Clustering requires modified methyl-accepting sites in low-abundance but not high-abundance chemoreceptors of Escherichia coli
dc.contributor.author | Lybarger, Suzanne R. | en_US |
dc.contributor.author | Nair, Usha | en_US |
dc.contributor.author | Lilly, Angela A. | en_US |
dc.contributor.author | Hazelbauer, Gerald L. | en_US |
dc.contributor.author | Maddock, Janine R. | en_US |
dc.date.accessioned | 2010-06-01T21:16:35Z | |
dc.date.available | 2010-06-01T21:16:35Z | |
dc.date.issued | 2005-05 | en_US |
dc.identifier.citation | Lybarger, Suzanne R.; Nair, Usha; Lilly, Angela A.; Hazelbauer, Gerald L.; Maddock, Janine R. (2005). "Clustering requires modified methyl-accepting sites in low-abundance but not high-abundance chemoreceptors of Escherichia coli ." Molecular Microbiology 56(4): 1078-1086. <http://hdl.handle.net/2027.42/74348> | en_US |
dc.identifier.issn | 0950-382X | en_US |
dc.identifier.issn | 1365-2958 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/74348 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=15853891&dopt=citation | en_US |
dc.description.abstract | Chemotaxis signalling complexes of Escherichia coli , composed of chemoreceptors, CheA and CheW, form clusters located predominately at cell poles. As the only kind of receptor in a cell, high-abundance receptors are polar and clustered whereas low-abundance chemoreceptors are polar but largely unclustered. We found that clustering was a function of the cytoplasmic, carboxyl-terminal domain and that effective clustering was conferred on low-abundance receptors by addition of the ∼20-residue sequence from the carboxyl terminus of either high-abundance receptor. These sequences are different but share a carboxyl-terminal pentapeptide that enhances adaptational covalent modification and allows a physiological balance between modified and unmodified methyl-accepting sites, implying that receptor modification might influence clustering. Thus we investigated directly effects of modification state on chemoreceptor clustering. As the sole receptor type in a cell, low-abundance receptors were clustered only if modified, but high-abundance receptors were clustered independent of extent of modification. This difference could mean that the two receptor types are fundamentally different or that they are poised at different positions in the same conformational equilibrium. Notably, no receptor perturbation we tested altered a predominant location at cell poles, emphasizing a distinction between determinants of clustering and polar localization. | en_US |
dc.format.extent | 118563 bytes | |
dc.format.extent | 3109 bytes | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Science Ltd | en_US |
dc.rights | 2005 Blackwell Publishing Ltd | en_US |
dc.title | Clustering requires modified methyl-accepting sites in low-abundance but not high-abundance chemoreceptors of Escherichia coli | 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 Molecular, Cellular and Developmental Biology, University of Michigan, 830 North University, Ann Arbor, MI 48109, USA. | en_US |
dc.contributor.affiliationother | Department of Biochemistry, University of Missouri-Columbia, 117 Schweitzer Hall, Columbia, MO 65211, USA. | en_US |
dc.identifier.pmid | 15853891 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/74348/1/j.1365-2958.2005.04593.x.pdf | |
dc.identifier.doi | 10.1111/j.1365-2958.2005.04593.x | en_US |
dc.identifier.source | Molecular Microbiology | en_US |
dc.identifier.citedreference | Alley, M. R., Maddock, J. R., and Shapiro, L. ( 1992 ) Polar localization of a bacterial chemoreceptor. Genes Dev 6: 825 – 836. | en_US |
