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Polysaccharide export outer membrane proteins in Gram-negative bacteria

    Biao Yuan

    Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, Chengdu City, Sichuan 611130, China. .

    ,
    Anchun Cheng

    * Author for correspondence

    Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, Chengdu City, Sichuan 611130, China

    Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, 46 Xinkang Road, Ya’an, Sichuan 625014, China.

    Key Laboratory of Animal Disease & Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, Chengdu city, Sichuan 611130, China.

    &
    Mingshu Wang

    Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, Chengdu City, Sichuan 611130, China

    Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, 46 Xinkang Road, Ya’an, Sichuan 625014, China.

    Key Laboratory of Animal Disease & Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, Chengdu city, Sichuan 611130, China.

    Published Online:https://doi.org/10.2217/fmb.13.13

    Polysaccharide export outer membrane proteins of Gram-negative bacteria are involved in the export of polysaccharides across the outer membrane. The mechanisms of polysaccharide export across the outer membrane in Gram-negative bacteria are not yet completely clear. However, the mechanisms of polysaccharide assembly in Escherichia coli have been intensively investigated. Here, we mainly review the current understanding of the assembly mechanisms of group 1 capsular polysaccharide, group 2 capsular polysaccharide and lipopolysaccharide of E. coli, and the current structures and interactions of some polysaccharide export outer membrane proteins with other proteins involved in polysaccharide export in Gram-negative bacteria. In addition, LptD may be targeted by peptidomimetic antibiotics in Gram-negative bacteria. We also give insights into the directions of future research regarding the mechanisms of polysaccharide export.

    Papers of special note have been highlighted as: ▪ of interest ▪▪ of considerable interest

