Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

An important virulence factor of Salmonella spp. is their ability to gain access to host cells. A type III secretion system encoded in the inv and spa loci of these organisms is essential for this phenotype. We have identified two proteins, SipA and SipD, whose secretion from the bacterial cells is dependent on this system. The genes encoding these proteins are located at centisome 63 on the S. typhimurium chromosome, immediately downstream of the previously identified sipB and sipC genes (K. Kaniga, S. Tucker, D. Trollinger, and J. E. Galán, J. Bacteriol. 177:3965-3971, 1995). Nucleotide sequence analysis of the genes encoding these proteins indicated that SipA and SipD have significant sequence similarity to the Shigella IpaA and IpaD proteins. A nonpolar null mutation in sipD rendered S. typhimurium severely deficient for entry into cultured epithelial cells. In addition, this mutant strain exhibited increased secretion of a selected group of proteins whose export is controlled by the inv- and spa-encoded translocon. In contrast, a nonpolar mutation in sipA did not result in an invasion defect or in a significant decreased in virulence in a mouse model of infection. In addition, we have found an open reading frame immediately downstream of SipA that encodes a predicted protein with significant similarity to a family of acyl carrier proteins.

Bibliography

Kaniga, K., Trollinger, D., & Galán, J. E. (1995). Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. Journal of Bacteriology, 177(24), 7078–7085.

Authors 3
  1. K Kaniga (first)
  2. D Trollinger (additional)
  3. J E Galán (additional)
References 73 Referenced 193
  1. Allaoui , A. , P. J. Sansonetti , and C. Parsot . 1992 . MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins . J. Bacteriol. 174 : 7661 - 7669 . (10.1128/jb.174.23.7661-7669.1992) / J. Bacteriol. / MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins by Allaoui A. (1992)
  2. Allaoui , A. , P. J. Sansonetti , and C. Parsot . 1993 . MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins . Mol. Microbiol. 7 : 59 - 68 . (10.1111/j.1365-2958.1993.tb01097.x) / Mol. Microbiol. / MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins by Allaoui A. (1993)
  3. Allaoui , A. , S. Woestyn , C. Sluiters , and G. R. Cornelis . 1994 . YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion . J. Bacteriol. 176 : 4534 - 4542 . (10.1128/jb.176.15.4534-4542.1994) / J. Bacteriol. / YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion by Allaoui A. (1994)
  4. Altmeyer , R. M. , J. K. McNern , J. C. Bossio , I. Rosenshine , B. B. Finlay , and J. E. Galán . 1993 . Cloning and molecular characterization of a gene involved in Salmonella adherence and invasion of cultured epithelial cells . Mol. Microbiol. 7 : 89 - 98 . (10.1111/j.1365-2958.1993.tb01100.x) / Mol. Microbiol. / Cloning and molecular characterization of a gene involved in Salmonella adherence and invasion of cultured epithelial cells by Altmeyer R. M. (1993)
  5. Altschul , S. F. , W. Gish , W. Miller , E. W. Myers , and D. J. Lipman . 1990 . Basic local alignment search tool . J. Mol. Biol. 215 : 403 - 410 . (10.1016/S0022-2836(05)80360-2) / J. Mol. Biol. / Basic local alignment search tool by Altschul S. F. (1990)
  6. Andrews , G. P. , A. E. Hromockyj , C. Coker , and A. T. Maurelli . 1991 . Two novel virulence loci, mxiA and mxiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigen . Infect. Immun. 59 : 1997 - 2005 . (10.1128/iai.59.6.1997-2005.1991) / Infect. Immun. / Two novel virulence loci, mxiA and mxiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigen by Andrews G. P. (1991)