dc.identifier.citedreference | Ames, P., and Parkinson, J. S. ( 1994 ) Constitutively signaling fragments of Tsr, the Escherichia coli serine chemoreceptor. J Bacteriol 176: 6340 – 6348. | en_US |
dc.identifier.citedreference | Ames, P., Studdert, C. A., Reiser, R. H., and Parkinson, J. S. ( 2002 ) Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99: 7060 – 7065. | en_US |
dc.identifier.citedreference | Banno, S., Shiomi, D., Homma, M., and Kawagishi, I. ( 2004 ) Targeting of the chemotaxis methylesterase/deamidase CheB to the polar receptor-kinase cluster in an Escherichia coli cell. Mol Microbiol 53: 1051 – 1063. | en_US |
dc.identifier.citedreference | Barnakov, A. N., Barnakova, L. A., and Hazelbauer, G. L. ( 1998 ) Comparison in vitro of a high- and a low-abundance chemoreceptor of Escherichia coli: similar kinase activation but different methyl- accepting activities. J Bacteriol 180: 6713 – 6718. | en_US |
dc.identifier.citedreference | Barnakov, A. N., Barnakova, L. A., and Hazelbauer, G. L. ( 1999 ) Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proc Natl Acad Sci USA 96: 10667 – 10672. | en_US |
dc.identifier.citedreference | Barnakov, A. N., Barnakova, L. A., and Hazelbauer, G. L. ( 2001 ) Location of the receptor-interaction site on CheB, the methylesterase response regulator of bacterial chemotaxis. J Biol Chem 276: 32984 – 32989. | en_US |
dc.identifier.citedreference | Borkovich, K. A., and Simon, M. I. ( 1990 ) The dynamics of protein phosphorylation in bacterial chemotaxis. Cell 63: 1339 – 1348. | en_US |
dc.identifier.citedreference | Borkovich, K. A., Alex, L. A., and Simon, M. I. ( 1992 ) Attenuation of sensory receptor signaling by covalent modification. Proc Natl Acad Sci USA 89: 6756 – 6760. | en_US |
dc.identifier.citedreference | Bornhorst, J. A., and Falke, J. J. ( 2000 ) Attractant regulation of the aspartate receptor-kinase complex: limited cooperative interactions between receptors and effects of the receptor modification state. Biochemistry 39: 9486 – 9493. | en_US |
dc.identifier.citedreference | Bray, D., Levin, M. D., and Morton-Firth, C. J. ( 1998 ) Receptor clustering as a cellular mechanism to control sensitivity. Nature 393: 85 – 88. | en_US |
dc.identifier.citedreference | Bren, A., and Eisenbach, M. ( 2000 ) How signals are heard during bacterial chemotaxis: protein–protein interactions in sensory signal propagation. J Bacteriol 182: 6865 – 6873. | en_US |
dc.identifier.citedreference | Burrows, G. G., Newcomer, M. E., and Hazelbauer, G. L. ( 1989 ) Purification of receptor protein Trg by exploiting a property common to chemotactic transducers of Escherichia coli. J Biol Chem 264: 17309 – 17315. | en_US |
dc.identifier.citedreference | Cantwell, B. J., Draheim, R. R., Weart, R. B., Nguyen, C., Stewart, R. C., and Manson, M. D. ( 2003 ) CheZ phosphatase localizes to chemoreceptor patches via CheA-short. J Bacteriol 185: 2354 – 2361. | en_US |
dc.identifier.citedreference | Djordjevic, S., and Stock, A. M. ( 1998 ) Chemotaxis receptor recognition by protein methyltransferase CheR. Nat Struct Biol 5: 446 – 450. | en_US |
dc.identifier.citedreference | Duke, T. A., and Bray, D. ( 1999 ) Heightened sensitivity of a lattice of membrane receptors. Proc Natl Acad Sci USA 96: 10104 – 10108. | en_US |
dc.identifier.citedreference | Duke, T. A., Novere, N. L., and Bray, D. ( 2001 ) Conformational spread in a ring of proteins: a stochastic approach to allostery. J Mol Biol 308: 541 – 553. | en_US |
dc.identifier.citedreference | Falke, J. J., and Hazelbauer, G. L. ( 2001 ) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26: 257 – 265. | en_US |
dc.identifier.citedreference | Feng, X., Baumgartner, J. W., and Hazelbauer, G. L. ( 1997 ) High- and low-abundance chemoreceptors in Escherichia coli: differential activities associated with closely related cytoplasmic domains. J Bacteriol 179: 6714 – 6720. | en_US |
