eIF2α confers cellular tolerance to S. aureus α-toxin

Frontiers in Immunology

Volumn 6, Issue JUL, 2015, Pages

  Hoven, Gisela von ^a   Neukirch, Claudia ^a   Meyenburg, Martina ^a   Füser, Sabine ^a   Petrivna, Maria Bidna ^a   Rivas, Amable J ^a   Ryazanov, Alexey ^b   Kaufman, Randal J ^c   Aroian, Raffi V ^d   Husmann, Matthias ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Cellular tolerance; EIF2AK4; MAPK; Pore forming toxins; S. aureus toxin

Indexed keywords

ADAM10 ENDOPEPTIDASE; ALPHA TOXIN; INITIATION FACTOR 2ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; STRESS ACTIVATED PROTEIN KINASE;

AMINO ACID SEQUENCE; ANTIBODY RESPONSE; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BACTERIUM ISOLATION; CELL FUNCTION; CELLULAR TOLERANCE; ENZYME ACTIVITY; FIBROBLAST CULTURE; GENE EXPRESSION; IMMUNE RESPONSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POTASSIUM TRANSPORT; PROTEIN PHOSPHORYLATION; QUANTITATIVE ASSAY; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TRANSLATION INITIATION; WESTERN BLOTTING;

EID: 84938533044     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00383     Document Type: Article

References (64)