  7. Andrews , G. P. , and A. T. Maurelli . 1992 . 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. 60 : 3287 - 3295 . (10.1128/iai.60.8.3287-3295.1992) / Infect. Immun. / 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 by Andrews G. P. (1992)
  8. Arlat , M. , F. Van Gijsegem , J. C. Pernollet , and C. A. Boucher . 1994 . PopA1, a protein which induces a hypersensitivity-like response on specific petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum . EMBO J. 13 : 543 - 553 . (10.1002/j.1460-2075.1994.tb06292.x) / EMBO J. / PopA1, a protein which induces a hypersensitivity-like response on specific petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum by Arlat M. (1994)
  9. Behlau , I. , and S. J. Miller . 1993 . A Pho-P-repressed gene promotes Salmonella typhimurium invasion of epithelial cells . J. Bacteriol. 175 : 4475 - 4484 . (10.1128/jb.175.14.4475-4484.1993) / J. Bacteriol. / A Pho-P-repressed gene promotes Salmonella typhimurium invasion of epithelial cells by Behlau I. (1993)
  10. Bergman , T. , K. Erickson , E. Galyov , C. Persson , and H. Wolf-Watz . 1994 . The lcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium . J. Bacteriol. 176 : 2619 - 2626 . (10.1128/jb.176.9.2619-2626.1994) / J. Bacteriol. / The lcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium by Bergman T. (1994)
  11. Chang , Y. , R. Young , and D. K. Struck . 1989 . Cloning and characterization of a hemolysin gene from Actinobacillus (Haemphilus) pleuropneumoniae . DNA 8 : 635 - 647 . (10.1089/dna.1.1989.8.635) / DNA / Cloning and characterization of a hemolysin gene from Actinobacillus (Haemphilus) pleuropneumoniae by Chang Y. (1989)
  12. Cheret , G. , L. C. Mattheakis , and F. Sor . 1993 . DNA sequence analysis of the YCN2 region of chromosome XI in Saccharomyces cerevisiae . Yeast 9 : 661 - 667 . (10.1002/yea.320090612) / Yeast / DNA sequence analysis of the YCN2 region of chromosome XI in Saccharomyces cerevisiae by Cheret G. (1993)
  13. Collazo , C. M. , M. K. Zierler , and J. E. Galán . 1995 . Functional analysis of the Salmonella typhimurium invasion genes invI and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus . Mol. Microbiol. 15 : 25 - 38 . (10.1111/j.1365-2958.1995.tb02218.x) / Mol. Microbiol. / Functional analysis of the Salmonella typhimurium invasion genes invI and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus by Collazo C. M. (1995)
  14. Cooper , C. L. , S. G. Boyce , and D. R. Lueking . 1987 . Purification and characterization of Rhodobacter sphaeroides acyl carrier protein . Biochemistry 26 : 2740 - 2746 . (10.1021/bi00384a013) / Biochemistry / Purification and characterization of Rhodobacter sphaeroides acyl carrier protein by Cooper C. L. (1987)
  15. Debelle , F. , and S. B. Sharma . 1986 . Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation . Gene 14 : 7453 - 7471 . / Gene / Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation by Debelle F. (1986)
  16. Devereux , J. , P. Haeberli , and O. Smithies . 1984 . A comprehensive set of sequence analysis programs for the VAX . Nucleic Acids Res. 12 : 387 - 395 . (10.1093/nar/12.1Part1.387) / Nucleic Acids Res. / A comprehensive set of sequence analysis programs for the VAX by Devereux J. (1984)
  17. Donnenberg , M. S. , J. Yu , and J. B. Kaper . 1993 . A second chromosomal gene necessary for intimate attachment of enteropathogenic Escherichia coli to epithelial cells . J. Bacteriol. 175 : 4670 - 4680 . (10.1128/jb.175.15.4670-4680.1993) / J. Bacteriol. / A second chromosomal gene necessary for intimate attachment of enteropathogenic Escherichia coli to epithelial cells by Donnenberg M. S. (1993)
  18. Eichelberg , K. , C. Ginocchio , and J. E. Galán . 1994 . Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: homology of InvC to the F0F1 ATPase family of proteins . J. Bacteriol. 176 : 4501 - 4510 . (10.1128/jb.176.15.4501-4510.1994) / J. Bacteriol. / Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: homology of InvC to the F0F1 ATPase family of proteins by Eichelberg K. (1994)
