Mitochondria mediate septin cage assembly to promote autophagy of Shigella

EMBO Reports

Volumn 17, Issue 7, 2016, Pages 1029-1043

  Sirianni, Andrea ^a   Krokowski, Sina ^a   Lobato Márquez, Damián ^a   Buranyi, Stephen ^a   Pfanzelter, Julia ^b   Galea, Dieter ^a   Willis, Alexandra ^a   Culley, Siân ^c   Henriques, Ricardo ^c   Larrouy Maumus, Gerald ^a   Hollinshead, Michael ^d   Sancho Shimizu, Vanessa ^a   Way, Michael ^a,b   Mostowy, Serge ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

autophagy; cytoskeleton; mitochondria; septin; Shigella

Indexed keywords

DYNAMIN RELATED PROTEIN 1; GUANOSINE TRIPHOSPHATASE; MITOCHONDRIAL PROTEIN; PEPTIDE FRAGMENT; SEPTIN; SEPTIN 2; SEPTIN 3; SEPTIN 6; SEPTIN 7; SMALL INTERFERING RNA; SYNAPSIN I; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; BACTERIAL INFECTION; CELL PROLIFERATION; FEMALE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MITOPHAGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SEPTIN CAGE ASSEMBLY; SHIGELLA FLEXNERI;

EID: 84977490585     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201541832     Document Type: Article

References (54)

