Skip to main content

Advertisement

SpringerLink
Log in

Genome scale identification, structural analysis, and classification of periplasmic binding proteins from Mycobacterium tuberculosis

  • Original Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Periplasmic-binding proteins occupy the periplasmic space of bacteria and are involved in binding and transport of various ions, siderophores, and other diverse types of solutes. These proteins may be associated with membrane transport systems or may help in activation of signal transducers. There is limited information available on Mycobacterium tuberculosis (Mtb) periplasm-inhabiting proteins. In the present study, we have performed genome-wide identification and functional annotation of periplasmic-binding proteins of Mtb on the basis of signature characteristics and their functional motifs. 37 putative periplasmic-binding proteins were identified in Mtb proteome and categorized into different classes mainly known for their association with membrane transport and signaling pathways. Conclusively, this study adds 11 completely novel proteins to the periplasmic binding proteome of Mtb, which were not annotated as PBPs earlier. This study provides an overview of the periplasmic binding proteome of Mtb, which may be involved in various important patho-physiological functions of the bacteria. These proteins may serve as novel drug targets, which may lead to better treatment strategies against this deadly pathogen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Mtb :

Mycobacterium tuberculosis

SBP:

Substrate-binding proteins

PBP:

Periplasmic-binding proteins

TM:

Transmembrane

References

  • Bamford V, Dobbin PS, Richardson DJ, Hemmings AM (1999) Open conformation of a flavocytochrome c3 fumarate reductase. Nat Struct Mol Biol 6:1104–1107

    Article  CAS  Google Scholar 

  • Banerjee S, Farhana A, Ehtesham NZ, Hasnain SE (2011) Iron acquisition, assimilation and regulation in mycobacteria. Infect Genet Evol 11:825–838

    Article  CAS  PubMed  Google Scholar 

  • Banerjee S, Paul S, Nguyen LT, Chu BC, Vogel HJ (2016) FecB, a periplasmic ferric-citrate transporter from E. coli, can bind different forms of ferric-citrate as well as a wide variety of metal-free and metal-loaded tricarboxylic acids. Metallomics Integr Biometal Sci 8:125–133

    Article  CAS  Google Scholar 

  • Banfield MJ, Barker JJ, Perry AC, Brady RL (1998) Function from structure? The crystal structure of human phosphatidylethanolamine-binding protein suggests a role in membrane signal transduction. Structure 6:1245–1254

    Article  CAS  PubMed  Google Scholar 

  • Bashyam MD, Hasnain SE (2004) The extracytoplasmic function sigma factors: role in bacterial pathogenesis. Infect Genet Evol 4:301–308

    Article  CAS  PubMed  Google Scholar 

  • Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beasley FC, Vinés ED, Grigg JC, Zheng Q, Liu S, Lajoie GA, Murphy ME, Heinrichs DE (2009) Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol Microbiol 72:947–963

    Article  CAS  PubMed  Google Scholar 

  • Bendtsen JD, Jensen LJ, Blom N, Von Heijne G, Brunak S (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Design Sel PEDS 17:349–356

    Article  CAS  Google Scholar 

  • Berks BC, Sargent F, Palmer T (2000) The Tat protein export pathway. Mol Microbiol 35:260–274

    Article  CAS  PubMed  Google Scholar 

  • Bernstein FC, Koetzle TF, Williams GJ, Meyer EF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) The protein data bank. Eur J Biochem 80:319–324

    Article  CAS  PubMed  Google Scholar 

  • Berntsson RP-A, Smits SH, Schmitt L, Slotboom D-J, Poolman B (2010) A structural classification of substrate-binding proteins. FEBS Lett 584:2606–2617

    Article  CAS  PubMed  Google Scholar 

  • Bhakta S, Basu J (2002) Overexpression, purification and biochemical characterization of a class A high-molecular-mass penicillin-binding protein (PBP), PBP1* and its soluble derivative from Mycobacterium tuberculosis. Biochem J 361:635–639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Billman-Jacobe H, Haites RE, Coppel RL (1999) Characterization of a Mycobacterium smegmatis mutant lacking penicillin binding protein 1. Antimicrob Agents Chemother 43:3011–3013

