1887

Abstract

The ability of serovar Typhimurium (. Typhimurium) to penetrate the intestinal epithelium is key to its pathogenesis. Bacterial invasion can be seen as a two-step process initially requiring adherence to the host cell surface followed by internalization into the host cell. Evidence suggests that adherence of . Typhimurium to host cells is receptor-mediated; however, the host cell receptor(s) has/have not been identified. Internalization of . Typhimurium absolutely requires the actin cytoskeleton yet only a few of the cytoskeletal components involved in this process have been identified. In order to identify host proteins that may play a role in Typhimurium invasion, the recruitment of actin-associated proteins was investigated. The contribution of recruited Src homology 2 adaptor proteins to invasion was further investigated and it was found that, while not involved in bacterial internalization itself, the adaptors Nck and ShcA influenced adherence of Typhimurium to non-phagocytic cells.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/008581-0
2007-10-01
2022-07-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/10/3517.html?itemId=/content/journal/micro/10.1099/mic.0.2007/008581-0&mimeType=html&fmt=ahah

References

  1. Baumler A. J., Tsolis R. M., Heffron F. 1997; Fimbrial adhesins of Salmonella typhimurium . Role in bacterial interactions with epithelial cells. Adv Exp Med Biol 412:149–158
    [Google Scholar]
  2. Becker E., Huynh-Do U., Holland S., Pawson T., Daniel T. O., Skolnik E. Y. 2000; Nck-interacting Ste20 kinase couples Eph receptors to c-Jun N-terminal kinase and integrin activation. Mol Cell Biol 20:1537–1545
    [Google Scholar]
  3. Benesch S., Lommel S., Steffen A., Stradal T. E., Scaplehorn N., Way M., Wehland J., Rottner K. 2002; Phosphatidylinositol 4,5-biphosphate (PIP2)-induced vesicle movement depends on N-WASP and involves Nck, WIP, and Grb2. J Biol Chem 277:37771–37776
    [Google Scholar]
  4. Bladt F., Aippersbach E., Gelkop S., Strasser G. A., Nash P., Tafuri A., Gertler F. B., Pawson T. 2003; The murine Nck SH2/SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol Cell Biol 23:4586–4597
    [Google Scholar]
  5. Bougneres L., Girardin S. E., Weed S. A., Karginov A. V., Olivo-Marin J. C., Parsons J. T., Sansonetti P. J., Van Nhieu G. T. 2004; Cortactin and Crk cooperate to trigger actin polymerization during Shigella invasion of epithelial cells. J Cell Biol 166:225–235
    [Google Scholar]
  6. Boyle E. C., Brown N. F., Finlay B. B. 2006; Salmonella enterica serovar Typhimurium effectors SopB, SopE, SopE2 and SipA disrupt tight junction structure and function. Cell Microbiol 8:1946–1957
    [Google Scholar]
  7. Bracke M., Nijhuis E., Lammers J. W., Coffer P. J., Koenderman L. 2000; A critical role for PI 3-kinase in cytokine-induced F α -receptor activation. Blood 95:2037–2043
    [Google Scholar]
  8. Braverman L. E., Quilliam L. A. 1999; Identification of Grb4/Nck β , a Src homology 2 and 3 domain-containing adapter protein having similar binding and biological properties to Nck. J Biol Chem 274:5542–5549
    [Google Scholar]
  9. Bruce-Staskal P. J., Weidow C. L., Gibson J. J., Bouton A. H. 2002; Cas, Fak and Pyk2 function in diverse signaling cascades to promote Yersinia uptake. J Cell Sci 115:2689–2700
    [Google Scholar]
  10. Buday L. 1999; Membrane-targeting of signalling molecules by SH2/SH3 domain-containing adaptor proteins. Biochim Biophys Acta 1422:187–204
    [Google Scholar]
  11. Buday L., Wunderlich L., Tamas P. 2002; The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal 14:723–731
    [Google Scholar]
  12. Burton E. A., Plattner R., Pendergast A. M. 2003; Abl tyrosine kinases are required for infection by Shigella flexneri . EMBO J 22:5471–5479
    [Google Scholar]
  13. Caunt C. J., Hislop J. N., Kelly E., Matharu A. L., Green L. D., Sedgley K. R., Finch A. R., McArdle C. A. 2004; Regulation of gonadotropin-releasing hormone receptors by protein kinase C: inside out signalling and evidence for multiple active conformations. Endocrinology 145:3594–3602
    [Google Scholar]
  14. Criss A. K., Casanova J. E. 2003; Coordinate regulation of Salmonella enterica serovar Typhimurium invasion of epithelial cells by the Arp2/3 complex and Rho GTPases. Infect Immun 71:2885–2891
