A phylum level analysis reveals lipoprotein biosynthesis to be a fundamental property of bacteria

References

[1] Asanuma, M., Kurokawa, K., Ichikawa, R., Ryu, K.-H., Chae, J.-H., Dohmae, N., Lee, B.L., and Nakayama, H. (2011). Structural evidence of α-aminoacylated lipoproteins of Staphylococcus aureus. FEBS J 278, 716-728 .10.1111/j.1742-4658.2010.07990.x
[2] Babu, M.M., Priya, M.L., Selvan, A.T., Madera, M., Gough, J., Aravind, L., and Sankaran, K. (2006). A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J Bacteriol 188, 2761-2773 .10.1128/JB.188.8.2761-2773.2006
[3] Bagos, P.G., Tsirigos, K.D., Liakopoulos, T.D., and Hamodrakas, S.J. (2008). Prediction of lipoprotein signal peptides in Gram-positive bacteria with a Hidden Markov Model. J Proteome Res 7, 5082-5093 .10.1021/pr800162c
[4] Bardy, S.L., Eichler, J., and Jarrell, K.F. (2003). Archaeal signal peptides—a comparative survey at the genome level. Protein Sci 12, 1833-1843 .10.1110/ps.03148703
[5] Bendtsen, J.D., Binnewies, T.T., Hallin, P.F., Sicheritz-Pontén, T., and Ussery, D.W. (2005). Genome update: prediction of secreted proteins in 225 bacterial proteomes. Microbiology 151, 1725-1727 .10.1099/mic.0.28029-0
[6] Braun, V., and Wu, H.C. (1994). Lipoproteins: structure function, biosynthesis and model for protein export. New Comp. Biochem . 27, 319-341 .10.1016/S0167-7306(08)60417-2
[7] Bubeck Wardenburg, J., Williams, W.A., and Missiakas, D. (2006). Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc Natl Acad Sci U S A 103, 13831-13836 .10.1073/pnas.0603072103
[8] Buddelmeijer, N., and Young, R. (2010). The essential Escherichia coli apolipoprotein N-acyltransferase (Lnt) exists as an extracytoplasmic thioester acyl-enzyme intermediate. Biochemistry 49, 341-346 .10.1021/bi9020346
[9] Celebi, N., Dalbey, R.E., and Yuan, J. (2008). Mechanism and hydrophobic forces driving membrane protein insertion of subunit II of cytochrome bo₃ oxidase. J Mol Biol 375, 1282-1292 .10.1016/j.jmb.2007.11.054
[10] Chandler, J.R., and Dunny, G.M. (2004). Enterococcal peptide sex pheromones: synthesis and control of biological activity. Peptides 25, 1377-1388 .10.1016/j.peptides.2003.10.020
[11] Daley, D.O., Rapp, M., Granseth, E., Melén, K., Drew, D., and von Heijne, G. (2005). Global topology analysis of the Escherichia coli inner membrane proteome. Science 308, 1321-1323 .10.1126/science.1109730
[12] Denham, E.L., Ward, P.N., and Leigh, J.A. (2008). Lipoprotein signal peptides are processed by Lsp and Eep of Streptococcus uberis. J Bacteriol 190, 4641-4647 .10.1128/JB.00287-08
[13] Fernández Robledo, J.A., Caler, E., Matsuzaki, M., Keeling, P.J., Shanmugam, D., Roos, D.S., and Vasta, G.R. (2011). The search for the missing link: a relic plastid in Perkinsus? Int J Parasitol 41, 1217-1229 .10.1016/j.ijpara.2011.07.008
[14] Fukuda, A., Matsuyama, S., Hara, T., Nakayama, J., Nagasawa, H., and Tokuda, H. (2002). Aminoacylation of the N-terminal cysteine is essential for Lol-dependent release of lipoproteins from membranes but does not depend on lipoprotein sorting signals. J Biol Chem 277, 43512-43518 .10.1074/jbc.M206816200
[15] Giménez, M.I., Dilks, K., and Pohlschr?der, M. (2007). Haloferax volcanii twin-arginine translocation substates include secreted soluble, C-terminally anchored and lipoproteins. Mol Microbiol 66, 1597-1606 .10.1111/j.1365-2958.2007.06034.x
[16] Gupta, S.D., and Wu, H.C. (1991). Identification and subcellular localization of apolipoprotein N-acyltransferase in Escherichia coli. FEMS Microbiol Lett 62, 37-41 .10.1111/j.1574-6968.1991.tb04413.x
[17] Henneke, P., Dramsi, S., Mancuso, G., Chraibi, K., Pellegrini, E., Theilacker, C., Hübner, J., Santos-Sierra, S., Teti, G., Golenbock, D.T., . (2008). Lipoproteins are critical TLR2 activating toxins in group B streptococcal sepsis. J Immunol 180, 6149-6158 .