    CAS  PubMed  PubMed Central  Google Scholar 

  • Borich S, Murray A, Gormley E (1999) Genomic arrangement of a putative operon involved in maltose transport in the Mycobacterium tuberculosis complex and Mycobacterium leprae. Microbios 102:7–15

    Google Scholar 

  • Bowler LD, Spratt BG (1989) Membrane topology of penicillin-binding protein 3 of Escherichia coli. Mol Microbiol 3:1277–1286

    Article  CAS  PubMed  Google Scholar 

  • Boyd JM, Endrizzi JA, Hamilton TL, Christopherson MR, Mulder DW, Downs DM, Peters JW (2011) FAD binding by ApbE protein from Salmonella enterica: a new class of FAD-binding proteins. J Bacteriol 193:887–895

    Article  CAS  PubMed  Google Scholar 

  • Braibant M, Gilot P, Content J (2000) The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiol Rev 24:449–467

    Article  CAS  PubMed  Google Scholar 

  • Brakeman PR, Lanahan AA, O’Brien R, Roche K, Barnes CA, Huganir RL, Worley PF (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386:284–288

    Article  CAS  PubMed  Google Scholar 

  • Brodin P, Majlessi L, Marsollier L, de Jonge MI, Bottai D, Demangel C, Hinds J, Neyrolles O, Butcher PD, Leclerc C (2006) Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 74:88–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brzostek A, Dziadek B, Rumijowska-Galewicz A, Pawelczyk J, Dziadek J (2007) Cholesterol oxidase is required for virulence of Mycobacterium tuberculosis. FEMS Microbiol Lett 275:106–112

    Article  PubMed  CAS  Google Scholar 

  • Chaudhary N, Kumari I, Sandhu P, Ahmed M, Akhter Y (2016) Proteome scale census of major facilitator superfamily transporters in Trichoderma reesei using protein sequence and structure based classification enhanced ranking. Gene 585:166–176

    Article  CAS  PubMed  Google Scholar 

  • Chu BC, Vogel HJ (2011) A structural and functional analysis of type III periplasmic and substrate binding proteins: their role in bacterial siderophore and heme transport. Biol Chem 392:39–52

    Article  CAS  PubMed  Google Scholar 

  • Cohen KA, El-Hay T, Wyres KL, Weissbrod O, Munsamy V, Yanover C, Aharonov R, Shaham O, Conway TC, Goldschmidt Y, Bishai WR, Pym AS (2016) Paradoxical hypersusceptibility of drug-resistant Mycobacterium tuberculosis to beta-lactam antibiotics. EBioMedicine 9:170–179

    Article  PubMed  PubMed Central  Google Scholar 

  • Cole ST (1999) Learning from the genome sequence of Mycobacterium tuberculosis H37Rv. FEBS Lett 452:7–10

    Article  CAS  PubMed  Google Scholar 

  • Counago RM, McDevitt CA, Ween MP, Kobe B (2012) Prokaryotic substrate-binding proteins as targets for antimicrobial therapies. Curr Drug Targets 13:1400–1410

    Article  CAS  PubMed  Google Scholar 

  • Daffé M, Reyrat J-M (2008) The mycobacterial cell envelope. ASM Press, Washington

    Google Scholar 

  • Datta P, Dasgupta A, Singh AK, Mukherjee P, Kundu M, Basu J (2006) Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol 62:1655–1673

    Article  CAS  PubMed  Google Scholar 

  • Devi A, McCurdy H (1984) Cyclic GMP and cyclic AMP binding proteins in Myxococcus xanthus. Microbiology 130:1845–1849

    Article  CAS  Google Scholar 

  • Diez J, Diederichs K, Greller G, Horlacher R, Boos W, Welte W (2001) The crystal structure of a liganded trehalose/maltose-binding protein from the hyperthermophilic archaeon Thermococcus litoralis at 1.85 Å. J Mol Biol 305:905–915

    Article  CAS  PubMed  Google Scholar 

  • Elliott SR, Tischler AD (2016) Phosphate responsive regulation provides insights for ESX-5 function in Mycobacterium tuberculosis. Curr Genet 1–5