    References

    • Cuthbertson L, Mainprize IL, Naismith JH, Whitfield C. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in Gram-negative bacteria. Microbiol. Mol. Biol. Rev.73(1),155–177 (2009).
    • Whitfield C, Roberts IS. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol.31(5),1307–1319 (1999).
    • Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem.75,39–68 (2006).▪ The biosynthesis and translocation pathways of group 1 and group 2 capsular polysaccharides.
    • Russo TA, Luke NR, Beanan JM et al. The K1 capsular polysaccharide of Acinetobacter baumannii strain 307-0294 is a major virulence factor. Infect. Immun.78(9),3993–4000 (2010).
    • Goller CC, Seed PC. Revisiting the Escherichia coli polysaccharide capsule as a virulence factor during urinary tract infection: contribution to intracellular biofilm development. Virulence1(4),333–337 (2010).
    • Stein DM, Robbins J, Miller MA, Lin FY, Schneerson R. Are antibodies to the capsular polysaccharide of Neisseria meningitides group B and Escherichia coli K1 associated with immunopathology? Vaccine24(3),221–228 (2006).
    • Monteiro MA, Baqar S, Hall ER et al. Capsule polysaccharide conjugate vaccine against diarrheal disease caused by Campylobacter jejuni. Infect. Immun.77(3),1128–1136 (2009).
    • Khan MI, Ochiai RL, Clemens JD. Population impact of Vi capsular polysaccharide vaccine. Expert Rev. Vaccines9(5),485–496 (2010).
    • Robbins JB, Schneerson R, Xie G, Hanson LÅ, Miller MA. Capsular polysaccharide vaccine for group B Neisseria meningitidis, Escherichia coli K1, and Pasteurella haemolytica A2. Proc. Natl Acad. Sci. USA108(44),17871–17875 (2011).
    • 10  Lindahl U, Li JP, Kusche-Gullberg M et al. Generation of “neoheparin” from E. coli K5 capsular polysaccharide. J. Med. Chem.8(2),349–352 (2005).
    • 11  Ly M, Wang Z, Laremore TN et al. Analysis of E. coli K5 capsular polysaccharide heparosan. Anal. Bioanal. Chem.399(2),737–745 (2011).
    • 12  Raetz CRH, Whitfield C. Lipopolysaccharide endotoxins. Annu. Rev. Biochem.71,635–700 (2002).
    • 13  Kabanov DS, Prokhorenko IR. Structural analysis of lipopolysaccharides from Gram-negative bacteria. Biochemistry (Mosc.)75(4),383–404 (2010).
    • 14  Focà A, Liberto MC, Quirino A, Matera G. Lipopolysaccharides: from erinyes to charites. Mediators Inflamm.2012,684274 (2012).
    • 15  Arenas J. The role of bacterial lipopolysaccharides as immune modulator in vaccine and drug development. Endocr. Metab. Immune Disord. Drug Targets12(3),221–235 (2012).
    • 16  Vuong C, Kocianova S, Voyich JM et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem.279(52),54881–54886 (2004).
    • 17  Yamanaka T, Yamane K, Furukawa T et al. Comparison of the virulence of exopolysaccharide producing Prevotella intermedia to exopolysaccharide non-producing periodontopathic organisms. BMC Infect. Dis.11,228 (2011).
    • 18  Ryder C, Byrd M, Wozniak DJ. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr. Opin. Microbiol.10(6),644–668 (2007).
    • 19  Vu B, Chen M, Crawford RJ, Ivanova EP. Bacterial extracellular polysaccharides involved in biofilm formation. Molecules14(7),2535–2554 (2009).
    • 20  Patel R. Biofilms and antimicrobial resistance. Clin. Orthop. Relat. Res.437,41–47 (2005).
    • 21  Mah TF, O’Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol.9(1),34–39 (2001).
    • 22  Freitas F, Alves VD, Reis MA. Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol.29(8),388–398 (2011).▪ Some bacterial exopolysaccharides are used in commercial applications.
    • 23  Cuthbertson L, Kos V, Whitfield C. ABC transporters involved in export of cell surface glycoconjugates. Microbiol. Mol. Biol. Rev.74(3),341–629 (2010).
    • 24  Islam ST, Lam JS. Wzx flippase-mediated membrane translocation of sugar polymer precursors in bacteria. Environ. Microbiol. doi:10.1111/j.1462–2920.02890.x (2012) (Epub ahead of print).
    • 25  Hagelueken G, Huang H, Mainprize IL, Whitfield C, Naismith JH. Crystal structures of Wzb of Escherichia coli and CpsB of Streptococcus pneumoniae, representatives of two families of tyrosine phosphatases that regulate capsule assembly. J. Mol. Biol.392(3),678–688 (2009).
    • 26  Wugeditsch T, Paiment A, Hocking J, Drummelsmith J, Forrester C, Whitfield C. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J. Biol. Chem.276(4),2361–2371 (2001).
    • 27  Collins RF, Beis K, Dong C et al. The 3D structure of a periplasm-spanning platform required for assembly of group 1 capsular polysaccharides in Escherichia coli. Proc. Natl Acad. Sci. USA104(7),2390–2395 (2007).