  19. Fenselau , S. , I. Balbo , and U. Bonas . 1992 . Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in the secretion in bacterial pathogens of animals . Mol. Plant-Microbe Interact. 5 : 390 - 396 . (10.1094/MPMI-5-390) / Mol. Plant-Microbe Interact. / Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in the secretion in bacterial pathogens of animals by Fenselau S. (1992)
  20. Galán , J. E. , and R. Curtiss III . 1989 . Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells . Proc. Natl. Acad. Sci. USA 86 : 6383 - 6387 . (10.1073/pnas.86.16.6383) / Proc. Natl. Acad. Sci. USA / Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells by Galán J. E. (1989)
  21. Galán , J. E. , and C. Ginocchio . 1994 . The molecular genetic bases Salmonella entry into mammalian cells . Biochem. Soc. Trans. 22 : 301 - 306 . (10.1042/bst0220301) / Biochem. Soc. Trans. / The molecular genetic bases Salmonella entry into mammalian cells by Galán J. E. (1994)
  22. Galán , J. E. , C. Ginocchio , and P. Costeas . 1992 . Molecular and functional characterization of the Salmonella typhimurium invasion gene invA: homology of InvA to members of a new protein family . J. Bacteriol. 17 : 4338 - 4349 . (10.1128/jb.174.13.4338-4349.1992) / J. Bacteriol. / Molecular and functional characterization of the Salmonella typhimurium invasion gene invA: homology of InvA to members of a new protein family by Galán J. E. (1992)
  23. Genin , S. , and C. Boucher . 1994 . A superfamily of proteins involved in different secretion pathways in Gram-negative bacteria: modular structure and specificity of the N-terminal domain . Mol. Gen. Genet. 243 : 112 - 118 . (10.1007/BF00283883) / Mol. Gen. Genet. / A superfamily of proteins involved in different secretion pathways in Gram-negative bacteria: modular structure and specificity of the N-terminal domain by Genin S. (1994)
  24. Ginocchio , C. , S. B. Olmsted , C. L. Wells , and J. E. Galán . 1994 . Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium . Cell 76 : 717 - 724 . (10.1016/0092-8674(94)90510-X) / Cell / Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium by Ginocchio C. (1994)
  25. Ginocchio , C. , J. Pace , and J. E. Galán . 1992 . Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells . Proc. Natl. Acad. Sci. USA 89 : 5976 - 5980 . (10.1073/pnas.89.13.5976) / Proc. Natl. Acad. Sci. USA / Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells by Ginocchio C. (1992)
  26. Ginocchio C. K. Rahn R. C. Clarke and J. E. Galán. Naturally occurring deletions in the inv locus of environmental isolates of S. senftenberg and S. litchfield. Submitted for publication.
  27. .Goldschmidt R. Unpublished data.
  28. Gough , C. L. , S. Genin , V. Lopes , and C. A. Boucher . 1993 . Homology between the HrpO protein of Pseudomonas solanacearum and bacterial proteins implicated in a signal peptide-independent secretion mechanism . Mol. Gen. Genet. 239 : 378 - 392 . (10.1007/BF00276936) / Mol. Gen. Genet. / Homology between the HrpO protein of Pseudomonas solanacearum and bacterial proteins implicated in a signal peptide-independent secretion mechanism by Gough C. L. (1993)
  29. Gough , C. L. , S. Genin , C. Zischek , and C. Boucher . 1992 . hrp genes of Pseudomonas solanacecearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria . Mol. Plant-Microbe Interact. 5 : 384 - 389 . (10.1094/MPMI-5-384) / Mol. Plant-Microbe Interact. / hrp genes of Pseudomonas solanacecearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria by Gough C. L. (1992)
