LplA1-dependent utilization of host lipoyl peptides enables Listeria cytosolic growth and virulence
dc.contributor.author | Keeney, Kristie Miller | en_US |
dc.contributor.author | Stuckey, Jeanne A. | en_US |
dc.contributor.author | O'Riordan, Mary X. D. | en_US |
dc.date.accessioned | 2010-06-01T19:23:12Z | |
dc.date.available | 2010-06-01T19:23:12Z | |
dc.date.issued | 2007-11 | en_US |
dc.identifier.citation | Keeney, Kristie M.; Stuckey, Jeanne A.; O'Riordan, Mary X. D. (2007). "LplA1-dependent utilization of host lipoyl peptides enables Listeria cytosolic growth and virulence." Molecular Microbiology 66(3): 758-770. <http://hdl.handle.net/2027.42/72528> | en_US |
dc.identifier.issn | 0950-382X | en_US |
dc.identifier.issn | 1365-2958 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/72528 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=17908209&dopt=citation | en_US |
dc.description.abstract | The bacterial pathogen Listeria monocytogenes replicates within the cytosol of mammalian cells. Mechanisms by which the bacterium exploits the host cytosolic environment for essential nutrients are poorly defined. L. monocytogenes is a lipoate auxotroph and must scavenge this critical cofactor, using lipoate ligases to facilitate attachment of the lipoyl moiety to metabolic enzyme complexes. Although the L. monocytogenes genome encodes two putative lipoate ligases, LplA1 and LplA2, intracellular replication and virulence require only LplA1. Here we show that LplA1 enables utilization of host-derived lipoyl peptides by L. monocytogenes . LplA1 is dispensable for growth in the presence of free lipoate, but necessary for growth on low concentrations of mammalian lipoyl peptides. Furthermore, we demonstrate that the intracellular growth defect of the δ lplA1 mutant is rescued by addition of exogenous lipoic acid to host cells, suggesting that L. monocytogenes dependence on LplA1 is dictated by limiting concentrations of available host lipoyl substrates. Thus, the ability of L. monocytogenes and other intracellular pathogens to efficiently use host lipoyl peptides as a source of lipoate may be a requisite adaptation for life within the mammalian cell. | en_US |
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dc.format.extent | 629275 bytes | |
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dc.format.mimetype | application/pdf | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Publishing Ltd | en_US |
dc.rights | © 2007 The Authors; Journal compilation © 2007 Blackwell Publishing Ltd | en_US |
dc.title | LplA1-dependent utilization of host lipoyl peptides enables Listeria cytosolic growth and virulence | en_US |
dc.type | Article | en_US |
dc.subject.hlbsecondlevel | Microbiology and Immunology | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Life Sciences Institute, University of Michigan Medical School, 1150 W. Medical Center Drive, 5641 Medical Sciences II, Ann Arbor, MI 48109-0620, USA. | en_US |
dc.contributor.affiliationother | Departments of Microbiology and Immunology and | en_US |
dc.contributor.affiliationother | Biological Chemistry, and | en_US |
dc.identifier.pmid | 17908209 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/72528/1/MMI+5956+Supp.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/72528/2/j.1365-2958.2007.05956.x.pdf | |
dc.identifier.doi | 10.1111/j.1365-2958.2007.05956.x | en_US |
dc.identifier.source | Molecular Microbiology | en_US |
dc.identifier.citedreference | Akiba, S., Matsugo, S., Packer, L., and Konishi, T. ( 1998 ) Assay of protein-bound lipoic acid in tissues by a new enzymatic method. Anal Biochem 258: 299 – 304. | en_US |
dc.identifier.citedreference | Allary, M., Lu, J.Z., Zhu, L., and Prigge, S.T. ( 2007 ) Scavenging of the cofactor lipoate is essential for the survival of the malaria parasite Plasmodium falciparum. Mol Microbiol 63: 1331 – 1344. | en_US |
dc.identifier.citedreference | Auerbuch, V., Lenz, L.L., and Portnoy, D.A. ( 2001 ) Development of a competitive index assay to evaluate the virulence of Listeria monocytogenes actA mutants during primary and secondary infection of mice. Infect Immun 69: 5953 – 5957. | en_US |
dc.identifier.citedreference | Baker, H., Deangelis, B., Baker, E.R., and Hutner, S.H. ( 1998 ) A practical assay of lipoate in biologic fluids and liver in health and disease. Free Radic Biol Med 25: 473 – 479. | en_US |
