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Interaction between Intracellular Bacterial Pathogens and Host Cell Mitochondria

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  • Authors: Anna Spier1,2,3,4, Fabrizia Stavru5,6,7,8, Pascale Cossart9,10,11
  • Editors: Pascale Cossart12, Craig R. Roy13, Philippe Sansonetti14
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institut Pasteur, Unité des Interactions Bactéries-Cellules, Paris, France; 2: Institut National de la Santé et de la Recherche Médicale, U604, Paris, France; 3: Institut National de la Recherche Agronomique, USC2020, Paris, France; 4: Bio Sorbonne Paris Cité, Université Paris Diderot, Paris, France; 5: Institut Pasteur, Unité des Interactions Bactéries-Cellules, Paris, France; 6: Institut National de la Santé et de la Recherche Médicale, U604, Paris, France; 7: Institut National de la Recherche Agronomique, USC2020, Paris, France; 8: Centre National de la Recherche Scientifique, SNC 5101, France; 9: Institut Pasteur, Unité des Interactions Bactéries-Cellules, Paris, France; 10: Institut National de la Santé et de la Recherche Médicale, U604, Paris, France; 11: Institut National de la Recherche Agronomique, USC2020, Paris, France; 12: Institut Pasteur, Paris, France; 13: Yale University School of Medicine, New Haven, Connecticut; 14: Institut Pasteur, Paris, France
  • Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0016-2019
  • Received 08 August 2018 Accepted 10 January 2019 Published 08 March 2019
  • Pascale Cossart, [email protected]; Fabrizia Stavru, [email protected]
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  • Abstract:

    Mitochondria are essential and highly dynamic organelles whose morphology is determined by a steady-state balance between fusion and fission. Mitochondrial morphology and function are tightly connected. Because they are involved in many important cellular processes, including energy production, cell-autonomous immunity, and apoptosis, mitochondria present an attractive target for pathogens. Here, we explore the relationship between host cell mitochondria and intracellular bacteria, with a focus on mitochondrial morphology and function, as well as apoptosis. Modulation of apoptosis can allow bacteria to establish their replicative niche or support bacterial dissemination. Furthermore, bacteria can manipulate mitochondrial morphology and function through secreted effector proteins and can also contribute to the establishment of a successful infection, e.g., by favoring access to nutrients and/or evasion of the immune system.

  • Citation: Spier A, Stavru F, Cossart P. 2019. Interaction between Intracellular Bacterial Pathogens and Host Cell Mitochondria. Microbiol Spectrum 7(2):BAI-0016-2019. doi:10.1128/microbiolspec.BAI-0016-2019.

References

1. Roger AJ, Muñoz-Gómez SA, Kamikawa R. 2017. The origin and diversification of Mitochondria. Curr Biol 27:R1177–R1192 http://dx.doi.org/10.1016/j.cub.2017.09.015. [PubMed]
2. Nunnari J, Suomalainen A. 2012. Mitochondria: in sickness and in health. Cell 148:1145–1159 http://dx.doi.org/10.1016/j.cell.2012.02.035. [PubMed]
3. Seth RB, Sun L, Ea C-K, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122:669–682 http://dx.doi.org/10.1016/j.cell.2005.08.012. [PubMed]
4. Tait SWG, Green DR. 2010. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11:621–632 http://dx.doi.org/10.1038/nrm2952. [PubMed]
5. Pagliuso A, Cossart P, Stavru F. 2018. The ever-growing complexity of the mitochondrial fission machinery. Cell Mol Life Sci 75:355–374 http://dx.doi.org/10.1007/s00018-017-2603-0. [PubMed]
6. Wai T, Langer T. 2016. Mitochondrial dynamics and metabolic regulation. Trends Endocrinol Metab 27:105–117 http://dx.doi.org/10.1016/j.tem.2015.12.001. [PubMed]
7. Mishra P, Chan DC. 2014. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 15:634–646 http://dx.doi.org/10.1038/nrm3877. [PubMed]
8. Hamon MA, Ribet D, Stavru F, Cossart P. 2012. Listeriolysin O: the Swiss army knife of Listeria. Trends Microbiol 20:360–368 http://dx.doi.org/10.1016/j.tim.2012.04.006. [PubMed]
9. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, Cossart P. 1992. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68:521–531 http://dx.doi.org/10.1016/0092-8674(92)90188-I.