  30. Groisman , E. A. , and H. Ochman . 1993 . Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri . EMBO J. 12 : 3779 - 3787 . (10.1002/j.1460-2075.1993.tb06056.x) / EMBO J. / Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri by Groisman E. A. (1993)
  31. Hackett , M. , L. Guo , J. Shabanowitz , D. F. Hunt , and E. L. Hewlett . 1994 . Internal Iysine palmitoylation in adenylate cyclase toxin from Bordetella pertussis . Science 266 : 433 - 435 . (10.1126/science.7939682) / Science / Internal Iysine palmitoylation in adenylate cyclase toxin from Bordetella pertussis by Hackett M. (1994)
  32. Hansen , L. , and P. von Wettstein-Knowles . 1991 . The barley genes Acl1 and Acl3 encoding acyl carrier proteins I and III are located on different chromosomes . Mol. Gen. Genet. 229 : 467 - 478 . (10.1007/BF00267471) / Mol. Gen. Genet. / The barley genes Acl1 and Acl3 encoding acyl carrier proteins I and III are located on different chromosomes by Hansen L. (1991)
  33. Harlow E. and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
  34. He , S. Y. , H. -C. Huang , and A. Collmer . 1993 . Pseudomonas syringae pv. syringae HarpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants . Cell 73 : 1255 - 1266 . (10.1016/0092-8674(93)90354-S) / Cell / Pseudomonas syringae pv. syringae HarpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants by He S. Y. (1993)
  35. Hoiseth , S. K. , and B. A. Stocker . 1981 . Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines . Nature (London) 291 : 238 - 239 . (10.1038/291238a0) / Nature (London) / Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines by Hoiseth S. K. (1981)
  36. Huang , H. - C. , Y. Xiao , R. -H. Lin , Y. Lu , S. W. Hutcheson , and A. Collmer . 1993 . Characterization of the Pseudomonas syringae pv. syringae 61 hrpJ and hrpI genes: homology of HrpI to a superfamily of proteins associated with protein translocation . Mol. Plant-Microbe Interact. 6 : 515 - 520 . (10.1094/MPMI-6-515) / Mol. Plant-Microbe Interact. / Characterization of the Pseudomonas syringae pv. syringae 61 hrpJ and hrpI genes: homology of HrpI to a superfamily of proteins associated with protein translocation by Huang H. (1993)
  37. Issartel , J. - P. , V. Koronakis , and C. Hughes . 1991 . Activation of Escherichia coli prohaemolysin to the mature toxin by acyl carrier protein-dependent fatty acylation . Nature (London) 351 : 759 - 761 . (10.1038/351759a0) / Nature (London) / Activation of Escherichia coli prohaemolysin to the mature toxin by acyl carrier protein-dependent fatty acylation by Issartel J. (1991)
  38. Jarvis K. T. McDaniel M. Donnenberg and J. Kaper. 1994. Sequence analysis of a putative type III secretory pathway in enteropathogenic Escherichia coli (EPEC) abstr. B-295 p. 81. In Abstracts of the 94th General Meeting of the American Society for Microbiology 1994. American Society for Microbiology Washington D.C.
  39. Jones , B. D. , and S. Falkow . 1994 . Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial internalization . Infect. Immun. 62 : 3745 - 3752 . (10.1128/iai.62.9.3745-3752.1994) / Infect. Immun. / Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial internalization by Jones B. D. (1994)
  40. Kaniga , K. , J. C. Bossio , and J. E. Galán . 1994 . The Salmonella typhimurium invasion genes invF and invG encode homologues to the PulD and AraC family of proteins . Mol. Microbiol. 13 : 555 - 568 . (10.1111/j.1365-2958.1994.tb00450.x) / Mol. Microbiol. / The Salmonella typhimurium invasion genes invF and invG encode homologues to the PulD and AraC family of proteins by Kaniga K. (1994)
  41. Kaniga , K. , S. C. Tucker , D. Trollinger , and J. E. Galán . 1995 . Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured cells . J. Bacteriol. 177 : 3965 - 3971 . (10.1128/jb.177.14.3965-3971.1995) / J. Bacteriol. / Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured cells by Kaniga K. (1995)