dc.identifier.citedreference | Feng, X., Lilly, A. A., and Hazelbauer, G. L. ( 1999 ) Enhanced function conferred on low-abundance chemoreceptor Trg by a methyltransferase-docking site. J Bacteriol 181: 3164 – 3171. | en_US |
dc.identifier.citedreference | Gardina, P., Conway, C., Kossman, M., and Manson, M. ( 1992 ) Aspartate and maltose-binding protein interact with adjacent sites in the Tar chemotactic signal transducer of Escherichia coli. J Bacteriol 174: 1528 – 1536. | en_US |
dc.identifier.citedreference | Gegner, J. A., Graham, D. R., Roth, A. F., and Dahlquist, F. W. ( 1992 ) Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell 70: 975 – 982. | en_US |
dc.identifier.citedreference | Gestwicki, J. E., and Kiessling, L. L. ( 2002 ) Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415: 81 – 84. | en_US |
dc.identifier.citedreference | Gestwicki, J. E., Lamanna, A., Harshey, R. M., McCarter, L. L., Kiessling, L. L., and Adler, J. ( 2000 ) Evolutionary conservation of methyl-accepting chemotaxis protein localization in Bacteria and Archaea. J Bacteriol 182: 6499 – 6502. | en_US |
dc.identifier.citedreference | Harlow, E., and Lane, D. (eds) ( 1988 ) Antibodies: A Laboratory Manual. Plainview, NY: Cold Spring Harbor Laboratory Press. | en_US |
dc.identifier.citedreference | Harrison, D. M., Skidmore, J., Armitage, J. P., and Maddock, J. R. ( 1999 ) Localization and environmental regulation of MCP-like proteins in Rhodobacter sphaeroides. Mol Microbiol 31: 885 – 892. | en_US |
dc.identifier.citedreference | Hazelbauer, G. L. ( 2004 ) Bacterial chemotaxis: a model for sensory receptor systems. In Encyclopedia of Neuroscience, 3rd edn. Adelman, G., and Smith, B. H. (eds). Amsterdam: Elsevier, CD-ROM. | en_US |
dc.identifier.citedreference | Hazelbauer, G. L., and EngstrÖm, P. ( 1980 ) Parallel pathways for transduction of chemotactic signals in Escherichia coli. Nature 283: 98 – 100. | en_US |
dc.identifier.citedreference | Kim, K. K., Yokota, H., and Kim, S. H. ( 1999 ) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400: 787 – 792. | en_US |
dc.identifier.citedreference | Kirby, J. R., Niewold, T. B., Maloy, S., and Ordal, G. W. ( 2000 ) CheB is required for behavioural responses to negative stimuli during chemotaxis in Bacillus subtilis. Mol Microbiol 35: 44 – 57. | en_US |
dc.identifier.citedreference | Le Moual, H., Quang, T., and Koshland, D. E., Jr. ( 1997 ) Methylation of the Escherichia coli chemotaxis receptors: intra- and interdimer mechanisms. Biochemistry 36: 13441 – 13448. | en_US |
dc.identifier.citedreference | Li, G., and Weis, R. M. ( 2000 ) Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100: 357 – 365. | en_US |
dc.identifier.citedreference | Li, J., Li, G., and Weis, R. M. ( 1997 ) The serine chemoreceptor from Escherichia coli is methylated through an inter-dimer process. Biochemistry 36: 11851 – 11857. | en_US |
dc.identifier.citedreference | Li, M., and Hazelbauer, G. L. ( 2004 ) Cellular stoichiometry of the components of the chemotaxis signaling complex. J Bacteriol 186: 3687 – 3694. | en_US |
dc.identifier.citedreference | Liberman, L., Berg, H. C., and Sourjik, V. ( 2004 ) Effect of chemoreceptor modification on assembly and activity of the receptor-kinase complex in Escherichia coli. J Bacteriol 186: 6643 – 6646. | en_US |
dc.identifier.citedreference | Liu, Y., Levit, M., Lurz, R., Surette, M. G., and Stock, J. B. ( 1997 ) Receptor-mediated protein kinase activation and the mechanism of transmembrane signaling in bacterial chemotaxis. EMBO J 16: 7231 – 7240. | en_US |
