Home LiteratureArticle Details
PMID: 23245322 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium.

Cell host & microbe ·Vol. 12 ·No. 6 ·2012-12-13 ·Pages 778-90

Huett A, Heath RJ, Begun J, Sassi SO, Baxt LA, Vyas JM, Goldberg MB, Xavier RJ

Abstract

Several species of pathogenic bacteria replicate within an intracellular vacuolar niche. Bacteria that escape into the cytosol are captured by the autophagic pathway and targeted for lysosomal degradation, representing a defense against bacterial exploitation of the host cytosol. Autophagic capture of Salmonella Typhimurium occurs predominantly via generation of a polyubiquitin signal around cytosolic bacteria, binding of adaptor proteins, and recruitment of autophagic machinery. However, the components mediating bacterial target selection and ubiquitination remain obscure. We identify LRSAM1 as the E3 ligase responsible for anti-Salmonella autophagy-associated ubiquitination. LRSAM1 localizes to several intracellular bacterial pathogens and generates the bacteria-associated ubiquitin signal; these functions require LRSAM1's leucine-rich repeat and RING domains, respectively. Using cells from LRSAM1-deficient individuals, we confirm that LRSAM1 is required for ubiquitination associated with intracellular bacteria but dispensable for ubiquitination of aggregated proteins. LRSAM1 is therefore a bacterial recognition protein and ubiquitin ligase that defends the cytoplasm from invasive pathogens.

