Home LiteratureArticle Details
PMID: 8404849 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri.

The EMBO journal ·Vol. 12 ·No. 10 ·1993-10-00 ·Pages 3779-87

Groisman EA, Ochman H

Abstract

The enteric pathogens Salmonella typhimurium and Shigella flexneri differ in most virulence attributes including infectivity, pathology and host range. We have identified a new assemblage of genes responsible for invasion properties of Salmonella which is remarkably similar in order, arrangement and sequence to the gene cluster controlling the presentation of surface antigens (spa) on the virulence plasmid of Shigella. In Salmonella, this chromosomally encoded complex consists of over 12 genes, mutations in which abolish bacterial entry into epithelial cells. Although these genera use distinct invasion antigens, a non-invasive spa mutant of Salmonella could be rescued by the corresponding Shigella homolog. While spa promotes equivalent functions in Shigella and Salmonella, this constellation of genes has been acquired independently by each genus and displays motifs used by diverse antigen export systems including those required for flagellar assembly and protein secretion.

Related Genes
spa
MeSH Terms
Amino Acid Sequence Animals Antigens, Bacterial/genetics Antigens, Surface/genetics Base Sequence Blotting, Southern Chromosomes, Bacterial DNA Epithelial Cells Epithelium/microbiology Genes, Bacterial Genetic Complementation Test Humans Mice Molecular Sequence Data Multigene Family Mutation Restriction Mapping Salmonella typhimurium/genetics,immunology,pathogenicity Sequence Homology, Amino Acid Shigella flexneri/genetics,immunology,pathogenicity Tumor Cells, Cultured
Chemicals
Antigens, Bacterial Antigens, Surface DNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Groisman E A
Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110.
Ochman H
References (67)
67 references, click to expand
  1. 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
  2. Membrane traffic wardens and protein secretion in gram-negative bacteria.
    Trends Biochem Sci. 1993 Jan;18(1):7-12 PMID: 8438237
  3. Identification of novel loci affecting entry of Salmonella enteritidis into eukaryotic cells.
    J Bacteriol. 1992 Jun;174(12):3945-52 PMID: 1317843
  4. Resistance to host antimicrobial peptides is necessary for Salmonella virulence.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11939-43 PMID: 1465423
  5. YopB and YopD constitute a novel class of Yersinia Yop proteins.
    Infect Immun. 1993 Jan;61(1):71-80 PMID: 8418066
  6. Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor.
    J Bacteriol. 1993 Feb;175(3):802-10 PMID: 8423152
  7. Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri.
    Infect Immun. 1985 Jul;49(1):164-71 PMID: 2989179
  8. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis.
    Infect Immun. 1986 Feb;51(2):461-9 PMID: 3510976
  9. Comparison of the ability of enteroinvasive Escherichia coli, Salmonella typhimurium, Yersinia pseudotuberculosis, and Yersinia enterocolitica to enter and replicate within HEp-2 cells.
    Infect Immun. 1987 Jul;55(7):1674-9 PMID: 3298064
  10. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells.
    Cell. 1987 Aug 28;50(5):769-78 PMID: 3304658
  11. Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation.
    Infect Immun. 1987 Nov;55(11):2681-8 PMID: 3312007
  12. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic.
    Infect Immun. 1987 Dec;55(12):3035-43 PMID: 3316029
  13. Identification of regions on a 230-kilobase plasmid from enteroinvasive Escherichia coli that are required for entry into HEp-2 cells.
    Infect Immun. 1988 Jan;56(1):225-9 PMID: 2826335
  14. Development and testing of invasion-associated DNA probes for detection of Shigella spp. and enteroinvasive Escherichia coli.
    J Clin Microbiol. 1988 Feb;26(2):261-6 PMID: 2830310
  15. Evolution of antibiotic resistance genes: the DNA sequence of a kanamycin resistance gene from Staphylococcus aureus.
