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

Volumn 153, Issue 12, 2007, Pages 4240-4252

  Burnham, Carey Ann D ^a   Shokoples, Sandra E ^b   Tyrrell, Gregory J ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b PROVINCIAL LABORATORY FOR PUBLIC HEALTH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 6 HYDROXYMETHYLCHIRO INOSITOL 2,2 O METHYL 3 O OCTADECYLCARBONATE; CAMPTOTHECIN; CASPASE 3; GLYCOGEN SYNTHASE KINASE 3; MANUMYCIN; MANUMYCIN A; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; PROTEIN P110; PROTEIN P110ALPHA; PROTEIN P85; PROTEIN P85ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL INVASION; CELL SURVIVAL; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE INACTIVATION; HELA CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS INFECTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; BACTERIAL ADHESION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASES; HELA CELLS; HUMANS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STREPTOCOCCUS AGALACTIAE;

BACTERIA (MICROORGANISMS); EUKARYOTA; STREPTOCOCCUS SP. 'GROUP B';

EID: 37449032424     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2007/008417-0     Document Type: Article

References (51)

1. Bollag, D. M. & Edelstein, S. J. (1991). Protein Methods. New York: Wiley-Liss.
2. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
3. Burnham, C. A., Shokoples, S. E. & Tyrrell, G. J. (2007). Rac1, RhoA, and Cdc42 participate in HeLa cell invasion by group B streptococcus. FEMS Microbiol Lett 272, 8-14.
4. Chan, T. O., Rittenhouse, S. E. & Tsichlis, P. N. (1999). AKT/ PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu Rev Biochem 68, 965-1014.
5. Chan, T. O., Rodeck, U., Chan, A. M., Kimmelman, A. C., Rittenhouse, S. E., Panayotou, G. & Tsichlis, P. N. (2002). Small GTPases and tyrosine kinases coregulate a molecular switch in the phosphoinositide 3-kinase regulatory subunit. Cancer Cell 1, 181-191.
6. Chou, M. M., Hou, W., Johnson, J., Graham, L. K., Lee, M. H., Chen, C. S., Newton, A. C., Schaffhausen, B. S. & Taker, A. (1998). Regulation of protein kinase C ζ by PI 3-kinase and PDK-1. Curr Biol 8, 1069-1077.
7. Coombes, B. K. & Mahony, J. B. (2002). Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells. Cell Microbiol 4, 447-460.
8. Cox, D., Tseng, C. C., Bjekic, G. & Greenberg, S. (1999). A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J Biol Chem 274, 1240-1247.
9. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. & Hemmings, B. A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
10. Datta, S. R., Brunet, A. & Greenberg, M. E. (1999). Cellular survival: a play in three Akts. Genes Dev 13, 2905-2927.
11. Davies, S. P., Reddy, H., Calvano, M. & Cohen, P. (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351, 95-105.
12. Embi, N., Rylatt, D. B. & Cohen, P. (1980). Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur J Biochem 107, 519-527.
13. Farley, M. M., Harvey, R. C., Stull, T., Smith, J. D., Schuchat, A, Wenger, J. D. & Stephens, D. S. (1993). A population-based assessment of invasive disease due to group B streptococcus in nonpregnant adults. N Engl J Med 328, 1807-1811.
14. Finlay, B. B. & Cossart, P. (1997). Exploitation of mammalian host cell functions by bacterial pathogens. Science 276, 718-725.
