PLEKHM1 regulates salmonella-containing vacuole biogenesis and infection

Cell Host and Microbe

Volumn 17, Issue 1, 2015, Pages 58-71

  McEwan, David G ^a   Richter, Benjamin ^a   Claudi, Beatrice ^b   Wigge, Christoph ^c   Wild, Philipp ^a   Farhan, Hesso ^b,d   McGourty, Kieran ^e   Coxon, Fraser P ^f   Franz Wachtel, Mirita ^g   Perdu, Bram ^h   Akutsu, Masato ^b   Habermann, Anja ^c   Kirchof, Anja ^a   Helfrich, Miep H ^f   Odgren, Paul R ⁱ   Van Hul, Wim ^h   Frangakis, Achilleas S ^b   Rajalingam, Krishnaraj ^j   Macek, Boris ^g   Holden, David W ^e   Bumann, Dirk ^b   Dikic, Ivan ^a,c,k   more..

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c GOETHE UNIVERSITY   (Germany)

^d UNIVERSITY OF KONSTANZ   (Switzerland)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF ABERDEEN   (United Kingdom)

^g UNIVERSITY OF TÜBINGEN   (Germany)

^h UNIVERSITY OF ANTWERP   (Belgium)

ⁱ UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^j JOHANNES GUTENBERG UNIVERSITY   (Germany)

^k UNIVERSITY OF SPLIT   (Croatia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BACTERIAL PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; PLECKSTRIN HOMOLOGY DOMAIN CONTAINING PROTEIN FAMILY MEMBER 1; RAB7 PROTEIN; SALMONELLA INDUCED FILAMENT PROTEIN A; UNCLASSIFIED DRUG; CARRIER PROTEIN; GLYCOPROTEIN; HOPS PROTEIN, MOUSE; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PLEKHM1 PROTEIN, HUMAN; PROTEIN BINDING; RAB PROTEIN; SIFA PROTEIN, SALMONELLA; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIUM COLONY; BIOGENESIS; CELL PROLIFERATION; CELL VACUOLE; CONTROLLED STUDY; EMBRYO; HELA CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; TYPE III SECRETION SYSTEM; ANIMAL; C57BL MOUSE; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PROTEIN ANALYSIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

BACTERIA (MICROORGANISMS); MUS; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; STRAWBERRY CRINKLE VIRUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; GLYCOPROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RAB GTP-BINDING PROTEINS; SALMONELLA TYPHIMURIUM; VACUOLES;

EID: 84920984853     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.11.011     Document Type: Article

References (49)

