SpoT governs Legionella pneumophila differentiation in host macrophages
dc.contributor.author | Dalebroux, Zachary D. | en_US |
dc.contributor.author | Edwards, Rachel L. | en_US |
dc.contributor.author | Swanson, Michele S. | en_US |
dc.date.accessioned | 2010-06-01T20:11:11Z | |
dc.date.available | 2010-06-01T20:11:11Z | |
dc.date.issued | 2009-02 | en_US |
dc.identifier.citation | Dalebroux, Zachary D.; Edwards, Rachel L.; Swanson, Michele S. (2009). "SpoT governs Legionella pneumophila differentiation in host macrophages." Molecular Microbiology 71(3): 640-658. <http://hdl.handle.net/2027.42/73309> | en_US |
dc.identifier.issn | 0950-382X | en_US |
dc.identifier.issn | 1365-2958 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/73309 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=19040633&dopt=citation | en_US |
dc.description.abstract | During its life cycle, Legionella pneumophila alternates between a replicative and a transmissive state. To determine their contributions to L. pneumophila differentiation, the two ppGpp synthetases, RelA and SpoT, were disrupted. Synthesis of ppGpp was required for transmission, as relA spoT mutants were killed during entry to and exit from macrophages. RelA, which senses amino acid starvation induced by serine hydroxamate, is dispensable in macrophages, as relA mutants spread efficiently. SpoT monitors fatty acid biosynthesis (FAB), since following cerulenin treatment, wild-type and relA strains expressed the flaA transmissive gene, but relA spoT mutants did not. As in Escherichia coli , the SpoT response to FAB perturbation likely required an interaction with acyl-carrier protein (ACP), as judged by the failure of the spoT-A413E allele to rescue transmissive trait expression of relA spoT bacteria. Furthermore, SpoT was essential for transmission between macrophages, since secondary infections by relA spoT mutants were restored by induction of spoT , but not relA . To resume replication, ppGpp must be degraded, as mutants lacking spoT hydrolase activity failed to convert from the transmissive to the replicative phase in either bacteriological medium or macrophages. Thus, L. pneumophila requires SpoT to monitor FAB and to alternate between replication and transmission in macrophages. | en_US |
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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 | Journal compilation © 2009 Blackwell Publishing | en_US |
dc.title | SpoT governs Legionella pneumophila differentiation in host macrophages | 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 | Cellular and Molecular Biology Program, University of Michigan Medical School, Ann Arbor, MI, USA. | en_US |
dc.contributor.affiliationother | Department of Microbiology & Immunology and | en_US |
dc.identifier.pmid | 19040633 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/73309/1/j.1365-2958.2008.06555.x.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/73309/2/MMI_6555_sm_Figure_S1.pdf | |
dc.identifier.doi | 10.1111/j.1365-2958.2008.06555.x | en_US |
dc.identifier.source | Molecular Microbiology | en_US |
dc.identifier.citedreference | Abdelrahman, Y.M., and Belland, R.J. ( 2005 ) The chlamydial developmental cycle. FEMS Microbiol Rev 29: 949 – 959. | en_US |
dc.identifier.citedreference | Aberg, A., Shingler, V., and Balsalobre, C. ( 2006 ) (p)ppGpp regulates type 1 fimbriation of Escherichia coli by modulating the expression of the site-specific recombinase FimB. Mol Microbiol 60: 1520 – 1533. | en_US |