15. Gibson, R. L., Lee, M. K, Soderland, C., Chi, E. Y. & Rubens, C. E. (1993). Group B streptococci invade endothelial cells: type III capsular polysaccharide attenuates invasion. Infect Immun 61, 478-485.
16. Greco, R., De, M. L., Donnarumma, G., Conte, M. P., Seganti, L. & Valenti, P. (1995). Invasion of cultured human cells by Streptococcus pyogenes. Res Microbiol 146, 551-560.
17. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
18. Hiromura, M., Okada, F., Obata, T., Auguin, D., Shibata, T., Rournestand, C. & Noguchi, M. (2004). Inhibition of Akt kinase activity by a peptide spanning the βA strand of the proto-oncogene TCL1. J Biol Chem 279, 53407-53418.
19. Hu, Y., Qiao, L., Wang, S., Rong, S. B., Meuillet, E. J, Berggren, M., Gallegos, A., Powis, G. & Kozikowski, A. P. (2000). 3-(Hydroxymethyl)-bearing phosphatidylinositol ether lipid analogues and carbonate surrogates block PI3-K, Akt, and cancer cell growth. J Med Chem 43, 3045-3051.
20. Ireton, K., Payrastre, B. & Cossart, P. (1999). The Listeria monocytogenes protein InlB is an agonist of mammalian phosphoinositide 3-kinase. J Biol Chem 274, 17025-17032.
21. Knodler, L. A., Finlay, B. B. & Steele-Mortimer, O. (2005). The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 280, 9058-9064.
22. Kwok, T., Backert, S., Schwarz, H., Berger, J. & Meyer, T. F. (2002). Specific entry of Helicobacter pylori into cultured gastric epithelial cells via a zipper-like mechanism. Infect Immun 70, 2108-2120.
23. Lalonde, M., Segura, M., Lacouture, S. & Gottschalk M. (2000). Interactions between Streptococcus suis serotype 2 and different epithelial cell lines. Microbiology 146, 1913-1921.
24. Nizet, V., Kim, K. S., Stins, M., Jonas, M., Chi, E. Y., Nguyen, D. & Rubens, C. E. (1997). Invasion of brain microvascular endothelial cells by group B streptococci. Infect Immun 65, 5074-5081.
25. Pap, M. & Cooper, G. M. (1998). Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273, 19929-19932.
26. Pizarro-Cerda, J. & Cossart, P. (2004). Subversion of phosphoinositide metabolism by intracellular bacterial pathogens. Nat Cell Biol 6, 1026-1033.
27. Purushothaman, S. S., Wang, B. & Cleary, P. P. (2003). M1 protein triggers a phosphoinositide cascade for group A Streptococcus invasion of epithelial cells. Infect Immun 71, 5823-5830.
28. Reuther, G. W. & Der, C. J. (2000). The Ras branch of small GTPases: Ras family members don't fall far from the tree. Curr Gpin Cell Biol 12, 157-165.
29. Rubens, C. E., Smith, S., Hulse, M., Chi, E. Y. & van Belle, G. (1992). Respiratory epithelial cell invasion by group B streptococci. Infect Immun 60, 5157-5163.
30. Sattler, I., Thiericke, R. & Zeeck, A. (1998). The Manumycin-group metabolites. Nat Prod Rep 15, 221-240.
31. Schuchat, A. (1998). Epidemiology of group B streptococcal disease in the United States: shifting paradigms. Clin Microbiol Rev 11, 497-513.
32. Schuchat, A., Oxtoby, M., Cochl, S., Sikes, R. K., Hightower, A., Plikaytis, B. & Broome, C. V. (1990). Population-based risk factors for neonatal group B streptococcal disease: results of a cohort study in metropolitan Atlanta. J Infect Dis 162, 672-677.
33. Schuchat, A., Robinson, K., Wenger, J. D., Harrison, L. H., Farley, M., Reingold, A. L., Lefkowitz, L. & Perkins, B. A. (1997). Bacterial meningitis in the United States in 1995. N Engl J Med 337, 970-976.
34. Segura, M., Gottschalk, M. & Olivier, M. (2004). Encapsulated Streptococcus suis inhibits activation of signaling pathways involved in phagocytosis. Infect Immun 72, 5322-5330.