  • Eulenburg G, Higman VA, Diehl A, Wilmanns M, Holton SJ (2013) Structural and biochemical characterization of Rv2140c, a phosphatidylethanolamine-binding protein from Mycobacterium tuberculosis. FEBS Lett 587:2936–2942

    Article  CAS  PubMed  Google Scholar 

  • Fedarovich A, Nicholas RA, Davies C (2010) Unusual conformation of the SxN motif in the crystal structure of penicillin-binding protein A from Mycobacterium tuberculosis. J Mol Biol 398:54–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felder CB, Graul RC, Lee AY, Merkle H-P, Sadee W (1999) The Venus flytrap of periplasmic binding proteins: an ancient protein module present in multiple drug receptors. AAps Pharmsci 1:7–26

    Article  PubMed Central  Google Scholar 

  • Fullam E, Prokes I, Fütterer K, Besra GS (2016) Structural and functional analysis of the solute-binding protein UspC from Mycobacterium tuberculosis that is specific for amino sugars. Open Biol 6:160105

    Article  PubMed  PubMed Central  Google Scholar 

  • Garavaglia S, Bruzzone S, Cassani C, Canella L, Allegrone G, Sturla L, Mannino E, Millo E, De Flora A, Rizzi M (2012) The high-resolution crystal structure of periplasmic Haemophilus influenzae NAD nucleotidase reveals a novel enzymatic function of human CD73 related to NAD metabolism. Biochem J 441:131–141

    Article  CAS  PubMed  Google Scholar 

  • Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, Beyers AD (2001) The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G + C Gram-positive bacteria. Genome Biol 2: RESEARCH0044

  • Guinane CM, Cotter PD, Ross RP, Hill C (2006) Contribution of penicillin-binding protein homologs to antibiotic resistance, cell morphology, and virulence of Listeria monocytogenes EGDe. Antimicrob Agents Chemother 50:2824–2828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gulick AM, Starai VJ, Horswill AR, Homick KM, Escalante-Semerena JC (2003) The 1.75 Å crystal structure of acetyl-CoA synthetase bound to adenosine-5′-propylphosphate and coenzyme A. Biochemistry 42:2866–2873

    Article  CAS  PubMed  Google Scholar 

  • He JJ, Quiocho FA (1993) Dominant role of local dipoles in stabilizing uncompensated charges on a sulfate sequestered in a periplasmic active transport protein. Protein Sci 2:1643–1647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hengst U, Albrecht H, Hess D, Monard D (2001) The phosphatidylethanolamine-binding protein is the prototype of a novel family of serine protease inhibitors. J Biol Chem 276:535–540

    Article  CAS  PubMed  Google Scholar 

  • Hett EC, Rubin EJ (2008) Bacterial growth and cell division: a mycobacterial perspective. Microbiol Mol Biol Rev 72:126–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins CF (2001) ABC transporters: physiology, structure and mechanism—an overview. Res Microbiol 152:205–210

    Article  CAS  PubMed  Google Scholar 

  • Ho WW, Li H, Eakanunkul S, Tong Y, Wilks A, Guo M, Poulos TL (2007) Holo- and apo-bound structures of bacterial periplasmic heme-binding proteins. J Biol Chem 282:35796–35802

    Article  CAS  PubMed  Google Scholar 

  • Houben EN, Bestebroer J, Ummels R, Wilson L, Piersma SR, Jiménez CR, Ottenhoff TH, Luirink J, Bitter W (2012) Composition of the type VII secretion system membrane complex. Mol Microbiol 86:472–484

    Article  CAS  PubMed  Google Scholar 

  • Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37:D211–D215

    Article  CAS  PubMed  Google Scholar 

  • Hutchings MI, Palmer T, Harrington DJ, Sutcliffe IC (2009) Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold ‘em, knowing when to fold ‘em. Trends Microbiol 17:13–21