1. H.J. Balderhaar, and C. Ungermann CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion J. Cell Sci. 126 2013 1307 1316
2. W. Berón, M.G. Gutierrez, M. Rabinovitch, and M.I. Colombo Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics Infect. Immun. 70 2002 5816 5821
3. C.R. Beuzón, S. Méresse, K.E. Unsworth, J. Ruíz-Albert, S. Garvis, S.R. Waterman, T.A. Ryder, E. Boucrot, and D.W. Holden Salmonella maintains the integrity of its intracellular vacuole through the action of SifA EMBO J. 19 2000 3235 3249
4. C.L. Birmingham, A.C. Smith, M.A. Bakowski, T. Yoshimori, and J.H. Brumell Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole J. Biol. Chem. 281 2006 11374 11383
5. E. Boucrot, T. Henry, J.P. Borg, J.P. Gorvel, and S. Méresse The intracellular fate of Salmonella depends on the recruitment of kinesin Science 308 2005 1174 1178
6. C. Bröcker, A. Kuhlee, C. Gatsogiannis, H.J. Balderhaar, C. Hönscher, S. Engelbrecht-Vandré, C. Ungermann, and S. Raunser Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex Proc. Natl. Acad. Sci. USA 109 2012 1991 1996
7. J.H. Brumell, D.L. Goosney, and B.B. Finlay SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules Traffic 3 2002 407 415
8. S. Caplan, L.M. Hartnell, R.C. Aguilar, N. Naslavsky, and J.S. Bonifacino Human Vam6p promotes lysosome clustering and fusion in vivo J. Cell Biol. 154 2001 109 122
9. J.E. Carette, M. Raaben, A.C. Wong, A.S. Herbert, G. Obernosterer, N. Mulherkar, A.I. Kuehne, P.J. Kranzusch, A.M. Griffin, and G. Ruthel Ebola virus entry requires the cholesterol transporter Niemann-Pick C1 Nature 477 2011 340 343
10. M. Cemma, P.K. Kim, and J.H. Brumell The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteria-associated microdomains to target Salmonella to the autophagy pathway Autophagy 7 2011 341 345
11. L. Diacovich, A. Dumont, D. Lafitte, E. Soprano, A.A. Guilhon, C. Bignon, J.P. Gorvel, Y. Bourne, and S. Méresse Interaction between the SifA virulence factor and its host target SKIP is essential for Salmonella pathogenesis J. Biol. Chem. 284 2009 33151 33160
12. A. Dumont, E. Boucrot, S. Drevensek, V. Daire, J.P. Gorvel, C. Poüs, D.W. Holden, and S. Méresse SKIP, the host target of the Salmonella virulence factor SifA, promotes kinesin-1-dependent vacuolar membrane exchanges Traffic 11 2010 899 911
13. L.C. Gomes, and I. Dikic Autophagy in antimicrobial immunity Mol. Cell 54 2014 224 233
14. J.P. Gorvel, and S. Meresse Maturation steps of the Salmonella-containing vacuole Microbes Infect. 3 2001 1299 1303
15. J. Guignot, E. Caron, C. Beuzón, C. Bucci, J. Kagan, C. Roy, and D.W. Holden Microtubule motors control membrane dynamics of Salmonella-containing vacuoles J. Cell Sci. 117 2004 1033 1045
16. R.E. Harrison, J.H. Brumell, A. Khandani, C. Bucci, C.C. Scott, X. Jiang, B.B. Finlay, and S. Grinstein Salmonella impairs RILP recruitment to Rab7 during maturation of invasion vacuoles Mol. Biol. Cell 15 2004 3146 3154
17. L.K. Jackson, P. Nawabi, C. Hentea, E.A. Roark, and K. Haldar The Salmonella virulence protein SifA is a G protein antagonist Proc. Natl. Acad. Sci. USA 105 2008 14141 14146
18. V.I. Korolchuk, S. Saiki, M. Lichtenberg, F.H. Siddiqi, E.A. Roberts, S. Imarisio, L. Jahreiss, S. Sarkar, M. Futter, and F.M. Menzies Lysosomal positioning coordinates cellular nutrient responses Nat. Cell Biol. 13 2011 453 460
19. V. Krieger, D. Liebl, Y. Zhang, R. Rajashekar, P. Chlanda, K. Giesker, D. Chikkaballi, and M. Hensel Reorganization of the endosomal system in Salmonella-infected cells: the ultrastructure of Salmonella-induced tubular compartments PLoS Pathog. 10 2014 e1004374
20. V. Kuhle, D. Jäckel, and M. Hensel Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells Traffic 5 2004 356 370
21. D.G. McEwan, D. Popovic, A. Gubas, S. Terawaki, and H. Suzuki PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins Mol. Cell 57 2015 39 54 this issue
22. K. McGourty, T.L. Thurston, S.A. Matthews, L. Pinaud, L.J. Mota, and D.W. Holden Salmonella inhibits retrograde trafficking of mannose-6-phosphate receptors and lysosome function Science 338 2012 963 967
23. S. Méresse, O. Steele-Mortimer, B.B. Finlay, and J.P. Gorvel The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells EMBO J. 18 1999 4394 4403
24. L.J. Mota, A.E. Ramsden, M. Liu, J.D. Castle, and D.W. Holden SCAMP3 is a component of the Salmonella-induced tubular network and reveals an interaction between bacterial effectors and post-Golgi trafficking Cell. Microbiol. 11 2009 1236 1253
