Role of proapoptotic BH3-only proteins in Listeria monocytogenes infection

European Journal of Immunology

Volumn 46, Issue 6, 2016, Pages 1427-1437

  Margaroli, Camilla ^a   Oberle, Susanne ^b   Lavanchy, Christine ^a   Scherer, Stefanie ^b   Rosa, Muriel ^a   Strasser, Andreas ^c,d   Pellegrini, Marc ^c,d   Zehn, Dietmar ^e   Acha Orbea, Hans ^a   Ehirchiou, Driss ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Apoptosis; Cytokines; Host pathogens interactions; Immune evasion; TNF; Transgenic models

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; PROTEIN BID; PROTEIN NOXA; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BACTERIAL LOAD; BACTERIAL VIRULENCE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HOST CELL; KNOCKOUT MOUSE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SURVIVAL; UPREGULATION;

EID: 84973638744     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545857     Document Type: Article

References (49)

1. Czabotar, P. E., Lessene, G., Strasser, A. and Adams, J. M., Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 2014. 15: 49–63.
2. Elmore, S., Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007. 35: 495–516.
3. Youle, R. J. and Strasser, A., The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 2008. 9: 47–59.
4. Happo, L., Strasser, A. and Cory, S., BH3-only proteins in apoptosis at a glance. J. Cell Sci. 2012. 125: 1081–1087.
5. Strasser, A., The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 2005. 5: 189–200.
6. Lamkanfi, M. and Dixit, V. M., Manipulation of host cell death pathways during microbial infections. Cell Host. Microbe. 2010. 8: 44–54.
7. Rudel, T., Kepp, O. and Kozjak-Pavlovic, V., Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat. Rev. Microbiol. 2010. 8: 693–705.
8. Kepp, O., Gottschalk, K., Churin, Y., Rajalingam, K., Brinkmann, V., Machuy, N., Kroemer, G. et al., Bim and Bmf synergize to induce apoptosis in Neisseria gonorrhoeae infection. PLoS Pathog. 2009. 5: e1000348.
9. Pamer, E. G., Cellular immunity to intracellular bacteria. Curr. Opin. Immunol. 1993. 5: 492–496.
10. Mostowy, S. and Cossart, P., Virulence factors that modulate the cell biology of Listeria infection and the host response. Adv. Immunol. 2012. 113: 19–32.
11. Stavru, F., Archambaud, C. and Cossart, P., Cell biology and immunology of Listeria monocytogenes infections: novel insights. Immunol. Rev. 2011. 240: 160–184.
12. Buchmeier, N. A. and Schreiber, R. D., Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. Proc. Natl. Acad. Sci. USA 1985. 82: 7404–7408.
13. Pamer, E. G., Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 2004. 4: 812–823.
14. Rothe, J., Lesslauer, W., Lotscher, H., Lang, Y., Koebel, P., Kontgen, F., Althage, A. et al., Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 1993. 364: 798–802.
15. Williams, M. A., Schmidt, R. L. and Lenz, L. L., Early events regulating immunity and pathogenesis during Listeria monocytogenes infection. Trends Immunol. 2012. 33: 488–495.
16. Nathan, C. and Shiloh, M. U., Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 2000. 97: 8841–8848.
17. Shiloh, M. U., MacMicking, J. D., Nicholson, S., Brause, J. E., Potter, S., Marino, M., Fang, F. et al., Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 1999. 10: 29–38.
18. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y. et al., Neutrophil extracellular traps kill bacteria. Science 2004. 303: 1532–1535.
19. Brinkmann, V. and Zychlinsky, A., Neutrophil extracellular traps: is immunity the second function of chromatin? J. Cell Biol. 2012. 198: 773–783.
20. Chu, T., Tyznik, A. J., Roepke, S., Berkley, A. M., Woodward-Davis, A., Pattacini, L., Bevan, M. J. et al., Bystander-activated memory CD8 T cells control early pathogen load in an innate-like, NKG2D-dependent manner. Cell Rep. 2013. 3: 701–708.
21. Carrero, J. A. and Unanue, E. R., Mechanisms and immunological effects of apoptosis caused by Listeria monocytogenes. Adv. Immunol. 2012. 113: 157–174.
22. Merrick, J. C., Edelson, B. T., Bhardwaj, V., Swanson, P. E. and Unanue, E. R., Lymphocyte apoptosis during early phase of Listeria infection in mice. Am. J. Pathol. 1997. 151: 785–792.
23. Mueller, N. J., Wilkinson, R. A., and Fishman, J. A., Listeria monocytogenes infection in caspase-11-deficient mice. Infect. Immun. 2002. 70: 2657–2664.
24. Fuse, Y., Nishimura, H., Maeda, K. and Yoshikai, Y., CD95 (Fas) may control the expansion of activated T cells after elimination of bacteria in murine listeriosis. Infect. Immun. 1997. 65: 1883–1891.
25. Wiley, S. R., Schooley, K., Smolak, P. J., Din, W. S., Huang, C. P., Nicholl, J. K., Sutherland, G. R. et al., Identification and characterization of a new member of the TNF-TNF family that induces apoptosis. Immunity 1995. 3: 673–682.
