Shiga toxin 1-induced proinflammatory cytokine production is regulated by the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin signaling pathway

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3919-3931

  Cherla, Rama P ^a   Lee, Sang Yun ^a   Mulder, Renée A ^a   Lee, Moo Seung ^a   Tesh, Vernon L ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3 ALPHA BETA; INITIATION FACTOR 4E; INTERLEUKIN 1BETA; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; SERINE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VEROTOXIN 1;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; TRANSLATION INITIATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CALCIUM; CELL LINE, TUMOR; CYTOKINES; ENDOPLASMIC RETICULUM; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SHIGA TOXIN 1; SIGNAL TRANSDUCTION;

EID: 69049120323     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00738-09     Document Type: Article

References (53)

1. Asnaghi, L., P. Bruno, M. Priulla, and A. Nicolin. 2004. mTOR: a protein kinase switching between life and death. Pharmacol. Res. 50:545-549.
2. Berridge, M. J. 1993. Inositol trisphosphate and calcium signalling. Nature 361:315-325.
3. Cameron, P., S. J. Smith, M. A. Giembycz, D. Rotondo, and R. Plevin. 2003. Verotoxin activates mitogen-activated protein kinase in human peripheral blood monocytes: role in apoptosis and proinflammatory cytokine release. Br. J. Pharmacol. 140:1320-1330.
4. Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296:1655-1657.
5. Cherla, R. P., S.-Y. Lee, P. L. Mees, and V. L. Tesh. 2006. Shiga toxin 1-induced cytokine production is mediated by MAP kinase pathways and translation initiation factor eIF4E in the macrophage-like THP-1 cell line. J. Leukoc. Biol. 79:397-407.
6. Clapham, D. E. 2007. Calcium signaling. Cell 131:1047-1058.
7. Coller, J., and R. Parker. 2004. Eukaryotic mRNA decapping. Annu. Rev. Biochem. 73:861-890.
8. Coller, J., and R. Parker. 2005. General translational repression by activators of mRNA decapping. Cell 122:875-886.
9. Colpoys, W. E., B. H. Cochran, T. M. Carducci, and C. M. Thorpe. 2004. Shiga toxins activate translational regulation pathways in intestinal epithelial cells. Cell. Signal. 17:891-899.
10. Cross, D. A., D. R. Alessi, P. Cohen, M. Andjelkovich, and B. A. Hemmings. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
11. Endo, Y., K. Tsurugi, T. Yutsudo, Y. Takeda, Y. Ogasawara, and K. Igarashi. 1988. Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur. J. Biochem. 171:45-50.
12. Foster, G. H., C. S. Armstrong, R. Sakiri, and V. L. Tesh. 2000. Shiga toxin-induced tumor necrosis factor alpha expression: requirement for toxin enzymatic activity and monocyte protein kinase C and protein tyrosine kinases. Infect. Immun. 68:5183-5189.
13. Franke, T. F., D. R. Kaplan, L. C. Cantley, and A. Toker. 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4- bisphosphate. Science 275:665-668.
14. Garneau, N. L., J. Wilusz, and C. J. Wilusz. 2007. The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8:113-126.
15. Gingras, A.-C., S. G. Kennedy, M. A. O'Leary, N. Sonenberg, and N. Hay. 1998. 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt (PKB) signaling pathway. Genes Dev. 12:502-513.
16. Gingras, A.-C., B. Raught, S. P. Gygi, A. Niedzwiecka, M. Miron, S. K. Burley, R. D. Polakiewicz, A. Wyslouch-Cieszynska, R. Aebersold, and N. Sonenberg. 2001. Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev. 15:2852-2864.
17. Gingras, A.-C., B. Raught, and N. Sonenberg. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913-963.
