Dynamin-related protein Drp1 and mitochondria are important for Shigella flexneri infection

International Journal of Medical Microbiology

Volumn 304, Issue 5-6, 2014, Pages 530-541

  Lum, Mabel ^a   Morona, Renato ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Cell death; Cell to cell spreading; Drp1; Mdivi 1; Mitochondria; Shigella flexneri

Indexed keywords

DYNAMIN; DYNAMIN RELATED PROTEIN DRP1; LACTATE DEHYDROGENASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; DNM1L PROTEIN, MOUSE;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL DEATH; CONTROLLED STUDY; CULTURE MEDIUM; ENTEROBACTERIACEAE; ENZYME RELEASE; HELA CELL LINE; HUMAN; HUMAN CELL; MITOCHONDRION; MOUSE; NONHUMAN; SHIGELLA FLEXNERI; SHIGELLOSIS; SUPERNATANT; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL DEATH; DISEASE MODELS, ANIMAL; DYNAMINS; DYSENTERY, BACILLARY; EPITHELIAL CELLS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; L-LACTATE DEHYDROGENASE; MICE, INBRED BALB C; MITOCHONDRIA; SHIGELLA FLEXNERI;

EID: 84903814955     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.03.006     Document Type: Article

References (59)

1. Ashida H., Mimuro H., Ogawa M., Kobayashi T., Sanada T., Kim M., Sasakawa C. Cell death and infection: a double-edged sword for host and pathogen survival. J. Cell Biol. 2011, 195:931-942.
2. Bardhan P., Faruque A., Naheed A., Sack D. Decrease in Shigellosis-related deaths without Shigella spp.-specific interventions, Asia. Emerg. Infect. Dis. 2010, 16:1718-1723.
3. Bergounioux J., Elisee R., Prunier A.-L., Donnadieu F., Sperandio B., Sansonetti P., Arbibe L. Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium's epithelial niche. Cell Host Microbe 2012, 11:240-252.
4. Bernardini M.L., Mounier J., d'Hauteville H., Coquis-Rondon M., Sansonetti P.J. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:3867-3871.
5. Bishai E.A., Sidhu G.S., Li W., Dhillon J., Bohil A.B., Cheney R.E., Hartwig J.H., Southwick F.S. Myosin-X facilitates Shigella-induced membrane protrusions and cell-to-cell spread. Cell. Microbiol. 2012, 15:353-367.
6. Carneiro L.A.M., Travassos L.H., Soares F., Tattoli I., Magalhaes J.G., Bozza M.T., Plotkowski M.C., Sansonetti P.J., Molkentin J.D., Philpott D.J., Girardin S.E. Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 2009, 5:123-136.
7. Cassidy-Stone A., Chipuk J.E., Ingerman E., Song C., Yoo C., Kuwana T., Kurth M.J., Shaw J.T., Hinshaw J.E., Green D.R., Nunnari J. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 2008, 14:193-204.
8. Cossart P., Sansonetti P.J. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 2004, 304:242-248.
9. Degterev A., Hitomi J., Germscheid M., Ch'en I.L., Korkina O., Teng X., Abbott D., Cuny G.D., Yuan C., Wagner G., Hedrick S.M., Gerber S.A., Lugovskoy A., Yuan J. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 2008, 4:313-321.
10. Dodo K., Katoh M., Shimizu T., Takahashi M., Sodeoka M. Inhibition of hydrogen peroxide-induced necrotic cell death with 3-amino-2-indolylmaleimide derivatives. Bioorg. Med. Chem. Lett. 2005, 15:3114-3118.
11. DuBoff B., Götz J., Feany, Mel B. Tau promotes neurodegeneration via DRP1 mislocalization in vivo. Neuron 2012, 75:618-632.
12. Faherty C.S., Maurelli A.T. Spa15 of Shigella flexneri is secreted through the type III secretion system and prevents staurosporine-induced apoptosis. Infect. Immun. 2009, 77:5281-5290.
13. Ferrari L.F., Chum A., Bogen O., Reichling D.B., Levine J.D. Role of Drp1, a key mitochondrial fission protein, in neuropathic pain. J. Neurosci. 2011, 31:11404-11410.
14. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 2001, 1:515-525.
15. Friedman J.R., Lackner L.L., West M., DiBenedetto J.R., Nunnari J., Voeltz G.K. ER tubules mark sites of mitochondrial division. Science 2011, 334:358-362.
