DOI: 10.1146/annurev.micro.57.030502.090832. How Bacteria Assemble Flagella

10.1146/annurev.micro.57.030502.090832

Crossref journal-article

Annual Reviews

Annual Review of Microbiology (22)

Abstract

▪ Abstract The bacterial flagellum is both a motor organelle and a protein export/assembly apparatus. It extends from the cytoplasm to the cell exterior. All the protein subunits of the external elements have to be exported. Export employs a type III pathway, also utilized for secretion of virulence factors. Six of the components of the export apparatus are integral membrane proteins and are believed to be located within the flagellar basal body. Three others are soluble: the ATPase that drives export, a regulator of the ATPase, and a general chaperone. Exported substrates diffuse down a narrow channel in the growing structure and assemble at the distal end, often with the help of a capping structure.

Bibliography

Macnab, R. M. (2003). How Bacteria Assemble Flagella. Annual Review of Microbiology, 57(1), 77â100.

Authors 1

Robert M. Macnab (first)

References 97 Referenced 845

10.1046/j.1365-2443.1998.00219.x
10.1126/science.278.5340.1140
10.1016/S0022-2836(02)00172-9
10.1006/jmbi.2001.4597
10.1016/S0966-842X(00)01751-0
10.1046/j.1365-2958.2001.02268.x
10.1038/239500a0
10.1126/science.2849208
10.1074/jbc.R100066200
10.1021/bi011264g
10.1128/JB.181.11.3542-3551.1999 / J. Bacteriol. by Braun TF (1999)
10.1006/jmbi.1998.1730
10.1128/JB.182.24.6865-6873.2000
Calladine CR. 1982. Construction of bacterial flagellar filaments, and aspects of their conversion to different helical forms. InProkaryotic and Eukaryotic Flagella, ed. WB Amos, JG Duckett, pp. 33–51. Cambridge, UK: Cambridge Univ. Press
10.1016/S0966-842X(99)01665-0
10.1046/j.1365-2958.1998.01131.x
10.1074/jbc.271.44.27237
10.1046/j.1365-2958.1997.6412010.x
10.1073/pnas.89.14.6304
10.1006/jmbi.1994.1079
10.1046/j.1365-2958.1999.01372.x
10.1046/j.1365-2958.2003.03487.x
10.1046/j.1365-2958.2002.03047.x
10.1006/jmbi.2001.4963
10.1128/JB.185.8.2485-2492.2003
10.1128/jb.176.17.5439-5449.1994
10.1128/jb.164.3.1370-1372.1985 / J. Bacteriol. by Homma M (1985)
10.1128/jb.169.4.1493-1498.1987
10.1016/0022-2836(90)90365-S
10.1128/jb.163.2.464-471.1985 / J. Bacteriol. by Homma M (1985)
10.1126/science.8235660
10.1128/mr.52.4.533-535.1988 / Microbiol. Rev. by Iino T (1988)
10.1016/0022-2836(85)90317-1
10.1016/0022-2836(89)90174-5
10.1128/jb.169.3.1168-1173.1987
10.1006/jmbi.1998.1662
10.1007/BF00762688
10.1128/jb.172.3.1327-1339.1990
10.1016/0022-2836(90)90132-6
10.1016/S0092-8674(00)00053-2
10.1046/j.1365-2958.2000.02081.x
10.1006/jmbi.1996.0038
10.1128/JB.183.5.1655-1662.2001
10.1021/bi011263o
10.1111/j.1365-2958.1994.tb01268.x
10.1126/science.280.5363.602
10.1016/0022-2836(92)90958-M
10.1128/jb.179.3.813-817.1997
10.1007/BF00279569 / Mol. Gen. Genet. by Kutsukake K (1994)
10.1073/pnas.86.13.4953
10.1073/pnas.062065699
10.1128/JB.184.16.4500-4509.2002
10.1128/jb.178.1.223-231.1996
10.1073/pnas.74.1.221
Macnab RM. 1996. Flagella and motility. In Escherichia coliandSalmonella:Cellular and Molecular Biology, ed. FC Neidhardt, R Curtiss III, JL Ingraham, ECC Lin, KB Low, et al. pp. 123–45. Washington, DC: ASM Press
10.1073/pnas.69.9.2509
10.1016/S0022-2836(77)80153-8
10.1126/science.1058366
10.1073/pnas.74.7.3060
10.1016/0014-5793(77)80581-4
10.1006/jmbi.1995.0281
10.1128/JB.182.15.4207-4215.2000
10.1046/j.1365-2958.1999.01597.x
10.1128/JB.181.5.1388-1394.1999 / J. Bacteriol. by Minamino T (1999)
10.1128/JB.182.17.4906-4914.2000
10.1046/j.1365-2958.2000.01771.x
10.1046/j.1365-2958.2000.02106.x
10.1128/JB.182.11.3029-3036.2000
10.1006/jmbi.1993.1009
10.1006/jmbi.1995.0282
10.1128/jb.174.7.2298-2304.1992
10.1128/JB.181.18.5808-5813.1999 / J. Bacteriol. by Muramoto K (1999)
10.1099/00221287-146-5-1171
10.1128/JB.181.5.1555-1561.1999 / J. Bacteriol. by Nambu T (1999)
10.1128/JB.183.16.4823-4838.2001
10.1128/jb.179.19.6092-6099.1997
10.1128/jb.169.4.1485-1488.1987
10.1128/jb.176.8.2272-2281.1994
10.1128/jb.171.4.2075-2082.1989
10.1128/jb.179.17.5602-5604.1997
10.1016/0378-1097(85)90024-2
10.1128/JB.184.12.3321-3328.2002
10.1038/35066504
10.1074/jbc.275.8.5718
10.1038/249073a0
10.1128/jb.174.3.793-806.1992
10.1006/jsbi.1998.4048
10.1128/JB.182.10.2793-2801.2000
10.1128/jb.173.11.3564-3572.1991
10.1128/jb.178.10.2960-2970.1996
10.1128/jb.166.1.187-193.1986
10.1099/13500872-141-7-1715
10.1126/science.290.5499.2148
10.1128/jb.178.1.258-265.1996
10.1006/jmbi.1996.0452
10.1128/JB.180.10.2729-2735.1998 / J. Bacteriol. by Zhou J (1998)
10.1021/bi0203280

Dates

Type	When
Created	22 years, 3 months ago (May 5, 2003, 8:15 p.m.)
Deposited	3 years, 10 months ago (Oct. 14, 2021, 4:40 a.m.)
Indexed	2 days, 6 hours ago (Aug. 22, 2025, 12:45 a.m.)
Issued	21 years, 10 months ago (Oct. 1, 2003)
Published	21 years, 10 months ago (Oct. 1, 2003)
Published Print	21 years, 10 months ago (Oct. 1, 2003)

Funders 0

None

BibTeX

@article{Macnab_2003, title={How Bacteria Assemble Flagella}, volume={57}, ISSN={1545-3251}, url={http://dx.doi.org/10.1146/annurev.micro.57.030502.090832}, DOI={10.1146/annurev.micro.57.030502.090832}, number={1}, journal={Annual Review of Microbiology}, publisher={Annual Reviews}, author={Macnab, Robert M.}, year={2003}, month=oct, pages={77–100} }

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