10. Stavru F, Bouillaud F, Sartori A, Ricquier D, Cossart P. 2011. Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc Natl Acad Sci USA 108:3612–3617 http://dx.doi.org/10.1073/pnas.1100126108. [PubMed]
11. Stavru F, Palmer AE, Wang C, Youle RJ, Cossart P. 2013. Atypical mitochondrial fission upon bacterial infection. Proc Natl Acad Sci USA 110:16003–16008 http://dx.doi.org/10.1073/pnas.1315784110. [PubMed]
12. Gillmaier N, Götz A, Schulz A, Eisenreich W, Goebel W. 2012. Metabolic responses of primary and transformed cells to intracellular Listeria monocytogenes. PLoS One 7:e52378 http://dx.doi.org/10.1371/journal.pone.0052378. [PubMed]
13. Odendall C, Dixit E, Stavru F, Bierne H, Franz KM, Durbin AF, Boulant S, Gehrke L, Cossart P, Kagan JC. 2014. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat Immunol 15:717–726 http://dx.doi.org/10.1038/ni.2915. [PubMed]
14. Killackey SA, Sorbara MT, Girardin SE. 2016. Cellular aspects of Shigella pathogenesis: focus on the manipulation of host cell processes. Front Cell Infect Microbiol 6:38 http://dx.doi.org/10.3389/fcimb.2016.00038. [PubMed]
15. Tran Van Nhieu G, Kai Liu B, Zhang J, Pierre F, Prigent S, Sansonetti P, Erneux C, Kuk Kim J, Suh PG, Dupont G, Combettes L. 2013. Actin-based confinement of calcium responses during Shigella invasion. Nat Commun 4:1567 http://dx.doi.org/10.1038/ncomms2561. [PubMed]
16. Lum M, Morona R. 2014. Dynamin-related protein Drp1 and mitochondria are important for Shigella flexneri infection. Int J Med Microbiol 304:530–541 http://dx.doi.org/10.1016/j.ijmm.2014.03.006. [PubMed]
17. Mostowy S, Bonazzi M, Hamon MA, Tham TN, Mallet A, Lelek M, Gouin E, Demangel C, Brosch R, Zimmer C, Sartori A, Kinoshita M, Lecuit M, Cossart P. 2010. Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8:433–444 http://dx.doi.org/10.1016/j.chom.2010.10.009. [PubMed]
18. Sirianni A, Krokowski S, Lobato-Márquez D, Buranyi S, Pfanzelter J, Galea D, Willis A, Culley S, Henriques R, Larrouy-Maumus G, Hollinshead M, Sancho-Shimizu V, Way M, Mostowy S. 2016. Mitochondria mediate septin cage assembly to promote autophagy of Shigella. EMBO Rep 17:1029–1043 http://dx.doi.org/10.15252/embr.201541832. [PubMed]
19. Carneiro LAM, Travassos LH, Soares F, Tattoli I, Magalhaes JG, Bozza MT, Plotkowski MC, Sansonetti PJ, Molkentin JD, Philpott DJ, Girardin SE. 2009. Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 5:123–136 http://dx.doi.org/10.1016/j.chom.2008.12.011. [PubMed]
20. Koterski JF, Nahvi M, Venkatesan MM, Haimovich B. 2005. Virulent Shigella flexneri causes damage to mitochondria and triggers necrosis in infected human monocyte-derived macrophages. Infect Immun 73:504–513 http://dx.doi.org/10.1128/IAI.73.1.504-513.2005. [PubMed]
21. Sahni SK, Rydkina E. 2009. Host-cell interactions with pathogenic Rickettsia species. Future Microbiol 4:323–339 http://dx.doi.org/10.2217/fmb.09.6. [PubMed]
22. Martinez JJ, Cossart P. 2004. Early signaling events involved in the entry of Rickettsia conorii into mammalian cells. J Cell Sci 117:5097–5106 http://dx.doi.org/10.1242/jcs.01382. [PubMed]
23. Emelyanov VV, Vyssokikh MY. 2006. On the nature of obligate intracellular symbiosis of rickettsiae— Rickettsia prowazekii cells import mitochondrial porin. Biochemistry (Mosc) 71:730–735 http://dx.doi.org/10.1134/S0006297906070054.
