814-825 (2012).
28. Newman, J., Bränden, C.I. & Jones, T.A. Structure determination and refnement of ribulose 1, 5-bisphosphate carboxylase/oxygenase from Synechococcus PCC6301. Acta Crystallogr. D Biol. Crystallogr. 49, 548-560 (1993).
29. Pettersen, E.F. et al. UCSF chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
30. Chari, A. & Fischer, U. Cellular strategies for the assembly of molecular machines. Trends Biochem. Sci. 35, 676-683 (2010).
31. Ellis, R.J. Assembly chaperones: a perspective. Phil. Trans. R. Soc. Lond. B 368, 20110398 (2013).
32. Tanaka, S., Sawaya, M.R., Kerfeld, C.A. & Yeates, T.O. Structure of the RuBisCO chaperone RbcX from Synechocystis sp. PCC6803. Acta Crystallogr. D Biol. Crystallogr. 63, 1109-1112 (2007).
33. Kolesinski, P. et al. Insights into eukaryotic Rubisco assembly: crystal structures of RbcX chaperones from Arabidopsis thaliana. Biochim. Biophys. Acta 1830, 2899-2906 (2013).
34. Wheatley, N.M., Sundberg, C.D., Gidaniyan, S.D., Cascio, D. & Yeates, T.O. Structure and identifcation of a pterin dehydratase-like protein as a ribulose-bisphosphate carboxylase/oxygenase (RuBisCO) assembly factor in the alpha-carboxysome. J. Biol. Chem. 289, 7973-7981 (2014).
35. Feiz, L. et al. RAF2: a novel Rubisco biogenesis factor in maize. Plant J. 80, 862-869 (2014).
36. Hohmann-Marriott, M.F. & Blankenship, R.E. Evolution of photosynthesis. Annu. Rev. Plant Biol. 62, 515-548 (2011).
37. Kerner, M.J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (2005).
38. Georgescauld, F. et al. GroEL/ES chaperonin modulates the mechanism and accelerates the rate of TIM-barrel domain folding. Cell 157, 922-934 (2014).
39. Catanzariti, A.M., Soboleva, T.A., Jans, D.A., Board, P.G. & Baker, R.T. An effcient system for high-level expression and easy purifcation of authentic recombinant proteins. Protein Sci. 13, 1331-1339 (2004).
40. Baker, R.T. et al. Using deubiquitylating enzymes as research tools. Methods Enzymol. 398, 540-554 (2005).
41. Brinker, A. et al. Dual function of protein confnement in chaperonin-assisted protein folding. Cell 107, 223-233 (2001).
42. Wyatt, P.J. Light scattering and the absolute characterization of macromolecules. Anal. Chim. Acta 272, 1-40 (1993).
43. Mindell, J.A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
44. Scheres, S.H. Semi-automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189, 114-122 (2015).
45. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R. & Schatz, M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24 (1996).
46. Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996).
47. Rappsilber, J., Ishihama, Y. & Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670 (2003).
48. Götze, M. et al. Automated assignment of MS/MS cleavable crosslinks in protein 3D-structure analysis. J. Am. Soc. Mass Spectrom. 26, 83-97 (2015).
49. Vachette, P., Koch, M.H. & Svergun, D.I. Looking behind the beamstop: X-ray solution scattering studies of structure and conformational changes of biological macromolecules. Methods Enzymol. 374, 584-615 (2003).
50. Konarev, P.V., Volkov, V.V., Sokolova, A.V., Koch, M.H.J. & Svergun, D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282 (2003).
51. Svergun, D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503 (1992).
52. Bernadó, P., Mylonas, E., Petoukhov, M.V., Blackledge, M. & Svergun, D.I. Structural characterization of fexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc. 129, 5656-5664 (2007).
53. Petoukhov, M.V. et al. New developments in the program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350 (2012).
54. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
55. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82 (2006).
56. Evans, P.R. Scala. Joint CCP4 ESF-EACBM Newsl. Prot. Crystallogr. 33, 22-24 (1997).
57. French, G. & Wilson, K. On the treatment of negative intensity observations. Acta Crystallogr. A 34, 517-525 (1978).
58. Sheldrick, G.M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modifcation. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485 (2010).
59. Pape, T. & Schneider, T.R. HKL2MAP: a graphical user interface for phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844 (2004).
60. Vonrhein, C., Blanc, E., Roversi, P. & Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2007).
61. Terwilliger, T.C. Maximum-likelihood density modifcation. Acta Crystallogr. D Biol. Crystallogr. 56, 965-972 (2000).
62. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
63. Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011 (2006).
64. Vagin, A.A. & Isupov, M.N. Spherically averaged phased translation function and its application to the search for molecules and fragments in electron-density maps. Acta Crystallogr. D Biol. Crystallogr. 57, 1451-1456 (2001).
65. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refnement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
66. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
67. Afonine, P.V. et al. Towards automated crystallographic structure refnement with phenix.refne. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367 (2012).
68. Kleywegt, G.T. & Jones, T.A. A super position. CCP4 ESF-EACBM Newsl. Prot. Crystallogr. 31, 9-14 (1994).
69. Thompson, J.D., Higgins, D.G. & Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specifc gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (1994).
70. Larkin, M.A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
71. Gouet, P., Courcelle, E., Stuart, D.I. & Metoz, F. ESPript: multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999).
72. Cole, C., Barber, J.D. & Barton, G.J. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201 (2008).