1. Feng Y, He D, Yao Z, Klionsky DJ (2014) The machinery of macroautophagy. Cell Res 24: 24–41
2. Levine B, Mizushima N, Virgin HW (2011) Autophagy in immunity and inflammation. Nature 469: 323–335
3. Shibutani ST, Saitoh T, Nowag H, Munz C, Yoshimori T (2015) Autophagy and autophagy-related proteins in the immune system. Nat Immunol 16: 1014–1024
4. Randow F, Youle Richard J (2014) Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe 15: 403–411
5. Stolz A, Ernst A, Dikic I (2014) Cargo recognition and trafficking in selective autophagy. Nat Cell Biol 16: 495–501
6. Mostowy S (2014) Multiple roles of the cytoskeleton in bacterial autophagy. PLoS Pathog 10: e1004409
7. Monastyrska I, Rieter E, Klionsky DJ, Reggiori F (2009) Multiple roles of the cytoskeleton in autophagy. Biol Rev 84: 431–448
8. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M, Kim M, Mimuro H, Nakagawa I, Yanagawa T, Ishii T, et al (2009) Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 11: 1233–1240
9. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C (2005) Escape of intracellular Shigella from autophagy. Science 307: 727–731
10. Mostowy S, Cossart P (2012) Septins: the fourth component of the cytoskeleton. Nat Rev Mol Cell Biol 13: 183–194
11. Saarikangas J, Barral Y (2011) The emerging functions of septins in metazoans. EMBO Rep 12: 1118–1126
12. Mostowy S, Bonazzi M, Hamon MA, Tham TN, Mallet A, Lelek M, Gouin E, Demangel C, Brosch R, Zimmer C, et al (2010) Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8: 433–444
13. Mostowy S, Sancho-Shimizu V, Hamon MA, Simeone R, Brosch R, Johansen T, Cossart P (2011) p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J Biol Chem 286: 26987–26995
14. Mostowy S, Boucontet L, Mazon Moya MJ, Sirianni A, Boudinot P, Hollinshead M, Cossart P, Herbomel P, Levraud J-P, Colucci-Guyon E (2013) The zebrafish as a new model for the in vivo study of Shigella flexneri interaction with phagocytes and bacterial autophagy. PLoS Pathog 9: e1003588
15. Sirajuddin M, Farkasovsky M, Hauer F, Kuhlmann D, Macara IG, Weyand M, Stark H, Wittinghofer A (2007) Structural insight into filament formation by mammalian septins. Nature 449: 311–315
16. John CM, Hite RK, Weirich CS, Fitzgerald DJ, Jawhari H, Faty M, Schläpfer D, Kroschewski R, Winkler FK, Walz T, et al (2007) The Caenorhabditis elegans septin complex is nonpolar. EMBO J 26: 3296–3307
17. Bertin A, McMurray MA, Grob P, Park S-S, Garcia G, Patanwala I, Ng H-l, Alber T, Thorner J, Nogales E (2008) Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc Natl Acad Sci USA 105: 8274–8279
18. Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ (2002) Self- and actin-templated assembly of mammalian septins. Dev Cell 3: 791–802
19. Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J (2011) Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci USA 108: 10190–10195
20. Gomes LC, Benedetto GD, Scorrano L (2011) During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13: 589–598
21. Praefcke GJK, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5: 133–147
22. Schrepfer E, Scorrano L (2016) Mitofusins, from mitochondria to metabolism. Mol Cell 61: 683–694
23. Hatch AL, Gurel PS, Higgs HN (2014) Novel roles for actin in mitochondrial fission. J Cell Sci 127: 4549–4560
24. Li S, Xu S, Roelofs BA, Boyman L, Lederer WJ, Sesaki H, Karbowski M (2015) Transient assembly of F-actin on the outer mitochondrial membrane contributes to mitochondrial fission. J Cell Biol 208: 109–123
25. Manor U, Bartholomew S, Golani G, Christenson E, Kozlov M, Higgs H, Spudich J, Lippincott-Schwartz J (2015) A mitochondria-anchored isoform of the actin-nucleating Spire protein regulates mitochondrial division. eLife 4: e08828
26. Korobova F, Ramabhadran V, Higgs HN (2013) An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339: 464–467
27. Korobova F, Gauvin Timothy J, Higgs Henry N (2014) A role for myosin II in mammalian mitochondrial fission. Curr Biol 24: 409–414
28. De Vos KJ, Allan VJ, Grierson AJ, Sheetz MP (2005) Mitochondrial function and actin regulate dynamin-related protein 1-dependent mitochondrial fission. Curr Biol 15: 678–683
29. Glotzer M (2005) The molecular requirements for cytokinesis. Science 307: 1735–1739
30. Kissel H, Georgescu M-M, Larisch S, Manova K, Hunnicutt GR, Steller H (2005) The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev Cell 8: 353–364
31. Pistor S, Chakraborty T, Niebuhr K, Domann E, Wehland J (1994) The ActA protein of Listeria monocytogenes acts as a nucleator inducing reorganization of the actin cytoskeleton. EMBO J 13: 758–763
32. Chang C-R, Blackstone C (2010) Dynamic regulation of mitochondrial fission through modification of the dynamin-related protein Drp1. Ann N Y Acad Sci 1201: 34–39
33. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282: 11521–11529
34. Carneiro LAM, Travassos LH, Soares F, Tattoli I, Magalhaes JG, Bozza MT, Plotkowski MC, Sansonetti PJ, Molkentin JD, Philpott DJ, et al (2009) Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 5: 123–136
35. Tattoli I, Sorbara MT, Vuckovic D, Ling A, Soares F, Carneiro Leticia AM, Yang C, Emili A, Philpott Dana J, Girardin Stephen E (2012) Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe 11: 563–575
36. Lum M, Morona R (2014) Dynamin-related protein Drp1 and mitochondria are important for Shigella flexneri infection. Int J Med Microbiol 304: 530–541
37. 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
38. Welch MD, Way M (2013) Arp2/3-mediated actin-based motility: a tail of pathogen abuse. Cell Host Microbe 14: 242–255
39. Friedman JR, Nunnari J (2014) Mitochondrial form and function. Nature 505: 335–343
40. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK (2011) ER tubules mark sites of mitochondrial division. Science 334: 358–362
41. Phillips MJ, Voeltz GK (2016) Structure and function of ER membrane contact sites with other organelles. Nat Rev Mol Cell Biol 17: 69–82
42. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, Lippincott-Schwartz J (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141: 656–667
43. Bridges AA, Jentzsch MS, Oakes PW, Occhipinti P, Gladfelter AS (2016) Micron-scale plasma membrane curvature is recognized by the septin cytoskeleton. J Cell Biol 213: 23–32
44. Bezanilla M, Gladfelter AS, Kovar DR, Lee W-L (2015) Cytoskeletal dynamics: a view from the membrane. J Cell Biol 209: 329–337
45. Tanaka-Takiguchi Y, Kinoshita M, Takiguchi K (2009) Septin-mediated uniform bracing of phospholipid membranes. Curr Biol 19: 140–145
46. Mostowy S, Shenoy AR (2015) The cytoskeleton in cell-autonomous immunity: structural determinants of host defence. Nat Rev Immunol 15: 559–573
47. Mazon Moya MJ, Colucci-Guyon E, Mostowy S (2014) Use of Shigella flexneri to study autophagy-cytoskeleton interactions. J Vis Exp 91: e51601
48. Schlosser-Silverman E, Elgrably-Weiss M, Rosenshine I, Kohen R, Altuvia S (2000) Characterization of Escherichia coli DNA lesions generated within J774 macrophages. J Bacteriol 182: 5225–5230
49. Barry DJ, Durkin CH, Abella JV, Way M (2015) Open source software for quantification of cell migration, protrusions, and fluorescence intensities. J Cell Biol 209: 163–180
50. Santos J, Cerveira N, Bizarro S, Ribeiro FR, Correia C, Torres L, Lisboa S, Vieira J, Mariz JM, Norton L, et al (2010) Expression pattern of the septin gene family in acute myeloid leukemias with and without MLL-SEPT fusion genes. Leuk Res 34: 615–621
51. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676–682
52. de Chaumont F, Dallongeville S, Chenouard N, Herve N, Pop S, Provoost T, Meas-Yedid V, Pankajakshan P, Lecomte T, Le Montagner Y, et al (2012) Icy: an open bioimage informatics platform for extended reproducible research. Nat Meth 9: 690–696
53. Hollinshead M, Johns HL, Sayers CL, Gonzalez-Lopez C, Smith GL, Elliott G (2012) Endocytic tubules regulated by Rab GTPases 5 and 11 are used for envelopment of herpes simplex virus. EMBO J 31: 4204–4220
54. Dertinger T, Colyer R, Iyer G, Weiss S, Enderlein J (2009) Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI). Proc Natl Acad Sci USA 106: 22287–22292