The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular salmonella typhimurium

Cell Host and Microbe

Volumn 12, Issue 6, 2012, Pages 778-790

  Huett, Alan ^a,d   Heath, Robert J ^a,b   Begun, Jakob ^a   Sassi, Slim O ^a,c   Baxt, Leigh A ^a   Vyas, Jatin M ^a   Goldberg, Marcia B ^a   Xavier, Ramnik J ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE; LEUCINE RICH REPEAT; LRSAM1 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CELL INVASION; CYTOPLASM; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SALMONELLA TYPHIMURIUM; UBIQUITINATION;

AUTOPHAGY; GENE KNOCKOUT TECHNIQUES; HELA CELLS; HUMANS; PROTEIN STRUCTURE, TERTIARY; SALMONELLA TYPHIMURIUM; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 84871006349     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2012.10.019     Document Type: Article

References (34)

1. I. Amit, L. Yakir, M. Katz, Y. Zwang, M.D. Marmor, A. Citri, K. Shtiegman, I. Alroy, S. Tuvia, and Y. Reiss Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding Genes Dev. 18 2004 1737 1752
2. 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
3. V. Braun, A. Wong, M. Landekic, W.J. Hong, S. Grinstein, and J.H. Brumell Sorting nexin 3 (SNX3) is a component of a tubular endosomal network induced by Salmonella and involved in maturation of the Salmonella-containing vacuole Cell. Microbiol. 12 2010 1352 1367
4. K. Cadwell, J.Y. Liu, S.L. Brown, H. Miyoshi, J. Loh, J.K. Lennerz, C. Kishi, W. Kc, J.A. Carrero, and S. Hunt A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells Nature 456 2008 259 263
5. 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
6. L. Clark, C.A. Perrett, L. Malt, C. Harward, S. Humphrey, K.A. Jepson, I. Martinez-Argudo, L.J. Carney, R.M. La Ragione, T.J. Humphrey, and M.A. Jepson Differences in Salmonella enterica serovar Typhimurium strain invasiveness are associated with heterogeneity in SPI-1 gene expression Microbiology 157 2011 2072 2083
7. R.J. Deshaies, and C.A. Joazeiro RING domain E3 ubiquitin ligases Annu. Rev. Biochem. 78 2009 399 434
8. S. Geisler, K.M. Holmström, D. Skujat, F.C. Fiesel, O.C. Rothfuss, P.J. Kahle, and W. Springer PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1 Nat. Cell Biol. 12 2010 119 131
9. D.L. Guernsey, H. Jiang, K. Bedard, S.C. Evans, M. Ferguson, M. Matsuoka, C. Macgillivray, M. Nightingale, S. Perry, and A.L. Rideout Mutation in the gene encoding ubiquitin ligase LRSAM1 in patients with Charcot-Marie-Tooth disease PLoS Genet. 6 2010 e1001081
10. A. Huett, A. Ng, Z. Cao, P. Kuballa, M. Komatsu, M.J. Daly, D.K. Podolsky, and R.J. Xavier A novel hybrid yeast-human network analysis reveals an essential role for FNBP1L in antibacterial autophagy J. Immunol. 182 2009 4917 4930
11. Y. Jenkins, V. Markovtsov, W. Lang, P. Sharma, D. Pearsall, J. Warner, C. Franci, B. Huang, J. Huang, and G.C. Yam Critical role of the ubiquitin ligase activity of UHRF1, a nuclear RING finger protein, in tumor cell growth Mol. Biol. Cell 16 2005 5621 5629
12. D.C. Ko, K.P. Shukla, C. Fong, M. Wasnick, M.J. Brittnacher, M.M. Wurfel, T.D. Holden, G.E. O'Keefe, B. Van Yserloo, J.M. Akey, and S.I. Miller A genome-wide in vitro bacterial-infection screen reveals human variation in the host response associated with inflammatory disease Am. J. Hum. Genet. 85 2009 214 227
13. P. Kuballa, A. Huett, J.D. Rioux, M.J. Daly, and R.J. Xavier Impaired autophagy of an intracellular pathogen induced by a Crohn's disease associated ATG16L1 variant PLoS ONE 3 2008 e3391
14. P. Lapaquette, A.L. Glasser, A. Huett, R.J. Xavier, and A. Darfeuille-Michaud Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly Cell. Microbiol. 12 2010 99 113
15. B. Li, Y. Su, J. Ryder, L. Yan, S. Na, and B. Ni RIFLE: a novel ring zinc finger-leucine-rich repeat containing protein, regulates select cell adhesion molecules in PC12 cells J. Cell. Biochem. 90 2003 1224 1241
