Prioritizing targets for structural biology through the lens of proteomics: The archaeal protein TGAM_1934 from Thermococcus gammatolerans

Proteomics

Volumn 15, Issue 1, 2015, Pages 114-123

  Yang, Yin Shan ^a   Fernandez, Bernard ^b   Lagorce, Arnaud ^c   Aloin, Valérie ^b   De Guillen, Karine Montet ^a   Boyer, Jean Baptiste ^b   Dedieu, Alain ^b   Confalonieri, Fabrice ^c   Armengaud, Jean ^b   Roumestand, Christian ^a  

^a CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^b DIF   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Genome annotation; High throughput proteomics; Microbiology; NMR structure; ORFan; Protein evolution

Indexed keywords

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; THERMOCOCCUS GAMMATOLERANS;

ARCHAEAL PROTEIN; FRATAXIN; IRON BINDING PROTEIN;

AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEOMICS; THERMOCOCCUS;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; IRON-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEOMICS; THERMOCOCCUS;

EID: 84920428616     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300535     Document Type: Article

References (54)

1. Galkin, A., Sarikaya, E., Lehmann, C., Howard, A., Herzberg, O., X-ray structure of HI0817 from Haemophilus influenzae: protein of unknown function with a novel fold. Proteins 2004, 57, 874-877.
2. Nair, R., Liu, J., Soong, T. T., Acton, T. B. et al., Structural genomics is the largest contributor of novel structural leverage. J. Struct. Funct. Genomics 2009, 10, 181-191.
3. Daubin, V., Ochman, H., Bacterial genomes as new gene homes: the genealogy of ORFans in E. coli. Genome Res. 2004, 14, 1036-1042.
4. Fischer, D., Rational structural genomics: affirmative action for ORFans and the growth in our structural knowledge. Protein Eng. 1999, 12, 1029-1030.
5. Hanson, A. D., Pribat, A., Waller, J. C., de Crecy-Lagard, V., "Unknown" proteins and "orphan" enzymes: the missing half of the engineering parts list-and how to find it. Biochem. J. 2010, 425, 1-11.
6. Siew, N., Azaria, Y., Fischer, D., The ORFanage: an ORFan database. Nucleic Acids Res. 2004, 32, D281-D283.
7. Siew, N., Fischer, D., Analysis of singleton ORFans in fully sequenced microbial genomes. Proteins 2003, 53, 241-251.
8. Siew, N., Fischer, D., Structural biology sheds light on the puzzle of genomic ORFans. J. Mol. Biol. 2004, 342, 369-373.
9. Yin, Y., Fischer, D., On the origin of microbial ORFans: quantifying the strength of the evidence for viral lateral transfer. BMC Evol. Biol. 2006, 6, 63.
10. Yin, Y., Fischer, D., Identification and investigation of ORFans in the viral world. BMC Genomics 2008, 9, 24.
11. Armengaud, J., A perfect genome annotation is within reach with the proteomics and genomics alliance. Curr. Opin. Microbiol. 2009, 12, 292-300.
12. Abergel, C., Monchois, V., Chenivesse, S., Jeudy, S., Claverie, J. M., Crystallization and preliminary crystallographic study of b0220, an "ORFan" protein of unknown function from Escherichia coli. Acta Crystallogr. D Biol. Crystallogr. 2000, 56, 1694-1695.
13. Ang, D., Georgopoulos, C., An ORFan no more: the bacteriophage T4 39.2 gene product, NwgI, modulates GroEL chaperone function. Genetics 2012, 190, 989-1000.
14. Hakim, M., Ezerina, D., Alon, A., Vonshak, O., Fass, D., Exploring ORFan domains in giant viruses: structure of mimivirus sulfhydryl oxidase R596. PLoS One 2012, 7, e50649.
15. Shmuely, H., Dinitz, E., Dahan, I., Eichler, J. et al., Poorly conserved ORFs in the genome of the archaea Halobacterium sp. NRC-1 correspond to expressed proteins. Bioinformatics 2004, 20, 1248-1253.
16. Armengaud, J., Microbiology and proteomics, getting the best of both worlds! Environ. Microbiol. 2013, 15, 12-23.
17. Kim, K. M., Caetano-Anolles, G., The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms. BMC Evol. Biol. 2012, 12, 13.
18. Jolivet, E., L'Haridon, S., Corre, E., Forterre, P., Prieur, D., Thermococcus gammatolerans sp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int. J. Syst. Evol. Microbiol. 2003, 53, 847-851.
19. Zivanovic, Y., Armengaud, J., Lagorce, A., Leplat, C. et al., Genome analysis and genome-wide proteomics of Thermococcus gammatolerans, the most radioresistant organism known amongst the Archaea. Genome Biol. 2009, 10, R70.
20. Lagorce, A., Fourcans, A., Dutertre, M., Bouyssiere, B. et al., Genome-wide transcriptional response of the archaeon Thermococcus gammatolerans to cadmium. PLoS One 2012, 7, e41935.
21. Tapias, A., Leplat, C., Confalonieri, F., Recovery of ionizing-radiation damage after high doses of gamma ray in the hyperthermophilic archaeon Thermococcus gammatolerans. Extremophiles 2009, 13, 333-343.
22. de Groot, A., Dulermo, R., Ortet, P., Blanchard, L. et al., Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet. 2009, 5, e1000434.
23. Dupierris, V., Masselon, C., Court, M., Kieffer-Jaquinod, S., Bruley, C., A toolbox for validation of mass spectrometry peptides identification and generation of database: IRMa. Bioinformatics 2009, 25, 1980-1981.
24. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A. et al., The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 2013, 41, D1063-D1069.
25. Armengaud, J., Fernandez, B., Chaumont, V., Rollin-Genetet, F. et al., Identification, purification, and characterization of an eukaryotic-like phosphopantetheine adenylyltransferase (coenzyme A biosynthetic pathway) in the hyperthermophilic archaeon Pyrococcus abyssi. J. Biol. Chem. 2003, 278, 31078-31087.
26. Gabant, G., Auxilien, S., Tuszynska, I., Locard, M. et al., THUMP from archaeal tRNA:m22G10 methyltransferase, a genuine autonomously folding domain. Nucleic Acids Res. 2006, 34, 2483-2494.
27. Sattler, M., Schleucher, J., Griesinger, C., Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Mag. Reson. Spectrosc. 1999, 34, 93-158.
28. Piotto, M., Saudek, V., Sklenar, V., Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 1992, 2, 661-665.
29. Cornilescu, G., Delaglio, F., Bax, A., Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 1999, 13, 289-302.
30. Guntert, P., Automated NMR structure calculation with CYANA. Methods Mol. Biol. 2004, 278, 353-378.
31. Nederveen, A. J., Doreleijers, J. F., Vranken, W., Miller, Z. et al., RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins 2005, 59, 662-672.
32. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., Thornton, J. M., AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 1996, 8, 477-486.
33. Koradi, R., Billeter, M., Wuthrich, K., MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 1996, 14, 51-55, 29-32.
34. Christie-Oleza, J. A., Fernandez, B., Nogales, B., Bosch, R., Armengaud, J., Proteomic insights into the lifestyle of an environmentally relevant marine bacterium. ISME J. 2012, 6, 124-135.
35. Baudet, M., Ortet, P., Gaillard, J. C., Fernandez, B. et al., Proteomics-based refinement of Deinococcus deserti genome annotation reveals an unwonted use of non-canonical translation initiation codons. Mol. Cell. Proteomics 2010, 9, 415-426.
36. Gorlas, A., Croce, O., Oberto, J., Gauliard, E. et al., Thermococcus nautili sp. nov., a hyperthermophilic archaeon isolated from a hydrothermal deep-sea vent. Int. J. Syst. Evol. Microbiol. 2014, 64, 1802-1810.
37. Alonso, B., Beraud, C., Meguellati, S., Chen, S. W. et al., Eukaryotic GPN-loop GTPases paralogs use a dimeric assembly reminiscent of archeal GPN. Cell Cycle 2013, 12, 463-472.
38. Alonso, B., Chaussinand, G., Armengaud, J., Godon, C., A role for GPN-loop GTPase yGPN1 in sister chromatid cohesion. Cell Cycle 2011, 10, 1828-1837.
39. Gras, S., Chaumont, V., Fernandez, B., Carpentier, P. et al., Structural insights into a new homodimeric self-activated GTPase family. EMBO Rep. 2007, 8, 569-575.
40. Sakai, N., Yao, M., Itou, H., Watanabe, N. et al., The three-dimensional structure of septum site-determining protein MinD from Pyrococcus horikoshii OT3 in complex with Mg-ADP. Structure 2001, 9, 817-826.
41. Bulyha, I., Lindow, S., Lin, L., Bolte, K. et al., Two small GTPases act in concert with the bactofilin cytoskeleton to regulate dynamic bacterial cell polarity. Dev. Cell. 2013, 25, 119-131.
42. Wirth, R., Bellack, A., Bertl, M., Bilek, Y. et al., The mode of cell wall growth in selected archaea is similar to the general mode of cell wall growth in bacteria as revealed by fluorescent dye analysis. Appl. Environ. Microbiol. 2011, 77, 1556-1562.
43. Richardson, J. S., The anatomy and taxonomy of protein structure. Adv. Protein Chem. 1981, 34, 167-339.
44. Holm, L., Sander, C., Protein folds and families: sequence and structure alignments. Nucleic Acids Res. 1999, 27, 244-247.
45. Cho, S. J., Lee, M. G., Yang, J. K., Lee, J. Y. et al., Crystal structure of Escherichia coli CyaY protein reveals a previously unidentified fold for the evolutionarily conserved frataxin family. Proc. Natl. Acad. Sci. USA 2000, 97, 8932-8937.
46. Nair, M., Adinolfi, S., Pastore, C., Kelly, G. et al., Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure 2004, 12, 2037-2048.
47. Armengaud, J., Marie Hartmann, E., Bland, C., Proteogenomics for environmental microbiology. Proteomics 2013, 13, 2731-2742.
48. Brodie, E. D., 3rd, Convergent evolution: pick your poison carefully. Curr. Biol. 2010, 20, R152-R154.
49. Schaeffer, R. D., Daggett, V., Protein folds and protein folding. Protein Eng. Des. Sel. 2011, 24, 11-19.
50. Te Velthuis, A. J., Bagowski, C. P., Linking fold, function and phylogeny: a comparative genomics view on protein (domain) evolution. Curr. Genomics 2008, 9, 88-96.
51. Boyer, M., Gimenez, G., Suzan-Monti, M., Raoult, D., Classification and determination of possible origins of ORFans through analysis of nucleocytoplasmic large DNA viruses. Intervirology 2010, 53, 310-320.
52. Cortez, D., Forterre, P., Gribaldo, S., A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol. 2009, 10, R65.
53. Yomtovian, I., Teerakulkittipong, N., Lee, B., Moult, J., Unger, R., Composition bias and the origin of ORFan genes. Bioinformatics 2010, 26, 996-999.
54. Yu, G., Stoltzfus, A., Population diversity of ORFan genes in Escherichia coli. Genome Biol. Evol. 2012, 4, 1176-1187.