1. Bhakdi S, Tranum-Jensen J. Membrane damage by pore-forming bacterial cytolysins. Microb Pathog (1986) 1:5-14. doi:10.1016/0882-4010(86)90027-6
2. Iacovache I, Van Der Goot FG, Pernot L. Pore formation: an ancient yet complex form of attack. Biochim Biophys Acta (2008) 1778:1611-23. doi:10.1016/j.bbamem.2008.01.026
3. Los FC, Randis TM, Aroian RV, Ratner AJ. Role of pore-forming toxins in bacterial infectious diseases. Microbiol Mol Biol Rev (2013) 77:173-207. doi:10.1128/MMBR.00052-12
4. Bischofberger M, Iacovache I, Van Der Goot FG. Pathogenic pore-forming proteins: function and host response. Cell Host Microbe (2012) 12:266-75. doi:10.1016/j.chom.2012.08.005
5. Thelestam M, Mollby R. Survival of cultured-cells after functional and structural disorganization of plasma-membrane by bacterial hemolysins and phospholipases. Toxicon (1983) 21:805-15. doi:10.1016/0041-0101(83)90069-7
6. Walev I, Palmer M, Martin E, Jonas D, Weller U, Hohn-Bentz H, et al. Recovery of human fibroblasts from attack by the pore-forming alpha-toxin of Staphylococcus aureus. Microb Pathog (1994) 17:187-201. doi:10.1006/mpat.1994.1065
7. Huffman DL, Abrami L, Sasik R, Corbeil J, Van Der Goot FG, Aroian RV. Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci U S A (2004) 101:10995-1000. doi:10.1073/pnas.0404073101
8. Husmann M, Dersch K, Bobkiewicz W, Beckmann E, Veerachato G, Bhakdi S. Differential role of p38 mitogen activated protein kinase for cellular recovery from attack by pore-forming S. aureus alpha-toxin or streptolysin O. Biochem Biophys Res Commun (2006) 344:1128-34. doi:10.1016/j.bbrc.2006.03.241
9. Aroian R, Van Der Goot FG. Pore-forming toxins and cellular non-immune defenses (CNIDs). Curr Opin Microbiol (2007) 10:57-61. doi:10.1016/j.mib.2006.12.008
10. Husmann M, Beckmann E, Boller K, Kloft N, Tenzer S, Bobkiewicz W, et al. Elimination of a bacterial pore-forming toxin by sequential endocytosis and exocytosis. FEBS Lett (2009) 583:337-44. doi:10.1016/j.febslet.2008.12.028
11. Kloft N, Busch T, Neukirch C, Weis S, Boukhallouk F, Bobkiewicz W, et al. Pore-forming toxins activate MAPK p38 by causing loss of cellular potassium. Biochem Biophys Res Commun (2009) 385:503-6. doi:10.1016/j.bbrc.2009.05.121
12. Kloft N, Neukirch C, Bobkiewicz W, Veerachato G, Busch T, Von Hoven G, et al. Pro-autophagic signal induction by bacterial pore-forming toxins. Med Microbiol Immunol (2010) 199:299-309. doi:10.1007/s00430-010-0163-0
13. Kloft N, Neukirch C, Von Hoven G, Bobkiewicz W, Weis S, Boller K, et al. A subunit of eukaryotic translation initiation factor 2alpha-phosphatase (CreP/PPP1R15B) regulates membrane traffic. J Biol Chem (2012) 287:35299-317. doi:10.1074/jbc.M112.379883
14. Stuart LM, Paquette N, Boyer L. Effector-triggered versus pattern-triggered immunity: how animals sense pathogens. Nat Rev Immunol (2013) 13:199-206. doi:10.1038/nri3398
15. Kao CY, Los FC, Huffman DL, Wachi S, Kloft N, Husmann M, et al. Global functional analyses of cellular responses to pore-forming toxins. PLoS Pathog (2011) 7:e1001314. doi:10.1371/journal.ppat.1001314
16. Gonzalez MR, Bischofberger M, Pernot L, Van Der Goot FG, Freche B. Bacterial pore-forming toxins: the (w)hole story? Cell Mol Life Sci (2008) 65:493-507. doi:10.1007/s00018-007-7434-y
17. Porta H, Cancino-Rodezno A, Soberon M, Bravo A. Role of MAPK p38 in the cellular responses to pore-forming toxins. Peptides (2011) 32:601-6. doi:10.1016/j.peptides.2010.06.012
18. Von Hoven G, Kloft N, Neukirch C, Ebinger S, Bobkiewicz W, Weis S, et al. Modulation of translation and induction of autophagy by bacterial exoproducts. Med Microbiol Immunol (2012) 201:409-18. doi:10.1007/s00430-012-0271-0
19. Stassen M, Muller C, Richter C, Neudorfl C, Hultner L, Bhakdi S, et al. The streptococcal exotoxin streptolysin O activates mast cells to produce tumor necrosis factor alpha by p38 mitogen-activated protein kinase-and protein kinase C-dependent pathways. Infect Immun (2003) 71:6171-7. doi:10.1128/IAI.71.11.6171-6177.2003
20. Gonzalez MR, Bischofberger M, Freche B, Ho S, Parton RG, Van Der Goot FG. Pore-forming toxins induce multiple cellular responses promoting survival. Cell Microbiol (2011) 13(7):1026-43. doi:10.1111/j.1462-5822.2011.01600.x