24. Emelyanov VV. 2009. Mitochondrial porin VDAC 1 seems to be functional in rickettsial cells. Ann N Y Acad Sci 1166:38–48 http://dx.doi.org/10.1111/j.1749-6632.2009.04513.x. [PubMed]
25. Clifton DR, Goss RA, Sahni SK, van Antwerp D, Baggs RB, Marder VJ, Silverman DJ, Sporn LA. 1998. NF-κB-dependent inhibition of apoptosis is essential for host cellsurvival during Rickettsia rickettsii infection. Proc Natl Acad Sci USA 95:4646–4651 http://dx.doi.org/10.1073/pnas.95.8.4646. [PubMed]
26. Joshi SG, Francis CW, Silverman DJ, Sahni SK. 2003. Nuclear factor κB protects against host cell apoptosis during Rickettsia rickettsii infection by inhibiting activation of apical and effector caspases and maintaining mitochondrial integrity. Infect Immun 71:4127–4136 http://dx.doi.org/10.1128/IAI.71.7.4127-4136.2003. [PubMed]
27. Joshi SG, Francis CW, Silverman DJ, Sahni SK. 2004. NF-kappaB activation suppresses host cell apoptosis during Rickettsia rickettsii infection via regulatory effects on intracellular localization or levels of apoptogenic and anti-apoptotic proteins. FEMS Microbiol Lett 234:333–341. [PubMed]
28. Newton HJ, Ang DKY, van Driel IR, Hartland EL. 2010. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23:274–298 http://dx.doi.org/10.1128/CMR.00052-09. [PubMed]
29. Horwitz MA. 1983. Formation of a novel phagosome by the Legionnaires’ disease bacterium ( Legionella pneumophila) in human monocytes. J Exp Med 158:1319–1331 http://dx.doi.org/10.1084/jem.158.4.1319. [PubMed]
30. Newsome AL, Baker RL, Miller RD, Arnold RR. 1985. Interactions between Naegleria fowleri and Legionella pneumophila. Infect Immun 50:449–452. [PubMed]
31. Sun EW, Wagner ML, Maize A, Kemler D, Garland-Kuntz E, Xu L, Luo ZQ, Hollenbeck PJ. 2013. Legionella pneumophila infection of Drosophila S2 cells induces only minor changes in mitochondrial dynamics. PLoS One 8:e62972 http://dx.doi.org/10.1371/journal.pone.0062972. [PubMed]
32. Escoll P, Song OR, Viana F, Steiner B, Lagache T, Olivo-Marin JC, Impens F, Brodin P, Hilbi H, Buchrieser C. 2017. Legionella pneumophila modulates mitochondrial dynamics to trigger metabolic repurposing of infected macrophages. Cell Host Microbe 22:302–316.E7 http://dx.doi.org/10.1016/j.chom.2017.07.020. [PubMed]
33. Derré I, Isberg RR. 2004. Macrophages from mice with the restrictive Lgn1 allele exhibit multifactorial resistance to Legionella pneumophila. Infect Immun 72:6221–6229 http://dx.doi.org/10.1128/IAI.72.11.6221-6229.2004. [PubMed]
34. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR. 2006. A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc Natl Acad Sci USA 103:18745–18750 http://dx.doi.org/10.1073/pnas.0609012103. [PubMed]
35. Banga S, Gao P, Shen X, Fiscus V, Zong W-X, Chen L, Luo Z-Q. 2007. Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc Natl Acad Sci USA 104:5121–5126 http://dx.doi.org/10.1073/pnas.0611030104. [PubMed]
36. Dolezal P, Aili M, Tong J, Jiang JH, Marobbio CM, Lee SF, Schuelein R, Belluzzo S, Binova E, Mousnier A, Frankel G, Giannuzzi G, Palmieri F, Gabriel K, Naderer T, Hartland EL, Lithgow T. 2012. Legionella pneumophila secretes a mitochondrial carrier protein during infection. PLoS Pathog 8:e1002459. CORRECTION PLoS Pathog 8:10.1371/annotation/5039541e-b48a-4cfc-84b1-21566e311a62. CORRECTION PLoS Pathog 8:10.1371/annotation/ee7c807b-032c-4d1f-b5ac-0f6620a2ef24. http://dx.doi.org/10.1371/journal.ppat.1002459.
