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Site-specific receptor methylation of FrzCD in Myxococcus xanthus is controlled by a tetra-trico peptide repeat (TPR) containing regulatory domain of the FrzF methyltransferase

dc.contributor.authorScott, Ansley E.en_US
dc.contributor.authorSimon, Eric S.en_US
dc.contributor.authorPark, Samuel K.en_US
dc.contributor.authorAndrews, Philipen_US
dc.contributor.authorZusman, David R.en_US
dc.date.accessioned2010-06-01T21:20:55Z
dc.date.available2010-06-01T21:20:55Z
dc.date.issued2008-08en_US
dc.identifier.citationScott, Ansley E.; Simon, Eric; Park, Samuel K.; Andrews, Philip; Zusman, David R. (2008). "Site-specific receptor methylation of FrzCD in Myxococcus xanthus is controlled by a tetra-trico peptide repeat (TPR) containing regulatory domain of the FrzF methyltransferase." Molecular Microbiology 69(3): 724-735. <http://hdl.handle.net/2027.42/74414>en_US
dc.identifier.issn0950-382Xen_US
dc.identifier.issn1365-2958en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/74414
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=18554333&dopt=citationen_US
dc.description.abstractMyxococcus xanthus is a gliding bacterium with a complex life cycle that includes swarming, predation and fruiting body formation. Directed movements in M. xanthus are regulated by the Frz chemosensory system, which controls cell reversals. The Frz pathway requires the activity of FrzCD, a cytoplasmic methyl-accepting chemotaxis protein, and FrzF, a methyltransferase (CheR) containing an additional domain with three tetra trico-peptide repeats (TPRs). To investigate the role of the TPRs in FrzCD methylation, we used full-length FrzF and FrzF lacking its TPRs (FrzF CheR ) to methylate FrzCD in vitro . FrzF methylated FrzCD on a single residue, E182, while FrzF CheR methylated FrzCD on three residues, E168, E175 and E182, indicating that the TPRs regulate site-specific methylation. E168 and E182 were predicted consensus methylation sites, but E175 is methylated on an HE pair. To determine the roles of these sites in vivo , we substituted each methylatable glutamate with either an aspartate or an alanine residue and determined the impact of the point mutants on single cell reversals, swarming and fruiting body formation. Single, double and triple methylation site mutants revealed that each site played a unique role in M. xanthus behaviour and that the pattern of receptor methylation determined receptor activity. This work also shows that methylation can both activate and inactivate the receptor.en_US
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dc.format.mimetypeapplication/pdf
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dc.publisherBlackwell Publishing Ltden_US
dc.rightsJournal compilation © 2008 Blackwell Publishingen_US
dc.titleSite-specific receptor methylation of FrzCD in Myxococcus xanthus is controlled by a tetra-trico peptide repeat (TPR) containing regulatory domain of the FrzF methyltransferaseen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Biological Chemistry, University of Michigan, Ann Arbor, MI, USAen_US
dc.contributor.affiliationotherDepartment of Molecular and Cell Biology, University of California, Berkeley, CA, USA.en_US
dc.identifier.pmid18554333en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/74414/1/MMI_6323_sm_Table_S1_and_Figures_S1-S5.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/74414/2/j.1365-2958.2008.06323.x.pdf
dc.identifier.doi10.1111/j.1365-2958.2008.06323.xen_US
dc.identifier.sourceMolecular Microbiologyen_US
dc.identifier.citedreferenceAltschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. ( 1990 ) Basic Local Alignment Search Tool. J Mol Biol 215: 403 – 410.en_US
dc.identifier.citedreferenceAstling, D.P. ( 2003 ) Novel regulatory mechanisms of a chemotaxis pathway in the gliding bacterium Myxococcus xanthus. PhD Thesis. Berkeley, CA: University of California, pp. 60 – 93.en_US