    Article  CAS  PubMed  Google Scholar 

  • Jaiswal RK, Prabha TS, Manjeera G, Gopal B (2013) Mycobacterium tuberculosis RsdA provides a conformational rationale for selective regulation of sigma-factor activity by proteolysis. Nucleic Acids Res 41:3414–3423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon B, Zhang Q (2007) Cj0011c, a periplasmic single-and double-stranded DNA-binding protein, contributes to natural transformation in Campylobacter jejuni. J Bacteriol 189:7399–7407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Zhang Q, Zheng Q, Zhou H, Jin J, Zhou W, Bartlam M, Rao Z (2014) Structural analysis of Mycobacterium tuberculosis ATP-binding cassette transporter subunit UgpB reveals specificity for glycerophosphocholine. FEBS J 281:331–341

    Article  CAS  PubMed  Google Scholar 

  • Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12:1652–1662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalscheuer R, Weinrick B, Veeraraghavan U, Besra GS, Jacobs WR (2010) Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci 107:21761–21766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur AP, Lansky IB, Wilks A (2009) The role of the cytoplasmic heme-binding protein (PhuS) of Pseudomonas aeruginosa in intracellular heme trafficking and iron homeostasis. J Biol Chem 284:56–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kendall SL, Withers M, Soffair CN, Moreland NJ, Gurcha S, Sidders B, Frita R, Ten Bokum A, Besra GS, Lott JS, Stoker NG (2007) A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis. Mol Microbiol 65:684–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kieser KJ, Rubin EJ (2014) How sisters grow apart: mycobacterial growth and division. Nat Rev Microbiol 12:550–562

    Article  CAS  PubMed  Google Scholar 

  • Kim KK, Yokota H, Kim S-H (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400:787–792

    Article  CAS  PubMed  Google Scholar 

  • Koch C, Neumann P, Valerius O, Feussner I, Ficner R (2016) Crystal structure of alcohol oxidase from Pichia pastoris. PLoS One 11:e0149846

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  CAS  PubMed  Google Scholar 

  • Książkiewicz M, Rychel S, Nelson MN, Wyrwa K, Naganowska B, Wolko B (2016) Expansion of the phosphatidylethanolamine binding protein family in legumes: a case study of Lupinus angustifolius L. FLOWERING LOCUS T homologs, LanFTc1 and LanFTc2. BMC Genom 17:820

    Article  Google Scholar 

  • Kumar A, Bose M, Brahmachari V (2003) Analysis of expression profile of mammalian cell entry (mce) operons of Mycobacterium tuberculosis. Infect Immun 71:6083–6087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee I, Berdis AJ, Suzuki CK (2006) Recent developments in the mechanistic enzymology of the ATP-dependent Lon protease from Escherichia coli: highlights from kinetic studies. Mol BioSyst 2:477–483

    Article  CAS  PubMed  Google Scholar 

  • Lew JM, Kapopoulou A, Jones LM, Cole ST (2011) TubercuList—10 years after. Tuberculosis 91:1–7

    Article  PubMed  Google Scholar 

  • Lim D, Strynadka NC (2002) Structural basis for the β lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus. Nat Struct Mol Biol 9:870–876

    CAS  Google Scholar 

  • Linton KJ, Higgins CF (1998) The Escherichia coli ATP-binding cassette (ABC) proteins. Mol Microbiol 28:5–13

    Article  CAS  PubMed  Google Scholar 

  • Lovering AL, De Castro L, Strynadka NC (2008) Identification of dynamic structural motifs involved in peptidoglycan glycosyltransfer. J Mol Biol 383:167–177

    Article  CAS  PubMed  Google Scholar 

  • Lv W, Xu Y, Guo Y, Yu Z, Feng G, Liu P, Luan M, Zhu H, Liu G, Zhang M (2016) The drug target genes show higher evolutionary conservation than non-target genes. Oncotarget 7:4961

    PubMed  Google Scholar 

  • Mahram A, Herbordt MC (2010) Fast and accurate NCBI BLASTP: acceleration with multiphase FPGA-based prefiltering Proceedings of the 24th ACM International Conference on Supercomputing. ACM, p 73–82

  • Målen H, Berven FS, Fladmark KE, Wiker HG (2007) Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv. Proteomics 7:1702–1718