    • 28  Reid AN, Whitfield C. Functional analysis of conserved gene products involved in assembly of Escherichia coli capsules and exopolysaccharides: evidence for molecular recognition between Wza and Wzc for colanic acid biosynthesis. J. Bacteriol.187(15),5470–5481 (2005).
    • 29  Bushell SR, Lou H, Wallat GD, Beis K, Whitfield C, Naismith JH. Crystallization and preliminary diffraction analysis of Wzi, a member of the capsule export andassembly pathway in Escherichia coli. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun.66(12),1621–1625 (2010).
    • 30  Rahn A, Beis K, Naismith JH, Whitfield C. A novel outer membrane protein, Wzi, is involved in surface assembly of the Escherichia coli K30 group 1 capsule. J. Bacteriol.185(19),5882–5890 (2003).
    • 31  Kerr ID. Structure and association of ATP-binding cassette transporter nucleotide-binding domains. Biochim. Biophys. Acta1561(1),47–64 (2002).
    • 32  Nsahlai CJ, Silver RP. Purification and characterization of KpsT, the ATP-binding component of the ABC-capsule exporter of Escherichia coli K1. FEMS Microbiol. Lett.224(1),113–118 (2003).
    • 33  Andreishcheva EN, Vann WF. Gene products required for de novo synthesis of polysialic acid in Escherichia coli K1. J. Bacteriol.188(5),1786–1797 (2006).
    • 34  Vimr ER, Steenbergen SM. Early molecular-recognition events in the synthesis and export of group 2 capsular polysaccharides. Microbiology155(Pt 1),9–15 (2009).
    • 35  Steenbergen SM, Vimr ER. Biosynthesis of the Escherichia coli K1 group 2 polysialic acid capsule occurs within a protected cytoplasmic compartment. Mol. Microbiol.68(5),1252–1267 (2008).
    • 36  Greenfield LK, Whitfield C. Synthesis of lipopolysaccharide O-antigens by ABC transporter-dependent pathways. Carbohydr. Res.356,12–24 (2012).
    • 37  Narita S. ABC transporters involved in the biogenesis of the outer membrane in Gram-negative bacteria. Biosci. Biotechnol. Biochem.75(6),1044–1054 (2011).
    • 38  Marolda CL, Haggerty ER, Lung M, Valvano MA. Functional analysis of predicted coiled-coil regions in the Escherichia coli K-12 O-antigen polysaccharide chain length determinant Wzz. J. Bacteriol.190(6),2128–2137 (2008).
    • 39  Woodward R, Yi W, Li L et al.In vitro bacterial polysaccharide biosynthesis: defining the functions of Wzy and Wzz. Nat. Chem. Biol.6(6),418–423 (2010).
    • 40  Morona R, Purins L, Tocilj A, Matte A, Cygler M. Sequence–structure relationships in polysaccharide co-polymerase (PCP) proteins. Trends Biochem. Sci.34(2),78–84 (2009).
    • 41  Pérez JM, McGarry MA, Marolda CL, Valvano MA. Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase. Mol. Microbiol.70(6),1424–1440 (2008).
    • 42  Sperandeo P, Lau FK, Carpentieri A et al. Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J. Bacteriol.190(13),4460–4469 (2008).
    • 43  Sperandeo P, Villa R, Martorana AM et al. New insights into the Lpt machinery for lipopolysaccharide transport to the cell surface: LptA–LptC interaction and LptA stability as sensors of a properly assembled transenvelope complex. J. Bacteriol.193(5),1042–1053 (2011).
    • 44  Narita S, Tokuda H. Biochemical characterization of an ABC transporter LptBFGC complex required for the outer membrane sorting of lipopolysaccharides. FEBS Lett.583(13),2160–2164 (2009).
    • 45  Freinkman E, Okuda S, Ruiz N, Kahne D. Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry51(24),4800–4806 (2012).
    • 46  Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, Kahne D. Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc. Natl Acad. Sci. USA103(31),11754–11759 (2006).
    • 47  Chng SS, Ruiz N, Chimalakonda G, Silhavy TJ, Kahne D. Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc. Natl Acad. Sci. USA107(12),5363–5368 (2010).
    • 48  Freinkman E, Chng SS, Kahne D. The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc. Natl Acad. Sci. USA108(6),2486–2491 (2011).
    • 49  Bowyer A, Baardsnes J, Ajamian E, Zhang L, Cygler M. Characterization of interactions between LPS transport proteins of the Lpt system. Biochem. Biophys. Res. Commun.404(4),1093–1098 (2011).▪ Reviews the interactions of lipopolysaccharide transport proteins of the Lpt transport system.
    • 50  Chimalakonda G, Ruiz N, Chng SS, Garner RA, Kahne D, Silhavy TJ. Lipoprotein LptE is required for the assembly of LptD by the beta-barrel assembly machine in the outer membrane of Escherichia coli. Proc. Natl Acad. Sci. USA108(6),2492–2497 (2011).
    • 51  Saier MH. A functional–phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev.64(2),354–411 (2000).