[18] Hillmann, F., Argentini, M., and Buddelmeijer, N. (2011). Kinetics and phospholipid specificity of apolipoprotein N-acyltransferase. J Biol Chem 286, 27936-27946 .10.1074/jbc.M111.243519
[19] Hutchings, M.I., Hong, H.-J., Leibovitz, E., Sutcliffe, I.C., and Buttner, M.J. (2006). The CseBC-σ^E cell envelope stress signal transduction system of Streptomyces coelicolor is modulated by a novel lipoprotein. CseA. J. Bacteriol . 188, 7222-7229 .10.1128/JB.00818-06
[20] Hutchings, M.I., Palmer, T., Harrington, D.J., and Sutcliffe, I.C. (2009). Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold ‘em, knowing when to fold ’em. Trends Microbiol 17, 13-21 .10.1016/j.tim.2008.10.001
[21] Ito, H., Ura, A., Oyamada, Y., Yoshida, H., Yamagishi, J., Narita, S., Matsuyama, S., and Tokuda, H. (2007). A new screening method to identify inhibitors of the Lol (localization of lipoproteins) system, a novel antibacterial target. Microbiol Immunol 51, 263-270 .
[22] Johnston, K.L., Wu, B., Guimar?es, A., Ford, L., Slatko, B.E., and Taylor, M.J. (2010). Lipoprotein biosynthesis as a target for anti-Wolbachia treatment of filarial nematodes. Parasit Vectors 3, 99.10.1186/1756-3305-3-99
[23] Joseph, S.J., Fernández-Robledo, J.A., Gardner, M.J., El-Sayed, N.M., Kuo, C.-H., Schott, E.J., Wang, H., Kissinger, J.C., and Vasta, G.R. (2010). The Alveolate Perkinsus marinus: biological insights from EST gene discovery. BMC Genomics 11, 228.10.1186/1471-2164-11-228
[24] Juncker, A.S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H., and Krogh, A. (2003). Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12, 1652-1662 .10.1110/ps.0303703
[25] Kiho, T., Nakayama, M., Yasuda, K., Miyakoshi, S., Inukai, M., and Kogen, H. (2004). Structure-activity relationships of globomycin analogues as antibiotics. Bioorg Med Chem 12, 337-361 .10.1016/j.bmc.2003.10.055
[26] Kumru, O.S., Schulze, R.J., Rodnin, M.V., Ladokhin, A.S., and Zückert, W.R. (2011). Surface localization determinants of Borrelia OspC/Vsp family lipoproteins. J Bacteriol 193, 2814-2825 .10.1128/JB.00015-11
[27] Le Hénaff, M., Crémet, J.Y., and Fontenelle, C. (2002). Purification and characterization of the major lipoprotein (P28) of Spiroplasma apis. Protein Expr Purif 24, 489-496 .10.1006/prep.2001.1600
[28] Lewenza, S., Mhlanga, M.M., and Pugsley, A.P. (2008). Novel inner membrane retention signals in Pseudomonas aeruginosa lipoproteins. J Bacteriol 190, 6119-6125 .10.1128/JB.00603-08
[29] Lewenza, S., Vidal-Ingigliardi, D., and Pugsley, A.P. (2006). Direct visualization of red fluorescent lipoproteins indicates conservation of the membrane sorting rules in the family Enterobacteriaceae. J Bacteriol 188, 3516-3524 .10.1128/JB.188.10.3516-3524.2006
[30] Mattar, S., Scharf, B., Kent, S.B.H., Rodewald, K., Oesterhelt, D., and Engelhard, M. (1994). The primary structure of halocyanin, an archaeal blue copper protein, predicts a lipid anchor for membrane fixation. J Biol Chem 269, 14939-14945 .