18. Guha, M., and N. Mackman. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277:32124-32132.
19. Harrison, L. M., C. van den Hoogen, W. C. E. van Haaften, and V. L. Tesh. 2005. Chemokine expression in the monocytic cell line THP-1 in response to purified Shiga toxin 1 and/or lipopolysaccharides. Infect. Immun. 73:403-412.
20. Harrison, L. M., W. C. E. van Haaften, and V. L. Tesh. 2004. Regulation of proinflammatory cytokine expression by Shiga toxin 1 and/or lipopolysaccharides in the human monocytic cell line THP-1. Infect. Immun. 72:2618-2627.
21. 473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes. J. Biol. Chem. 280:40406-40416.
22. Kabbara, A. A., and D. G. Allen. 2001. The use of the indicator fluo-5N to measure sarcoplasmic reticulum calcium in single muscle fibers of the cane toad. J. Physiol. 534:87-97.
23. Keepers, T. R., L. K. Gross, and T. G. Obrig. 2007. Monocyte chemoattractant protein 1, macrophage inflammatory protein 1α, and RANTES recruit macrophages to the kidney in a mouse model of hemolytic-uremic syndrome. Infect. Immun. 75:1229-1236.
24. Kidd, L. B., G. A. Schabbauer, J. P. Luyendyk, T. D. Holscher, R. E. Tilley, M. Tencati, and N. Mackman. 2008. Insulin activation of the phosphatidylinositol 3-kinase/protein kinase B (Akt) pathway reduces lipopolysaccharide-induced inflammation in mice. J. Pharmacol. Exp. Ther. 326:348-353.
25. Kyriakis, J. M., and J. Avruch. 1996. Sounding the alarm: protein kinase cascades activated by stress and inflammation. J. Biol. Chem. 271:24313-24316.
26. Lee, J. S., W. M. Nauseef, A. Moeenrezakhanlou, L. M. Sly, S. Noubir, K. G. Leidal, J. M. Schlomann, G. Krystal, and N. E. Reiner. 2007. Monocyte p110alpha phosphatidylinositol 3-kinase regulates phagocytosis, the phagocyte oxidase, and cytokine production. J. Leukoc. Biol. 81:1548-1561.
27. Lee, S.-Y., M.-S. Lee, R. P. Cherla, and V. L. Tesh. 2008. Shiga toxin 1 induces apoptosis through the endoplasmic reticulum stress response in human monocytic cells. Cell. Microbiol. 10:770-780.
28. Lingwood, C. A. 2003. Shiga toxin receptor glycolipid binding. Pathology and utility. Methods Mol. Med. 73:165-186.
29. Luyendyk, J. P., G. A. Schabbauer, M. Tencati, T. Holscher, R. Pawlinski, and N. Mackman. 2008. Genetic analysis of the role of the PI3K-Akt pathway in lipopolysaccharide-induced cytokine and tissue factor gene expression in monocytes/macrophages. J. Immunol. 180:4218-4226.
30. Mamane, Y., E. Petroulakis, L. Rong, K. Yoshida, L. W. Ler, and N. Sonenberg. 2004. eIF4E - from translation to transformation. Oncogene 23:3172-3179.
31. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6:777-784.
32. Ohmura, M., S. Yamasaki, H. Kurazono, K. Kashiwagi, K. Igarashi, and Y. Takeda. 1993. Characterization of non-toxic mutant toxins of Vero toxin 1 that were constructed by replacing amino acids in the A subunit. Microb. Pathog. 15:169-176.
33. 2+ movements and equilibration. EMBO J. 19:5729-5739.
34. Ramegowda, B., and V. L. Tesh. 1996. Differentiation-associated toxin receptor modulation, cytokine production and sensitivity to Shiga-like toxins in human monocytes and monocytic cell lines. Infect. Immun. 64:1173-1180.
35. Ramegowda, B., J. E. Samuel, and V. L. Tesh. 1999. Interaction of Shiga toxins with human brain microvascular endothelial cells: cytokines as sensitizing agents. J. Infect. Dis. 180:1205-1213.
36. Reddy, S. A. G., J. H. Huang, and W. S.-L. Liao. 2000. Phosphatidylinositol 3-kinase as a mediator of TNF-induced activation of NF-κB. J. Immunol. 164:1355-1363.