    Mol Biol Evol. 1983 Dec;1(1):57-66 PMID: 6100986
  16. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella.
    J Gen Microbiol. 1983 Sep;129(9):2715-26 PMID: 6355392
  17. Temperature-dependent expression of virulence genes in Shigella species.
    Infect Immun. 1984 Jan;43(1):195-201 PMID: 6360895
  18. Nucleotide sequences of Bacillus subtilis flagellar biosynthetic genes fliP and fliQ and identification of a novel flagellar gene, fliZ.
    J Bacteriol. 1992 Jun;174(12):4017-25 PMID: 1597417
  19. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family.
    J Bacteriol. 1992 Jul;174(13):4338-49 PMID: 1624429
  20. Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells.
    Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5976-80 PMID: 1631083
  21. mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homolog of the low-calcium-response protein, LcrD, of Yersinia pestis.
    Infect Immun. 1992 Aug;60(8):3287-95 PMID: 1639496
  22. 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
  23. Evolution of structure and function of V-ATPases.
    J Bioenerg Biomembr. 1992 Aug;24(4):415-24 PMID: 1400286
  24. 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
  25. Identification and characterization of FliY, a novel component of the Bacillus subtilis flagellar switch complex.
    Mol Microbiol. 1992 Sep;6(18):2715-23 PMID: 1447979
  26. Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella typhimurium grown under low-oxygen conditions.
    Mol Microbiol. 1992 Nov;6(21):3077-87 PMID: 1360615
  27. Identification of Salmonella typhimurium invasiveness loci.
    Can J Microbiol. 1992 Aug;38(8):852-7 PMID: 1458375
  28. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold.
    EMBO J. 1982;1(8):945-51 PMID: 6329717
  29. Penetration of Salmonella through a polarized Madin-Darby canine kidney epithelial cell monolayer.
    J Cell Biol. 1988 Jul;107(1):221-30 PMID: 3292541
  30. Intact motility as a Salmonella typhi invasion-related factor.
    Infect Immun. 1988 Aug;56(8):1967-73 PMID: 2840399
  31. Roles of motility, chemotaxis, and penetration through and growth in intestinal mucus in the ability of an avirulent strain of Salmonella typhimurium to colonize the large intestine of streptomycin-treated mice.
    Infect Immun. 1988 Sep;56(9):2209-17 PMID: 3044995
  32. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection.
    Nature. 1988 Sep 8;335(6186):167-70 PMID: 3412472
  33. Characterization of invasion plasmid antigen genes (ipaBCD) from Shigella flexneri.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):9317-21 PMID: 3057506
  34. Identification and characterization of TnphoA mutants of Salmonella that are unable to pass through a polarized MDCK epithelial cell monolayer.
    Mol Microbiol. 1988 Nov;2(6):757-66 PMID: 2850443
  35. Comparison of the invasion strategies used by Salmonella cholerae-suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication.
    Biochimie. 1988 Aug;70(8):1089-99 PMID: 3147700
  36. Linkage map of Salmonella typhimurium, edition VII.
    Microbiol Rev. 1988 Dec;52(4):485-532 PMID: 3070321
  37. Determinants for thermoinducible cell binding and plasmid-encoded cellular penetration detected in the absence of the Yersinia pseudotuberculosis invasin protein.
    Infect Immun. 1989 Jul;57(7):1998-2005 PMID: 2543628
  38. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5054-8 PMID: 2544889
  39. Penetration of human intestinal epithelial cells by Salmonella: molecular cloning and expression of Salmonella typhi invasion determinants in Escherichia coli.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5173-7 PMID: 2662196
  40. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells.
    Proc Natl Acad Sci U S A. 1989 Aug;86(16):6383-7 PMID: 2548211
  41. Salmonella as an intracellular parasite.
    Mol Microbiol. 1989 Dec;3(12):1833-41 PMID: 2695752