26. Pan, G., O'Rourke, K., Chinnaiyan, A. M., Gentz, R., Ebner, R., Ni, J. and Dixit, V. M., The receptor for the cytotoxic ligand TRAIL. Science 1997. 276: 111–113.
27. Zheng, S. J., Jiang, J., Shen, H. and Chen, Y. H., Reduced apoptosis and ameliorated listeriosis in TRAIL-null mice. J. Immunol. 2004. 173: 5652–5658.
28. Conlan, J. W. and North, R. J., Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J. Exp. Med. 1994. 179: 259–268.
29. Czuprynski, C. J., Brown, J. F., Maroushek, N., Wagner, R. D. and Steinberg, H., Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J. Immunol. 1994. 152: 1836–1846.
30. Carrero, J. A., Calderon, B. and Unanue, E. R., Listeriolysin O from Listeria monocytogenes is a lymphocyte apoptogenic molecule. J. Immunol. 2004. 172: 4866–4874.
31. Kayal, S. and Charbit, A., Listeriolysin O: a key protein of Listeria monocytogenes with multiple functions. FEMS Microbiol. Rev. 2006. 30: 514–529.
32. Wadsworth, S. J. and Goldfine, H., Listeria monocytogenes phospholipase C-dependent calcium signaling modulates bacterial entry into J774 macrophage-like cells. Infect. Immun. 1999. 67: 1770–1778.
33. Stavru, F., Bouillaud, F., Sartori, A., Ricquier, D. and Cossart, P., Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc. Natl. Acad. Sci. USA 2011. 108: 3612–3617.
34. Carrero, J. A., Calderon, B. and Unanue, E. R., Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med. 2004. 200: 535–540.
35. Luo, Z., Li, Z., Chen, K., Liu, R., Li, X., Cao, H. and Zheng, S. J., Engagement of heterogeneous nuclear ribonucleoprotein M with listeriolysin O induces type I interferon expression and restricts Listeria monocytogenes groWTh in host cells. Immunobiology 2012. 217: 972–981.
36. Fuertes Marraco, S. A., Scott, C. L., Bouillet, P., Ives, A., Masina, S., Vremec, D., Jansen, E. S. et al., Type I interferon drives dendritic cell apoptosis via multiple BH3-only proteins following activation by PolyIC in vivo. PLoS One 2011. 6: e20189.
37. Hippe, D., Weber, A., Zhou, L., Chang, D. C., Hacker, G. and Luder, C. G., Toxoplasma gondii infection confers resistance against BimS-induced apoptosis by preventing the activation and mitochondrial targeting of pro-apoptotic Bax. J. Cell Sci. 2009. 122: 3511–3521.
38. Quan, J. H., Cha, G. H., Zhou, W., Chu, J. Q., Nishikawa, Y. and Lee, Y. H., Involvement of PI 3 kinase/Akt-dependent Bad phosphorylation in Toxoplasma gondii-mediated inhibition of host cell apoptosis. Exp. Parasitol. 2013. 133: 462–471.
39. Chang, K. C., Unsinger, J., Davis, C. G., Schwulst, S. J., Muenzer, J. T., Strasser, A. and Hotchkiss, R. S., Multiple triggers of cell death in sepsis: death receptor and mitochondrial-mediated apoptosis. FASEB J. 2007. 21: 708–719.
40. Yin, X. M., Wang, K., Gross, A., Zhao, Y., Zinkel, S., Klocke, B., Roth, K. A. et al., Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 1999. 400: 886–891.
41. Samba-Louaka, A., Pereira, J. M., Nahori, M. A., Villiers, V., Deriano, L., Hamon, M. A. and Cossart, P., Listeria monocytogenes dampens the DNA damage response. PLoS Pathog. 2014. 10: e1004470.
42. Villunger, A., Michalak, E. M., Coultas, L., Mullauer, F., Bock, G., Ausserlechner, M. J., Adams, J. M. et al., p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003. 302: 1036–1038.
43. Jeffers, J. R., Parganas, E., Lee, Y., Yang, C., Wang, J., Brennan, J., MacLean, K. H. et al., Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 2003. 4: 321–328.
44. Kirchner, T., Moller, S., Klinger, M., Solbach, W., Laskay, T. and Behnen, M., The impact of various reactive oxygen species on the formation of neutrophil extracellular traps. Mediators Inflamm. 2012. 2012: 849136.
45. Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N., Zbytnuik, L. D., Pittman, K. et al., Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med. 2012. 18: 1386–1393.
46. Havell, E. A., Evidence that tumor necrosis factor has an important role in antibacterial resistance. J. Immunol. 1989. 143: 2894–2899.
47. Han, J., Brown, T. and Beutler, B., Endotoxin-responsive sequences control cachectin/tumor necrosis factor biosynthesis at the translational level. J. Exp. Med. 1990. 171: 465–475.
48. Xanthoulea, S., Pasparakis, M., Kousteni, S., Brakebusch, C., Wallach, D., Bauer, J., Lassmann, H. et al., Tumor necrosis factor (TNF) receptor shedding controls thresholds of innate immune activation that balance opposing TNF functions in infectious and inflammatory diseases. J. Exp. Med. 2004. 200: 367–376.
49. Zehn, D., Turner, M. J., Lefrancois, L. and Bevan, M. J., Lack of original antigenic sin in recall CD8(+) T cell responses. J. Immunol. 2010. 184: 6320–6326.