Organelle targeting during bacterial infection: Insights from Listeria

Trends in Cell Biology

Volumn 25, Issue 6, 2015, Pages 330-338

  Lebreton, Alice ^a,b,c,d   Stavru, Fabrizia ^a,b,c   Cossart, Pascale ^a,b,c  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c CEMAGREF   (France)

^d ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Cellular microbiology; Endomembrane system; Listeria monocytogenes; Mitochondria; Nucleus; Organelle

Indexed keywords

BACTERIAL PROTEIN; CALCIUM; HISTONE; NUCLEOMODULIN LNTA; PROTEIN BAHD1; SIRTUIN 2; UNCLASSIFIED DRUG;

CALCIUM CELL LEVEL; CELL ORGANELLE; CELLS BY BODY ANATOMY; CHROMATIN; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FETOPLACENTAL UNIT; FOOD POISONING; GENE EXPRESSION; HISTONE MODIFICATION; HOST CELL; INTESTINE; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYSOSOME; MITOCHONDRION; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; UNFOLDED PROTEIN RESPONSE; ANIMAL; BACTERIAL INFECTION; HUMAN; ISOLATION AND PURIFICATION; LISTERIA; METABOLISM; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); LISTERIA; LISTERIA MONOCYTOGENES;

ANIMALS; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; ENDOPLASMIC RETICULUM; HUMANS; LISTERIA; LISTERIA MONOCYTOGENES; MITOCHONDRIA;

EID: 84929517804     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2015.01.003     Document Type: Review

References (101)