dc.identifier.citedreference | Abu-Zant, A., Asare, R., Graham, J.E., and Abu Kwaik, Y. ( 2006 ) Role for RpoS but not RelA of Legionella pneumophila in modulation of phagosome biogenesis and adaptation to the phagosomal microenvironment. Infect Immun 74: 3021 – 3026. | en_US |
dc.identifier.citedreference | Alli, O.A., Gao, L.Y., Pedersen, L.L., Zink, S., Radulic, M., Doric, M., and Abu Kwaik, Y. ( 2000 ) Temporal pore formation-mediated egress from macrophages and alveolar epithelial cells by Legionella pneumophila. Infect Immun 68: 6431 – 6440. | en_US |
dc.identifier.citedreference | Bachman, M.A., and Swanson, M.S. ( 2001 ) RpoS co-operates with other factors to induce Legionella pneumophila virulence in the stationary phase. Mol Microbiol 40: 1201 – 1214. | en_US |
dc.identifier.citedreference | Battesti, A., and Bouveret, E. ( 2006 ) Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Mol Microbiol 62: 1048 – 1063. | en_US |
dc.identifier.citedreference | Berger, K.H., and Isberg, R.R. ( 1993 ) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7: 7 – 19. | en_US |
dc.identifier.citedreference | Bougdour, A., and Gottesman, S. ( 2007 ) ppGpp regulation of RpoS degradation via anti-adaptor protein IraP. Proc Natl Acad Sci USA 104: 12896 – 12901. | en_US |
dc.identifier.citedreference | Braeken, K., Moris, M., Daniels, R., Vanderlyden, J., and Michiels, J. ( 2006 ) New horizons for (p)ppGpp in bacterial and plant physiology. Trends Microbiol 14: 45 – 54. | en_US |
dc.identifier.citedreference | Bruggemann, H., Hagman, A., Jules, M., Sismeiro, O., Dillies, M.A., Gouyette, C., et al. ( 2006 ) Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell Microbiol 8: 1228 – 1240. | en_US |
dc.identifier.citedreference | Byrne, B., and Swanson, M.S. ( 1998 ) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66: 3029 – 3034. | en_US |
dc.identifier.citedreference | Cashel, M. ( 1969 ) The control of ribonucleic acid synthesis in Escherichia coli. J Biol Chem 244: 3133 – 3141. | en_US |
dc.identifier.citedreference | Cashel, M. ( 1994 ) Detection of (p)ppGpp accumulation patterns in Escherichia coli mutants. In Adolph, K.W. (ed.). Methods in Molecular Genetics, Vol. 3. Molecular Microbiology Techniques, Part A. New York: Academic Press, pp. 341 – 356. | en_US |
dc.identifier.citedreference | Chatfield, C.H., and Cianciotto, N.P. ( 2007 ) The secreted pyomelanin pigment of Legionella pneumophila confers ferric reductase activity. Infect Immun 75: 4062 – 4070. | en_US |
dc.identifier.citedreference | Dahl, J.L., Kraus, C.N., Boshoff, H.I., Doan, B., Foley, K., Avarbock, D., et al. ( 2003 ) The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc Natl Acad Sci USA 100: 10026 – 10031. | en_US |
dc.identifier.citedreference | Durfee, T., Hansen, A.M., Zhi, H., Blattner, F.R., and Jin, D.J. ( 2008 ) Transcription profiling of the stringent response in Escherichia coli. J Bacteriol 190: 1084 – 1096. | en_US |
dc.identifier.citedreference | Erickson, D.L., Lines, J.L., Pesci, E.C., Venturi, V., and Storey, D.G. ( 2004 ) Pseudomonas aeruginosa relA contributes to virulence in Drosophila melanogaster. Infect Immun 72: 5638 – 5645. | en_US |
dc.identifier.citedreference | GarduÑo, R.A., Chong, A., and Faulkner, G. ( 2008 ) Developmental cycle: differentiation of Legionella pneumophila. In Legionella: Molecular Microbiology. Heuner, K., and Swanson, M. (eds). Norfolk: Caister Academic Press, pp. 55 – 73. | en_US |
dc.identifier.citedreference | Gaynor, E.C., Wells, D.H., MacKichan, J.K., and Falkow, S. ( 2005 ) The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol Microbiol 56: 8 – 27. | en_US |
