Home LiteratureArticle Details
PMID: 10921870 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Supramolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors.

The EMBO journal ·Vol. 19 ·No. 15 ·2000-08-01 ·Pages 3876-87

Tamano K, Aizawa S, Katayama E, Nonaka T, Imajoh-Ohmi S, Kuwae A, Nagai S, Sasakawa C

Abstract

We investigated the supramolecular structure of the SHIGELLA: type III secretion machinery including its major components. Our results indicated that the machinery was composed of needle and basal parts with respective lengths of 45.4 +/- 3.3 and 31.6 +/- 0.3 nm, and contained MxiD, MxiG, MxiJ and MxiH. spa47, encoding a putative F(1)-type ATPase, was required for the secretion of effector proteins via the type III system and was involved in the formation of the needle. The spa47 mutant produced a defective, needle-less type III structure, which contained MxiD, MxiG and MxiJ but not MxiH. The mxiH mutant produced a defective type III structure lacking the needle and failed to secrete effector proteins. Upon overexpression of MxiH in the mxiH mutant, the bacteria produced type III structures with protruding dramatically long needles, and showed a remarkable increase in invasiveness. Our results suggest that MxiH is the major needle component of the type III machinery and is essential for delivery of the effector proteins, and that the level of MxiH affects the length of the needle.