37. Richter, J. D., and N. Sonenberg. 2005. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433:477-480.
38. Sakiri, R., B. Ramegowda, and V. L. Tesh. 1998. Shiga toxin type 1 activates tumor necrosis factor-α gene transcription and nuclear translocation of the transcriptional activators nuclear factor-κB and activator protein-1. Blood 92:558-566.
39. Sandvig, K., and B. van Deurs. 2002. Transport of protein toxins into cells: pathways used by ricin, cholera toxin and Shiga toxin. FEBS Lett. 529:49-53.
40. Sarbassov, D. D., D. A. Guertin, S. M. Ali, and D. M. Sabatini. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098-1101.
41. Saxena, S. K., A. D. O'Brien, and E. J. Ackerman. 1989. Shiga toxin, Shiga-like toxin II variant, and ricin are all single-site RNA N-glycosidases of 28S RNA when microinjected into Xenopus oocytes. J. Biol. Chem. 264:596-601.
42. Schaeffer, H. J., and M. J. Weber. 1999. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol. 19:2435-2444.
43. Shaw, R. J., and L. C. Cantley. 2006. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 441:424-430.
44. Stricklett, P. K., A. K. Hughes, Z. Ergonul, and D. E. Kohan. 2002. Molecular basis for up-regulation by inflammatory cytokines of Shiga toxin 1 cytotoxicity and globotriaosylceramide expression. J. Infect. Dis. 186:976-982.
45. Tarr, P. I., C. A. Gordon, and W. I. Chandler. 2005. Shiga toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365:1073-1086.
46. Taylor, F. B., Jr., V. L. Tesh, L. DeBault, A. Li, A. C. K. Chang, S. D. Kosanke, T. J. Pysher, and R. L. Siegler. 1999. Characterization of the baboon responses to Shiga-like toxin: descriptive study of a new primate model of toxic responses to Stx-1. Am. J. Pathol. 154:1285-1299.
47. Tesh, V. L., J. A. Burris, J. W. Owens, V. M. Gordon, E. A. Wadolkowski, A. D. O'Brien, and J. E. Samuel. 1993. Comparison of the relative toxicities of Shiga-like toxins type I and type II for mice. Infect. Immun. 61:3392-3402.
48. Thomas, K. W., M. M. Monack, J. M. Stabler, T. Yarovinsky, A. B. Carter, and G. W. Hunninghake. 2002. Respiratory syncytial virus inhibits apoptosis and induces NF-κB activity through a phosphatidylinositol 3-kinase-dependent pathway. J. Biol. Chem. 277:492-501.
49. Thorpe, C. M., W. E. Smith, B. P. Hurley, and D. W. K. Acheson. 2001. Shiga toxins induce, superinduce, and stabilize a variety of C-X-C chemokine mRNAs in intestinal epithelial cells, resulting in increased chemokine expression. Infect. Immun. 69:6140-6147.
50. van de Kar, N. C. A. J., L. A. H. Monnens, M. A. Karmali, and V. W. M. van Hinsbergh. 1992. Tumor necrosis factor and interleukin 1 induce expression of the verocytotoxin receptor globotriaosylceramide on human endothelial cells: implications for the pathogenesis of the hemolytic uremic syndrome. Blood 80:2755-2764.
51. van Setten, P. A., L. A. H. Monnens, R. G. G. Verstraten, L. P. W. J. van den Heuvel, and V. W. M. van Hinsbergh. 1996. Effects of verocytotoxin-1 on nonadherent monocytes: binding characteristics, protein synthesis inhibition, and induction of cytokine release. Blood 88:174-183.
52. von Manteuffel, S. R., A.-C. Gingras, X. F. Ming, N. Sonenberg, and G. Thomas. 1996. 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 93:4076-4080.
53. Zoja, C., S. Angioletti, R. Donadelli, C. Zanchi, S. Tomasoni, E. Binda, B. Imberti, M. te Loo, L. Monnens, G. Remuzzi, and M. Morigi. 2002. Shiga toxin-2 triggers endothelial leukocyte adhesion and transmigration via NF-κB dependent up-regulation of IL-8 and MCP-1. Kidney Int. 62:846-856.