25. M. Nordmann, M. Cabrera, A. Perz, C. Bröcker, C. Ostrowicz, S. Engelbrecht-Vandré, and C. Ungermann The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7 Curr. Biol. 20 2010 1654 1659
26. M.B. Ohlson, Z. Huang, N.M. Alto, M.P. Blanc, J.E. Dixon, J. Chai, and S.I. Miller Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation Cell Host Microbe 4 2008 434 446
27. S. Pankiv, E.A. Alemu, A. Brech, J.A. Bruun, T. Lamark, A. Overvatn, G. Bjørkøy, and T. Johansen FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport J. Cell Biol. 188 2010 253 269
28. E. Papini, M. de Bernard, E. Milia, M. Bugnoli, M. Zerial, R. Rappuoli, and C. Montecucco Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments Proc. Natl. Acad. Sci. USA 91 1994 9720 9724
29. J.C. Patel, and J.E. Galán Manipulation of the host actin cytoskeleton by Salmonella - all in the name of entry Curr. Opin. Microbiol. 8 2005 10 15
30. E.R. Peralta, B.C. Martin, and A.L. Edinger Differential effects of TBC1D15 and mammalian Vps39 on Rab7 activation state, lysosomal morphology, and growth factor dependence J. Biol. Chem. 285 2010 16814 16821
31. M.S. Pols, E. van Meel, V. Oorschot, C. ten Brink, M. Fukuda, M.G. Swetha, S. Mayor, and J. Klumperman hVps41 and VAMP7 function in direct TGN to late endosome transport of lysosomal membrane proteins Nat. Commun. 4 2013 10.1038/ncomms2360
32. A.E. Ramsden, D.W. Holden, and L.J. Mota Membrane dynamics and spatial distribution of Salmonella-containing vacuoles Trends Microbiol. 15 2007 516 524
33. J. Rink, E. Ghigo, Y. Kalaidzidis, and M. Zerial Rab conversion as a mechanism of progression from early to late endosomes Cell 122 2005 735 749
34. V.V. Rogov, H. Suzuki, E. Fiskin, P. Wild, A. Kniss, A. Rozenknop, R. Kato, M. Kawasaki, D.G. McEwan, and F. Löhr Structural basis for phosphorylation-triggered autophagic clearance of Salmonella Biochem. J. 454 2013 459 466
35. J. Ruiz-Albert, X.J. Yu, C.R. Beuzón, A.N. Blakey, E.E. Galyov, and D.W. Holden Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane Mol. Microbiol. 44 2002 645 661
36. N. Schroeder, T. Henry, C. de Chastellier, W. Zhao, A.A. Guilhon, J.P. Gorvel, and S. Méresse The virulence protein SopD2 regulates membrane dynamics of Salmonella-containing vacuoles PLoS Pathog. 6 2010 e1001002
37. M.N. Seaman, M.E. Harbour, D. Tattersall, E. Read, and N. Bright Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5 J. Cell Sci. 122 2009 2371 2382
38. S. Shahnazari, W.L. Yen, C.L. Birmingham, J. Shiu, A. Namolovan, Y.T. Zheng, K. Nakayama, D.J. Klionsky, and J.H. Brumell A diacylglycerol-dependent signaling pathway contributes to regulation of antibacterial autophagy Cell Host Microbe 8 2010 137 146
39. O. Steele-Mortimer, S. Méresse, J.P. Gorvel, B.H. Toh, and B.B. Finlay Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway Cell. Microbiol. 1 1999 33 49
40. M.A. Stein, K.Y. Leung, M. Zwick, F. Garcia-del Portillo, and B.B. Finlay Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells Mol. Microbiol. 20 1996 151 164
41. H. Stenmark Rab GTPases as coordinators of vesicle traffic Nat. Rev. Mol. Cell Biol. 10 2009 513 525
42. J. Sun, A.E. Deghmane, C. Bucci, and Z. Hmama Detection of activated Rab7 GTPase with an immobilized RILP probe Methods Mol. Biol. 531 2009 57 69
43. Q. Sun, W. Westphal, K.N. Wong, I. Tan, and Q. Zhong Rubicon controls endosome maturation as a Rab7 effector Proc. Natl. Acad. Sci. USA 107 2010 19338 19343
44. K. Tabata, K. Matsunaga, A. Sakane, T. Sasaki, T. Noda, and T. Yoshimori Rubicon and PLEKHM1 negatively regulate the endocytic/autophagic pathway via a novel Rab7-binding domain Mol. Biol. Cell 21 2010 4162 4172
45. T.L. Thurston, G. Ryzhakov, S. Bloor, N. von Muhlinen, and F. Randow The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria Nat. Immunol. 10 2009 1215 1221
46. R. van der Kant, A. Fish, L. Janssen, H. Janssen, S. Krom, N. Ho, T. Brummelkamp, J. Carette, N. Rocha, and J. Neefjes Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L J. Cell Sci. 126 2013 3462 3474
47. L.E. Via, D. Deretic, R.J. Ulmer, N.S. Hibler, L.A. Huber, and V. Deretic Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7 J. Biol. Chem. 272 1997 13326 13331
48. P. Wild, H. Farhan, D.G. McEwan, S. Wagner, V.V. Rogov, N.R. Brady, B. Richter, J. Korac, O. Waidmann, and C. Choudhary Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth Science 333 2011 228 233
49. Y.T. Zheng, S. Shahnazari, A. Brech, T. Lamark, T. Johansen, and J.H. Brumell The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway J. Immunol. 183 2009 5909 5916