37. Corbett EL, Watt CJ, Walker N, Maher D, Williams BG, Raviglione MC, Dye C. 2003. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163:1009–1021 http://dx.doi.org/10.1001/archinte.163.9.1009. [PubMed]
38. Dubey RK. 2016. Assuming the role of mitochondria in mycobacterial infection. Int J Mycobacteriol 5:379–383 http://dx.doi.org/10.1016/j.ijmyco.2016.06.001. [PubMed]
39. Keane J, Balcewicz-Sablinska MK, Remold HG, Chupp GL, Meek BB, Fenton MJ, Kornfeld H. 1997. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 65:298–304. [PubMed]
40. Zhang J, Jiang R, Takayama H, Tanaka Y. 2005. Survival of virulent Mycobacterium tuberculosis involves preventing apoptosis induced by Bcl-2 upregulation and release resulting from necrosis in J774 macrophages. Microbiol Immunol 49:845–852 http://dx.doi.org/10.1111/j.1348-0421.2005.tb03673.x. [PubMed]
41. Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR. 2003. Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J Immunol 170:430–437 http://dx.doi.org/10.4049/jimmunol.170.1.430. [PubMed]
42. Chen M, Gan H, Remold HG. 2006. A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J Immunol 176:3707–3716 http://dx.doi.org/10.4049/jimmunol.176.6.3707. [PubMed]
43. Abarca-Rojano E, Rosas-Medina P, Zamudio-Cortéz P, Mondragón-Flores R, Sánchez-García FJ. 2003. Mycobacterium tuberculosis virulence correlates with mitochondrial cytochrome c release in infected macrophages. Scand J Immunol 58:419–427 http://dx.doi.org/10.1046/j.1365-3083.2003.01318.x. [PubMed]
44. Jamwal S, Midha MK, Verma HN, Basu A, Rao KVS, Manivel V. 2013. Characterizing virulence-specific perturbations in the mitochondrial function of macrophages infected with Mycobacterium tuberculosis. Sci Rep 3:1328 http://dx.doi.org/10.1038/srep01328. [PubMed]
45. Cheng EH-Y, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ. 2003. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301:513–517. [PubMed]
46. Fine-Coulson K, Giguère S, Quinn FD, Reaves BJ. 2015. Infection of A549 human type II epithelial cells with Mycobacterium tuberculosis induces changes in mitochondrial morphology, distribution and mass that are dependent on the early secreted antigen, ESAT-6. Microbes Infect 17:689–697 http://dx.doi.org/10.1016/j.micinf.2015.06.003.
47. Cossart P, Sansonetti PJ. 2004. Bacterial invasion: the paradigm of enteroinvasive pathogens. Science 304:242–248. [PubMed]
48. Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH. 2015. Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci 8:284–293 http://dx.doi.org/10.1080/21553769.2015.1051243.
