Addressing the effects of Salmonella internalization in host cell signaling on a reverse-phase protein array

Proteomics

Volumn 9, Issue 14, 2009, Pages 3652-3665

  Molero, Cristina ^a   Rodríguez Escudero, Isabel ^a   Alemán, Ainel ^a   Rotger, Rafael ^a   Molina, María ^a   Cid, Víctor J ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Bacterial invasion; Cell signaling; Reverse phase protein array; Salmonella; Type III secretion

Indexed keywords

BACTERIAL PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATASE; PROTEIN KINASE B; PROTEIN SIGD; PROTEIN SOPE E2; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM MUTANT; CELL LYSATE; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVATION; HELA CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTERNALIZATION; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; SALMONELLA; SALMONELLA ENTERICA; SALMONELLOSIS; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; BLOTTING, WESTERN; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HUMANS; INTERLEUKIN-8; MICROSCOPY; MODELS, BIOLOGICAL; MUTATION; PHOSPHORYLATION; PROTEIN ARRAY ANALYSIS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 68049090013     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200800907     Document Type: Article

References (50)

1. Zhang, S., Kingsley, R. A., Santos, R. L., Andrews-Polymenis, H. et al., Molecular pathogenesis of Salmonella enterica serotype typhimurium-induced diarrhea. Infect. Immun. 2003, 71, 1-12.
2. Zhou, D., Galan, J., Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect. 2001, 3, 1293-1298.
3. Steele-Mortimer, O., The Salmonella-containing vacuole: moving with the times. Curr. Opin. Microbiol. 2008, 11, 38-45.
4. Steele-Mortimer, O., Infection of epithelial cells with Salmonella enterica. Methods Mol. Biol. 2008, 431, 201-211.
5. Galan, J. E.,Wolf-Watz, H., Protein delivery into eukaryotic cells by type III secretion machines. Nature 2006, 444, 567-573.
6. Schlumberger, M. C., Hardt, W. D., Salmonella type III secretion effectors: pulling the host cell's strings. Curr. Opin. Microbiol. 2006, 9, 46-54.
7. Patel, J. C., Galan, J. E., Manipulation of the host actin cytoskeleton by Salmonella -all in the name of entry. Curr. Opin. Microbiol. 2005, 8, 10-15.
8. Zhou, D., Chen, L. M., Hernandez, L., Shears, S. B. et al., A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 2001, 39, 248-259.
9. Lin, S. L., Le, T. X., Cowen, D. S., SptP, a Salmonella typhimurium type III-secreted protein, inhibits the mitogen-activated protein kinase pathway by inhibiting Raf activation. Cell Microbiol. 2003, 5, 267-275.
10. Terebiznik, M. R., Vieira, O. V., Marcus, S. L., Slade, A. et al., Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella. Nat. Cell Biol. 2002, 4, 766-773.
11. Drecktrah, D., Knodler, L. A., Steele-Mortimer, O., Modulation and utilization of host cell phosphoinositides by Salmonella spp. Infect. Immun. 2004, 72, 4331-4335.
12. Hernandez, L. D., Hueffer, K., Wenk, M. R., Galan, J. E., Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 2004, 304, 1805-1807.
13. Dukes, J. D., Lee, H., Hagen, R., Reaves, B. J. et al., The secreted Salmonella dublin phosphoinositide phosphatase, SopB, localizes to PtdIns(3)P-containing endosomes and perturbs normal endosome to lysosome trafficking. Biochem. J. 2006, 395, 239-247.
14. Mallo, G. V., Espina, M., Smith, A. C., Terebiznik, M. R. et al., SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34. J. Cell Biol. 2008, 182, 741-752.
15. Steele-Mortimer, O., Knodler, L. A., Marcus, S. L., Scheid, M. P. et al., Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J. Biol. Chem. 2000, 275, 37718-37724.
16. Knodler, L. A., Finlay, B. B., Steele-Mortimer, O., The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J. Biol. Chem. 2005, 280, 9058-9064.
17. Kuijl, C., Savage, N. D., Marsman, M., Tuin, A. W. et al., Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 2007, 450, 725-730.
18. Feng, Y., Wente, S. R., Majerus, P. W., Overexpression of the inositol phosphatase SopB in human 293 cells stimulates cellular chloride influx and inhibits nuclear mRNA export. Proc. Natl. Acad. Sci. USA 2001, 98, 875-879.
19. Bertelsen, L. S., Paesold, G., Marcus, S. L., Finlay, B. B. et al., Modulation of chloride secretory responses and barrier function of intestinal epithelial cells by the Salmonella effector protein SigD. Am. J. Cell Physiol. 2004, 287, C939-C948.
20. Aleman, A., Rodriguez-Escudero, I., Mallo, G. V., Cid, V. J. et al., The amino-terminal non-catalytic region of Salmonella typhimurium SigD affects actin organization in yeast and mammalian cells. Cell Microbiol. 2005, 7, 1432-1446.