dc.identifier.citedreferenceAstling, D.P., Lee, J.Y., and Zusman, D.R. ( 2006 ) Differential effects of chemoreceptor methylation-domain mutations on swarming and development in the social bacterium Myxococcus xanthus. Mol Microbiol 59: 45 – 55.en_US
dc.identifier.citedreferenceBerleman, J.E., Chumley, T., Cheung, P., and Kirby, J.R. ( 2006 ) Rippling is a predatory behavior in Myxococcus xanthus. J Bacteriol 188: 5888 – 5895.en_US
dc.identifier.citedreferenceBlackhart, B.D., and Zusman, D.R. ( 1985 ) ‘Frizzy’ genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc Natl Acad Sci USA 82: 8767 – 8770.en_US
dc.identifier.citedreferenceBlatch, G.L., and Lassle, M. ( 1999 ) The tetratricopeptide repeat: a structural motif mediating protein–protein interactions. Bioessays 21: 932 – 939.en_US
dc.identifier.citedreferenceBoysen, A., Ellehauge, E., Julien, B., and Sogaard-Andersen, L. ( 2002 ) The DevT protein stimulates synthesis of FruA, a signal transduction protein required for fruiting body morphogenesis in Myxococcus xanthus. J Bacteriol 184: 1540 – 1546.en_US
dc.identifier.citedreferenceBustamante, V.H., Martinez-Flores, I., Vlamakis, H.C., and Zusman, D.R. ( 2004 ) Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. Mol Microbiol 53: 1501 – 1513.en_US
dc.identifier.citedreferenceCampos, J.M., Geisselsoder, J., and Zusman, D.R. ( 1978 ) Isolation of bacteriophage MX4, a generalized transducing phage for Myxococcus xanthus. J Mol Biol 119: 167 – 178.en_US
dc.identifier.citedreferenceGeng, Y., Yang, Z., Downard, J., Zusman, D., and Shi, W. ( 1998 ) Methylation of FrzCD defines a discrete step in the developmental program of Myxococcus xanthus. J Bacteriol 180: 5765 – 5768.en_US
dc.identifier.citedreferenceHagen, D.C., Bretscher, A.P., and Kaiser, D. ( 1978 ) Synergism between morphogenetic mutants of Myxococcus xanthus. Dev Biol 64: 284 – 296.en_US
dc.identifier.citedreferenceHodgkin, J., and Kaiser, D. ( 1977 ) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci USA 74: 2938 – 2942.en_US
dc.identifier.citedreferenceIgoshin, O.A., Goldbeter, A., Kaiser, D., and Oster, G. ( 2004 ) A biochemical oscillator explains several aspects of Myxococcus xanthus behavior during development. Proc Natl Acad Sci USA 101: 15760 – 15765.en_US
dc.identifier.citedreferenceInclÁn, Y.F., Vlamakis, H.C., and Zusman, D.R. ( 2007 ) FrzZ, a dual CheY-like response regulator, functions as an output for the Frz chemosensory pathway of Myxococcus xanthus. Mol Microbiol 65: 90 – 102.en_US
dc.identifier.citedreferenceKaiser, D. ( 2003 ) Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1: 45 – 54.en_US
dc.identifier.citedreferenceKaiser, D. ( 2004 ) Signaling in myxobacteria. Annu Rev Microbiol 58: 75 – 98.en_US
dc.identifier.citedreferenceKehry, M.R., and Dahlquist, F.W. ( 1982 ) The methyl-accepting chemotaxis proteins of Escherichia coli. Identification of the multiple methylation sites on methyl-accepting chemotaxis protein I. J Biol Chem 257: 10378 – 10386.en_US
dc.identifier.citedreferenceMcBride, M.J., and Zusman, D.R. ( 1993 ) FrzCD, a methyl-accepting taxis protein from Myxococcus xanthus, shows modulated methylation during fruiting body formation. J Bacteriol 175: 4936 – 4940.en_US
dc.identifier.citedreferenceMcBride, M.J., Weinberg, R.A., and Zusman, D.R. ( 1989 ) ‘Frizzy’ aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc Natl Acad Sci USA 86: 424 – 428.en_US
dc.identifier.citedreferenceMcCleary, W.R., and Zusman, D.R. ( 1990 ) Purification and characterization of the Myxococcus xanthus FrzE protein shows that it has autophosphorylation activity. J Bacteriol 172: 6661 – 6668.en_US
dc.identifier.citedreferenceMcCleary, W.R., McBride, M.J., and Zusman, D.R. ( 1990 ) Developmental sensory transduction in Myxococcus xanthus involves methylation and demethylation of FrzCD. J Bacteriol 172: 4877 – 4887.en_US
dc.identifier.citedreferenceMignot, T. ( 2007 ) The elusive engine in Myxococcus xanthus gliding motility. Cell Mol Life Sci 64: 2733 – 2745.en_US