49. Ruan H, Zhang Z, Tian L, Wang S, Hu S, Qiao JJ. 2016. The Salmonella effector SopB prevents ROS-induced apoptosis of epithelial cells by retarding TRAF6 recruitment to mitochondria. Biochem Biophys Res Commun 478:618–623 http://dx.doi.org/10.1016/j.bbrc.2016.07.116. [PubMed]
50. Sukumaran SK, Fu NY, Tin CB, Wan KF, Lee SS, Yu VC. 2010. A soluble form of the pilus protein FimA targets the VDAC-hexokinase complex at mitochondria to suppress host cell apoptosis. Mol Cell 37:768–783 http://dx.doi.org/10.1016/j.molcel.2010.02.015. [PubMed]
51. Layton AN, Brown PJ, Galyov EE. 2005. The Salmonella translocated effector SopA is targeted to the mitochondria of infected cells. J Bacteriol 187:3565–3571 http://dx.doi.org/10.1128/JB.187.10.3565-3571.2005. [PubMed]
52. Kamanova J, Sun H, Lara-Tejero M, Galán JE. 2016. The Salmonella effector protein SopA modulates innate immune responses by targeting TRIM E3 ligase family members. PLoS Pathog 12:e1005552 http://dx.doi.org/10.1371/journal.ppat.1005552. [PubMed]
53. Hernandez LD, Pypaert M, Flavell RA, Galán JE. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy. J Cell Biol 163:1123–1131 http://dx.doi.org/10.1083/jcb.200309161. [PubMed]
54. Elwell C, Mirrashidi K, Engel J. 2016. Chlamydia cell biology and pathogenesis. Nat Rev Microbiol 14:385–400 http://dx.doi.org/10.1038/nrmicro.2016.30. [PubMed]
55. Fischer SF, Harlander T, Vier J, Häcker G. 2004. Protection against CD95-induced apoptosis by chlamydial infection at a mitochondrial step. Infect Immun 72:1107–1115 http://dx.doi.org/10.1128/IAI.72.2.1107-1115.2004. [PubMed]
56. Fischer SF, Vier J, Kirschnek S, Klos A, Hess S, Ying S, Häcker G. 2004. Chlamydia inhibit host cell apoptosis by degradation of proapoptotic BH3-only proteins. J Exp Med 200:905–916 http://dx.doi.org/10.1084/jem.20040402. [PubMed]
57. Fan T, Lu H, Hu H, Shi L, McClarty GA, Nance DM, Greenberg AH, Zhong G. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med 187:487–496 http://dx.doi.org/10.1084/jem.187.4.487. [PubMed]
58. Moulder JW. 1962. Structure and chemical composition of isolated particles. Ann N Y Acad Sci 98:92–99 http://dx.doi.org/10.1111/j.1749-6632.1962.tb30535.x. [PubMed]
59. Hatch TP, Al-Hossainy E, Silverman JA. 1982. Adenine nucleotide and lysine transport in Chlamydia psittaci. J Bacteriol 150:662–670. [PubMed]
60. Matsumoto A. 1981. Isolation and electron microscopic observations of intracytoplasmic inclusions containing Chlamydia psittaci. J Bacteriol 145:605–612. [PubMed]
61. Matsumoto A, Bessho H, Uehira K, Suda T. 1991. Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J Electron Microsc (Tokyo) 40:356–363.
62. Chowdhury SR, Reimer A, Sharan M, Kozjak-Pavlovic V, Eulalio A, Prusty BK, Fraunholz M, Karunakaran K, Rudel T. 2017. Chlamydia preserves the mitochondrial network necessary for replication via microRNA-dependent inhibition of fission. J Cell Biol 216:1071–1089 http://dx.doi.org/10.1083/jcb.201608063. [PubMed]
63. Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. 2010. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet 6:e1000795. CORRECTION PLoS Genet 6:10.1371/annotation/4050116d-8daa-4b5a-99e9-34cdd13f6a26. http://dx.doi.org/10.1371/journal.pgen.1000795.