[31] Narita, S.-I. (2011). ABC transporters involved in the biogenesis of the outer membrane in gram-negative bacteria. Biosci Biotechnol Biochem 75, 1044-1054 .10.1271/bbb.110115
[32] Narita, S.-I., and Tokuda, H. (2006). An ABC transporter mediating the membrane detachment of bacterial lipoproteins depending on their sorting signals. FEBS Lett 580, 1164-1170 .10.1016/j.febslet.2005.10.038
[33] Narita, S.-I., and Tokuda, H. (2007). Amino acids at positions 3 and 4 determine the membrane specificity of Pseudomonas aeruginosa lipoproteins. J Biol Chem 282, 13372-13378 .10.1074/jbc.M611839200
[34] Narita, S.-I., and Tokuda, H. (2011). Overexpression of LolCDE allows deletion of the Escherichia coli gene encoding apolipoprotein N-acyltransferase. J Bacteriol 193, 4832-4840 .10.1128/JB.05013-11
[35] Nowack, E.C.M., Melkonian, M., and Gl?ckner, G. (2008). Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18, 410-418 .10.1016/j.cub.2008.02.051
[36] Okuda, S., and Tokuda, H. (2009). Model of mouth-to-mouth transfer of bacterial lipoproteins through inner membrane LolC, periplasmic LolA, and outer membrane LolB. Proc Natl Acad Sci U S A 106, 5877-5882 .10.1073/pnas.0900896106
[37] Pailler, J., Aucher, W., Pires, M., and Buddelmeijer, N. (2012). Phosphatidylglycerol:prolipoprotein diacylglyceryl transferase (Lgt) of E. coli has seven transmembrane segments and its essential residues are embedded in the membrane. J Bacteriol . doi:10.1128/JB.06641-11.10.1128/JB.06641-11.10.1128/JB.06641-11
[38] Pathania, R., Zlitni, S., Barker, C., Das, R., Gerritsma, D.A., Lebert, J., Awuah, E., Melacini, G., Capretta, F.A., and Brown, E.D. (2009). Chemical genomics in Escherichia coli identifies an inhibitor of bacterial lipoprotein targeting. Nat Chem Biol 5, 849-856 .10.1038/nchembio.221
[39] Qi, H.-Y., Sankaran, K., Gan, K., and Wu, H.C. (1995). Structure-function relationship of bacterial prolipoprotein diacylglyceryl transferase: functionally significant conserved regions. J Bacteriol 177, 6820-6824 .
[40] Rahman, O., Cummings, S.P., Harrington, D.J., and Sutcliffe, I.C. (2008). Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria. World J Microbiol Biotechnol 24, 2377-2382 .10.1007/s11274-008-9795-2
[41] Reffuveille, F., Leneveu, C., Chevalier, S., Auffray, Y., and Rincé, A. (2011). Lipoproteins of Enterococcus faecalis: bioinformatic identification, expression analysis and relation to virulence. Microbiology 157, 3001-3013 .10.1099/mic.0.053314-0
[42] Réglier-Poupet, H., Frehel, C., Dubail, I., Beretti, J.-L., Berche, P., Charbit, A., and Raynaud, C. (2003). Maturation of lipoproteins by type II signal peptidase is required for phagosomal escape of Listeria monocytogenes. J Biol Chem 278, 49469-49477 .10.1074/jbc.M307953200
[43] Remans, K., Vercammen, K., Bodilis, J., and Cornelis, P. (2010). Genome-wide analysis and literature-based survey of lipoproteins in Pseudomonas aeruginosa. Microbiology 156, 2597-2607 .10.1099/mic.0.040659-0
[44] Rhodes, R.G., Samarasam, M.N., Van Groll, E.J., and McBride, M.J. (2011). Mutations in Flavobacterium johnsoniae sprE result in defects in gliding motility and protein secretion. J Bacteriol 193, 5322-5327 .10.1128/JB.05480-11
[45] Robichon, C., Vidal-Ingigliardi, D., and Pugsley, A.P. (2005). Depletion of apolipoprotein N-acyltransferase causes mislocalization of outer membrane lipoproteins in Escherichia coli. J Biol Chem 280, 974-983 .10.1074/jbc.M411059200
[46] Saleh, M., Song, C., Nasserulla, S., and Leduc, L.G. (2010). Indicators from archaeal secretomes. Microbiol Res 165, 1-10 .10.1016/j.micres.2008.03.002
[47] Sankaran, K., Gan, K., Rash, B., Qi, H.-Y., Wu, H.C., and Rick, P.D. (1997). Roles of histidine-103 and tyrosine-235 in the function of the prolipoprotein diacylglyceryl transferase of Escherichia coli. J Bacteriol 179, 2944-2948 .