    [Google Scholar]
  15. Criss A. K., Ahlgren D. M., Jou T. S., McCormick B. A., Casanova J. E. 2001; The GTPase Rac1 selectively regulates Salmonella invasion at the apical plasma membrane of polarized epithelial cells. J Cell Sci 114:1331–1341
    [Google Scholar]
  16. Dorsey C. W., Laarakker M. C., Humphries A. D., Weening E. H., Baumler A. J. 2005; Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol Microbiol 57:196–211
    [Google Scholar]
  17. Eden S., Rohatgi R., Podtelejnikov A. V., Mann M., Kirschner M. W. 2002; Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790–793
    [Google Scholar]
  18. Finlay B. B., Heffron F., Falkow S. 1989; Epithelial cell surfaces induce S almonella proteins required for bacterial adherence and invasion. Science 243:940–943
    [Google Scholar]
  19. Finlay B. B., Ruschkowski S., Dedhar S. 1991; Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J Cell Sci 99:283–296
    [Google Scholar]
  20. Friebel A., Ilchmann H., Aepfelbacher M., Ehrbar K., Machleidt W., Hardt W. D. 2001; SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem 276:34035–34040
    [Google Scholar]
  21. Frischknecht F., Moreau V., Rottger S., Gonfloni S., Reckmann I., Superti-Furga G., Way M. 1999; Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401:926–929
    [Google Scholar]
  22. Galan J. E., Curtiss R. III 1989; Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86:6383–6387
    [Google Scholar]
  23. Ganeshan R., Nowotarski K., Di A., Nelson D. J., Kirk K. L. 2007; CFTR surface expression and chloride currents are decreased by inhibitors of N-WASP and actin polymerization. Biochim Biophys Acta 1773192–200
    [Google Scholar]
  24. Gerlach R. G., Jackel D., Stecher B., Wagner C., Lupas A., Hardt W. D., Hensel M. 2007; Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol 9:1834–1850
    [Google Scholar]
  25. Ghosh P. 2004; Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68:771–795
    [Google Scholar]
  26. Ginsberg M. H., Partridge A., Shattil S. J. 2005; Integrin regulation. Curr Opin Cell Biol 17:509–516
    [Google Scholar]
  27. Gruenheid S., DeVinney R., Bladt F., Goosney D., Gelkop S., Gish G. D., Pawson T., Finlay B. B. 2001; Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3:856–859
    [Google Scholar]
  28. Gu J., Tamura M., Pankov R., Danen E. H., Takino T., Matsumoto K., Yamada K. M. 1999; Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J Cell Biol 146:389–403
    [Google Scholar]
  29. Hardt W. D., Chen L. M., Schuebel K. E., Bustelo X. R., Galan J. E. 1998; S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93:815–826
    [Google Scholar]
  30. Jiang Z. Y., Chawla A., Bose A., Way M., Czech M. P. 2002; A phosphatidylinositol 3-kinase-independent insulin signaling pathway to N-WASP/Arp2/3/F-actin required for GLUT4 glucose transporter recycling. J Biol Chem 277:509–515
    [Google Scholar]
  31. Kebache S., Zuo D., Chevet E., Larose L. 2002; Modulation of protein translation by Nck-1. Proc Natl Acad Sci U S A 99:5406–5411
    [Google Scholar]
  32. Kebache S., Cardin E., Nguyen D. T., Chevet E., Larose L. 2004; Nck-1 antagonizes the endoplasmic reticulum stress-induced inhibition of translation. J Biol Chem 279:9662–9671
    [Google Scholar]
  33. Kingsley R. A., Santos R. L., Keestra A. M., Adams L. G., Baumler A. J. 2002; Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol 43:895–905
    [Google Scholar]
  34. Kisielow M., Kleiner S., Nagasawa M., Faisal A., Nagamine Y. 2002; Isoform-specific knockdown and expression of adaptor protein ShcA using small interfering RNA. Biochem J 363:1–5
    [Google Scholar]
  35. Latasa C., Roux A., Toledo-Arana A., Ghigo J. M., Gamazo C., Penades J. R., Lasa I. 2005; BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58:1322–1339
    [Google Scholar]
  36. Latreille M., Larose L. 2006; Nck in a complex containing the catalytic subunit of protein phosphatase 1 regulates eukaryotic initiation factor 2 α signaling and cell survival to endoplasmic reticulum stress. J Biol Chem 281:26633–26644
    [Google Scholar]