dc.identifier.citedreference | Gentry, D.R., and Cashel, M. ( 1996 ) Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol Microbiol 19: 1373 – 1384. | en_US |
dc.identifier.citedreference | Hammer, B.K., and Swanson, M.S. ( 1999 ) Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol Microbiol 33: 721 – 731. | en_US |
dc.identifier.citedreference | Hammer, B.K., Tateda, E.S., and Swanson, M.S. ( 2002 ) A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol Microbiol 44: 107 – 118. | en_US |
dc.identifier.citedreference | Heath, R.J., Jackowski, S., and Rock, C.O. ( 1994 ) Guanosine tetraphosphate inhibition of fatty acid and phospholipid synthesis in Escherichia coli is relieved by overexpression of glycerol-3-phosphate acyltransferase ( plsB ). J Biol Chem 269: 26584 – 26590. | en_US |
dc.identifier.citedreference | Karakousis, P.C., Yoshimatsu, T., Lamichhane, G., Woolwine, S.C., Nuermberger, E.L., Grosset, J., and Bishai, W.R. ( 2004 ) Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J Exp Med 200: 647 – 657. | en_US |
dc.identifier.citedreference | Magnusson, L.U., Farewell, A., and Nystrom, T. ( 2005 ) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13: 236 – 242. | en_US |
dc.identifier.citedreference | Molofsky, A.B., and Swanson, M.S. ( 2003 ) Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol Microbiol 50: 445 – 461. | en_US |
dc.identifier.citedreference | Molofsky, A.B., and Swanson, M.S. ( 2004 ) Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53: 29 – 40. | en_US |
dc.identifier.citedreference | Molofsky, A.B., Shetron-Rama, L.M., and Swanson, M.S. ( 2005 ) Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect Immun 73: 5720 – 5734. | en_US |
dc.identifier.citedreference | Morales, V.M., Backman, A., and Bagdasarian, M. ( 1991 ) A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97: 39 – 47. | en_US |
dc.identifier.citedreference | Mouery, K., Rader, B.A., Gaynor, E.C., and Guillemin, K. ( 2006 ) The stringent response is required for Helicobacter pylori survival of stationary phase, exposure to acid, and aerobic shock. J Bacteriol 188: 5494 – 5500. | en_US |
dc.identifier.citedreference | Paredes, C.J., Alsaker, K.V., and Papoutsakis, E.T. ( 2005 ) A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol 3: 969 – 978. | en_US |
dc.identifier.citedreference | Pizarro-Cerda, J., and Tedin, K. ( 2004 ) The bacterial signal molecule, ppGpp, regulates Salmonella virulence gene expression. Mol Microbiol 52: 1827 – 1844. | en_US |
dc.identifier.citedreference | Potrykus, K., and Cashel, M. ( 2008 ) (p)ppGpp: still magical? Annu Rev Microbiol 62: 35 – 51. | en_US |
dc.identifier.citedreference | Primm, T.P., Andersen, S.J., Mizrahi, V., Avarbock, D., Rubin, H., and Barry, C.E., 3rd ( 2000 ) The stringent response of Mycobacterium tuberculosis is required for long-term survival. J Bacteriol 182: 4889 – 4898. | en_US |
dc.identifier.citedreference | Sauer, J.D., Bachman, M.A., and Swanson, M.S. ( 2005 ) The phagosomal transporter A couples threonine acquisition to differentiation and replication of Legionella pneumophila in macrophages. Proc Natl Acad Sci USA 102: 9924 – 9929. | en_US |
dc.identifier.citedreference | Seyfzadeh, M., Keener, J., and Nomura, M. ( 1993 ) spoT -dependent accumulation of guanosine tetraphosphate in response to fatty acid starvation in Escherichia coli. Proc Natl Acad Sci USA 90: 11004 – 11008. | en_US |
dc.identifier.citedreference | Shin, S., and Roy, C.R. ( 2008 ) Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 10: 1209 – 1220. | en_US |
