Helicobacter pylori promotes eukaryotic protein translation by activating phosphatidylinositol 3 kinase/mTOR

International Journal of Biochemistry and Cell Biology

Volumn 55, Issue , 2014, Pages 157-163

  Sokolova, Olga ^a   Vieth, Michael ^b   Gnad, Thorsten ^a,c   Bozko, Przemyslaw M ^a,d   Naumann, Michael ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b INSTITUTE OF PATHOLOGY   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

eIF4; H. pylori; mTOR; Protein synthesis; S6 ribosomal protein

Indexed keywords

CAGA PROTEIN; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; METHIONINE TRANSFER RNA; OUTER MEMBRANE PROTEIN; PEPTIDOGLYCAN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN S6; EEF2K PROTEIN, HUMAN; EIF4EBP1 PROTEIN, HUMAN; ELONGATION FACTOR 2 KINASE; MTOR PROTEIN, HUMAN; PHOSPHOPROTEIN; S6 KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SOMATOMEDIN C RECEPTOR; TARGET OF RAPAMYCIN KINASE;

ADULT; AGED; ARTICLE; AUTOPHAGY; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL TRANSLOCATION; CELL ENERGY; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; FEMALE; GASTRITIS; GLYCOLYSIS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; STOMACH ADENOCARCINOMA; STOMACH ADENOMA; STOMACH BIOPSY; STOMACH CARCINOMA; TRANSLATION INITIATION; TRANSLATION REGULATION; TYPE IV SECRETION SYSTEM; WESTERN BLOTTING; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE; VERY ELDERLY; YOUNG ADULT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT; AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; CELL LINE, TUMOR; ELONGATION FACTOR 2 KINASE; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-4E; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; MIDDLE AGED; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, IGF TYPE 1; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; YOUNG ADULT;

EID: 84907463651     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2014.08.023     Document Type: Article

References (39)