dc.identifier.citedreference | Baker, N.A., Sept, D., Joseph, S., Holst, M.J., and McCammon, J.A. ( 2001 ) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98: 10037 – 10041. | en_US |
dc.identifier.citedreference | Bast, A., and Haenen, G.R. ( 2003 ) Lipoic acid: a multifunctional antioxidant. Biofactors 17: 207 – 213. | en_US |
dc.identifier.citedreference | Bouwer, H.G., Nelson, C.S., Gibbins, B.L., Portnoy, D.A., and Hinrichs, D.J. ( 1992 ) Listeriolysin O is a target of the immune response to Listeria monocytogenes. J Exp Med 175: 1467 – 1471. | en_US |
dc.identifier.citedreference | Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., et al. ( 1998 ) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905 – 921. | en_US |
dc.identifier.citedreference | Bryk, R., Lima, C.D., Erdjument-Bromage, H., Tempst, P., and Nathan, C. ( 2002 ) Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295: 1073 – 1077. | en_US |
dc.identifier.citedreference | Chico-Calero, I., Suarez, M., Gonzalez-Zorn, B., Scortti, M., Slaghuis, J., Goebel, W., et al. ( 2002 ) Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc Natl Acad Sci USA 99: 431 – 436. | en_US |
dc.identifier.citedreference | Crawford, M.J., Thomsen-Zieger, N., Ray, M., Schachtner, J., Roos, D.S., and Seeber, F. ( 2006 ) Toxoplasma gondii scavenges host-derived lipoic acid despite its de novo synthesis in the apicoplast. EMBO J 25: 3214 – 3222. | en_US |
dc.identifier.citedreference | DeLano, W.L. ( 2002 ) The PyMOL Molecular Graphics System on World Wide Web. [WWW] URL http://pymol.sourceforge.net | en_US |
dc.identifier.citedreference | Freitag, N.E., Rong, L., and Portnoy, D.A. ( 1993 ) Regulation of the prfA transcriptional activator of Listeria monocytogenes: multiple promoter elements contribute to intracellular growth and cell-to-cell spread. Infect Immun 61: 2537 – 2544. | en_US |
dc.identifier.citedreference | Fujiwara, K., Toma, S., Okamura-Ikeda, K., Motokawa, Y., Nakagawa, A., and Taniguchi, H. ( 2005 ) Crystal structure of lipoate-protein ligase A from Escherichia coli. Determination of the lipoic acid-binding site. J Biol Chem 280: 33645 – 33651. | en_US |
dc.identifier.citedreference | Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., et al. ( 2001 ) Comparative genomics of Listeria species. Science 294: 849 – 852. | en_US |
dc.identifier.citedreference | Goetz, M., Bubert, A., Wang, G., Chico-Calero, I., Vazquez-Boland, J.A., Beck, M., et al. ( 2001 ) Microinjection and growth of bacteria in the cytosol of mammalian host cells. Proc Natl Acad Sci USA 98: 12221 – 12226. | en_US |
dc.identifier.citedreference | Hodgson, D.A. ( 2000 ) Generalized transduction of serotype 1/2 and serotype 4b strains of Listeria monocytogenes. Mol Microbiol 35: 312 – 323. | en_US |
dc.identifier.citedreference | Horton, R.M., Cai, Z.L., Ho, S.N., and Pease, L.R. ( 1990 ) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528 – 535. | en_US |
dc.identifier.citedreference | Jiang, Y., and Cronan, J.E. ( 2005 ) Expression cloning and demonstration of Enterococcus faecalis lipoamidase (pyruvate dehydrogenase inactivase) as a Ser-Ser-Lys triad amidohydrolase. J Biol Chem 280: 2244 – 2256. | en_US |
dc.identifier.citedreference | Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. ( 1991 ) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47: 110 – 119. | en_US |
dc.identifier.citedreference | Jordan, S.W., and Cronan, J.E., Jr ( 1997 ) A new metabolic link. The acyl carrier protein of lipid synthesis donates lipoic acid to the pyruvate dehydrogenase complex in Escherichia coli and mitochondria. J Biol Chem 272: 17903 – 17906. | en_US |
dc.identifier.citedreference | Kim, D.J., Kim, K.H., Lee, H.H., Lee, S.J., Ha, J.Y., Yoon, H.J., and Suh, S.W. ( 2005 ) Crystal structure of lipoate-protein ligase A bound with the activated intermediate: insights into interaction with lipoyl domains. J Biol Chem 280: 38081 – 38089. | en_US |
dc.identifier.citedreference | Konishi, T., Handelman, G., Matsugo, S., Mathur, V.V., Tritschler, H.J., and Packer, L. ( 1996 ) Amplified determination of lipoyl groups by lipoamide dehydrogenase in the presence of oxidized glutathione. Biochem Mol Biol Int 38: 1155 – 1161. | en_US |
dc.identifier.citedreference | Ma, Q., Zhao, X., Nasser Eddine, A., Geerlof, A., Li, X., Cronan, J.E., et al. ( 2006 ) The Mycobacterium tuberculosis LipB enzyme functions as a cysteine/lysine dyad acyltransferase. Proc Natl Acad Sci USA 103: 8662 – 8667. | en_US |