MeSH Terms
Adhesins, Bacterial Bacterial Outer Membrane Proteins/genetics,ultrastructure Bacterial Proteins/biosynthesis,genetics,metabolism,ultrastructure Cell Membrane/metabolism,ultrastructure Lipoproteins/genetics,ultrastructure Macromolecular Substances Models, Biological Mutation Proton-Translocating ATPases/genetics,ultrastructure Recombinant Proteins/biosynthesis Sequence Analysis, Protein Shigella flexneri/metabolism,pathogenicity,ultrastructure
Chemicals
Adhesins, Bacterial Bacterial Outer Membrane Proteins Bacterial Proteins Lipoproteins Macromolecular Substances MxiD protein, Shigella MxiH protein, Shigella Recombinant Proteins invasin, Yersinia mxiJ protein, Shigella flexneri Proton-Translocating ATPases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Tamano K
Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo 108-8639, Japan.
Aizawa S
Katayama E
Nonaka T
Imajoh-Ohmi S
Kuwae A
Nagai S
Sasakawa C
References (45)
45 references, click to expand
  1. MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins.
    J Bacteriol. 1992 Dec;174(23):7661-9 PMID: 1332940
  2. vacB, a novel chromosomal gene required for expression of virulence genes on the large plasmid of Shigella flexneri.
    J Bacteriol. 1992 Oct;174(20):6359-67 PMID: 1400189
  3. MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri lpa invasins.
    Mol Microbiol. 1993 Jan;7(1):59-68 PMID: 8437520
  4. Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a.
    J Bacteriol. 1993 Apr;175(8):2334-46 PMID: 8385666
  5. Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus.
    Infect Immun. 1993 May;61(5):1707-14 PMID: 8478058
  6. Genetic and biochemical analysis of Salmonella typhimurium FliI, a flagellar protein related to the catalytic subunit of the F0F1 ATPase and to virulence proteins of mammalian and plant pathogens.
    J Bacteriol. 1993 May;175(10):3131-8 PMID: 8491729
  7. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells.
    J Bacteriol. 1993 Sep;175(18):5899-906 PMID: 8376337
  8. Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium.
    J Bacteriol. 1994 Sep;176(17):5439-49 PMID: 8071222
  9. The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD.
    EMBO J. 1994 Nov 15;13(22):5293-302 PMID: 7957095
  10. Shigella flexneri: genetics of entry and intercellular dissemination in epithelial cells.
    Curr Top Microbiol Immunol. 1994;192:217-41 PMID: 7859507
  11. Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness.
    EMBO J. 1995 Jun 1;14(11):2461-70 PMID: 7781600
  12. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells.
    J Bacteriol. 1995 Jul;177(14):3965-71 PMID: 7608068
  13. Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures.
    Mol Microbiol. 1995 Apr;16(2):291-300 PMID: 7565091
  14. Identification of a novel virulence gene, virA, on the large plasmid of Shigella, involved in invasion and intercellular spreading.
    Mol Microbiol. 1995 Jul;17(2):241-50 PMID: 7494473
  15. MxiG, a membrane protein required for secretion of Shigella spp. Ipa invasins: involvement in entry into epithelial cells and in intercellular dissemination.
    Mol Microbiol. 1995 Aug;17(3):461-70 PMID: 8559065
  16. Geometry of the flagellar motor in the cytoplasmic membrane of Salmonella typhimurium as determined by stereo-photogrammetry of quick-freeze deep-etch replica images.
    J Mol Biol. 1996 Jan 26;255(3):458-75 PMID: 8568890
  17. Molecular genetic bases of Salmonella entry into host cells.
    Mol Microbiol. 1996 Apr;20(2):263-71 PMID: 8733226
  18. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity.
    EMBO J. 1996 Nov 1;15(21):5812-23 PMID: 8918459
  19. Enzymatic characterization of FliI. An ATPase involved in flagellar assembly in Salmonella typhimurium.
    J Biol Chem. 1996 Dec 13;271(50):31981-8 PMID: 8943245
  20. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells.
    Mol Microbiol. 1997 Mar;23(5):861-7 PMID: 9076724
  21. Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells?
    Trends Microbiol. 1997 Apr;5(4):148-56 PMID: 9141189
  22. Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin.
    EMBO J. 1997 May 15;16(10):2717-29 PMID: 9184218
  23. Coiled-coil domains in proteins secreted by type III secretion systems.
    Mol Microbiol. 1997 Jul;25(2):423-5 PMID: 9282753
  24. Kinetic analysis of the growth rate of the flagellar hook in Salmonella typhimurium by the population balance method.
    Biophys J. 1998 Jan;74(1):436-43 PMID: 9449344
  25. Supramolecular structure of the Salmonella typhimurium type III protein secretion system.
    Science. 1998 Apr 24;280(5363):602-5 PMID: 9554854
  26. Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins.
    EMBO J. 1998 May 15;17(10):2894-903 PMID: 9582283
  27. Type III protein secretion systems in bacterial pathogens of animals and plants.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):379-433 PMID: 9618447
  28. The Yersinia deadly kiss.
    J Bacteriol. 1998 Nov;180(21):5495-504 PMID: 9791096
  29. Bacterial flagellation and cell division.
    Genes Cells. 1998 Oct;3(10):625-34 PMID: 9893020
  30. Mechanism of Shigella entry into epithelial cells.
    Curr Opin Microbiol. 1999 Feb;2(1):51-5 PMID: 10047558
  31. Type III secretion machines: bacterial devices for protein delivery into host cells.
    Science. 1999 May 21;284(5418):1322-8 PMID: 10334981
  32. IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells.
    EMBO J. 1999 Jun 15;18(12):3249-62 PMID: 10369666
  33. Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization.
    EMBO J. 1999 Nov 1;18(21):5853-62 PMID: 10545097
  34. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes.
    J Cell Biol. 1999 Nov 1;147(3):683-93 PMID: 10545510
  35. A new fla gene in Salmonella typhimurium--flaR--and its mutant phenotype-superhooks.
    Arch Mikrobiol. 1973 Mar 26;90(2):107-20 PMID: 4575053
  36. The current picture of the structure and assembly of tobacco mosaic virus.
    J Gen Virol. 1984 Feb;65 ( Pt 2):253-79 PMID: 6363621
  37. Molecular alteration of the 140-megadalton plasmid associated with loss of virulence and Congo red binding activity in Shigella flexneri.
    Infect Immun. 1986 Feb;51(2):470-5 PMID: 3002985
  38. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a.
    Cell. 1986 Aug 15;46(4):551-5 PMID: 3524856
  39. Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a.
    J Bacteriol. 1988 Jun;170(6):2480-4 PMID: 2836357
  40. Functional organization and nucleotide sequence of virulence Region-2 on the large virulence plasmid in Shigella flexneri 2a.
    Mol Microbiol. 1989 Sep;3(9):1191-201 PMID: 2552264
  41. Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus.
    J Bacteriol. 1992 Mar;174(6):1990-2001 PMID: 1312536
  42. Morphological pathway of flagellar assembly in Salmonella typhimurium.
    J Mol Biol. 1992 Jul 20;226(2):433-46 PMID: 1640458
  43. icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread.
    Mol Microbiol. 1992 Jun;6(12):1605-16 PMID: 1495389
  44. The large virulence plasmid of Shigella.
    Curr Top Microbiol Immunol. 1992;180:21-44 PMID: 1505205
  45. Genetics and biogenesis of bacterial flagella.
    Annu Rev Genet. 1992;26:131-58 PMID: 1482109
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/19.15.3876
Published
2000-08-01
Pages
3876-87
Language
English
Region
England
NLM ID
8208664
PMCID
PMC306602
Subset
IM
External Links
PubMed source DOI: 10.1093/emboj/19.15.3876 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2