21. Rodriguez-Escudero, I., Rotger, R., Cid, V. J., Molina, M., Inhibition of Cdc42-dependent signalling in Saccharomyces cerevisiae by phosphatase-dead SigD/SopB from Salmonella typhimurium. Microbiology 2006, 152, 3437-3452.
22. Rogers, L. D., Kristensen, A. R., Boyle, E. C., Robinson, D. P. et al., Identification of cognate host targets and specific ubiquitylation sites on the Salmonella SPI-1 effector SopB/SigD. J. Proteomics 2008, 71, 97-108.
23. Haab, B. B., Antibody arrays in cancer research. Mol. Cell Proteomics 2005, 4, 377-383.
24. Cho, C. R., Labow, M., Reinhardt, M., van Oostrum, J. et al., The application of systems biology to drug discovery. Curr. Opin. Chem. Biol. 2006, 10, 294-302.
25. Espina, V., Wulfkuhle, J. D., Calvert, V. S., Petricoin, E. F. et al., Reverse phase protein microarrays for monitoring biological responses. Methods Mol. Biol. 2007, 383, 321-336.
26. Spurrier, B., Ramalingam, S., Nishizuka, S., Reverse-phase protein lysate microarrays for cell signaling analysis. Nat. Protoc. 2008, 3, 1796-1808.
27. Kreutzberger, J., Protein microarrays: a chance to study microorganisms? Appl. Microbiol. Biotechnol. 2006, 70, 383-390.
28. Pawlak, M., Schick, E., Bopp, M. A., Schneider, M. J. et al., Zeptosens' protein microarrays: a novel high performance microarray platform for low abundance protein analysis. Proteomics 2002, 2, 383-393.
29. Hoiseth, S. K., Stocker, B. A., Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981, 291, 238-239.
30. Datsenko, K. A., Wanner, B. L., One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 2000, 97, 6640-6645.
31. van Oostrum, J., Calonder, C., Rechsteiner, D., Ehrat, M. et al., Tracing pathway activities with kinase inhibitors and reverse phase protein arrays. Proteomics Clin. Appl. 2009, 3, 412-422.
32. Galan, J. E., Curtiss, R., III, 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, 59, 2901-2908.
33. Mirold, S., Ehrbar, K., Weissmuller, A., Prager, R. et al., Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2. J. Bacteriol. 2001, 183, 2348-2358.
34. Mercurio, F., Zhu, H., Murray, B. W., Shevchenko, A. et al., IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 1997, 278, 860-866.
35. Collier-Hyams, L. S., Zeng, H., Sun, J., Tomlinson, A. D. et al., Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J. Immunol. 2002, 169, 2846-2850.
36. Haraga, A., Miller, S. I., A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol. 2006, 8, 837-846.
37. Hobbie, S., Chen, L. M., Davis, R. J., Galan, J. E., Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J. Immunol. 1997, 159, 5550-5559.
38. Hoffmann, E., Dittrich-Breiholz, O., Holtmann, H., Kracht, M., Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 2002, 72, 847-855.
39. Patel, J. C., Galan, J. E., Differential activation and function of Rho GTPases during Salmonella- host cell interactions. J. Cell Biol. 2006, 175, 453-463.
40. Manning, B. D., Cantley, L. C., AKT/PKB signaling: navigating downstream. Cell 2007, 129, 1261-1274.
41. Burgering, B. M., Kops, G. J., Cell cycle and death control: long live Forkheads. Trends Biochem. Sci. 2002, 27, 352-360.
42. Pace, J., Hayman, M. J., Galan, J. E., Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 1993, 72, 505-514.
43. Chen, L. M., Hobbie, S., Galan, J. E., Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 1996, 274, 2115-2118.
44. Ye, Z., Petrof, E. O., Boone, D., Claud, E. C. et al., Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am. J. Pathol. 2007, 171, 882-892.
45. Jones, R. M., Wu, H., Wentworth, C., Luo, L. et al., Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 2008, 3, 233-244.
46. Huang, F. C., Werne, A., Li, Q., Galyov, E. E. et al., Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica serovar typhimurium infection. Infect. Immun. 2004, 72, 5052-5062.
47. Tang, E. D., Nunez, G., Barr, F. G., Guan, K. L., Negative regulation of the forkhead transcription factor FKHR by Akt. J. Biol. Chem. 1999, 274, 16741-16746.
48. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. et al., Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378, 785-789.
49. Burnham, C. A., Shokoples, S. E., Tyrrell, G. J., Invasion of HeLa cells by group B streptococcus requires the phosphoinositide-3-kinase signalling pathway and modulates phosphorylation of host-cell Akt and glycogen synthase kinase-3. Microbiology 2007, 153, 4240-4252.
50. Duan, Y., Liao, A. P., Kuppireddi, S., Ye, Z. et al., Beta-catenin activity negatively regulates bacteria-induced inflammation. Lab. Invest. 2007, 87, 613-624.