Cytoprotective roles of ERK and Akt in endoplasmic reticulum stress triggered by subtilase cytotoxin

Biochemical and Biophysical Research Communications

Volumn 410, Issue 4, 2011, Pages 852-858

  Tian, Tian ^a   Zhao, Yang ^a   Nakajima, Shotaro ^a   Huang, Tao ^a   Yao, Jian ^a   Paton, Adrienne W ^b   Paton, James C ^b   Kitamura, Masanori ^a  

^a UNIVERSITY OF YAMANASHI   (Japan)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Akt; Apoptosis; Endoplasmic reticulum stress; Extracellular signal regulated kinase (ERK); Subtilase cytotoxin; Unfolded protein response (UPR)

Indexed keywords

CYTOTOXIN; INITIATION FACTOR 2ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SUBTILASE CYTOTOXIN; UNCLASSIFIED DRUG; VEROTOXIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; CELL LINE; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ESCHERICHIA COLI PROTEINS; EUKARYOTIC INITIATION FACTOR-2; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; STRESS, PHYSIOLOGICAL; SUBTILISINS;

ESCHERICHIA COLI; EUKARYOTA;

EID: 79960318824     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2011.06.078     Document Type: Article

References (39)

1. Paton J.C., Paton A.W. Pathogenesis and diagnosis of shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 1998, 11:450-479.
2. Fan E., Merritt E.A., Verline C.L., Hol W.G. AB5 toxins: structures and inhibitor design. Curr. Opin. Struct. Biol. 2000, 10:680-686.
3. Paton A.W., Srimanote P., Talbot U.M., Wang H., Paton J.C. A new family of potent AB5 cytotoxins produced by Shiga toxigenic Escherichia coli. J. Exp. Med. 2004, 200:35-46.
4. Paton A.W., Paton J.C. Multiplex PCR for direct detection of Shiga toxigenic Escherichia coli producing the novel subtilase cytotoxin. J. Clin. Microbiol. 2005, 43:2944-2947.
5. Byres E., Paton A.W., Paton J.C., Löfling J.C., Smith D.F., Wilce M.C.J., Talbot U.M., Chong D.C., Yu H., Huang S., Chen X., Varki N.M., Varki A., Rossjohn J., Beddoe T. Incorporation of a non-human glycan mediates human susceptibility to a bacterial toxin. Nature 2008, 456:648-652.
6. Paton A.W., Beddoe T., Thorpe C.M., Whisstock J.C., Wilce M.C., Rossjohn J., Talbot U.M., Paton J.C. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 2006, 443:548-552.
7. Matsuura G., Morinaga N., Yahiro K., Komine R., Moss J., Yoshida H., Noda M. Novel subtilase cytotoxin produced by Shiga-toxigenic Escherichia coli induces apoptosis in vero cells via mitochondrial membrane damage. Infect. Immun. 2009, 77:2919-2924.
8. Yahiro K., Morinaga N., Moss J., Noda M. Subtilase cytotoxin induces apoptosis in HeLa cells by mitochondrial permeabilization via activation of Bax/Bak, independent of C/EBP-homologue protein (CHOP), Ire1α or JNK signaling. Microb. Pathogen. 2010, 49:153-163.
9. Wang H., Paton J.C., Paton A.W. Pathologic changes in mice induced by subtilase cytotoxin, a potent new Escherichia coli AB5 toxin that targets the endoplasmic reticulum. J. Infect. Dis. 2007, 196:1093-1101.
10. May K.L., Paton J.C., Paton A.W. Escherichia coli subtilase cytotoxin induces apoptosis regulated by host Bcl-2 family proteins, Bax/Bak. Infect. Immun. 2010, 78:4691-4696.
11. Kim E.K., Choi E.J. Pathological roles of MAPK signaling pathways in human diseases. Biochim. Biophys. Acta 2010, 1802:396-405.
12. Foster G.H., Tesh V.L. Shiga toxin 1-induced activation of c-Jun NH2-terminal kinase and p38 in the human monocytic cell line THP-1: possible involvement in the production of TNF-α. J. Leukocyte Biol. 2002, 71:107-114.
13. Saenz J.B., Li J., Haslam D.B. The MAP kinase-activated protein kinase 2 (MK2) contributes to the Shiga toxin-induced inflammatory response. Cell. Microbiol. 2010, 12:516-529.
14. Stricklett P.K., Hughes A.K., Kohan D.E. Inhibition of p38 mitogen-activated protein kinase ameliorates cytokine up-regulated shigatoxin-1 toxicity in human brain microvascular endothelial cells. J. Infect. Dis. 2005, 191:461-471.
15. Fu X.J., Iijima K., Nozu K., Hamahira K., Tanaka R., Oda T., Yoshikawa N., Matsuo M. Role of p38 MAP kinase pathway in a toxin-induced model of hemolytic uremic syndrome. Pediatr. Nephrol. 2004, 19:844-852.