  42. Klein , P. , and C. Delisi . 1986 . Prediction of protein structural class from the amino acid sequence . Biopolymers 25 : 1659 - 1672 . (10.1002/bip.360250909) / Biopolymers / Prediction of protein structural class from the amino acid sequence by Klein P. (1986)
  43. Klein , P. , M. Kanehisa , and C. DeLisi . 1985 . The detection and classification of membrane-spanning proteins . Biochim. Biophys. Acta 815 : 468 - 476 . (10.1016/0005-2736(85)90375-X) / Biochim. Biophys. Acta / The detection and classification of membrane-spanning proteins by Klein P. (1985)
  44. Lee , C. A. , B. D. Jones , and S. Falkow . 1992 . Identification of a Salmonella typhimurium invasion locus by selection of hyperinvasive mutants . Proc. Natl. Acad. Sci. USA 89 : 1847 - 1851 . (10.1073/pnas.89.5.1847) / Proc. Natl. Acad. Sci. USA / Identification of a Salmonella typhimurium invasion locus by selection of hyperinvasive mutants by Lee C. A. (1992)
  45. Lidell , M. C. , and S. W. Hutcheson . 1994 . Characterization of the hrpJ and hrpU operons of Pseudomonas syringae pv. syringae Pss61: similarity with components of enteric bacteria involved in flagellar biogenesis and demonstration of their role in harpin Pss secretion . Mol. Plant-Microbe Interact. 7 : 488 - 497 . (10.1094/MPMI-7-0488) / Mol. Plant-Microbe Interact. / Characterization of the hrpJ and hrpU operons of Pseudomonas syringae pv. syringae Pss61: similarity with components of enteric bacteria involved in flagellar biogenesis and demonstration of their role in harpin Pss secretion by Lidell M. C. (1994)
  46. Lo , R. Y. C. , C. A. Strathdee , and P. E. Shewen . 1987 . Nucleotide sequence of the leukotoxin genes of Pasteurella haemolytica A1 . Infect. Immun. 55 : 1987 - 1996 . (10.1128/iai.55.9.1987-1996.1987) / Infect. Immun. / Nucleotide sequence of the leukotoxin genes of Pasteurella haemolytica A1 by Lo R. Y. C. (1987)
  47. Macnab , R. M. 1992 . Genetics and biogenesis of bacterial flagella. Annu . Rev. Genet. 26 : 131 - 158 . (10.1146/annurev.ge.26.120192.001023) / Rev. Genet. / Genetics and biogenesis of bacterial flagella. Annu by Macnab R. M. (1992)
  48. Magnuson , K. , S. Jackowski , C. O. Rock , and J. E. Cronan . 1993 . Regulation of fatty acid biosynthesis in Escherichia coli . Microbiol. Rev. 57 : 522 - 542 . (10.1128/mr.57.3.522-542.1993) / Microbiol. Rev. / Regulation of fatty acid biosynthesis in Escherichia coli by Magnuson K. (1993)
  49. Maniatis T. E. F. Fritsch and J. Sambrook. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  50. Maurelli , A. 1994 . Virulence protein export systems in Salmonella and Shigella: a new family or lost relatives ? Trends Cell. Biol. 4 : 240 - 242 . (10.1016/0962-8924(94)90116-3) / Trends Cell. Biol. / Virulence protein export systems in Salmonella and Shigella: a new family or lost relatives by Maurelli A. (1994)
  51. Ménard , R. , P. J. Sansonetti , and C. Parsot . 1993 . Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells . J. Bacteriol. 175 : 5899 - 5906 . (10.1128/jb.175.18.5899-5906.1993) / J. Bacteriol. / Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells by Ménard R. (1993)
  52. Ménard , R. , P. J. Sansonetti , and C. Parsot . 1994 . The secretion of the Shigella flexneri Ipa invasins is induced by the epithelial cell and controlled by IpaB and IpaD . EMBO J. 13 : 5293 - 5302 . (10.1002/j.1460-2075.1994.tb06863.x) / EMBO J. / The secretion of the Shigella flexneri Ipa invasins is induced by the epithelial cell and controlled by IpaB and IpaD by Ménard R. (1994)
  53. Michiels , T. , and G. R. Cornelis . 1991 . Secretion of hybrid proteins by the Yersinia Yop export system . J. Bacteriol. 173 : 1677 - 1685 . (10.1128/jb.173.5.1677-1685.1991) / J. Bacteriol. / Secretion of hybrid proteins by the Yersinia Yop export system by Michiels T. (1991)