dc.identifier.citedreference | Margineantu, D.H., Brown, R.M., Brown, G.K., Marcus, A.H., and Capaldi, R.A. ( 2002 ) Heterogeneous distribution of pyruvate dehydrogenase in the matrix of mitochondria. Mitochondrion 1: 327 – 338. | en_US |
dc.identifier.citedreference | Marquis, H., Bouwer, H.G., Hinrichs, D.J., and Portnoy, D.A. ( 1993 ) Intracytoplasmic growth and virulence of Listeria monocytogenes auxotrophic mutants. Infect Immun 61: 3756 – 3760. | en_US |
dc.identifier.citedreference | Morris, T.W., Reed, K.E., and Cronan, J.E., Jr ( 1994 ) Identification of the gene encoding lipoate-protein ligase A of Escherichia coli. Molecular cloning and characterization of the lplA gene and gene product. J Biol Chem 269: 16091 – 16100. | en_US |
dc.identifier.citedreference | Morris, T.W., Reed, K.E., and Cronan, J.E., Jr ( 1995 ) Lipoic acid metabolism in Escherichia coli: the lplA and lipB genes define redundant pathways for ligation of lipoyl groups to apoprotein. J Bacteriol 177: 1 – 10. | en_US |
dc.identifier.citedreference | O'Riordan, M., Moors, M.A., and Portnoy, D.A. ( 2003 ) Listeria intracellular growth and virulence require host-derived lipoic acid. Science 302: 462 – 464. | en_US |
dc.identifier.citedreference | Perham, R.N. ( 2000 ) Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annu Rev Biochem 69: 961 – 1004. | en_US |
dc.identifier.citedreference | Phan-Thanh, L., and Gormon, T. ( 1997 ) A chemically defined minimal medium for the optimal culture of Listeria. Int J Food Microbiol 35: 91 – 95. | en_US |
dc.identifier.citedreference | Podda, M., Tritschler, H.J., Ulrich, H., and Packer, L. ( 1994 ) Alpha-lipoic acid supplementation prevents symptoms of vitamin E deficiency. Biochem Biophys Res Commun 204: 98 – 104. | en_US |
dc.identifier.citedreference | Portnoy, D.A., Tweten, R.K., Kehoe, M., and Bielecki, J. ( 1992 ) Capacity of listeriolysin O, streptolysin O, and perfringolysin O to mediate growth of Bacillus subtilis within mammalian cells. Infect Immun 60: 2710 – 2717. | en_US |
dc.identifier.citedreference | Portnoy, D.A., Auerbuch, V., and Glomski, I.J. ( 2002 ) The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 158: 409 – 414. | en_US |
dc.identifier.citedreference | Reed, L.J., De, B.B., Gunsalus, I.C., and Hornberger, C.S., Jr ( 1951 ) Crystalline alpha-lipoic acid; a catalytic agent associated with pyruvate dehydrogenase. Science 114: 93 – 94. | en_US |
dc.identifier.citedreference | Skaar, E.P., Humayun, M., Bae, T., DeBord, K.L., and Schneewind, O. ( 2004 ) Iron-source preference of Staphylococcus aureus infections. Science 305: 1626 – 1628. | en_US |
dc.identifier.citedreference | Smith, K., and Youngman, P. ( 1992 ) Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie 74: 705 – 711. | en_US |
dc.identifier.citedreference | Stein, A., and Firshein, W. ( 2000 ) Probable identification of a membrane-associated repressor of Bacillus subtilis DNA replication as the E2 subunit of the pyruvate dehydrogenase complex. J Bacteriol 182: 2119 – 2124. | en_US |
dc.identifier.citedreference | Stritzker, J., Janda, J., Schoen, C., Taupp, M., Pilgrim, S., Gentschev, I., et al. ( 2004 ) Growth, virulence, and immunogenicity of Listeria monocytogenes aro mutants. Infect Immun 72: 5622 – 5629. | en_US |
dc.identifier.citedreference | Tsai, H.N., and Hodgson, D.A. ( 2003 ) Development of a synthetic minimal medium for Listeria monocytogenes. Appl Environ Microbiol 69: 6943 – 6945. | en_US |
dc.identifier.citedreference | Wada, M., Yasuno, R., Jordan, S.W., Cronan, J.E., Jr and Wada, H. ( 2001 ) Lipoic acid metabolism in Arabidopsis thaliana: cloning and characterization of a cDNA encoding lipoyltransferase. Plant Cell Physiol 42: 650 – 656. | en_US |
dc.identifier.citedreference | Welshimer, H.J. ( 1963 ) Vitamin requirements of Listeria monocytogenes. J Bacteriol 85: 1156 – 1159. | en_US |
dc.identifier.citedreference | Wrenger, C., and Muller, S. ( 2004 ) The human malaria parasite Plasmodium falciparum has distinct organelle-specific lipoylation pathways. Mol Microbiol 53: 103 – 113. | en_US |
dc.identifier.citedreference | Zhao, X., Miller, J.R., Jiang, Y., Marletta, M.A., and Cronan, J.E. ( 2003 ) Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem Biol 10: 1293 – 1302. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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