64. Liang P, Rosas-Lemus M, Patel D, Fang X, Tuz K, Juárez O. 2018. Dynamic energy dependency of Chlamydia trachomatis on host cell metabolism during intracellular growth: role of sodium-based energetics in chlamydial ATP generation. J Biol Chem 293:510–522 http://dx.doi.org/10.1074/jbc.M117.797209. [PubMed]
65. Käding N, Kaufhold I, Müller C, Szaszák M, Shima K, Weinmaier T, Lomas R, Conesa A, Schmitt-Kopplin P, Rattei T, Rupp J. 2017. Growth of Chlamydia pneumoniae is enhanced in cells with impaired mitochondrial function. Front Cell Infect Microbiol 7:499 http://dx.doi.org/10.3389/fcimb.2017.00499. [PubMed]
66. Rikihisa Y. 2015. Molecular pathogenesis of Ehrlichia chaffeensis infection. Annu Rev Microbiol 69:283–304 http://dx.doi.org/10.1146/annurev-micro-091014-104411. [PubMed]
67. Popov VL, Chen S-M, Feng H-M, Walker DH. 1995. Ultrastructural variation of cultured Ehrlichia chaffeensis. J Med Microbiol 43:411–421 http://dx.doi.org/10.1099/00222615-43-6-411. [PubMed]
68. Liu Y, Zhang Z, Jiang Y, Zhang L, Popov VL, Zhang J, Walker DH, Yu XJ. 2011. Obligate intracellular bacterium Ehrlichia inhibiting mitochondrial activity. Microbes Infect 13:232–238 http://dx.doi.org/10.1016/j.micinf.2010.10.021. [PubMed]
69. Von Ohlen T, Luce-Fedrow A, Ortega MT, Ganta RR, Chapes SK. 2012. Identification of critical host mitochondrion-associated genes during Ehrlichia chaffeensis infections. Infect Immun 80:3576–3586 http://dx.doi.org/10.1128/IAI.00670-12. [PubMed]
70. Liu H, Bao W, Lin M, Niu H, Rikihisa Y. 2012. Ehrlichia type IV secretion effector ECH0825 is translocated to mitochondria and curbs ROS and apoptosis by upregulating host MnSOD. Cell Microbiol 14:1037–1050 http://dx.doi.org/10.1111/j.1462-5822.2012.01775.x. [PubMed]
71. Zhang JZ, Sinha M, Luxon BA, Yu XJ. 2004. Survival strategy of obligately intracellular Ehrlichia chaffeensis: novel modulation of immune response and host cell cycles. Infect Immun 72:498–507 http://dx.doi.org/10.1128/IAI.72.1.498-507.2004. [PubMed]
72. Khan M, Syed GH, Kim SJ, Siddiqui A. 2015. Mitochondrial dynamics and viral infections: a close nexus. Biochim Biophys Acta 1853(10 Pt B) :2822–2833 http://dx.doi.org/10.1016/j.bbamcr.2014.12.040. [PubMed]
73. Willhite DC, Blanke SR. 2004. Helicobacter pylori vacuolating cytotoxin enters cells, localizes to the mitochondria, and induces mitochondrial membrane permeability changes correlated to toxin channel activity. Cell Microbiol 6:143–154 http://dx.doi.org/10.1046/j.1462-5822.2003.00347.x.
