A Sco protein among the hypothetical proteins of Bacillus lehensis G1: Its 3D macromolecular structure and association with Cytochrome C Oxidase

BMC Structural Biology

Mohd Basyaruddin Abdul Rahman³  Nor Muhammad Mahadi³  Abdul Munir Abdul Murad⁴  Roghayeh Abedi Karjiban²  Abu Bakar Salleh¹  Adam Thean Chor Leow¹  Yahaya M Normi¹  Soo Huei Tan¹ 

[1] Center for Enzyme and Microbial Biotechnology (EMTECH), Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia;Department of Chemistry, Faculty of Science, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia;Malaysia Genome Institute, Ministry of Science, Technology and Innovation, Jalan Bangi, Kajang, Selangor 43000, Malaysia;School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 UKM, Bangi, Selangor, Malaysia

关键词: Cytochrome c oxidase;    Redox reaction;    Copper binding;    Thioredoxin;    Sco;    Bleg1_2507;    Hypothetical proteins;   

Others  :  793096
DOI  :  10.1186/1472-6807-14-11

 received in 2013-09-13, accepted in 2014-03-14,  发布年份 2014

【 摘 要 】

Background

At least a quarter of any complete genome encodes for hypothetical proteins (HPs) which are largely non-similar to other known, well-characterized proteins. Predicting and solving their structures and functions is imperative to aid understanding of any given organism as a complete biological system. The present study highlights the primary effort to classify and cluster 1202 HPs of Bacillus lehensis G1 alkaliphile to serve as a platform to mine and select specific HP(s) to be studied further in greater detail.

Results

All HPs of B. lehensis G1 were grouped according to their predicted functions based on the presence of functional domains in their sequences. From the metal-binding group of HPs of the cluster, an HP termed Bleg1_2507 was discovered to contain a thioredoxin (Trx) domain and highly-conserved metal-binding ligands represented by Cys69, Cys73 and His159, similar to all prokaryotic and eukaryotic Sco proteins. The built 3D structure of Bleg1_2507 showed that it shared the βαβαββ core structure of Trx-like proteins as well as three flanking β-sheets, a 3₁₀ –helix at the N-terminus and a hairpin structure unique to Sco proteins. Docking simulations provided an interesting view of Bleg1_2507 in association with its putative cytochrome c oxidase subunit II (COXII) redox partner, Bleg1_2337, where the latter can be seen to hold its partner in an embrace, facilitated by hydrophobic and ionic interactions between the proteins. Although Bleg1_2507 shares relatively low sequence identity (47%) to BsSco, interestingly, the predicted metal-binding residues of Bleg1_2507 i.e. Cys-69, Cys-73 and His-159 were located at flexible active loops similar to other Sco proteins across biological taxa. This highlights structural conservation of Sco despite their various functions in prokaryotes and eukaryotes.

Conclusions

We propose that HP Bleg1_2507 is a Sco protein which is able to interact with COXII, its redox partner and therefore, may possess metallochaperone and redox functions similar to other documented bacterial Sco proteins. It is hoped that this scientific effort will help to spur the search for other physiologically relevant proteins among the so-called “orphan” proteins of any given organism.