  54. Michiels , T. , J. C. Vanooteghem , C. Lambert de Rouvroit , B. China , A. Gustin , P. Boudry , and G. R. Cornelis . 1991 . Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica . J. Bacteriol. 173 : 4994 - 5009 . (10.1128/jb.173.16.4994-5009.1991) / J. Bacteriol. / Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica by Michiels T. (1991)
  55. Michiels , T. , P. Wattiau , R. Brasseur , J. M. Ruysschaert , and G. Cornelis . 1990 . Secretion of Yop proteins by yersiniae . Infect. Immun. 58 : 2840 - 2849 . (10.1128/iai.58.9.2840-2849.1990) / Infect. Immun. / Secretion of Yop proteins by yersiniae by Michiels T. (1990)
  56. Miller , V. L. , and J. J. Mekalanos . 1988 . A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerea requires toxR . J. Bacteriol. 170 : 2575 - 2583 . (10.1128/jb.170.6.2575-2583.1988) / J. Bacteriol. / A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerea requires toxR by Miller V. L. (1988)
  57. Mills , D. B. , V. Bajaj , and C. A. Lee . 1995 . A 40 kilobase chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome . Mol. Microbiol. 15 : 749 - 759 . (10.1111/j.1365-2958.1995.tb02382.x) / Mol. Microbiol. / A 40 kilobase chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome by Mills D. B. (1995)
  58. Platt , M. W. , K. J. Miller , W. S. Lane , and E. P. Kennedy . 1990 . Isolation and characterization of the constitutive acyl carrier protein from Rhizobium meliloti . J. Bacteriol. 172 : 5440 - 5444 . (10.1128/jb.172.9.5440-5444.1990) / J. Bacteriol. / Isolation and characterization of the constitutive acyl carrier protein from Rhizobium meliloti by Platt M. W. (1990)
  59. Rawlings , M. , and J. E. Cronan . 1992 . The gene encoding Escherichia coli acyl carrier protein lies within a cluster of fatty acid biosynthetic genes . J. Biol. Chem. 267 : 5751 - 5754 . (10.1016/S0021-9258(18)42616-6) / J. Biol. Chem. / The gene encoding Escherichia coli acyl carrier protein lies within a cluster of fatty acid biosynthetic genes by Rawlings M. (1992)
  60. Sansonetti , P. J. 1992 . Molecular and cellular biology of Shigella flexneri invasiveness: from cell assay systems to shigellosis . Curr. Top. Microbiol. Immunol. 180 : 1 - 19 . / Curr. Top. Microbiol. Immunol. / Molecular and cellular biology of Shigella flexneri invasiveness: from cell assay systems to shigellosis by Sansonetti P. J. (1992)
  61. Sasakawa , C. , K. Komatsu , T. Tobe , T. Suzuki , and M. Yoshikawa . 1993 . Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a . J. Bacteriol. 175 : 2334 - 2346 . (10.1128/jb.175.8.2334-2346.1993) / J. Bacteriol. / Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a by Sasakawa C. (1993)
  62. Shearman , C. A. , L. Rossen , A. W. B. Johnston , and J. A. Downie . 1986 . The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl carrier protein and is regulated by nodD plus a factor in pea-root exudate . EMBO J. 5 : 647 - 652 . (10.1002/j.1460-2075.1986.tb04262.x) / EMBO J. / The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl carrier protein and is regulated by nodD plus a factor in pea-root exudate by Shearman C. A. (1986)
  63. Stanley , P. , L. C. Packman , V. Koronakis , and C. Hughes . 1994 . Fatty acylation of two internal Iysine residues required for the toxic activity of Escherichia coli hemolysin . Science 266 : 1992 - 1996 . (10.1126/science.7801126) / Science / Fatty acylation of two internal Iysine residues required for the toxic activity of Escherichia coli hemolysin by Stanley P. (1994)
  64. Straley , S. C. , E. Skrzypek , G. V. Plano , and J. B. Bliska . 1993 . Yops of Yersinia spp. pathogenic for humans . Infect. Immun. 61 : 3105 - 3110 . (10.1128/iai.61.8.3105-3110.1993) / Infect. Immun. / Yops of Yersinia spp. pathogenic for humans by Straley S. C. (1993)