    • 52  Xiao AY, Wang J, Saier MH. Bacterial adaptor membrane fusion proteins and the structurally dissimilar outer membrane auxiliary proteins have exchanged central domains in alpha-Proteobacteria. Int. J. Microbiol.2010,589391 (2010).
    • 53  Jiang JH, Tong J, Tan KS, Gabriel K. From evolution to pathogenesis: the link between β-barrel assembly machineries in the outer membrane of mitochondria and Gram-negative bacteria. Int. J. Mol. Sci.13(7),8038–8050 (2012).
    • 54  Nesper J, Hill CM, Paiment A et al. Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30. Structural and functional analysis of the outer membrane lipoprotein Wza. J. Biol. Chem.278(50),49763–49772 (2003).
    • 55  Karuppiah V, Berry JL, Derrick JP. Outer membrane translocons: structural insights into channel formation. Trends Microbiol.19(1),40–48 (2011).
    • 56  Tamm LK, Hong H, Liang B. Folding and assembly of beta-barrel membrane proteins. Biochim. Biophys. Acta1666(1–2),250–263 (2004).
    • 57  Fairman JW, Noinaj N, Buchanan SK. The structural biology of β-barrel membrane proteins: a summary of recent reports. Curr. Opin. Struct. Biol.21(4),523–531 (2011).
    • 58  Collins RF, Derrick JP. Wza: a new structural paradigm for outer membrane secretory proteins? Trends Microbiol.15(3),96–100 (2007).
    • 59  Dong C, Beis K, Nesper J et al. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature444(7116),226–229 (2006).▪▪ First paper to show the 3D structure of an α-helical barrel outer membrane protein Wza.
    • 60  Wunder DE, Aaronson W, Hayes SF, Bliss JM, Silver RP. Nucleotide sequence and mutational analysis of the gene encoding KpsD, a periplasmic protein involved in transport of polysialic acid in Escherichia coli K1. J. Bacteriol.176(13),4025–4033 (1994).
    • 61  Arrecubieta C, Hammarton TC, Barrett B et al. The transport of group 2 capsular polysaccharides across the periplasmic space in Escherichia coli. Roles for the KpsE and KpsD proteins. J. Biol. Chem.276(6),4245–4250 (2001).
    • 62  McNulty C, Thompson J, Barrett B, Lord L, Andersen C, Roberts IS. The cell surface expression of group 2 capsular polysaccharides in Escherichia coli: the role of KpsD, RhsA and a multi-protein complex at the pole of the cell. Mol. Microbiol.59(3),907–922 (2006).
    • 63  Frosch M, Müller D, Bousset K, Müller A. Conserved outer membrane protein of Neisseria meningitidis involved in capsule expression. Infect. Immun.60(3),798–803 (1992).
    • 64  Larue K, Ford RC, Willis LM, Whitfield C. Functional and structural characterization of polysaccharide co-polymerase proteins required for polymer export in ATP-binding cassette transporter-dependent capsule biosynthesis pathways. J. Biol. Chem.286(19),16658–16668 (2011).
    • 65  Hashimoto Y, Li N, Yokoyama H, Ezaki T. Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi. J. Bacteriol.175(14),4456–4465 (1993).
    • 66  Virlogeux I, Waxin H, Ecobichon C, Popoff MY. Role of the viaB locus in synthesis, transport and expression of Salmonella typhi Vi antigen. Microbiology141,3039–3047 (1995).
    • 67  Santander J, Roland KL, Curtiss R 3rd. Regulation of Vi capsular polysaccharide synthesis in Salmonella enterica serotype Typhi. J. Infect. Dev. Ctries2(6),412–420 (2008).
    • 68  Wetter M, Goulding D, Pickard D et al. Molecular characterization of the viaB locus encoding the biosynthetic machinery for Vi capsule formation in Salmonella typhi. PLoS One7(9),e45609 (2012).
    • 69  Russo TA, Wenderoth S, Carlino UB, Merrick JM, Lesse AJ. Identification, genomic organization, and analysis of the group III capsular polysaccharide genes kpsD, kpsM, kpsT, and kpsE from an extraintestinal isolate of Escherichia coli (CP9, O4/K54/H5). J. Bacteriol.180(2),338–349 (1998).
    • 70  Clarke BR, Pearce R, Roberts IS. Genetic organization of the Escherichia coli K10 capsule gene cluster: identification and characterization of two conserved regions in group III capsule gene clusters encoding polysaccharide transport functions. J. Bacteriol.181(7),2279–2285 (1999).
    • 71  Peleg A, Shifrin Y, Ilan O et al. Identification of an Escherichia coli operon required for formation of the O-antigen capsule. J. Bacteriol.187(15),5259–5266 (2005).
    • 72  Chng SS, Xue M, Garner RA et al. Disulfide rearrangement triggered by translocon assembly controls lipopolysaccharide export. Science337(6102),1665–1668 (2012).▪ First paper to report the model of maturation processes of the LptD protein triggered by LptE.
    • 73  Bos MP, Tefsen B, Geurtsen J, Tommassen J. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc. Natl Acad. Sci. USA101(25),9417–9422 (2004).