[48] Sankaran, K., Gupta, S.D., and Wu, H.C. (1995). Modification of bacterial lipoproteins. Methods Enzymol 250, 683-697 .10.1016/0076-6879(95)50105-3
[49] Sankaran, K., and Wu, H.C. (1995). Bacterial prolipoprotein signal peptidase. Methods Enzymol 248, 169-180 .10.1016/0076-6879(95)48014-5
[50] Schenk, M., Belisle, J.T., and Modlin, R.L. (2009). TLR2 looks at lipoproteins. Immunity 31, 847-849 .10.1016/j.immuni.2009.11.008
[51] Schulze, R.J., Chen, S.Y., Kumru, O.S., and Zückert, W.R. (2010). Translocation of Borrelia burgdorferi surface lipoprotein OspA through the outer membrane requires an unfolded conformation and can initiate at the C-terminus. Mol Microbiol 76, 1266-1278 .10.1111/j.1365-2958.2010.07172.x
[52] Schulze, R.J., and Zückert, W.R. (2006). Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol Microbiol 59, 1473-1484 .10.1111/j.1365-2958.2006.05039.x
[53] Selvan, A.T., and Sankaran, K. (2008). Localization and characterization of prolipoprotein diacylglyceryl transferase (Lgt) critical in bacterial lipoprotein biosynthesis. Biochimie 90, 1647-1655 .10.1016/j.biochi.2008.06.005
[54] Serebryakova, M.V., Demina, I.A., Galyamina, M.A., Kondratov, I.G., Ladygina, V.G., and Govorun, V.M. (2011). The acylation state of surface lipoproteins of mollicute Acholeplasma laidlawii. J Biol Chem 286, 22769-22776 .10.1074/jbc.M111.231316
[55] Setubal, J.C., Reis, M., Matsunaga, J., and Haake, D.A. (2006). Lipoprotein computational prediction in spirochaetal genomes. Microbiology 152, 113-121 .10.1099/mic.0.28317-0
[56] Shruthi, H., Babu, M.M., and Sankaran, K. (2010). TAT-pathway-dependent lipoproteins as a niche-based adaptation in prokaryotes. J Mol Evol 70, 359-370 .10.1007/s00239-010-9334-2
[57] Storf, S., Pfeiffer, F., Dilks, K., Chen, Z.Q., Imam, S., and Pohlschr?der, M. (2010). Mutational and bioinformatic analysis of haloarchaeal lipobox-containing proteins. Archaea 2010 , 410975.10.1155/2010/410975
[58] Sutcliffe, I.C. (2010). A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18, 464-470 .10.1016/j.tim.2010.06.005
[59] Sutcliffe, I.C., and Harrington, D.J. (2002). Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes. Microbiology 148, 2065-2077 .
[60] Suzuki, T., Itoh, A., Ichihara, S., and Mizushima, S. (1987). Characterization of the sppA gene coding for protease IV, a signal peptide peptidase of Escherichia coli. J Bacteriol 169, 2523-2528 .
[61] Thompson, B.J., Widdick, D.A., Hicks, M.G., Chandra, G., Sutcliffe, I.C., Palmer, T., and Hutchings, M.I. (2010). Investigating lipoprotein biogenesis and function in the model Gram-positive bacterium Streptomyces coelicolor. Mol Microbiol 77, 943-957 .
[62] Tjalsma, H., Zanen, G., Venema, G., Bron, S., and van Dijl, J.M. (1999). The potential active site of the lipoprotein-specific (type II) signal peptidase of Bacillus subtilis. J Biol Chem 274, 28191-28197 .10.1074/jbc.274.40.28191
[63] Tokuda, H. (2009). Biogenesis of outer membranes in Gram-negative bacteria. Biosci Biotechnol Biochem 73, 465-473 .10.1271/bbb.80778
[64] Tschumi, A., Nai, C., Auchli, Y., Hunziker, P., Gehrig, P., Keller, P., Grau, T., and Sander, P. (2009). Identification of apolipoprotein N-acyltransferase (Lnt) in mycobacteria. J Biol Chem 284, 27146-27156 .10.1074/jbc.M109.022715
[65] Tsukahara, J., Mukaiyama, K., Okuda, S., Narita, S.-I., and Tokuda, H. (2009). Dissection of LolB function—lipoprotein binding, membrane targeting and incorporation of lipoproteins into lipid bilayers. FEBS J 276, 4496-4504 .10.1111/j.1742-4658.2009.07156.x
[66] van Bloois, E., Haan, G.-J., de Gier, J.-W., Oudega, B., and Luirink, J. (2006). Distinct requirements for translocation of the N-tail and C-tail of the Escherichia coli inner membrane protein CyoA. J Biol Chem 281, 10002-10009 .10.1074/jbc.M511357200
[67] Vidal-Ingigliardi, D., Lewenza, S., and Buddelmeijer, N. (2007). Identification of essential residues in apolipoprotein N-acyl transferase, a member of the CN hydrolase family. J Bacteriol 189, 4456-4464 .10.1128/JB.00099-07
[68] Widdick, D.A., Hicks, M.G., Thompson, B.J., Tschumi, A., Chandra, G., Sutcliffe, I.C., Brülle, J.K., Sander, P., Palmer, T., and Hutchings, M.I. (2011). Dissecting the complete lipoprotein biogenesis pathway in Streptomyces scabies. Mol Microbiol 80, 1395-1412 .10.1111/j.1365-2958.2011.07656.x
[69] Yu, Z., Lavèn, M., Klepsch, M., de Gier, J.-W., Bitter, W., van Ulsen, P., and Luirink, J. (2011). Role for Escherichia coli YidD in membrane protein insertion. J Bacteriol 193, 5242-5251 .10.1128/JB.05429-11