21. Nagahama M, Shibutani M, Seike S, Yonezaki M, Takagishi T, Oda M, et al. The p38 MAPK and JNK pathways protect host cells against Clostridium perfringens beta-toxin. Infect Immun (2013) 81:3703-8. doi:10.1128/IAI.00579-13
22. Haugwitz U, Bobkiewicz W, Han SR, Beckmann E, Veerachato G, Shaid S, et al. Pore-forming Staphylococcus aureus alpha-toxin triggers epidermal growth factor receptor-dependent proliferation. Cell Microbiol (2006) 8:1591-600. doi:10.1111/j.1462-5822.2006.00733.x
23. Richter E, Harms M, Ventz K, Gierok P, Chilukoti RK, Hildebrandt JP, et al. A multi-omics approach identifies key hubs associated with cell type-specific responses of airway epithelial cells to staphylococcal alpha-toxin. PLoS One (2015) 10:e0122089. doi:10.1371/journal.pone.0122089
24. Hamon MA, Cossart P. K+ efflux, is required for histone-H3 dephosphorylation by Listeria LLO and other pore forming toxins. Infect Immun (2011) 79(7):2839-46. doi:10.1128/IAI.01243-10
25. Imre G, Heering J, Takeda AN, Husmann M, Thiede B, Zu Heringdorf DM, et al. Caspase-2 is an initiator caspase responsible for pore-forming toxin-mediated apoptosis. EMBO J (2012) 31(11):2615-28. doi:10.1038/emboj.2012.93
26. Idone V, Tam C, Goss JW, Toomre D, Pypaert M, Andrews NW. Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. J Cell Biol (2008) 180:905-14. doi:10.1083/jcb.200708010
27. Tam C, Idone V, Devlin C, Fernandes MC, Flannery A, He X, et al. Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. J Cell Biol (2010) 189:1027-38. doi:10.1083/jcb.201003053
28. Babiychuk EB, Monastyrskaya K, Potez S, Draeger A. Blebbing confers resistance against cell lysis. Cell Death Differ (2011) 18:80-9. doi:10.1038/cdd.2010.81
29. Draeger A, Monastyrskaya K, Babiychuk EB. Plasma membrane repair and cellular damage control: the annexin survival kit. Biochem Pharmacol (2011) 81:703-12. doi:10.1016/j.bcp.2010.12.027
30. Corrotte M, Fernandes MC, Tam C, Andrews NW. Toxin pores endocytosed during plasma membrane repair traffic into the lumen of MVBs for degradation. Traffic (2012) 13:483-94. doi:10.1111/j.1600-0854.2011.01323.x
31. Corrotte M, Almeida PE, Tam C, Castro-Gomes T, Fernandes MC, Millis BA, et al. Caveolae internalization repairs wounded cells and muscle fibers. Elife (2013) 2:e00926. doi:10.7554/eLife.00926
32. Castro-Gomes T, Koushik AB, Andrews NW. ESCRT: nipping the wound in the bud?. Trends Biochem Sci (2014) 39:307-9. doi:10.1016/j.tibs.2014.06.001
33. Tattoli I, Sorbara MT, Vuckovic D, Ling A, Soares F, Carneiro LA, et al. Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe (2012) 11:563-75. doi:10.1016/j.chom.2012.04.012
34. Lemaitre B, Girardin SE. Translation inhibition and metabolic stress pathways in the host response to bacterial pathogens. Nat Rev Microbiol (2013) 11:365-9. doi:10.1038/nrmicro3029
35. Chakrabarti S, Liehl P, Buchon N, Lemaitre B. Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe (2012) 12:60-70. doi:10.1016/j.chom.2012.06.001
36. Wek RC, Jiang HY, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans (2006) 34:7-11. doi:10.1042/BST0340007
37. Dever TE, Feng L, Wek RC, Cigan AM, Donahue TF, Hinnebusch AG. Phosphorylation of initiation factor 2 alpha by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell (1992) 68:585-96. doi:10.1016/0092-8674(92)90193-G
38. Dong J, Qiu H, Garcia-Barrio M, Anderson J, Hinnebusch AG. Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. Mol Cell (2000) 6:269-79. doi:10.1016/S1097-2765(00)00028-9
39. Deloche O, De La Cruz J, Kressler D, Doere M, Linder P. A membrane transport defect leads to a rapid attenuation of translation initiation in Saccharomyces cerevisiae. Mol Cell (2004) 13:357-66. doi:10.1016/S1097-2765(04)00008-5
40. De Filippi L, Fournier M, Cameroni E, Linder P, De Virgilio C, Foti M, et al. Membrane stress is coupled to a rapid translational control of gene expression in chlorpromazine-treated cells. Curr Genet (2007) 52:171-85. doi:10.1007/s00294-007-0151-0
41. Schneider DS, Ayres JS. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol (2008) 8:889-95. doi:10.1038/nri2432