16. Fukumatsu M., Ogawa M., Arakawa S., Suzuki M., Nakayama K., Shimizu S., Kim M., Mimuro H., Sasakawa C. Shigella targets epithelial tricellular junctions and uses a noncanonical clathrin-dependent endocytic pathway to spread between cells. Cell Host Microbe 2012, 11:325-336.
17. Golstein P., Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 2007, 32:37-43.
18. Gouin E., Welch M.D., Cossart P. Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 2005, 8:35-45.
19. Heindl J.E., Saran I., Yi C.-r., Lesser C.F., Goldberg M.B. Requirement for formin-induced actin polymerization during spread of Shigella. Infect. Immun. 2009, 78:193-203.
20. Jain P., Luo Z.-Q., Blanke S.R. 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.
21. Kadurugamuwa J.L., Rohde M., Wehland J., Timmis K.N. Intercellular spread of Shigella flexneri through a monolayer mediated by membranous protrusions and associated with reorganization of the cytoskeletal protein vinculin. Infect. Immun. 1991, 59:3463-3471.
22. Kim H.J., Koo S.Y., Ahn B.H., Park O., Park D.H., Seo D.O., Won J.H., Yim H.J., Kwak H.S., Park H.S., Chung C.W., Oh Y.L., Kim S.H. NecroX as a novel class of mitochondrial reactive oxygen species and ONOO(-) scavenger. Arch. Pharm. Res. 2010, 33:1813-1823.
23. Kobayashi T., Ogawa M., Sanada T., Mimuro H., Kim M., Ashida H., Akakura R., Yoshida M., Kawalec M., Reichhart J.-M., Mizushima T., Sasakawa C. The Shigella OspC3 effector inhibits caspase-4, antagonizes inflammatory cell death, and promotes epithelial infection. Cell Host Microbe 2013, 13:570-583.
24. Korobova F., Ramabhadran V., Higgs H.N. An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 2013, 339:464-467.
25. Kwon C.H., Wheeldon I., Kachouie N.N., Lee S.H., Bae H., Sant S., Fukuda J., Kang J.W., Khademhosseini A. Drug-eluting microarrays for cell-based screening of chemical-induced apoptosis. Anal. Chem. 2011, 83:4118-4125.
26. Lacayo C.I., Theriot J.A. Listeria monocytogenes actin-based motility varies depending on subcellular location: a kinematic probe for cytoarchitecture. Mol. Biol. Cell 2004, 15:2164-2175.
27. Lamkanfi M., Dixit V.M. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 2010, 8:44-54.
28. Lembo-Fazio L., Nigro G., Noel G., Rossi G., Chiara F., Tsilingiri K., Rescigno M., Rasola A., Bernardini M.L. Gadd45[alpha] activity is the principal effector of Shigella mitochondria-dependent epithelial cell death in vitro and ex vivo. Cell Death Dis. 2011, 2:e122.
29. Lett M.C., Sasakawa C., Okada N., Sakai T., Makino S., Yamada M., Komatsu K., Yoshikawa M. virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J. Bacteriol. 1989, 171:353-359.
30. Lum M., Attridge S.R., Morona R. Impact of dynasore an inhibitor of dynamin II on Shigella flexneri infection. PLoS ONE 2013, 8:e84975.
31. Makino S., Sasakawa C., Kamata K., Kurata T., Yoshikawa M. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a. Cell 1986, 46:551-555.
32. Mantis N., Prévost M.C., Sansonetti P. Analysis of epithelial cell stress response during infection by Shigella flexneri. Infect. Immun. 1996, 64:2474-2482.
33. Morona R., Daniels C., Van Den Bosch L. Genetic modulation of Shigella flexneri 2a lipopolysaccharide O antigen modal chain length reveals that it has been optimized for virulence. Microbiol. 2003, 149:925-939.
34. Morona R., Van Den Bosch L. Lipopolysaccharide O antigen chains mask IcsA (VirG) in Shigella flexneri. FEMS Microbiol. Lett. 2003, 221:173-180.
35. Murayama S.Y., Sakai T., Makino S., Kurata T., Sasakawa C., Yoshikawa M. The use of mice in the Sereny test as a virulence assay of Shigellae and enteroinvasive Escherichia coli. Infect. Immun. 1986, 51:696-698.
36. Nicolier M., Decrion-Barthod A.-Z., Launay S., Prétet J.-L., Mougin C. Spatiotemporal activation of caspase-dependent and -independent pathways in staurosporine-induced apoptosis of p53wt and p53mt human cervical carcinoma cells. Biol. Cell 2009, 101:455-467.