    Article  PubMed  CAS  Google Scholar 

  • Malinverni JC, Silhavy TJ (2009) An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc Natl Acad Sci 106:8009–8014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maqbool A, Levdikov VM, Blagova EV, Hervé M, Horler RS, Wilkinson AJ, Thomas GH (2011) Compensating stereochemical changes allow murein tripeptide to be accommodated in a conventional peptide-binding protein. J Biol Chem 286:31512–31521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marland Z, Beddoe T, Zaker-Tabrizi L, Lucet IS, Brammananth R, Whisstock JC, Wilce MC, Coppel RL, Crellin PK, Rossjohn J (2006) Hijacking of a substrate-binding protein scaffold for use in mycobacterial cell wall biosynthesis. J Mol Biol 359:983–997

    Article  CAS  PubMed  Google Scholar 

  • Melak T, Gakkhar S (2014) Potential non homologous protein targets of Mycobacterium tuberculosis H37Rv identified from protein-protein interaction network. J Theor Biol 361:152–158

    Article  CAS  PubMed  Google Scholar 

  • Mettrick KA, Lamont IL (2009) Different roles for anti-sigma factors in siderophore signalling pathways of Pseudomonas aeruginosa. Mol Microbiol 74:1257–1271

    Article  CAS  PubMed  Google Scholar 

  • Miot M, Betton J-M (2004) Protein quality control in the bacterial periplasm. Microb Cell Fact 3:1

    Article  Google Scholar 

  • Mohn WW, Van Der Geize R, Stewart GR, Okamoto S, Liu J, Dijkhuizen L, Eltis LD (2008) The actinobacterial mce4 locus encodes a steroid transporter. J Biol Chem 283:35368–35374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulligan C, Fischer M, Thomas GH (2011) Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea. FEMS Microbiol Rev 35:68–86

    Article  CAS  PubMed  Google Scholar 

  • Ncbi RC (2013) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 41:D8

    Article  CAS  Google Scholar 

  • Neumann M, Mittelstädt G, Iobbi-Nivol C, Saggu M, Lendzian F, Hildebrandt P, Leimkühler S (2009) A periplasmic aldehyde oxidoreductase represents the first molybdopterin cytosine dinucleotide cofactor containing molybdo-flavoenzyme from Escherichia coli. FEBS J 276:2762–2774

    Article  CAS  PubMed  Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  CAS  PubMed  Google Scholar 

  • Panas MW, Jain P, Yang H, Mitra S, Biswas D, Wattam AR, Letvin NL, Jacobs WR (2014) Noncanonical SMC protein in Mycobacterium smegmatis restricts maintenance of Mycobacterium fortuitum plasmids. Proc Natl Acad Sci 111:13264–13271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park SJ, Son WS, Lee B-J (2012) Structural analysis of hypothetical proteins from Helicobacter pylori: an approach to estimate functions of unknown or hypothetical proteins. Int J Mol Sci 13:7109–7137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Payne TM, Yee EF, Dzikovski B, Crane BR (2016) Constraints on the radical cation center of cytochrome c peroxidase for electron transfer from cytochrome c. Biochemistry 55(34):4807–4822

    Article  CAS  PubMed  Google Scholar 

  • Peirs P, Lefevre P, Boarbi S, Wang X-M, Denis O, Braibant M, Pethe K, Locht C, Huygen K, Content J (2005) Mycobacterium tuberculosis with disruption in genes encoding the phosphate binding proteins PstS1 and PstS2 is deficient in phosphate uptake and demonstrates reduced in vivo virulence. Infect Immun 73:1898–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollard AM, Bilwes AM, Crane BR (2009) The structure of a soluble chemoreceptor suggests a mechanism for propagating conformational signals. Biochemistry 48:1936–1944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulsen C, Panjikar S, Holton SJ, Wilmanns M, Song Y-H (2014) WXG100 protein superfamily consists of three subfamilies and exhibits an α-helical C-terminal conserved residue pattern. PLoS One 9:e89313

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prakash P, Yellaboina S, Ranjan A, Hasnain SE (2005) Computational prediction and experimental verification of novel IdeR binding sites in the upstream sequences of Mycobacterium tuberculosis open reading frames. Bioinformatics (Oxford, England) 21:2161–2166

    Article  CAS  Google Scholar 

  • Rahman O, Cummings SP, Harrington DJ, Sutcliffe IC (2008) Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria. World J Microbiol Biotechnol 24:2377–2382