【 授权许可】

   
2014 Tan et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Bork P: Powers and pitfalls in sequence analysis: the 70% hurdle. Genome Res 2000, 10(4):398-400.
• [2]Galperin MY, Koonin EV: ‘Conserved hypothetical’ proteins: prioritization of targets for experimental study. Nucl Acid Res 2004, 32(18):5452-5463.
• [3]Roberts RJ: Identifying Protein Function- A Call for Community Action. PLoS Biol 2004, 2(3):e42.
• [4]Desler C, Suravajhala P, Sanderhoff M, Rasmussen M, Rasmussen LJ: In Silico screening for functional candidates amongst hypothetical proteins. BMC Bioinforma 2009, 10(289):1471-2105.
• [5]Samsulrizal NH, Abdul Murad AM, Noor YM, Jema'on NA, Najimudin N, Illias RM, Abu Bakar FD, Mahadi NM: Genome Sequencing and Annotation of Alkaliphilic Bacterium Bacillus lehensis G1. India: The Eighth Asia Pacific Bioinformatics Conference, Bangalore (APBC 2010); 2010:18-21.
• [6]Balatri E, Banci L, Bertini I, Cantini F, Baffoni-Ciofi S: Solution Structure of Sco1: A Thioredoxin-like Protein Invovled in Cytochrome c Oxidase Assembly. Structure 2003, 11(11):1431-1443.
• [7]Glerum DM, Shtanko A, Tzagoloff A: Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Biol Chem 2003, 271(24):14504-14509.
• [8]Krummeck G, Rӧdel G: Yeast Sco1 protein is required for a post-translational step in the accumulation of mitochondrial cytochrome c oxidase subunits I and II. Curr Genet 1990, 18(1):13-15.
• [9]Schulze M, Rӧdel G: SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II. Mol Gen Genet 1988, 211(3):492-498.
• [10]Abajian C, Rosenzweig CA: Crystal structure of yeast Sco1. J Biol Inorg Chem 2006, 11(4):459-466.
• [11]Papadopoulou LC, Sue CM, Davidson MM, Tanji K, Nishino I, Sadlock JE, Krishna S, Walker W, Selby J, Glerum DM, Coster RV, Lyon G, Scalais E, Lebel R, Kaplan P, Shanske S, De Vivo DC, Bonilla E, Hirano M, DiMauro S, Schon EA: Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat Genet 1999, 23(3):333-337.
• [12]Attallah CV, Welchen E, Martin AP, Spinelli SV, Bonnard G, Palatnik JF, Gonzalez DH: Plants contain two SCO proteins that are differentially involved in cytochrome c oxidase function and copper and redox homeostasis. J Exp Bol 2011, 62(12):4281-4294.
• [13]Valnot I, Osmond S, Gigarel N, Mehaye B, Amiel J, Cormier-Daire V, Munnich A, Bonnefont JP, Rustin P, Rӧtig A: Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy. Am J Hum Genet 2000, 67(5):1104-1109.
• [14]Quevillon E, Silventoinen V, Pillai NS, Harte N, Mulder N, Apweile R, Lopez R: InterProScan: protein domains identifier. Nucl Acids Res 2005, 33(Web Server Issue):W116-W120.
• [15]Marchler-Bauer A, Anderson JB, Derbyshire MK, DeWeese SC, Gonzales NR, Gwadz M, Hao L, He S, Hurwitz DI, Jackson JD, Ke Z, Krylov D, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Thanki N, Yamashita RA, Yin JJ, Zhang D, Bryant : CDD: a conserved domains and protein three-dimensional structure. Nucl Acids Res 2013, 41(D1):D348-D352.
• [16]Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped-BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 1997, 25(17):3389-3402.
• [17]De Castro E, Sigrist CJA, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N: ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucl Acids Res 2006, 34(Web Server Issue):W362-W365.
• [18]Ashkenazy H, Erez E, Martz E, Pupko T, Ben TN: ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucl Acids Res 2010, 38(Suppl 2):W529-W533.
• [19]Passerini A, Lippi M, Frasconi P: MetalDetector v2.0: predicting the geometry of metal binding sites from protein sequence. Nucl Acids Res 2011, 39(Suppl 2):W288-W292.
• [20]Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD Bairoch A: Protein Identification and Analysis Tools on the ExPASy Server. In The Proteomics Protocols Handbook. Edited by John MW. Totowa, New Jersey, USA: Humana Press; 2005:571-607.
• [21]Rice P, Longen T, Bleasby A: The European Molecular Biology Open Software Suite. Trends Genet 2000, 16(6):276-277.
• [22]Felsenstein J: PHYLIP – Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164-166.
• [23]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallance IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
• [24]Ṧali A, Blundell TL: Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 1993, 234(3):779-815.
• [25]Delano WL: The PyMOL Molecular Graphics System. San Carlos, CA, USA: Delano Scientific; 2002.
• [26]Kojetin DJ, Thompson RJ, Cavanagh J: Hypothesis: Sub-classification of response regulators using the surface characteristics of their receiver domains. FEBS Lett 2004, 5601(1–3):227-228.
• [27]Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE: UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 2004, 25(13):1605-1612.
• [28]Schymkowitz JW, Rousseau F, Martins IC, Ferkinghoff-Berg J, Stricher F, Serrano L: Prediction of water and metal-binding sites and their affinities by using the Fold-X force field. Proc Natl Acad Sci USA 2005, 102(29):10147-10152.
• [29]Colovos C, Yeates OT: Verification of protein structures: Patterns of nonbonded atomic interactions. Prot Sci 1993, 2(9):1511-1519.
• [30]Laskoswki RA, MacArthur MW, Moss DS, Thornton JM: PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 1993, 26(2):283-291.
• [31]Kozakov D, Hall DR, Beglov D, Brenke R, Comeau SR, Shen Y, Keyong L, Jiefu Z, Vakili P, Paschalidis CI, Vajda S: Achieving reliability and high accuracy in automated protein docking: ClusPro, PIPER, SDU, and stability analysis in CAPRI rounds 13–19. Proteins 2004, 78:3124-3130.
• [32]Krieger E, Joo K, Lee J, Raman S, Thompson J, Tyka M, Baker D, Karplus L: Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 2009, 77(Suppl 9):114-122.
• [33]Banci L, Bertini I, Cavallaro G, Baffoni-Ciofi S: Seeking the determinants of the elusive functions of Sco proteins. FEBS J 2011, 278(13):2244-2262.
• [34]Blundell KL, Wilson MT, Svistunenko DA, Vijgenboom E, Worrall JA: Morphological development and cytochrome c oxidase activity in Streptomyces lividans are dependent on the action of a copper bound Sco protein. Open Biol 2013, 3(1):120163.
• [35]Banci L, Bertini I, Cavallaro G, Rosato A: The Functions of Sco Proteins from Genome-Based Analysis. J Proteome Res 2007, 6(4):1568-1579.
• [36]Lyons JA, Aragao D, Slattery O, Pisliakov AV, Soulimane T, Caffrey M: Structural insights into electron transfer in caa3-type cytochrome oxidase. Nature 2012, 487(7408):514-518.
• [37]Ye Q, Iveta SI, Hill BC, Chao JZ: Identification of a Disulfide Switch in BsSco, a Member of the Sco Family of Cytochrome c Oxidase Assembly Proteins. Biochemistry 2005, 44(14):5552-5560.
• [38]Kinch LN, Baker D, Grishin NV: Deciphering a Novel Thioredoxin-Like Fold Family. Proteins 2003, 52(3):323-331.
• [39]Banci L, Bertini I, Baffoni-Ciofi S, Kozyreva T, Mori M, Wang S: Sco proteins are involved in electron transfer processes. J Biol Inorg Chem 2011, 16(3):391-403.
• [40]Banci L, Bertini I, Calderone V, Ciofi-Baffoni S, Mangani S, Martinelli M, Palumaa P, Wang S: A hint for the function of human Sco1 from different structures. Proc Natl Acad Sci USA 2006, 103:8595-8600.
• [41]Andruzzi L, Nakano M, Nilges Mark J, Blackburn Ninian J: Spectroscopic Studies of Metal-Binding and Metal Selectivity in Bacillus subtilis BSco, a Homologue of the Yeast Mitochondrial Protein Sco1p. J Am Chem Soc 2005, 127(47):16548-16558.