37. Oaks E.V., Wingfield M.E., Formal S.B. Plaque formation by virulent Shigella flexneri. Infect. Immun. 1985, 48:124-129.
38. Ong S.B., Subrayan S., Lim S.Y., Yellon D.M., Davidson S.M., Hausenloy D.J. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 2010, 121:2012-2022.
39. Otera H., Ishihara N., Mihara K. New insights into the function and regulation of mitochondrial fission. BBA-Mol. Cell. Res. 2013, 1833:1256-1268.
40. Otera H., Wang C., Cleland M.M., Setoguchi K., Yokota S., Youle R.J., Mihara K. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 2010, 191:1141-1158.
41. Reed J.C. Mechanisms of apoptosis. Am. J. Pathol. 2000, 157:1415-1430.
42. Sansonetti P.J., Mounier J., Prévost M.C., Mege R.M. Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 1994, 76:829-839.
43. Sansonetti P.J., Phalipon A., Arondel J., Thirumalai K., Banerjee S., Akira S., Takeda K., Zychlinsky A. Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 2000, 12:581-590.
44. Sansonetti P.J., Ryter A., Clerc P., Maurelli A.T., Mounier J. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect. Immun. 1986, 51:461-469.
45. Schuch R., Sandlin R.C., Maurelli A.T. A system for identifying post-invasion functions of invasion genes: requirements for the Mxi-Spa type III secretion pathway of Shigella flexneri in intercellular dissemination. Mol. Microbiol. 1999, 34:675-689.
46. Senerovic L., Tsunoda S.P., Goosmann C., Brinkmann V., Zychlinsky A., Meissner F., Kolbe M. Spontaneous formation of IpaB ion channels in host cell membranes reveals how Shigella induces pyroptosis in macrophages. Cell Death Dis. 2012, 3:e384.
47. Smirnova E., Griparic L., Shurland D.-L., van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 2001, 12:2245-2256.
48. Smirnova E., Shurland D.-L., Ryazantsev S.N., van der Bliek A.M. A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 1998, 143:351-358.
49. Stavru F., Bouillaud F., Sartori A., Ricquier D., Cossart P. Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3612-3617.
50. Stavru F., Palmer A.E., Wang C., Youle R.J., Cossart P. Atypical mitochondrial fission upon bacterial infection. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:16003-16008.
51. Sun L., Wang H., Wang Z., He S., Chen S., Liao D., Wang L., Yan J., Liu W., Lei X., Wang X. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012, 148:213-227.
52. Suzuki T., Franchi L., Toma C., Ashida H., Ogawa M., Yoshikawa Y., Mimuro H., Inohara N., Sasakawa C., Nunez G. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 2007, 3:e111.
53. Tang W.X., Wu W.H., Qiu H.Y., Bo H., Huang S.M. Amelioration of rhabdomyolysis-induced renal mitochondrial injury and apoptosis through suppression of Drp-1 translocation. J. Nephrol. 2013, 26:1073-1082.
54. Tran Van Nhieu G., Clair C., Bruzzone R., Mesnil M., Sansonetti P., Combettes L. Connexin-dependent inter-cellular communication increases invasion and dissemination of Shigella in epithelial cells. Nat. Cell Biol. 2003, 5:720-726.
55. Vandenabeele P., Galluzzi L., Vanden Berghe T., Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11:700-714.
56. Wang Z., Jiang H., Chen S., Du F., Wang X. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 2012, 148:228-243.
57. Wasiak S., Zunino R., McBride H.M. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 2007, 177:439-450.
58. Willingham S.B., Bergstralh D.T., O'Connor W., Morrison A.C., Taxman D.J., Duncan J.A., Barnoy S., Venkatesan M.M., Flavell R.A., Deshmukh M., Hoffman H.M., Ting J.P. Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2007, 2:147-159.
59. Zheng W., Degterev A., Hsu E., Yuan J., Yuan C. Structure-activity relationship study of a novel necroptosis inhibitor, necrostatin-7. Bioorg. Med. Chem. Lett. 2008, 18:4932-4935.