    Article  CAS  Google Scholar 

  • Rana A, Ahmed M, Rub A, Akhter Y (2015) A tug-of-war between the host and the pathogen generates strategic hotspots for the development of novel therapeutic interventions against infectious diseases. Virulence 6:566–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reimer JM, Aloise MN, Harrison PM, Schmeing TM (2016) Synthetic cycle of the initiation module of a formylating nonribosomal peptide synthetase. Nature 529:239–242

    Article  CAS  PubMed  Google Scholar 

  • Saikrishnan K, Jeyakanthan J, Venkatesh J, Acharya N, Sekar K, Varshney U, Vijayan M (2003) Structure of Mycobacterium tuberculosis single-stranded DNA-binding protein. Variability in quaternary structure and its implications. J Mol Biol 331:385–393

    Article  CAS  PubMed  Google Scholar 

  • Sainsbury S, Bird L, Rao V, Shepherd SM, Stuart DI, Hunter WN, Owens RJ, Ren J (2011) Crystal structures of penicillin-binding protein 3 from Pseudomonas aeruginosa: comparison of native and antibiotic-bound forms. J Mol Biol 405:173–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandhu P, Akhter Y (2015) The internal gene duplication and interrupted coding sequences in the MmpL genes of Mycobacterium tuberculosis: towards understanding the multidrug transport in an evolutionary perspective. Int J Med Microbiol IJMM 305:413–423

    Article  CAS  PubMed  Google Scholar 

  • Sandhu P, Akhter Y (2016) The drug binding sites and transport mechanism of the RND pumps from Mycobacterium tuberculosis: insights from molecular dynamics simulations. Arch Biochem Biophys 592:38–49

    Article  CAS  PubMed  Google Scholar 

  • Saurin W, Dassa E (1994) Sequence relationships between integral inner membrane proteins of binding protein-dependent transport systems: evolution by recurrent gene duplications. Protein Sci 3:325–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32:234–258

    Article  CAS  PubMed  Google Scholar 

  • Serafini A, Pisu D, Palu G, Rodriguez GM, Manganelli R (2013) The ESX-3 secretion system is necessary for iron and zinc homeostasis in Mycobacterium tuberculosis. PLoS One 8:e78351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serre L, Vallée B, Bureaud N, Schoentgen F, Zelwer C (1998) Crystal structure of the phosphatidylethanolamine-binding protein from bovine brain: a novel structural class of phospholipid-binding proteins. Structure 6:1255–1265

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Röhm K-H (2008) Characterization of a Pseudomonas putida ABC transporter (AatJMQP) required for acidic amino acid uptake: biochemical properties and regulation by the Aau two-component system. Microbiology 154:797–809

    Article  CAS  PubMed  Google Scholar 

  • Staudenmaier H, Van Hove B, Yaraghi Z, Braun V (1989) Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-protein-dependent transport mechanism for iron (III) dicitrate in Escherichia coli. J Bacteriol 171:2626–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tam R, Saier M (1993) Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57:320–346

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tasneem A, Iyer LM, Jakobsson E, Aravind L (2004) Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels. Genome Biol 6:1

    Article  Google Scholar 

  • Titgemeyer F, Amon J, Parche S, Mahfoud M, Bail J, Schlicht M, Rehm N, Hillmann D, Stephan J, Walter B, Burkovski A, Niederweis M (2007) A genomic view of sugar transport in Mycobacterium smegmatis and Mycobacterium tuberculosis. J Bacteriol 189:5903–5915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tjalsma H, Bolhuis A, Jongbloed JD, Bron S, van Dijl JM (2000) Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol Mol Biol Rev 64:515–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tullius MV, Harmston CA, Owens CP, Chim N, Morse RP, McMath LM, Iniguez A, Kimmey JM, Sawaya MR, Whitelegge JP (2011) Discovery and characterization of a unique mycobacterial heme acquisition system. Proc Natl Acad Sci 108:5051–5056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vetrivel U, Subramanian G, Dorairaj S (2011) A novel in silico approach to identify potential therapeutic targets in human bacterial pathogens. HUGO J 5:25

