Home LiteratureArticle Details
PMID: 16344480 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus.

Divakaruni AV, Loo RR, Xie Y, Loo JA, Gober JW

Abstract

The bacterial actin homolog, MreB, forms helical cables within the cell that are required for maintenance of a rod shape. These helical structures are thought to be involved in the spatial organization of cell wall (peptidoglycan) synthesizing complexes of penicillin-binding proteins (PBPs). Here, we examined the role of the MreC cell shape protein in this process in Caulobacter crescentus. Subcellular fractionation experiments showed that MreC is a periplasmic protein and, as assayed by immunofluorescence microscopy, adopted helical or banded patterns along the cell length reminiscent of those formed by MreB and PBP2. The pattern of MreC and PBP2 localization remained when MreB cables were disrupted by treatment with the inhibitor A22. However, long-term absence of MreB led to cell shape changes and an eventual loss of MreC localization, suggesting that an independent structure, perhaps an intact peptidoglycan layer, contributes to the MreC localization pattern. Using affinity chromatography with MreC covalently bound to Sepharose, we isolated several PBPs from cell extracts that eluted from the column as heterogeneous complexes. In this same experiment, using mass spectrometry-based protein identification, we identified several outer membrane proteins, including TonB-dependent receptor transport proteins, that interacted with MreC. Imaging live cells containing fusions of these outer membrane proteins to green fluorescent protein showed that they adopted a subcellular localization pattern that was similar to that of MreC. These results suggest that MreC may function in the spatial organization of PBPs as well as other proteins that lie outside the cytoplasmic membrane.

MeSH Terms
Bacterial Proteins/chemistry,metabolism Caulobacter crescentus/chemistry,cytology,metabolism Cell Wall/chemistry,metabolism Cytoplasm Penicillin-Binding Proteins/metabolism Protein Binding Protein Conformation
Chemicals
Bacterial Proteins MreC protein, Bacteria Penicillin-Binding Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Divakaruni Arun V
Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095, USA.
Loo Rachel R Ogorzalek
Xie Yongming
Loo Joseph A
Gober James W
References (37)
37 references, click to expand
  1. MreB actin-mediated segregation of a specific region of a bacterial chromosome.
    Cell. 2005 Feb 11;120(3):329-41 PMID: 15707892
  2. Structure-activity relationship of S-benzylisothiourea derivatives to induce spherical cells in Escherichia coli.
    Biosci Biotechnol Biochem. 2004 Nov;68(11):2265-9 PMID: 15564663
  3. A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis.
    Mol Microbiol. 2005 Mar;55(6):1646-57 PMID: 15752190
  4. Roles for MreC and MreD proteins in helical growth of the cylindrical cell wall in Bacillus subtilis.
    Mol Microbiol. 2005 Sep;57(5):1196-209 PMID: 16101995
  5. Two independent spiral structures control cell shape in Caulobacter.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18608-13 PMID: 16344481
  6. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli.
    J Biol Chem. 1999 Nov 5;274(45):32031-9 PMID: 10542235
  7. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis.
    Cell. 2001 Mar 23;104(6):913-22 PMID: 11290328
  8. Prokaryotic origin of the actin cytoskeleton.
    Nature. 2001 Sep 6;413(6851):39-44 PMID: 11544518
  9. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell.
    Cell. 2003 Jun 13;113(6):767-76 PMID: 12809607
  10. Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7865-70 PMID: 12766229
  11. Essential nature of the mreC determinant of Bacillus subtilis.
    J Bacteriol. 2003 Aug;185(15):4490-8 PMID: 12867458
  12. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex.
    Mol Microbiol. 2005 Jan;55(1):78-89 PMID: 15612918
  13. Touch and go: tying TonB to transport.
    Mol Microbiol. 2003 Aug;49(4):869-82 PMID: 12890014
  14. Rod shape determination by the Bacillus subtilis class B penicillin-binding proteins encoded by pbpA and pbpH.
    J Bacteriol. 2003 Aug;185(16):4717-26 PMID: 12896990
  15. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli.
    EMBO J. 2003 Oct 1;22(19):5283-92 PMID: 14517265
  16. Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins.
    Curr Biol. 2003 Oct 28;13(21):1916-20 PMID: 14588250
  17. Role of penicillin-binding proteins in bacterial cell morphogenesis.
    Curr Opin Microbiol. 2003 Dec;6(6):594-9 PMID: 14662355
  18. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus.
    Mol Microbiol. 2004 Mar;51(5):1321-32 PMID: 14982627
  19. Branching sites and morphological abnormalities behave as ectopic poles in shape-defective Escherichia coli.
    Mol Microbiol. 2004 May;52(4):1045-54 PMID: 15130123
  20. An actin-like gene can determine cell polarity in bacteria.
    Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8643-8 PMID: 15159537
  21. Dynamic movement of actin-like proteins within bacterial cells.
    EMBO Rep. 2004 Aug;5(8):789-94 PMID: 15272301
  22. Subcellular sites for bacterial protein export.
    Mol Microbiol. 2004 Sep;53(6):1583-99 PMID: 15341641
  23. Complex spatial distribution and dynamics of an abundant Escherichia coli outer membrane protein, LamB.
    Mol Microbiol. 2004 Sep;53(6):1771-83 PMID: 15341654
  24. Penicillin-binding proteins and cell shape in E. coli.
    Nature. 1975 Apr 10;254(5500):516-7 PMID: 1091862
  25. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12.
    Proc Natl Acad Sci U S A. 1975 Aug;72(8):2999-3003 PMID: 1103132
  26. Cluster of mrdA and mrdB genes responsible for the rod shape and mecillinam sensitivity of Escherichia coli.
    J Bacteriol. 1980 Jan;141(1):52-7 PMID: 6243629
  27. Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli.
    J Bacteriol. 1987 Nov;169(11):4935-40 PMID: 2822655
  28. Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells.
    J Bacteriol. 1988 Oct;170(10):4619-24 PMID: 3049542
  29. Negative control of cell division by mreB, a gene that functions in determining the rod shape of Escherichia coli cells.
    J Bacteriol. 1989 Jun;171(6):3123-7 PMID: 2656641
  30. Expert system for predicting protein localization sites in gram-negative bacteria.
    Proteins. 1991;11(2):95-110 PMID: 1946347
  31. Identification of Bacillus subtilis genes for septum placement and shape determination.
    J Bacteriol. 1992 Nov;174(21):6717-28 PMID: 1400224
  32. The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants.
    J Bacteriol. 1992 Nov;174(21):6729-42 PMID: 1400225
  33. Cell cycle-dependent polar localization of chromosome partitioning proteins in Caulobacter crescentus.
    Cell. 1997 Mar 7;88(5):675-84 PMID: 9054507
  34. Identification of the fliI and fliJ components of the Caulobacter flagellar type III protein secretion system.
    J Bacteriol. 1997 Sep;179(17):5355-65 PMID: 9286988
  35. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli.
    Microbiol Mol Biol Rev. 1998 Mar;62(1):181-203 PMID: 9529891
  36. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli.
    J Biol Chem. 1999 Mar 5;274(10):6726-34 PMID: 10037771
  37. Helical disposition of proteins and lipopolysaccharide in the outer membrane of Escherichia coli.
    J Bacteriol. 2005 Mar;187(6):1913-22 PMID: 15743937
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-12-20
Epub
2005-00-12
Pages
18602-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1317943
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com