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.author | Scott, Ansley E. | en_US |
dc.contributor.author | Simon, Eric S. | en_US |
dc.contributor.author | Park, Samuel K. | en_US |
dc.contributor.author | Andrews, Philip | en_US |
dc.contributor.author | Zusman, David R. | en_US |
dc.date.accessioned | 2010-06-01T21:20:55Z | |
dc.date.available | 2010-06-01T21:20:55Z | |
dc.date.issued | 2008-08 | en_US |
dc.identifier.citation | Scott, 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.issn | 0950-382X | en_US |
dc.identifier.issn | 1365-2958 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/74414 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=18554333&dopt=citation | en_US |
dc.description.abstract | Myxococcus 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.mimetype | application/pdf | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Publishing Ltd | en_US |
dc.rights | Journal compilation © 2008 Blackwell Publishing | en_US |
dc.title | 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 | 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 | Department of Biological Chemistry, University of Michigan, Ann Arbor, MI, USA | en_US |
dc.contributor.affiliationother | Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA. | en_US |
dc.identifier.pmid | 18554333 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/74414/1/MMI_6323_sm_Table_S1_and_Figures_S1-S5.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/74414/2/j.1365-2958.2008.06323.x.pdf | |
dc.identifier.doi | 10.1111/j.1365-2958.2008.06323.x | en_US |
dc.identifier.source | Molecular Microbiology | en_US |
dc.identifier.citedreference | Altschul, 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.citedreference | Astling, 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.citedreference | Astling, 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.citedreference | Berleman, 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.citedreference | Blackhart, 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.citedreference | Blatch, G.L., and Lassle, M. ( 1999 ) The tetratricopeptide repeat: a structural motif mediating protein–protein interactions. Bioessays 21: 932 – 939. | en_US |
dc.identifier.citedreference | Boysen, 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.citedreference | Bustamante, 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.citedreference | Campos, 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.citedreference | Geng, 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.citedreference | Hagen, 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.citedreference | Hodgkin, 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.citedreference | Igoshin, 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.citedreference | InclÁn, 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.citedreference | Kaiser, D. ( 2003 ) Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1: 45 – 54. | en_US |
dc.identifier.citedreference | Kaiser, D. ( 2004 ) Signaling in myxobacteria. Annu Rev Microbiol 58: 75 – 98. | en_US |
dc.identifier.citedreference | Kehry, 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.citedreference | McBride, 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.citedreference | McBride, 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.citedreference | McCleary, 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.citedreference | McCleary, 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.citedreference | Mignot, T. ( 2007 ) The elusive engine in Myxococcus xanthus gliding motility. Cell Mol Life Sci 64: 2733 – 2745. | en_US |
dc.identifier.citedreference | Mignot, 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.citedreference | Nowlin, 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.citedreference | Nowlin, 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.citedreference | Park, 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.citedreference | Perez, 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.citedreference | Rasmussen, 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.citedreference | Reichenbach, H. ( 1999 ) The ecology of the myxobacteria. Environ Microbiol 1: 15 – 21. | en_US |
dc.identifier.citedreference | Scott, 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.citedreference | Shapiro, 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.citedreference | Shapiro, 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.citedreference | Shimkets, L.J. ( 1999 ) Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol 53: 525 – 549. | en_US |
dc.identifier.citedreference | Shiomi, 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.citedreference | Sogaard-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.citedreference | Stock, 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.citedreference | Terwilliger, 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.citedreference | Terwilliger, 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.citedreference | Terwilliger, 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.citedreference | Wu, 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.citedreference | Zusman, 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.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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