  65. Van Gijsegem , F. , C. Gough , C. Zischek , E. Niqueux , M. Arlat , S. Genin , P. Barberis , S. German , P. Castello , and C. Boucher . 1995 . The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex . Mol. Microbiol. 15 : 1095 - 1114 . (10.1111/j.1365-2958.1995.tb02284.x) / Mol. Microbiol. / The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex by Van Gijsegem F. (1995)
  66. Venkatesan , M. M. , J. M. Buysse , and E. V. Oaks . 1992 . Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus . J. Bacteriol. 174 : 1990 - 2001 . (10.1128/jb.174.6.1990-2001.1992) / J. Bacteriol. / Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus by Venkatesan M. M. (1992)
  67. Voetz , M. , B. Klein , J. Schell , and R. Topfer . 1994 . Three different cDNAs encoding acyl carrier proteins from Cuphea lanceolata . Plant Physiol. 106 : 785 - 786 . (10.1104/pp.106.2.785) / Plant Physiol. / Three different cDNAs encoding acyl carrier proteins from Cuphea lanceolata by Voetz M. (1994)
  68. von Heijne , G. 1986 . A new method for predicting signal sequence cleavage sites . Nucleic Acids Res. 14 : 4683 - 4690 . (10.1093/nar/14.11.4683) / Nucleic Acids Res. / A new method for predicting signal sequence cleavage sites by von Heijne G. (1986)
  69. Wei , Z. M. , and S. V. Beer . 1993 . HrpI of Erwinia amylovora functions in secretion of harpin and is a member of a new protein family . J. Bacteriol. 175 : 7958 - 7967 . (10.1128/jb.175.24.7958-7967.1993) / J. Bacteriol. / HrpI of Erwinia amylovora functions in secretion of harpin and is a member of a new protein family by Wei Z. M. (1993)
  70. Wei , Z. M. , R. J. Laby , C. H. Zumoff , D. W. Bauer , S. Y. He , A. Collmer , and S. V. Beer . 1992 . Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora . Science 257 : 85 - 88 . (10.1126/science.1621099) / Science / Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora by Wei Z. M. (1992)
  71. Woestyn , S. , A. Allaoui , P. Wattiau , and G. R. Cornelis . 1994 . YscN, the putative energizer of the Yersinia Yop secretion machinery . J. Bacteriol. 176 : 1561 - 1569 . (10.1128/jb.176.6.1561-1569.1994) / J. Bacteriol. / YscN, the putative energizer of the Yersinia Yop secretion machinery by Woestyn S. (1994)
  72. Yao , R. , and S. Palchauduri . 1992 . Nucleotide sequence and transcriptional regulation of a positive regulatory gene of Shigella dysenteriae . Infect. Immun. 60 : 1163 - 1169 . (10.1128/iai.60.3.1163-1169.1992) / Infect. Immun. / Nucleotide sequence and transcriptional regulation of a positive regulatory gene of Shigella dysenteriae by Yao R. (1992)
  73. Zierler , M. , and J. E. Galán . 1995 . Contact with cultured epithelial cells induces the secretion of the Salmonella typhimurium invasion protein InvJ . Infect. Immun. 63 : 4024 - 4028 . (10.1128/iai.63.10.4024-4028.1995) / Infect. Immun. / Contact with cultured epithelial cells induces the secretion of the Salmonella typhimurium invasion protein InvJ by Zierler M. (1995)
Dates
Type When
Created 8 years, 9 months ago (Nov. 9, 2016, 9:22 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:54 p.m.)
Indexed 2 months, 3 weeks ago (June 10, 2025, 1:28 p.m.)
Issued 29 years, 9 months ago (Dec. 1, 1995)
Published 29 years, 9 months ago (Dec. 1, 1995)
Published Print 29 years, 9 months ago (Dec. 1, 1995)
Funders 0

None

@article{Kaniga_1995, title={Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins}, volume={177}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.177.24.7078-7085.1995}, DOI={10.1128/jb.177.24.7078-7085.1995}, number={24}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Kaniga, K and Trollinger, D and Galán, J E}, year={1995}, month=dec, pages={7078–7085} }