dc.identifier.citedreference | Song, M., Kim, H.J., Kim, E.Y., Shin, M., Lee, H.C., Hong, Y., et al. ( 2004 ) ppGpp-dependent stationary phase induction of genes on Salmonella pathogenicity island 1. J Biol Chem 279: 34183 – 34190. | en_US |
dc.identifier.citedreference | Spira, B., and Yagil, E. ( 1998 ) The relation between ppGpp and the PHO regulon in Escherichia coli. Mol Gen Genet 257: 469 – 477. | en_US |
dc.identifier.citedreference | Srivatsan, A., and Wang, J.D. ( 2008 ) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11: 100 – 105. | en_US |
dc.identifier.citedreference | Stone, B.J., and Abu Kwaik, Y. ( 1999 ) Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J Bacteriol 181: 1395 – 1402. | en_US |
dc.identifier.citedreference | Swanson, M.S., and Hammer, B.K. ( 2000 ) Legionella pneumophila pathogesesis: a fateful journey from amoebae to macrophages. Annu Rev Microbiol 54: 567 – 613. | en_US |
dc.identifier.citedreference | Swanson, M.S., and Isberg, R.R. ( 1995 ) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609 – 3620. | en_US |
dc.identifier.citedreference | Taylor, C.M., Beresford, M., Epton, H.A., Sigee, D.C., Shama, G., Andrew, P.W., and Roberts, I.S. ( 2002 ) Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J Bacteriol 184: 621 – 628. | en_US |
dc.identifier.citedreference | Tesh, M.J., and Miller, R.D. ( 1981 ) Amino acid requirements for Legionella pneumophila growth. J Clin Microbiol 13: 865 – 869. | en_US |
dc.identifier.citedreference | Tesh, M.J., Morse, S.A., and Miller, R.D. ( 1983 ) Intermediary metabolism in Legionella pneumophila: utilization of amino acids and other compounds as energy sources. J Bacteriol 154: 1104 – 1109. | en_US |
dc.identifier.citedreference | Thompson, A., Rolfe, M.D., Lucchini, S., Schwerk, P., Hinton, J.C., and Tedin, K. ( 2006 ) The bacterial signal molecule, ppGpp, mediates the environmental regulation of both the invasion and intracellular virulence gene programs of Salmonella. J Biol Chem 281: 30112 – 30121. | en_US |
dc.identifier.citedreference | Tosa, T., and Pizer, L.I. ( 1971 ) Biochemical bases for the antimetabolite action of l-serine hydroxamate. J Bacteriol 106: 972 – 982. | en_US |
dc.identifier.citedreference | Traxler, M.F., Summers, S.M., Nguyen, H.T., Zacharia, V.M., Hightower, G.A., Smith, J.T., and Conway, T. ( 2008 ) The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Mol Microbiol 68: 1128 – 1148. | en_US |
dc.identifier.citedreference | Voth, D.E., and Heinzen, R.A. ( 2007 ) Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol 9: 829 – 840. | en_US |
dc.identifier.citedreference | Warner, D.F., and Mizrahi, V. ( 2006 ) Tuberculosis chemotherapy: the influence of bacillary stress and damage response pathways on drug efficacy. Clin Microbiol Rev 19: 558 – 570. | en_US |
dc.identifier.citedreference | Xiao, H., Kalman, M., Ikehara, K., Zemel, S., Glaser, G., and Cashel, M. ( 1991 ) Residual guanosine 3′,5′-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J Biol Chem 266: 5980 – 5990. | en_US |
dc.identifier.citedreference | Zusman, T., Gal-Mor, O., and Segal, G. ( 2002 ) Characterization of a Legionella pneumophila relA insertion mutant and roles of RelA and RpoS in virulence gene expression. J Bacteriol 184: 67 – 75. | en_US |
dc.identifier.citedreference | Zusman, D.R., Scott, A.E., Yang, Z., and Kirby, J.R. ( 2007 ) Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5: 862 – 872. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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