1. Salcedo S.P., Holden D.W. Bacterial interactions with the eukaryotic secretory pathway. Curr. Opin. Microbiol. 2005, 8:92-98.
2. Cossart P., Maloy S.R. Bacterial Pathogenesis 2014, Cold Spring Harbor Laboratory Press.
3. Sassera D., et al. 'Candidatus Midichloria mitochondrii', an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int. J. Syst. Evol. Microbiol. 2006, 56:2535-2540.
4. Fujishima M., Kodama Y. Endosymbionts in paramecium. Eur. J. Protistol. 2012, 48:124-137.
5. Schulz F., et al. Life in an unusual intracellular niche: a bacterial symbiont infecting the nucleus of amoebae. ISME J. 2014, 8:1634-1644.
6. Kay S., et al. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 2007, 318:648-651.
7. Malhas A., et al. The nucleoplasmic reticulum: form and function. Trends Cell Biol. 2011, 21:362-373.
8. Tait S.W.G., Green D.R. Mitochondria and cell signalling. J. Cell Sci. 2012, 125:807-815.
9. Allerberger F., Wagner M. Listeriosis: a resurgent foodborne infection. Clin. Microbiol. Infect. 2010, 16:16-23.
10. Cossart P. Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:19484-19491.
11. Pizarro-Cerda J., et al. Entry of Listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harb. Perspect. Med. 2012, 2:a010009.
12. Nikitas G., et al. Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J. Exp. Med. 2011, 208:2263-2277.
13. Gaillard J.L., et al. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect. Immun. 1987, 55:2822-2829.
14. Gründling A., et al. Requirement of the Listeria monocytogenes broad-range phospholipase PC-PLC during infection of human epithelial cells. J. Bacteriol. 2003, 185:6295-6307.
15. Alberti-Segui C., et al. Differential function of Listeria monocytogenes listeriolysin O and phospholipases C in vacuolar dissolution following cell-to-cell spread. Cell. Microbiol. 2007, 9:179-195.
16. Hamon M.A., et al. Listeriolysin O: the Swiss army knife of Listeria. Trends Microbiol. 2012, 20:360-368.
17. Birmingham C.L., et al. Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 2008, 451:350-354.
18. Meyer-Morse N., et al. Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection. PLoS ONE 2010, 5:e8610.
19. Tattoli I., et al. Listeria phospholipases subvert host autophagic defenses by stalling pre-autophagosomal structures. EMBO J. 2013, 32:3066-3078.
20. Tilney L.G., Portnoy D.A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 1989, 109:1597-1608.
21. Kocks C., et al. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 1992, 68:521-531.
22. Yoshikawa Y., et al. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 2009, 11:1233-1240.
23. Dortet L., et al. Recruitment of the Major Vault Protein by InlK: A Listeria monocytogenes Strategy to Avoid Autophagy. PLoS Pathog. 2011, 7:e1002168.
24. Dortet L., et al. Listeria and autophagy escape: involvement of InlK, an internalin-like protein. Autophagy 2012, 8:132-134.
25. Wandinger-Ness A., Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb. Perspect. Biol. 2014, 6:a022616.
26. Pizarro-Cerda J., et al. Phosphoinositides and host-pathogen interactions. Biochim. Biophys. Acta 2014, Published online September 19, 2014. http://dx.doi.org/10.1016/j.bbalip.2014.09.011.
27. Prada-Delgado A., et al. Interferon-gamma listericidal action is mediated by novel Rab5a functions at the phagosomal environment. J. Biol. Chem. 2001, 276:19059-19065.
28. Alvarez-Domínguez C., et al. Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic 2008, 9:325-337.
29. Henry R., et al. Cytolysin-dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes. Cell. Microbiol. 2006, 8:107-119.
30. Shaughnessy L.M., et al. Membrane perforations inhibit lysosome fusion by altering pH and calcium in Listeria monocytogenes vacuoles. Cell. Microbiol. 2006, 8:781-792.
31. 2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 2000, 149:1053-1062.
32. Beauregard K.E., et al. pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J. Exp. Med. 1997, 186:1159-1163.
33. Radtke A.L., et al. Listeria monocytogenes exploits cystic fibrosis transmembrane conductance regulator (CFTR) to escape the phagosome. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:1633-1638.
34. 2+ oscillations. Cell. Microbiol. 2002, 4:483-491.
35. Dramsi S., Cossart P. Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect. Immun. 2003, 71:3614-3618.
36. + are required for the listeriolysin O-dependent internalization pathway of Listeria monocytogenes. Infect. Immun. 2014, 82:1084-1091.
37. Bierne H., et al. The invasion protein InIB from Listeria monocytogenes activates PLC-gamma1 downstream from PI 3-kinase. Cell. Microbiol. 2000, 2:465-476.
38. 2+ signalling by listeriolysin O, the cholesterol-dependent cytolysin of Listeria monocytogenes. Cell. Microbiol. 2007, 9:2008-2021.
39. Dewamitta S.R., et al. Listeriolysin O-dependent bacterial entry into the cytoplasm is required for calpain activation and interleukin-1 alpha secretion in macrophages infected with Listeria monocytogenes. Infect. Immun. 2010, 78:1884-1894.
40. Tsuchiya K., et al. Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes. J. Immunol. 2010, 185:1186-1195.
41. Cywes Bentley C., et al. Extracellular group A Streptococcus induces keratinocyte apoptosis by dysregulating calcium signalling. Cell. Microbiol. 2005, 7:945-955.
42. Pillich H., et al. Activation of the unfolded protein response by Listeria monocytogenes. Cell. Microbiol. 2012, 14:949-964.
43. Haynes C.M., et al. Evaluating and responding to mitochondrial dysfunction: the mitochondrial unfolded-protein response and beyond. Trends Cell Biol. 2013, 23:311-318.
44. Pellegrino M.W., et al. Mitochondrial UPR-regulated innate immunity provides resistance to pathogen infection. Nature 2014, 516:414-417.
45. Galluzzi L., et al. Viral control of mitochondrial apoptosis. PLoS Pathog. 2008, 4:e1000018.
46. Rudel T., et al. Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat. Rev. Microbiol. 2010, 8:693-705.
47. Ashida H., et al. Cell death and infection: a double-edged sword for host and pathogen survival. J. Cell Biol. 2011, 195:931-942.
48. Stavru F., et al. Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3612-3617.
49. Bielaszewska M., et al. Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog. 2013, 9:e1003797.
50. Jain P., et al. Helicobacter pylori vacuolating cytotoxin A (VacA) engages the mitochondrial fission machinery to induce host cell death. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:16032-16037.
51. Stavru F., et al. Atypical mitochondrial fission upon bacterial infection. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:16003-16008.