16. Grewal S.S., York R.D., Stork P.J. Extracellular signal-regulated kinase signalling in neurons. Curr. Opin. Neurobiol. 1999, 9:544-553.
17. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
18. Yamazaki H., Hiramatsu N., Hayakawa K., Tagawa Y., Okamura M., Ogata R., Huang T., Nakajima S., Yao J., Paton A.W., Paton J.C., Kitamura M. Activation of the Akt-NF-κB pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response. J. Immunol. 2009, 183:1480-1487.
19. Kennedy S.G., Wagner A.J., Conzen S.D., Jordán J., Bellacosa A., Tsichlis P.N., Hay H. The PI3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 1997, 11:701-713.
20. Wolfson J.J., May K.L., Thorpe C.M., Jandhyala D.M., C Paton J., Paton A.W. Subtilase cytotoxin activates PERK, IRE1 and ATF6 endoplasmic reticulum stress-signalling pathways. Cell. Microbiol. 2008, 10:1775-1786.
21. Harding H.P., Zhang Y., Bertolotti A., Zeng H., Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 2000, 5:897-904.
22. Boyce M., Bryant K.F., Jousse C., Long K., Harding H.P., Scheuner D., Kaufman R.J., Ma D., Coen D.M., Ron D., Yuan J. A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science 2005, 307:935-939.
23. Wiseman R.L., Balch W.E. A new pharmacology - drugging stressed folding pathways. Trends Mol. Med. 2005, 11:347-350.
24. Yokouchi M., Hiramatsu N., Hayakawa K., Kasai A., Takano Y., Yao J., Kitamura M. Atypical, bidirectional regulation of cadmium-induced apoptosis via distinct signaling of unfolded protein response. Cell Death Differ. 2007, 14:1467-1474.
25. M. Kitamura, H. Kato, Y. Saito, S. Nakajima, S. Takahashi, H. Johno, L. Gu, R. Katoh, Aberrant, differential and bidirectional regulation of the unfolded protein response towards cell survival by 3′-deoxyadenosine, Cell Death Differ, in press, doi:10.1038/cdd.2011.63.
26. Talbot U.M., Paton J.C., Paton A.W. Protective immunization of mice with an active-site mutant of subtilase cytotoxin of Shiga toxin-producing Escherichia coli. Infect. Immun. 2005, 73:4432-4436.
27. Fernandez J., Yaman I., Sarnow P., Snider M.D., Glou M. Regulation of internal ribosomal entry site-mediated translation by phosphorylation of the translation initiation factor eIF2α. J. Biol. Chem. 2001, 277:19198-19205.
28. Hayakawa K., Hiramatsu N., Okamura M., Yamazaki H., Nakajima S., Yao J., Paton A.W., Paton J.C., Kitamura M. Acquisition of anergy to proinflammatory cytokines in nonimmune cells through endoplasmic reticulum stress response: a mechanism for subsidence of inflammation. J. Immunol. 2009, 182:1182-1191.
29. Katayama T.K., Imaizumi K., Honda A., Yoneda T., Kudo T., Takeda M., Mori K., Rozmahel R., Fraser P., George-Hyslop P.S., Tohyama M. Disturbed activation of endoplasmic reticulum stress transducers by familial Alzheimer's disease-linked presenilin-1 mutations. J. Biol. Chem. 2001, 276:43446-43454.
30. Wang X.Z., Harding H.P., Zhang Y., Jolicoeur E.M., Kuroda M., Ron D. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 1998, 17:5708-5717.
31. Franke T.F., Kaplan D.R., Cantley L.C. PI3K: downstream AKTion blocks apoptosis. Cell 1997, 88:435-437.
32. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
33. Kitamura M. Biphasic, bidirectional regulation of NF-κB by endoplasmic reticulum stress. Antioxid. Redox Signal. 2009, 11:2353-2364.
34. Hu P., Han Z., Couvillon A.D., Exton J.H. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J. Biol. Chem. 2004, 279:49420-49429.
35. Lu Z., Xu S. ERK1/2 MAP kinases in cell survival and apoptosis. IUBMB Life 2006, 58:621-631.
36. Harding H.P., Zhang Y., Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397:271-274.
37. Li B., Yi P., Zhang B., Xu C., Liu Q., Pi Z., Xu X., Chevet E., Liu J. Differences in endoplasmic reticulum stress signalling kinetics determine cell survival outcome through activation of MKP-1. Cell Signal. 2011, 23:35-45.
38. Owens D.M., Keyse S.M. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 2007, 26:3203-3213.
39. Ishigaki S., Fonseca S.G., Oslowski C.M., Jurczyk A., Shearstone J.R., Zhu L.J., Permutt M.A., Greiner D.L., Bortell R., Urano F. AATF mediates an anti-apoptotic effect of the unfolded protein response through transcriptional regulation of AKT1. Cell Death Differ. 2010, 17:774-786.