dc.identifier.citedreference | Lybarger, S. R., and Maddock, J. R. ( 1999 ) Clustering of the chemoreceptor complex in Escherichia coli is independent of the methyltransferase CheR and the methylesterase CheB. J Bacteriol 181: 5527 – 5529. | en_US |
dc.identifier.citedreference | Lybarger, S. R., and Maddock, J. R. ( 2000 ) Differences in the polar clustering of the high- and low-abundance chemoreceptors of Escherichia coli. Proc Natl Acad Sci USA 97: 8057 – 8062. | en_US |
dc.identifier.citedreference | Lybarger, S. R., and Maddock, J. R. ( 2001 ) Polarity in action: asymmetric protein localization in bacteria. J Bacteriol 183: 3261 – 3267. | en_US |
dc.identifier.citedreference | Maddock, J. R., and Shapiro, L. ( 1993 ) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717 – 1723. | en_US |
dc.identifier.citedreference | Oosawa, K., Mutoh, N., and Simon, M. I. ( 1988 ) Cloning of the C-terminal cytoplasmic fragment of the tar protein and effects of the fragment on chemotaxis of Escherichia coli. J Bacteriol 170: 2521 – 2526. | 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 | Parkinson, J. S., and Houts, S. E. ( 1982 ) Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J Bacteriol 151: 106 – 113. | en_US |
dc.identifier.citedreference | Schuster, S. C., Swanson, R. V., Alex, L. A., Bourret, R. B., and Simon, M. I. ( 1993 ) Assembly and function of a quaternary signal transduction complex monitored by surface plasmon resonance. Nature 365: 343 – 347. | en_US |
dc.identifier.citedreference | Shapiro, L., McAdams, H. H., and Losick, R. ( 2002 ) Generating and exploiting polarity in bacteria. Science 298: 1942 – 1946. | en_US |
dc.identifier.citedreference | Shiomi, D., Zhulin, I. B., Homma, M., and Kawagishi, I. ( 2002 ) Dual recognition of the bacterial chemoreceptorby chemotaxis-specific domains of the CheR methyltransferase. J Biol Chem. | en_US |
dc.identifier.citedreference | Skidmore, J. M., Ellefson, D. D., McNamara, B. P., Couto, M. M., Wolfe, A. J., and Maddock, J. R. ( 2000 ) Polar clustering of the chemoreceptor complex in Escherichia coli occurs in the absence of complete CheA function. J Bacteriol 182: 967 – 973. | en_US |
dc.identifier.citedreference | Sourjik, V., and Berg, H. C. ( 2000 ) Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37: 740 – 751. | en_US |
dc.identifier.citedreference | Sourjik, V., and Berg, H. C. ( 2004 ) Functional interactions between receptors in bacterial chemotaxis. Nature 428: 437 – 441. | en_US |
dc.identifier.citedreference | Springer, M. S., Goy, M. F., and Adler, J. ( 1977 ) Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc Natl Acad Sci USA 74: 3312 – 3316. | en_US |
dc.identifier.citedreference | Studdert, C. A., and Parkinson, J. S. ( 2004 ) Crosslinking snapshots of bacterial chemoreceptor squads. Proc Natl Acad Sci USA 101: 2117 – 2122. | en_US |
dc.identifier.citedreference | Weerasuriya, S., Schneider, B. M., and Manson, M. D. ( 1998 ) Chimeric chemoreceptors in Escherichia coli: signaling properties of Tar-Tap and Tap-Tar hybrids. J Bacteriol 180: 914 – 920. | en_US |
dc.identifier.citedreference | Wright, R., and Rine, J. ( 1989 ) Transmission electron microscopy and immunocytochemical studies of yeast: analysis of HMG-CoA reductase overproduction by electron microscopy. Methods Cell Biol 31: 473 – 512. | en_US |
dc.identifier.citedreference | Wu, J., Li, J., Li, G., Long, D. G., and Weis, R. M. ( 1996 ) The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 35: 4984 – 4993. | en_US |
dc.identifier.citedreference | Yamamoto, K., Macnab, R. M., and Imae, Y. ( 1990 ) Repellent response functions of the Trg and Tap chemoreceptors of Escherichia coli. J Bacteriol 172: 383 – 388. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.