1. D. Allred, J. Harvey, M. Berardo, and G.M. Clark Prognostic and predictive factors in breast cancer by immunohistochemical analysis Mod Pathol 11 1998 155 168
2. K. Almhanna, J. Strosberg, and M. Malafa Targeting AKT protein kinase in gastric cancer Anticancer Res 31 2011 4387 4392
3. J. Averous, and C.G. Proud When translation meets transformation: the mTOR story Oncogene 25 2006 6423 6435
4. S. Backert, E. Ziska, V. Brinkmann, U. Zimny-Arndt, A. Fauconnier, and P.R. Jungblut Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus Cell Microbiol 2 2000 155 164
5. G.J. Brunn, J. Williams, C. Sabers, G. Wiederrecht, J.C. Lawrence Jr., and R.T. Abraham Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002 EMBO J. 15 1996 5256 5267
6. Y. Churin, L. Al-Ghoul, O. Kepp, T.F. Meyer, W. Birchmeier, and M. Naumann Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response J Cell Biol 161 2003 249 255
7. J. Cicenas The potential role of Akt phosphorylation in human cancers Int J Biol Markers 23 2008 1 9
8. C. Cinti, C. Vindigni, A. Zamparelli, D. La Sala, M.C. Epistolato, and D. Marrelli Activated Akt as an indicator of prognosis in gastric cancer Virchows Arch 453 2008 449 455
9. M. Clemens Protein kinases that phosphorylate eIF2 and eIF2B, their role in eukaryotic cell translational control J. Hershey, M. Mathews, N. Sonenberg, Translational control 1996 Cold Spring Harbor Laboratory Press Cold Spring Harbor 139 172
10. S.R. Datta, A. Brunet, and M.E. Greenberg Cellular survival: a play in three Akts Genes Dev 13 1999 2905 2927
11. M. Dixon, R. Genta, J. Yardley, and P. Correa Classification of grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994 Am J Surg Pathol 20 1996 1161 1181
12. N.V. Dorrello, A. Peschiaroli, D. Guardavaccaro, N.H. Colburn, N.E. Sherman, and M. Pagano S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth Science 314 2006 467 471
13. Y. Du, K. Danjo, P.A. Robinson, and J.E. Crabtree In-Cell Western analysis of Helicobacter pylori-induced phosphorylation of extracellular-signal related kinase via the transactivation of the epidermal growth factor receptor Microbes Infect 9 2007 838 846
14. J.R. Graff, and S.G. Zimmer Translational control and metastatic progression: enhanced activity of the mRNA cap-binding protein eIF-4E selectively enhances translation of metastasis-related mRNAs Clin Exp Metastasis 20 2003 265 273
15. B.A. Hemmings, and D.F. Restuccia PI3K-PKB/Akt pathway Cold Spring Harb Perspect Biol 4 2012 a011189
16. I. Hers, E.E. Vincent, and J.M. Tavaré Akt signalling in health and disease Cell Signal 23 2011 1515 1527
17. M.K. Holz, B.A. Ballif, S.P. Gygi, and J. Blenis mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events Cell 123 2005 569 580
18. B.A. Liu, B.W. Engelmann, and P.D. Nash The language of SH2 domain interactions defines phosphotyrosine-mediated signal transduction FEBS Lett 586 2012 2597 2605
19. L. Ma, Z. Chen, H. Erdjument-Bromage, P. Tempst, and P.P. Pandolfi Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis Cell 121 2005 179 193
20. Y. Mamane, E. Petroulakis, O. LeBacquer, and N. Sonenberg mTOR, translation initiation and cancer Oncogene 25 2006 6416 6422
21. B.D. Manning, and L.C. Cantley AKT/PKB signalling: navigating downstream Cell 129 2007 1261 1274
22. S. Martin, B. Saha, and J.L. Riley The battle over mTOR: an emerging theatre in host-pathogen immunity PLoS Pathog 8 2012 e1002894
23. P. Michl, and J. Downward Mechanisms of disease: PI3K/AKT signalling in gastrointestinal cancers Z Gastroenterol 43 2005 1133 1139
24. T.A. Nagy, M.R. Frey, F. Yan, D.A. Israel, D.B. Polk, and R.M. Peek Jr. Helicobacter pylori regulates cellular migration and apoptosis by activation of phosphatidylinositol 3-kinase signalling J Infect Dis 199 2009 641 651
25. B.T. Navé, M. Ouwens, D.J. Withers, D.R. Alessi, and P.R. Shepherd Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation Biochem J 344 Pt 2 1999 427 431
26. R.M.jr Peek, and J.E. Crabtree Helicobacter infection and gastric neoplasia J Pathol 208 2006 233 248
27. T. Pomorski, T.F. Meyer, and M. Naumann Helicobacter pylori-induced prostaglandin E(2) synthesis involves activation of cytosolic phospholipase A(2) in epithelial cells J Biol Chem 276 2001 804 810
28. W. Remmele, and H. Stegner Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue Pathology 8 1987 138 140
29. I. Ruvinsky, and O. Meyuhas Ribosomal protein S6 phosphorylation: from protein synthesis to cell size Trends Biochem Sci 31 2006 342 348
30. J.D. Richter, and N. Sonenberg Regulation of cap-dependent translation by eIF4E inhibitory proteins Nature 433 2005 477 480
31. C. Rieke, T. Kähne, K. Schweitzer, B. Schraven, J. Wienands, and M. Engelke Non-T cell activation linker regulates ERK activation in Helicobacter pylori-infected epithelial cells Cell Signal 22 2010 395 403
32. R.J. Schneider, and N. Sonenberg Translational control in cancer development and progression M. Mathews, N. Sonenberg, J. Hershey, Translational control in biology and medicine 2007 Cold Spring Harbor Laboratory Press Cold Spring Harbor 401 431
33. O. Sokolova, P.M. Bozko, and M. Naumann Helicobacter pylori suppresses glycogen synthase kinase 3beta to promote beta-catenin activity J Biol Chem 283 2008 29367 29374
34. O. Sokolova, M. Vieth, and M. Naumann Protein kinase C isozymes regulate matrix metalloproteinase-1 expression and cell invasion in Helicobacter pylori infection Gut 62 2013 358 367
35. F.H. Tabassam, D.Y. Graham, and Y. Yamaoka Helicobacter pylori activate epidermal growth factor receptor- and phosphatidylinositol 3-OH kinase-dependent Akt and glycogen synthase kinase 3beta phosphorylation Cell Microbiol 11 2009 70 82
36. T.N. Tran, K. Brettingham-Moore, C.P. Duong, C. Mitchell, N.J. Clemons, and W.A. Phillips Molecular changes in the phosphatidylinositide 3-kinase (PI3K) pathway are common in gastric cancer J Surg Oncol 108 2013 113 120
37. F.H. Tabassam, D.Y. Graham, and Y. Yamaoka OipA plays a role in Helicobacter pylori-induced focal adhesion kinase activation and cytoskeletal re-organization Cell Microbiol 10 2008 1008 1020
38. G. von Hoven, N. Kloft, C. Neukirch, S. Ebinger, W. Bobkiewicz, and S. Weis Modulation of translation and induction of autophagy by bacterial exoproducts Med Microbiol Immunol 201 2012 409 418
39. H.Y. Zhou, and A.S. Wong Activation of p70S6K induces expression of matrix metalloproteinase 9 associated with hepatocyte growth factor-mediated invasion in human ovarian cancer cells Endocrinology 147 2006 2557 2566