  42. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells.
    Cell. 1990 Mar 9;60(5):861-71 PMID: 2311122
  43. Mechanism and evolution of the uncoupling protein of brown adipose tissue.
    Trends Biochem Sci. 1990 Mar;15(3):108-12 PMID: 2158156
  44. Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium.
    Infect Immun. 1990 Jun;58(6):2014-6 PMID: 1971262
  45. The ability of Salmonella to enter mammalian cells is affected by bacterial growth state.
    Proc Natl Acad Sci U S A. 1990 Jun;87(11):4304-8 PMID: 2349239
  46. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts.
    Science. 1990 Aug 10;249(4969):641-6 PMID: 2200126
  47. Anaerobic growth of Salmonella typhimurium results in increased uptake by Henle 407 epithelial and mouse peritoneal cells in vitro and repression of a major outer membrane protein.
    Infect Immun. 1991 Jan;59(1):437-40 PMID: 1987056
  48. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells.
    Infect Immun. 1988 May;56(5):1242-8 PMID: 2833444
  49. Molecular genetic basis for complex flagellar antigen expression in a triphasic serovar of Salmonella.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):956-60 PMID: 1992487
  50. Effect of motility and chemotaxis on the invasion of Salmonella typhimurium into HeLa cells.
    Microb Pathog. 1990 Jul;9(1):47-53 PMID: 2077343
  51. Discrimination between intracellular uptake and surface adhesion of bacterial pathogens.
    Science. 1991 May 17;252(5008):934-8 PMID: 1674624
  52. Two novel virulence loci, mxiA and mxiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens.
    Infect Immun. 1991 Jun;59(6):1997-2005 PMID: 2037361
  53. Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of FliI to F0F1, vacuolar, and archaebacterial ATPase subunits.
    J Bacteriol. 1991 Jun;173(11):3564-72 PMID: 1646201
  54. The flaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide.
    J Bacteriol. 1991 Jun;173(11):3573-9 PMID: 1828465
  55. Genetic and molecular basis of epithelial cell invasion by Shigella species.
    Rev Infect Dis. 1991 Mar-Apr;13 Suppl 4:S285-92 PMID: 2047651
  56. Bacterial entry into eukaryotic cells.
    Cell. 1991 Jun 28;65(7):1099-102 PMID: 1905978
  57. Genetic analysis of the bacterial flagellum.
    Trends Genet. 1991 Jun;7(6):196-200 PMID: 2068793
  58. Distribution of the invA, -B, -C, and -D genes of Salmonella typhimurium among other Salmonella serovars: invA mutants of Salmonella typhi are deficient for entry into mammalian cells.
    Infect Immun. 1991 Sep;59(9):2901-8 PMID: 1879916
  59. Genetic basis of virulence in Shigella species.
    Microbiol Rev. 1991 Jun;55(2):206-24 PMID: 1886518
  60. Functional complementation between bacterial MDR-like export systems: colicin V, alpha-hemolysin, and Erwinia protease.
    J Bacteriol. 1991 Dec;173(23):7549-56 PMID: 1938950
  61. In vivo genetic engineering with bacteriophage Mu.
    Methods Enzymol. 1991;204:180-212 PMID: 1834917
  62. Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1847-51 PMID: 1311853
  63. Cloning and characterization of pathogenicity genes from Xanthomonas campestris pv. glycines.
    J Bacteriol. 1992 Mar;174(6):1923-31 PMID: 1312532
  64. 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
  65. Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation.
    Infect Immun. 1992 Jun;60(6):2475-80 PMID: 1587617
  66. Molecular, functional, and evolutionary analysis of sequences specific to Salmonella.
    Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1033-7 PMID: 8430070
  67. Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale.
    Trends Genet. 1993 Jan;9(1):17-22 PMID: 8434412
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1993-10-00
Pages
3779-87
Language
English
Region
England
NLM ID
8208664
PMCID
PMC413660
Subset
IM
Grants
NIGMS NIH HHS · GM40995 · United States
NIAID NIH HHS · R01 AI29554 · United States
Databases
GENBANK
X73525
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