42. Raberg L, Graham AL, Read AF. Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc Lond B Biol Sci (2009) 364:37-49. doi:10.1098/rstb.2008.0184
43. Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science (2012) 335:936-41. doi:10.1126/science.1214935
44. De S, Olson R. Crystal structure of the Vibrio cholerae cytolysin heptamer reveals common features among disparate pore-forming toxins. Proc Natl Acad Sci U S A (2011) 108:7385-90. doi:10.1073/pnas.1017442108
45. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science (2000) 288:870-4. doi:10.1126/science.288.5467.870
46. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, et al. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science (2005) 307:935-9. doi:10.1126/science.1101902
47. Jousse C, Oyadomari S, Novoa I, Lu P, Zhang Y, Harding HP, et al. Inhibition of a constitutive translation initiation factor 2alpha phosphatase, CReP, promotes survival of stressed cells. J Cell Biol (2003) 163:767-75. doi:10.1083/jcb.200308075
48. Ryazanov AG, Shestakova EA, Natapov PG. Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation. Nature (1988) 334:170-3. doi:10.1038/334170a0
49. Vadia S, Seveau S. Fluxes of Ca2+ and K+ are required for the listeriolysin O-dependent internalization pathway of Listeria monocytogenes. Infect Immun (2014) 82:1084-91. doi:10.1128/IAI.01067-13
50. Dunbar TL, Yan Z, Balla KM, Smelkinson MG, Troemel ER. C. elegans detects pathogen-induced translational inhibition to activate immune signaling. Cell Host Microbe (2012) 11:375-86. doi:10.1016/j.chom.2012.02.008
51. Arguello RJ, Rodriguez Rodrigues C, Gatti E, Pierre P. Protein synthesis regulation, a pillar of strength for innate immunity?. Curr Opin Immunol (2015) 32:28-35. doi:10.1016/j.coi.2014.12.001
52. Wilke GA, Bubeck Wardenburg J. Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc Natl Acad Sci U S A (2010) 107:13473-8. doi:10.1073/pnas.1001815107
53. Talloczy Z, Jiang W, Virgin HWT, Leib DA, Scheuner D, Kaufman RJ, et al. Regulation of starvation-and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci U S A (2002) 99:190-5. doi:10.1073/pnas.012485299
54. Maurer K, Reyes-Robles T, Alonzo F III, Durbin J, Torres VJ, Cadwell K. Autophagy mediates tolerance to Staphylococcus aureus alpha-toxin. Cell Host Microbe (2015) 17:429-40. doi:10.1016/j.chom.2015.03.001
55. Jursch R, Hildebrand A, Hobom G, Tranum-Jensen J, Ward R, Kehoe M, et al. Histidine residues near the N terminus of staphylococcal alpha-toxin as reporters of regions that are critical for oligomerization and pore formation. Infect Immun (1994) 62:2249-56.
56. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, et al. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol (2003) 23:5651-63. doi:10.1128/MCB.23.16.5651-5663.2003
57. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell (2001) 7:1165-76. doi:10.1016/S1097-2765(01)00265-9
58. Harding HP, Zhang Y, Scheuner D, Chen JJ, Kaufman RJ, Ron D. Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2alpha) dephosphorylation in mammalian development. Proc Natl Acad Sci U S A (2009) 106:1832-7. doi:10.1073/pnas.0809632106
59. Chu HP, Liao Y, Novak JS, Hu Z, Merkin JJ, Shymkiv Y, et al. Germline quality control: eEF2K stands guard to eliminate defective oocytes. Dev Cell (2014) 28:561-72. doi:10.1016/j.devcel.2014.01.027
60. Hartmann D, De Strooper B, Serneels L, Craessaerts K, Herreman A, Annaert W, et al. The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts. Hum Mol Genet (2002) 11:2615-24. doi:10.1093/hmg/11.21.2615
61. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol (1988) 106:761-71. doi:10.1083/jcb.106.3.761
62. Schmidt EK, Clavarino G, Ceppi M, Pierre P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods (2009) 6:275-7. doi:10.1038/nmeth.1314
63. Abrami L, Fivaz M, Glauser PE, Parton RG, Van Der Goot FG. A pore-forming toxin interacts with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J Cell Biol (1998) 140:525-40. doi:10.1083/jcb.140.3.525
64. Agerer F, Waeckerle S, Hauck CR. Microscopic quantification of bacterial invasion by a novel antibody-independent staining method. J Microbiol Methods (2004) 59:23-32. doi:10.1016/j.mimet.2004.05.008