16. J. Lim, T. Hao, C. Shaw, A.J. Patel, G. Szabó, J.F. Rual, C.J. Fisk, N. Li, A. Smolyar, and D.E. Hill A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration Cell 125 2006 801 814
17. P. Malik-Kale, S. Winfree, and O. Steele-Mortimer The bimodal lifestyle of intracellular Salmonella in epithelial cells: replication in the cytosol obscures defects in vacuolar replication PLoS ONE 7 2012 e38732
18. N. Meyer-Morse, J.R. Robbins, C.S. Rae, S.N. Mochegova, M.S. Swanson, Z. Zhao, H.W. Virgin, and D. Portnoy Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection PLoS ONE 5 2010 e8610
19. S. Mostowy, M. Bonazzi, M.A. Hamon, T.N. Tham, A. Mallet, M. Lelek, E. Gouin, C. Demangel, R. Brosch, and C. Zimmer Entrapment of intracytosolic bacteria by septin cage-like structures Cell Host Microbe 8 2010 433 444
20. A.C. Ng, J.M. Eisenberg, R.J. Heath, A. Huett, C.M. Robinson, G.J. Nau, and R.J. Xavier Human leucine-rich repeat proteins: a genome-wide bioinformatic categorization and functional analysis in innate immunity Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4631 4638
21. M. Ogawa, T. Yoshimori, T. Suzuki, H. Sagara, N. Mizushima, and C. Sasakawa Escape of intracellular Shigella from autophagy Science 307 2005 727 731
22. J.D. Rioux, R.J. Xavier, K.D. Taylor, M.S. Silverberg, P. Goyette, A. Huett, T. Green, P. Kuballa, M.M. Barmada, and L.W. Datta Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis Nat. Genet. 39 2007 596 604
23. J.F. Rual, K. Venkatesan, T. Hao, T. Hirozane-Kishikawa, A. Dricot, N. Li, G.F. Berriz, F.D. Gibbons, M. Dreze, and N. Ayivi-Guedehoussou Towards a proteome-scale map of the human protein-protein interaction network Nature 437 2005 1173 1178
24. 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
25. S. Shaid, C.H. Brandts, H. Serve, and I. Dikic Ubiquitination and selective autophagy Cell Death Differ. 2012 10.1038/cdd.2012.72 in press. Published online June 22, 2012
26. A.C. Smith, J.T. Cirulis, J.E. Casanova, M.A. Scidmore, and J.H. Brumell Interaction of the Salmonella-containing vacuole with the endocytic recycling system J. Biol. Chem. 280 2005 24634 24641
27. U. Stelzl, U. Worm, M. Lalowski, C. Haenig, F.H. Brembeck, H. Goehler, M. Stroedicke, M. Zenkner, A. Schoenherr, and S. Koeppen A human protein-protein interaction network: a resource for annotating the proteome Cell 122 2005 957 968
28. B. Tang, T. Seredenina, G. Coppola, A. Kuhn, D.H. Geschwind, R. Luthi-Carter, and E.A. Thomas Gene expression profiling of R6/2 transgenic mice with different CAG repeat lengths reveals genes associated with disease onset and progression in Huntington's disease Neurobiol. Dis. 42 2011 459 467
29. 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
30. T.L. Thurston, M.P. Wandel, N. von Muhlinen, A. Foeglein, and F. Randow Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion Nature 482 2012 414 418
31. S.J. van Wijk, E. Fiskin, M. Putyrski, F. Pampaloni, J. Hou, P. Wild, T. Kensche, H.E. Grecco, P. Bastiaens, and I. Dikic Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells Mol. Cell 47 2012 797 809
32. J.M. Vyas, Y.M. Kim, K. Artavanis-Tsakonas, J.C. Love, A.G. Van der Veen, and H.L. Ploegh Tubulation of class II MHC compartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells J. Immunol. 178 2007 7199 7210
33. M.A. Weterman, V. Sorrentino, P.R. Kasher, M.E. Jakobs, B.G. van Engelen, K. Fluiter, M.B. de Wissel, A. Sizarov, G. Nürnberg, and P. Nürnberg A frameshift mutation in LRSAM1 is responsible for a dominant hereditary polyneuropathy Hum. Mol. Genet. 21 2012 358 370
34. E. Wong, and A.M. Cuervo Autophagy gone awry in neurodegenerative diseases Nat. Neurosci. 13 2010 805 811