dc.identifier.citedreferenceMignot, T., Merlie, J.P., Jr and Zusman, D.R. ( 2007 ) Two localization motifs mediate polar residence of FrzS during cell movement and reversals of Myxococcus xanthus. Mol Microbiol 65: 363 – 372.en_US
dc.identifier.citedreferenceNowlin, D.M., Bollinger, J., and Hazelbauer, G.L. ( 1987 ) Sites of covalent modification in Trg, a sensory transducer of Escherichia coli. J Biol Chem 262: 6039 – 6045.en_US
dc.identifier.citedreferenceNowlin, D.M., Bollinger, J., and Hazelbauer, G.L. ( 1988 ) Site-directed mutations altering methyl-accepting residues of a sensory transducer protein. Proteins 3: 102 – 112.en_US
dc.identifier.citedreferencePark, C., Dutton, D.P., and Hazelbauer, G.L. ( 1990 ) Effects of glutamines and glutamates at sites of covalent modification of a methyl-accepting transducer. J Bacteriol 172: 7179 – 7187.en_US
dc.identifier.citedreferencePerez, E., Zheng, H., and Stock, A.M. ( 2006 ) Identification of methylation sites in Thermotoga maritima chemotaxis receptors. J Bacteriol 188: 4093 – 4100.en_US
dc.identifier.citedreferenceRasmussen, A.A., Porter, S.L., Armitage, J.P., and Sogaard-Andersen, L. ( 2005 ) Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase in Myxococcus xanthus. Mol Microbiol 56: 1358 – 1372.en_US
dc.identifier.citedreferenceReichenbach, H. ( 1999 ) The ecology of the myxobacteria. Environ Microbiol 1: 15 – 21.en_US
dc.identifier.citedreferenceScott, A.E. ( 2008 ) Receptor methylation controls single cell and group behaviors in the social bacterium Myxococcus xanthus. PhD Thesis. Berkeley, CA: University of California, p. 62.en_US
dc.identifier.citedreferenceShapiro, M.J., and Koshland, D.E., Jr ( 1994 ) Mutagenic studies of the interaction between the aspartate receptor and methyltransferase from Escherichia coli. J Biol Chem 269: 11054 – 11059.en_US
dc.identifier.citedreferenceShapiro, M.J., Chakrabarti, I., and Koshland, D.E., Jr ( 1995 ) Contributions made by individual methylation sites of the Escherichia coli aspartate receptor to chemotactic behavior. Proc Natl Acad Sci USA 92: 1053 – 1056.en_US
dc.identifier.citedreferenceShimkets, L.J. ( 1999 ) Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol 53: 525 – 549.en_US
dc.identifier.citedreferenceShiomi, D., Zhulin, I.B., Homma, M., and Kawagishi, I. ( 2002 ) Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J Biol Chem 277: 42325 – 42333.en_US
dc.identifier.citedreferenceSogaard-Andersen, L., and Kaiser, D. ( 1996 ) C factor, a cell-surface-associated intercellular signaling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xanthus. Proc Natl Acad Sci USA 93: 2675 – 2679.en_US
dc.identifier.citedreferenceStock, J.B., and Koshland, D.E., Jr ( 1978 ) A protein methylesterase involved in bacterial sensing. Proc Natl Acad Sci USA 75: 3659 – 3663.en_US
dc.identifier.citedreferenceTerwilliger, T.C., and Koshland, D.E., Jr ( 1984 ) Sites of methyl esterification and deamination on the aspartate receptor involved in chemotaxis. J Biol Chem 259: 7719 – 7725.en_US
dc.identifier.citedreferenceTerwilliger, T.C., Bogonez, E., Wang, E.A., and Koshland, D.E., Jr ( 1983 ) Sites of methyl esterification on the aspartate receptor involved in bacterial chemotaxis. J Biol Chem 258: 9608 – 9611.en_US
dc.identifier.citedreferenceTerwilliger, T.C., Wang, J.Y., and Koshland, D.E., Jr ( 1986 ) Surface structure recognized for covalent modification of the aspartate receptor in chemotaxis. Proc Natl Acad Sci USA 83: 6707 – 6710.en_US
dc.identifier.citedreferenceWu, S.S., and Kaiser, D. ( 1995 ) Genetic and functional evidence that Type IV pili are required for social gliding motility. Mol Microbiol 18: 547 – 558.en_US
dc.identifier.citedreferenceZusman, D.R. ( 1982 ) ‘Frizzy’ mutants: a new class of aggregation-defective developmental mutants of Myxococcus xanthus. J Bacteriol 150: 1430 – 1437.en_US
dc.identifier.citedreferenceZusman, 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.owningcollnameInterdisciplinary and Peer-Reviewed


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