74. Foo JH, Culvenor JG, Ferrero RL, Kwok T, Lithgow T, Gabriel K. 2010. Both the p33 and p55 subunits of the Helicobacter pylori VacA toxin are targeted to mammalian mitochondria. J Mol Biol 401:792–798 http://dx.doi.org/10.1016/j.jmb.2010.06.065. [PubMed]
75. Suzuki M, Danilchanka O, Mekalanos JJ. 2014. Vibrio cholerae T3SS effector VopE modulates mitochondrial dynamics and innate immune signaling by targeting Miro GTPases. Cell Host Microbe 16:581–591 http://dx.doi.org/10.1016/j.chom.2014.09.015. [PubMed]
76. Nougayrède JP, Donnenberg MS. 2004. Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell Microbiol 6:1097–1111 http://dx.doi.org/10.1111/j.1462-5822.2004.00421.x. [PubMed]
77. Kenny B, Jepson M. 2000. Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2:579–590 http://dx.doi.org/10.1046/j.1462-5822.2000.00082.x. [PubMed]
78. Papatheodorou P, Domańska G, Öxle M, Mathieu J, Selchow O, Kenny B, Rassow J. 2006. The enteropathogenic Escherichia coli (EPEC) Map effector is imported into the mitochondrial matrix by the TOM/Hsp70 system and alters organelle morphology. Cell Microbiol 8:677–689 http://dx.doi.org/10.1111/j.1462-5822.2005.00660.x. [PubMed]
79. Sassera D, Beninati T, Bandi C, Bouman EAP, Sacchi L, Fabbi M, Lo N. 2006. ‘ Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int J Syst Evol Microbiol 56:2535–2540 http://dx.doi.org/10.1099/ijs.0.64386-0. [PubMed]
80. Shin JH, Yang JY, Jeon BY, Yoon YJ, Cho SN, Kang YH, Ryu DH, Hwang GS. 2011. 1H NMR-based metabolomic profiling in mice infected with Mycobacterium tuberculosis. J Proteome Res 10:2238–2247 http://dx.doi.org/10.1021/pr101054m. [PubMed]
81. Wyatt EV, Diaz K, Griffin AJ, Rassmussen JA, Crane DD, Jones BD, Bosio CM. 2016. Metabolic reprogramming of host cells by virulent Francisella tularensis for optimal replication and modulation of inflammation. J Immunol 196:4227–4236. [PubMed]
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/content/journal/microbiolspec/10.1128/microbiolspec.BAI-0016-2019
2019-03-08
2019-08-19

Abstract:

Mitochondria are essential and highly dynamic organelles whose morphology is determined by a steady-state balance between fusion and fission. Mitochondrial morphology and function are tightly connected. Because they are involved in many important cellular processes, including energy production, cell-autonomous immunity, and apoptosis, mitochondria present an attractive target for pathogens. Here, we explore the relationship between host cell mitochondria and intracellular bacteria, with a focus on mitochondrial morphology and function, as well as apoptosis. Modulation of apoptosis can allow bacteria to establish their replicative niche or support bacterial dissemination. Furthermore, bacteria can manipulate mitochondrial morphology and function through secreted effector proteins and can also contribute to the establishment of a successful infection, e.g., by favoring access to nutrients and/or evasion of the immune system.

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FIGURE 1

Strategies of intracellular bacteria to interfere with mitochondrial morphology. In epithelial cells, the secreted toxin LLO induces rapid mitochondrial fragmentation by pore formation in the plasma membrane, enabling calcium influx. Independent of Drp1 and Opa1, -induced mitochondrial fragmentation is of an atypical type; however, the ER and actin appear to play a regulatory role. The surface protein IcsA leads to Drp1-dependent mitochondrial fission in epithelial cells. Infecting macrophages, induces mitochondrial fragmentation in macrophages by the secreted MitF, which activates Ran GTPase and triggers Drp1 recruitment. Infection of epithelial cells with leads to mitochondrial fission, induced by the bacterial pore-forming toxin ESAT-6. In contrast to the other bacteria shown here, stabilizes the mitochondrial network; downregulating p53, the bacterium inhibits Drp1 expression and recruitment and prevents mitochondrial fragmentation.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0016-2019
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Image of FIGURE 2
FIGURE 2

Relationship between extracellular bacteria and host cell mitochondria. The extracellular bacterium secretes VacA, a pore-forming toxin, which localizes to the mitochondrial inner membrane and induces MOMP, resulting in apoptosis. EPEC interferes with mitochondrial morphology and function by the secretion of the effector proteins Map and EspF. Both proteins localize to the mitochondrial matrix, where Map leads to mitochondrial fragmentation and EspF induces MOMP and subsequent apoptosis. secreted VopE is a GTPase-activating protein that inactivates Miro at mitochondria, causing mitochondrial fragmentation and inhibiting kinesin-dependent mitochondrial motility. Movement is represented by dashed arrows, while solid arrows indicate induction.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0016-2019
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