35. Shin, S. & Kim, K. S. (2006). RhoA and Rac1 contribute to type III group B streptococcal. invasion of human brain microvascular endothelial cells. Biochem Biophys Res Commun 345, 538-542.
36. Shin, S., Maneesh, P. S., Lee, J. S., Romer, L. H. & Kim, K. S. (2006). Focal adhesion kinase is involved in type III group B streptococcal invasion of human brain microvascular endothelial cells. Microb Pathog 41, 168-173.
37. Stokoe, D. (2005). The phosphoinositide 3-kinase pathway and cancer. Expert Rev Mol Med 7, 1-22.
38. Tafazoli, F., Magnusson, K. E. & Zheng, L. (2003). Disruption of epithelial barrier integrity by Salmonella enterica serovar Typhimurium requires geranylgeranylated proteins. Infect Immun 71, 872-881.
39. Takenawa, T. & Itoh, T. (2001). Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim Biophys Acta 1533, 190-206.
40. Tamura, G. S., Kuypers, J. M., Smith, S., Raff, H. & Rubens, C. E. (1994). Adherence of group B streptococci to cultured epithelial cells: roles of environmental factors and bacterial surface components. Infect Immun 62, 2450-2458.
41. Tapon, N. & Hall, A. (1997). Rho, Rac and Cdc42 GTPases regulate the organization of the actin cytoskeleton. Curr Opin Cell Biol 9, 86-92.
42. Taylor, S. J. & Shalloway, D. (1996). Cell cycle-dependent activation of Ras. Curr Biol 6, 1621-1627.
43. Tyrrell, G. J., Senzilet, L. D., Spika, J. S., Kertesz, D. A., Alagaratnam, M., Lovgren, M. & Talbot, J. A. (2000). Invasive disease due to group B streptococcal infection in adults: results from a Canadian, population-based, active laboratory surveillance study - 1996. J Infect Dis 182, 168-173.
44. Tyrrell, G. J., Kennedy, A., Shokoples, S. E. & Sherburne, R. K. (2002). Binding and invasion of HeLa and MRC-5 cells by Streptococcus agalactiae. Microbiology 148, 3921-3931.
45. Ulett, G. C., Maclean, K. H., Nekkalapu, S., Cleveland, J. L. & Adderson, E. E. (2005). Mechanisms of group B streptococcal-induced apoptosis of murine macrophages. J Immunol 175, 2555-2562.
46. Valentin-Weigand, P., Benkel, P., Rohde, M. & Chhatwal, G. S. (1996). Entry and intracellular survival of group B streptococci in J774 macrophages. Infect Immun 64, 2467-2473.
47. Valentin-Weigand, P., Jungnitz, H., Zock, A., Rohde, M. & Chhatwal, G. S. (1997). Characterization of group B streptococcal invasion in HEp-2 epithelial cells. FEMS Microbiol Lett 147, 69-74.
48. Vanhaesebroeck B. & Alessi, D. R. (2000). The PI3K-PDK1 connection: more than just a road to PKB. Biochem J 346, 561-576.
49. Vlahos, C. J., Matter, W. F., Hui, K. Y. & Brown, R. F. (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269, 5241-5248.
50. Wang, B., Lim, D. J., Han, J., Kim, Y. S., Basbaum, C. B. & Li, J. D. (2002). Novel cytoplasmic proteins of nontypeable Haemophilus influenzae up-regulate human MUC5AC mucin transcription via a positive p38 mitogen-activated protein kinase pathway and a negative phosphoinositide 3-kinase-Akt pathway. J Biol Chem 277, 949-957.
51. Yang, L., Dan, H. C., Sun, M., Liu, Q., Sun, X. M., Feldman, R. I., Hamilton, A. D., Polokoff, M., Nicosia, S. V. & other authors (2004). Akt/protein kinase B signaling inhibitor-2, a selective small molecule inhibitor of Akt signaling with antitumor activity in cancer cells overexpressing Akt. Cancer Res 64, 4394-4399.