52. Castanier C., Arnoult D. Mitochondrial localization of viral proteins as a means to subvert host defense. Biochim. Biophys. Acta 2011, 1813:575-583.
53. Onoguchi K., et al. Virus-infection or 5'ppp-RNA activates antiviral signal through redistribution of IPS-1 mediated by MFN1. PLoS Pathog. 2010, 6:e1001012.
54. Koshiba T., et al. Mitochondrial membrane potential is required for MAVS-mediated antiviral signaling. Sci. Signal. 2011, 4:ra7.
55. West A.P., et al. Mitochondria in innate immune responses. Nat. Rev. Immunol. 2011, 11:389-402.
56. Dixit E., et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 2010, 141:668-681.
57. Hagmann C.A., et al. RIG-I detects triphosphorylated RNA of Listeria monocytogenes during infection in non-immune cells. PLoS ONE 2013, 8:e62872.
58. Odendall C., et al. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 2014, 15:717-726.
59. Cohen P., et al. Monitoring cellular responses to Listeria monocytogenes with oligonucleotide arrays. J. Biol. Chem. 2000, 275:11181-11190.
60. Baldwin D.N., et al. A gene-expression program reflecting the innate immune response of cultured intestinal epithelial cells to infection by Listeria monocytogenes. Genome Biol. 2003, 4:R2.
61. McCaffrey R.L., et al. A specific gene expression program triggered by Gram-positive bacteria in the cytosol. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11386-11391.
62. Frande-Cabanes E., et al. Dissociation of innate immune responses in microglia infected with Listeria monocytogenes. Glia 2014, 62:233-246.
63. Lecuit M., et al. Functional genomic studies of the intestinal response to a foodborne enteropathogen in a humanized gnotobiotic mouse model. J. Biol. Chem. 2007, 282:15065-15072.
64. Archambaud C., et al. Impact of lactobacilli on orally acquired listeriosis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:16684-16689.
65. Eitel J., et al. Innate immune recognition and inflammasome activation in Listeria monocytogenes infection. Front. Microbiol. 2010, 1:149.
66. Bierne H., et al. Epigenetics and bacterial infections. Cold Spring Harb. Perspect. Med. 2012, 2:a010272.
67. Minàrovits J. Microbe-induced epigenetic alterations in host cells: the coming era of patho-epigenetics of microbial infections. A review. Acta Microbiol. Immunol. Hung. 2009, 56:1-19.
68. Hamon M.A., Cossart P. Histone modifications and chromatin remodeling during bacterial infections. Cell Host Microbe 2008, 4:100-109.
69. Bierne H., Cossart P. When bacteria target the nucleus: the emerging family of nucleomodulins. Cell. Microbiol. 2012, 14:622-633.
70. Felsenfeld G., Groudine M. Controlling the double helix. Nature 2003, 421:448-453.
71. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
72. Hamon M.A., et al. Histone modifications induced by a family of bacterial toxins. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:13467-13472.
73. + efflux is required for histone H3 dephosphorylation by Listeria monocytogenes listeriolysin O and other pore-forming toxins. Infect. Immun. 2011, 79:2839-2846.
74. Eskandarian H.A., et al. A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science 2013, 341:1238858.
75. +-dependent tubulin deacetylase. Mol. Cell 2003, 11:437-444.
76. Dussurget O., et al. The bacterial pathogen Listeria monocytogenes and the interferon family: type I, type II and type III interferons. Front. Cell Infect. Microbiol. 2014, 4:50.
77. Lebreton A., et al. A bacterial protein targets the BAHD1 chromatin complex to stimulate type III interferon response. Science 2011, 331:1319-1321.
78. Bierne H., et al. Human BAHD1 promotes heterochromatic gene silencing. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13826-13831.
79. Lebreton A., et al. Structural basis for the inhibition of the chromatin repressor BAHD1 by the bacterial nucleomodulin LntA. mBio 2014, 5:e00775-e813.
80. Decker T., et al. The yin and yang of type I interferon activity in bacterial infection. Nat. Rev. Immunol. 2005, 5:675-687.
81. Liu Y., et al. Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature 2014, 508:406-410.
82. Leitão E., et al. Listeria monocytogenes induces host DNA damage and delays the host cell cycle to promote infection. Cell Cycle 2014, 13:928-940.
83. Samba-Louaka A., et al. Listeria monocytogenes dampens the DNA Damage Response. PLoS Pathog. 2014, 10:e1004470.
84. Pennini M.E., et al. Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis. PLoS Pathog. 2010, 6:e1000995.
85. Rolando M., et al. Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe 2013, 13:395-405.
86. Anand S.K., Tikoo S.K. Viruses as modulators of mitochondrial functions. Adv. Virol. 2013, 2013:738794.
87. Yarbrough M.L., et al. Viral subversion of nucleocytoplasmic trafficking. Traffic 2014, 15:127-140.
88. Galmiche A., et al. The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO J. 2000, 19:6361-6370.
89. Kenny B., Jepson M. Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell. Microbiol. 2000, 2:579-590.
90. Nougayrède J-P., Donnenberg M.S. Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell. Microbiol. 2004, 6:1097-1111.
91. Suzuki M., et al. Vibrio cholerae T3SS effector VopE modulates mitochondrial dynamics and innate immune signaling by targeting miro GTPases. Cell Host Microbe 2014, 16:581-591.
92. Rodríguez-Herva J.J., et al. A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses. Cell. Microbiol. 2012, 14:669-681.
93. Jones T.C., Hirsch J.G. The interaction between Toxoplasma gondii and mammalian cells. II. The absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J. Exp. Med. 1972, 136:1173-1194.
94. Horwitz M.A. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 1983, 158:1319-1331.
95. Matsumoto A., et al. Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J. Electron. Microsc. (Tokyo) 1991, 40:356-363.
96. Pernas L., et al. Toxoplasma effector MAF1 mediates recruitment of host mitochondria and impacts the host response. PLoS Biol. 2014, 12:e1001845.
97. Görtz H.D., Wiemann M. Route of infection of the bacteria Holospora elegans and Holospora obtusa into the nuclei of Paramecium caudatum. Eur. J. Protistol. 1989, 24:101-109.
98. Wolbach S.B. Studies on Rocky Mountain spotted fever. J. Med. Res. 1919, 41:1-198.
99. Iwamasa K., et al. Ultrastructural study of the response of cells infected in vitro with causative agent of spotted fever group rickettsiosis in Japan. APMIS 1992, 100:535-542.
100. Schröder M. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 2008, 65:862-894.
101. Schrader M. Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta 2006, 1763:531-541.