    Article  PubMed  PubMed Central  Google Scholar 

  • Vollmer W, Seligman SJ (2010) Architecture of peptidoglycan: more data and more models. Trends Microbiol 18:59–66

    Article  CAS  PubMed  Google Scholar 

  • Vyas NK, Vyas MN, Quiocho FA (2003) Crystal structure of M. tuberculosis ABC phosphate transport receptor: specificity and charge compensation dominated by ion–dipole interactions. Structure 11:765–774

    Article  CAS  PubMed  Google Scholar 

  • Wagner JM, Chan S, Evans TJ, Kahng S, Kim J, Arbing MA, Eisenberg D, Korotkov KV (2016) Structures of EccB 1 and EccD 1 from the core complex of the mycobacterial ESX-1 type VII secretion system. BMC Struct Biol 16:1

    Article  CAS  Google Scholar 

  • WHO (2015) Global tuberculosis report 2015. World Health Organization, Geneva

    Google Scholar 

  • Wiker HG, Wilson MA, Schoolnik GK (2000) Extracytoplasmic proteins of Mycobacterium tuberculosis–mature secreted proteins often start with aspartic acid and proline. Microbiology 146:1525–1533

    Article  CAS  PubMed  Google Scholar 

  • Wooff E, Michell SL, Gordon SV, Chambers MA, Bardarov S, Jacobs WR Jr, Hewinson RG, Wheeler PR (2002) Functional genomics reveals the sole sulphate transporter of the Mycobacterium tuberculosis complex and its relevance to the acquisition of sulphur in vivo. Mol Microbiol 43:653–663

    Article  CAS  PubMed  Google Scholar 

  • Yoshida H, Kawai F, Obayashi E, Akashi S, Roper DI, Tame JR, Park S-Y (2012) Crystal structures of penicillin-binding protein 3 (PBP3) from methicillin-resistant Staphylococcus aureus in the apo and cefotaxime-bound forms. J Mol Biol 423:351–364

    Article  CAS  PubMed  Google Scholar 

  • Yu CS, Lin CJ, Hwang JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13:1402–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Xie JP (2011) Mammalian cell entry gene family of Mycobacterium tuberculosis. Mol Cell Biochem 352:1–10. doi:10.1007/s11010-011-0733-5

    Article  CAS  PubMed  Google Scholar 

  • Zhang X-L, Li D-F, Fleming J, Wang L-W, Zhou Y, Wang D-C, Zhang X-E, Bi L-J (2015) Core component EccB1 of the Mycobacterium tuberculosis type VII secretion system is a periplasmic ATPase. FASEB J 29:4804–4814

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Indian Council of Medical Research, Govt. of India for providing financial support in the form of senior research fellowship to PS. Research in YA lab is supported by extramural research funds from Science and Engineering Research Board (DST, SERB) and University Grant Commission. We thank The Bioinformatics Resources & Applications Facility, at CDAC, Pune and Central University of Himachal Pradesh for providing computational infrastructure used during this study. We thank Dr. K.B.S. Krishna, Department of English & European Languages, Central University of Himachal Pradesh, who has kindly proof read the final version of the manuscript for any grammatical or language problems. We would also like to express our gratitude for the two anonymous reviewers and Prof. Martin Kupiec (Editor-in-Chief, Current Genetics) whose precious inputs on the initial versions of this manuscript have improved our work enormously.

Author information

Authors and Affiliations

  1. Centre for Computational Biology and Bioinformatics, School of Life Sciences, Central University of Himachal Pradesh, Shahpur, District Kangra, Himachal Pradesh, 176206, India

    Padmani Sandhu, Monika Kumari, Kamal Naini & Yusuf Akhter

Authors
  1. Padmani Sandhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika Kumari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kamal Naini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yusuf Akhter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yusuf Akhter.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by M. Kupiec.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 357 kb)

Supplementary material 2 (XLSX 4656 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sandhu, P., Kumari, M., Naini, K. et al. Genome scale identification, structural analysis, and classification of periplasmic binding proteins from Mycobacterium tuberculosis . Curr Genet 63, 553–576 (2017). https://doi.org/10.1007/s00294-016-0664-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-016-0664-5

Keywords

Search

Navigation