  37. Lettau M., Qian J., Linkermann A., Latreille M., Larose L., Kabelitz D., Janssen O. 2006; The adaptor protein Nck interacts with Fas ligand: guiding the death factor to the cytotoxic immunological synapse. Proc Natl Acad Sci U S A 103:5911–5916
    [Google Scholar]
  38. Malacombe M., Bader M. F., Gasman S. 2006; Exocytosis in neuroendocrine cells: new tasks for actin. Biochim Biophys Acta 17631175–1183
    [Google Scholar]
  39. Mills D. M., Bajaj V., Lee C. A. 1995; A 40 kb 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
    [Google Scholar]
  40. Nagashima K., Endo A., Ogita H., Kawana A., Yamagishi A., Kitabatake A., Matsuda M., Mochizuki N. 2002; Adaptor protein Crk is required for ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells. Mol Biol Cell 13:4231–4242
    [Google Scholar]
  41. Patel J. C., Galan J. E. 2006; Differential activation and function of Rho GTPases during Salmonella -host cell interactions. J Cell Biol 175:453–463
    [Google Scholar]
  42. Pawson T. 2007; Dynamic control of signaling by modular adaptor proteins. Curr Opin Cell Biol 19:112–116
    [Google Scholar]
  43. Pier G. B., Grout M., Zaidi T., Meluleni G., Mueschenborn S. S., Banting G., Ratcliff R., Evans M. J., Colledge W. H. 1998; Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393:79–82
    [Google Scholar]
  44. Ravichandran K. S. 2001; Signaling via Shc family adapter proteins. Oncogene 20:6322–6330
    [Google Scholar]
  45. Rivera G. M., Antoku S., Gelkop S., Shin N. Y., Hanks S. K., Pawson T., Mayer B. J. 2006; Requirement of Nck adaptors for actin dynamics and cell migration stimulated by platelet-derived growth factor B. Proc Natl Acad Sci U S A 103:9536–9541
    [Google Scholar]
  46. Rohatgi R., Nollau P., Ho H. Y., Kirschner M. W., Mayer B. J. 2001; Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J Biol Chem 276:26448–26452
    [Google Scholar]
  47. Schlumberger M. C., Hardt W. D. 2006; Salmonella type III secretion effectors: pulling the host cell's strings. Curr Opin Microbiol 9:46–54
    [Google Scholar]
  48. Shi J., Casanova J. E. 2006; Invasion of host cells by Salmonella typhimurium requires focal adhesion kinase and p130Cas. Mol Biol Cell 17:4698–4708
    [Google Scholar]
  49. Shi J., Scita G., Casanova J. E. 2005; WAVE2 signaling mediates invasion of polarized epithelial cells by Salmonella typhimurium . J Biol Chem 280:29849–29855
    [Google Scholar]
  50. Soldati T., Schliwa M. 2006; Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol 7:897–908
    [Google Scholar]
  51. Stanasila L., Abuin L., Diviani D., Cotecchia S. 2006; Ezrin directly interacts with the α 1b-adrenergic receptor and plays a role in receptor recycling. J Biol Chem 281:4354–4363
    [Google Scholar]
  52. Stender S., Friebel A., Linder S., Rohde M., Mirold S., Hardt W. D. 2000; Identification of SopE2 from Salmonella typhimurium , a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol 36:1206–1221
    [Google Scholar]
  53. Tanaka M., Gupta R., Mayer B. J. 1995; Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol Cell Biol 15:6829–6837
    [Google Scholar]
  54. Tomasevic N., Jia Z., Russell A., Fujii T., Hartman J. J., Clancy S., Wang M., Beraud C., Wood K. W., Sakowicz R. 2007; Differential regulation of WASP and N-WASP by Cdc42, Rac1, Nck, and PI(4,5)P2. Biochemistry 46:3494–3502
    [Google Scholar]
  55. Unsworth K. E., Way M., McNiven M., Machesky L., Holden D. W. 2004; Analysis of the mechanisms of Salmonella -induced actin assembly during invasion of host cells and intracellular replication. Cell Microbiol 6:1041–1055
    [Google Scholar]
  56. Wray C., Sojka W. J. 1978; Experimental Salmonella typhimurium infection in calves. Res Vet Sci 25:139–143
    [Google Scholar]
  57. Yan Q., Sun W., Kujala P., Lotfi Y., Vida T. A., Bean A. J. 2005; CART: an Hrs/actinin-4/BERP/myosin V protein complex required for efficient receptor recycling. Mol Biol Cell 16:2470–2482
    [Google Scholar]
  58. Zhou D., Chen L. M., Hernandez L., Shears S. B., Galan J. E. 2001; A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 39:248–259
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/008581-0
Loading
/content/journal/micro/10.1099/mic.0.2007/008581-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error