    • 74  Bos MP, Tommassen J. The LptD chaperone LptE is not directly involved in lipopolysaccharide transport in Neisseria meningitidis. J. Biol. Chem.286(33),28688–28696 (2011).▪ The Lpt transport system of Escherichia coli is not suitable for all Gram-negative bacteria.
    • 75  Werneburg M, Zerbe K, Juhas M et al. Inhibition of lipopolysaccharide transport to the outer membrane in Pseudomonas aeruginosa by peptidomimetic antibiotics. Chembiochem13(12),1767–1775 (2012).
    • 76  Srinivas N, Jetter P, Ueberbacher BJ et al. Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science327(5968),1010–1013 (2010).
    • 77  Takase I, Ishino F, Wachi M et al. Genes encoding two lipoproteins in the leuS–dacA region of the Escherichia coli chromosome. J. Bacteriol.169(12),5692–5699 (1987).
    • 78  Wang X, Preston JF, Romeo T. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol.186(9),2724–2734 (2004).
    • 79  Izano EA, Sadovskaya I, Wang H et al. Poly-N-acetylglucosamine mediates biofilm formation and detergent resistance in Aggregatibacter actinomycetemcomitans. Microb. Pathog.44(1),52–60 (2008).
    • 80  Itoh Y, Rice JD, Goller C et al. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-D-glucosamine. J. Bacteriol.190(10),3670–3680 (2008).
    • 81  Little DJ, Poloczek J, Whitney JC, Robinson H, Nitz M, Howell PL. The structure and metal dependent activity of Escherichia coli PgaB provides insight into the partial de-N-acetylation of poly-β-1,6-N-acetyl-D-glucosamine. J. Biol. Chem.287(37),31126–31137 (2012).
    • 82  Vasseur P, Vallet-Gely I, Soscia C, Genin S, Filloux A. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology151(3),985–997 (2005).
    • 83  Vasseur P, Soscia C, Voulhoux R, Filloux A. PelC is a Pseudomonas aeruginosa outer membrane lipoprotein of the OMA family of proteins involved in exopolysaccharide transport. Biochimie89(8),903–915 (2007).
    • 84  Kowalska K, Soscia C, Combe H, Vasseur P, Voulhoux R, Filloux A. The C-terminal amphipathic alpha-helix of Pseudomonas aeruginosa PelC outer membrane protein is required for its function. Biochimie92(1),33–40 (2010).
    • 85  Campisano A, Schroeder C, Schemionek M, Overhage J, Rehm BH. PslD is a secreted protein required for biofilm formation by Pseudomonas aeruginosa. Appl. Environ. Microbiol.72(4),3066–3068 (2006).
    • 86  Whitney JC, Neculai AM, Ohman DE, Howell PL. Expression, refolding, crystallization and preliminary x-ray analysis of Pseudomonas aeruginosa AlgE. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun.65(Pt 5),463–466 (2009).
    • 87  Whitney JC, Hay ID, Li C et al. Structural basis for alginate secretion across the bacterial outer membrane. Proc. Natl Acad. Sci. USA108(32),13083–13088 (2011).
    • 88  Keiski CL, Harwich M, Jain S et al. AlgK is a TPR-containing protein and the periplasmic component of a novel exopolysaccharide secretin. Structure18(2),265–273 (2010).
    • 89  Franklin MJ, Nivens DE, Weadge JT, Howell PL. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front. Microbiol.2,167 (2011).▪ The assembly models of Pel, Psl and alginate are proposed for Pseudomonas aeruginosa.
    • 90  Mazur A, Król JE, Skorupska A. Isolation and sequencing of Rhizobium leguminosarum bv. trifolii PssN, PssO and PssP genes encoding the proteins involved in polymerization and translocation of exopolysaccharide. DNA Seq.12(1),1–12 (2001).
    • 91  Marczak M, Mazur A, Król JE, Gruszecki WI, Skorupska A. Lipoprotein PssN of Rhizobium leguminosarum bv. trifolii: subcellular localization and possible involvement in exopolysaccharide export. J. Bacteriol.188(19),6943–6952 (2006).
    • 92  Staehelin C, Forsberg LS, D’Haeze W et al. Exo-oligosaccharides of Rhizobium sp. strain NGR234 are required for symbiosis with various legumes. J. Bacteriol.188(17),6168–6178 (2006).
    • 93  Perry RD, Bobrov AG, Kirillina O et al. Temperature regulation of the hemin storage (Hms+) phenotype of Yersinia pestis is posttranscriptional. J. Bacteriol.186(6),1638–1647 (2004).
    • 94  Forman S, Bobrov AG, Kirillina O et al. Identification of critical amino acid residues in the plague biofilm Hms proteins. Microbiology152(Pt 11),3399–3410 (2006).
    • 95  Khweek AA, Fetherston JD, Perry RD. Analysis of HmsH and its role in plague biofilm formation. Microbiology156(5),1424–1438 (2010).
    • 96  Arco Y, Llamas I, Martínez-Checa F, Argandoña M, Quesada E, Moral A. epsABCJ genes are involved in the biosynthesis of the exopolysaccharide mauran produced by Halomonas maura. Microbiology151,2841–2851 (2005).