MeSH Terms
Autophagy Gene Knockout Techniques HeLa Cells Humans Protein Structure, Tertiary Salmonella typhimurium/immunology Ubiquitin/metabolism Ubiquitin-Protein Ligases/genetics,metabolism
Chemicals
Ubiquitin LRSAM1 protein, human Ubiquitin-Protein Ligases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Huett Alan
Center for Computational and Integrative Biology, Massachusetts General Hospital, Boston, MA 02114, USA.
Heath Robert J
Begun Jakob
Sassi Slim O
Baxt Leigh A
Vyas Jatin M
Goldberg Marcia B
Xavier Ramnik J
References (34)
34 references, click to expand
  1. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells.
    Nature. 2008 Nov 13;456(7219):259-63 PMID: 18849966
  2. 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. 2011 Jun;42(3):459-67 PMID: 21334439
  3. Human leucine-rich repeat proteins: a genome-wide bioinformatic categorization and functional analysis in innate immunity.
    Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4631-8 PMID: 20616063
  4. Escape of intracellular Shigella from autophagy.
    Science. 2005 Feb 4;307(5710):727-31 PMID: 15576571
  5. Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly.
    Cell Microbiol. 2010 Jan;12(1):99-113 PMID: 19747213
  6. A novel hybrid yeast-human network analysis reveals an essential role for FNBP1L in antibacterial autophagy.
    J Immunol. 2009 Apr 15;182(8):4917-30 PMID: 19342671
  7. Interaction of the Salmonella-containing vacuole with the endocytic recycling system.
    J Biol Chem. 2005 Jul 1;280(26):24634-41 PMID: 15886200
  8. The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteria-associated microdomains to target Salmonella to the autophagy pathway.
    Autophagy. 2011 Mar;7(3):341-5 PMID: 21079414
  9. RIFLE: a novel ring zinc finger-leucine-rich repeat containing protein, regulates select cell adhesion molecules in PC12 cells.
    J Cell Biochem. 2003 Dec 15;90(6):1224-41 PMID: 14635195
  10. The bimodal lifestyle of intracellular Salmonella in epithelial cells: replication in the cytosol obscures defects in vacuolar replication.
    PLoS One. 2012;7(6):e38732 PMID: 22719929
  11. Ubiquitination and selective autophagy.
    Cell Death Differ. 2013 Jan;20(1):21-30 PMID: 22722335
  12. A human protein-protein interaction network: a resource for annotating the proteome.
    Cell. 2005 Sep 23;122(6):957-68 PMID: 16169070
  13. 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. 2010 Sep 1;12(9):1352-67 PMID: 20482551
  14. Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells.
    Mol Cell. 2012 Sep 14;47(5):797-809 PMID: 22819327
  15. Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding.
    Genes Dev. 2004 Jul 15;18(14):1737-52 PMID: 15256501
  16. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole.
    J Biol Chem. 2006 Apr 21;281(16):11374-83 PMID: 16495224
  17. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion.
    Nature. 2012 Jan 15;482(7385):414-8 PMID: 22246324
  18. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1.
    Nat Cell Biol. 2010 Feb;12(2):119-31 PMID: 20098416
  19. A diacylglycerol-dependent signaling pathway contributes to regulation of antibacterial autophagy.
    Cell Host Microbe. 2010 Aug 19;8(2):137-46 PMID: 20674539
  20. Impaired autophagy of an intracellular pathogen induced by a Crohn's disease associated ATG16L1 variant.
    PLoS One. 2008;3(10):e3391 PMID: 18852889
  21. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis.
    Nat Genet. 2007 May;39(5):596-604 PMID: 17435756
  22. RING domain E3 ubiquitin ligases.
    Annu Rev Biochem. 2009;78:399-434 PMID: 19489725
  23. A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration.
    Cell. 2006 May 19;125(4):801-14 PMID: 16713569
  24. A genome-wide in vitro bacterial-infection screen reveals human variation in the host response associated with inflammatory disease.
    Am J Hum Genet. 2009 Aug;85(2):214-27 PMID: 19664744
  25. Tubulation of class II MHC compartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells.
    J Immunol. 2007 Jun 1;178(11):7199-210 PMID: 17513769
  26. Autophagy gone awry in neurodegenerative diseases.
    Nat Neurosci. 2010 Jul;13(7):805-11 PMID: 20581817
  27. Mutation in the gene encoding ubiquitin ligase LRSAM1 in patients with Charcot-Marie-Tooth disease.
    PLoS Genet. 2010 Aug 26;6(8): PMID: 20865121
  28. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria.
    Nat Immunol. 2009 Nov;10(11):1215-21 PMID: 19820708
  29. Critical role of the ubiquitin ligase activity of UHRF1, a nuclear RING finger protein, in tumor cell growth.
    Mol Biol Cell. 2005 Dec;16(12):5621-9 PMID: 16195352
  30. Entrapment of intracytosolic bacteria by septin cage-like structures.
    Cell Host Microbe. 2010 Nov 18;8(5):433-44 PMID: 21075354
  31. Towards a proteome-scale map of the human protein-protein interaction network.
    Nature. 2005 Oct 20;437(7062):1173-8 PMID: 16189514
  32. Differences in Salmonella enterica serovar Typhimurium strain invasiveness are associated with heterogeneity in SPI-1 gene expression.
    Microbiology (Reading). 2011 Jul;157(Pt 7):2072-2083 PMID: 21493681
  33. A frameshift mutation in LRSAM1 is responsible for a dominant hereditary polyneuropathy.
    Hum Mol Genet. 2012 Jan 15;21(2):358-70 PMID: 22012984
  34. Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection.
    PLoS One. 2010 Jan 06;5(1):e8610 PMID: 20062534
Article Info
Journal
Cell host & microbe
Abbr.
Cell Host Microbe
ISSN
1934-6069
Published
2012-12-13
Pages
778-90
Language
English
Region
United States
NLM ID
101302316
PMCID
PMC3785244
Subset
IM
Grants
NIDDK NIH HHS · R01 DK060049 · United States
NIDDK NIH HHS · R01 DK069344 · United States
NIDDK NIH HHS · P30 DK043351 · United States
NIAID NIH HHS · R21 AI103676 · United States
NIAID NIH HHS · R01 AI081724 · United States
NIAID NIH HHS · R56 AI081724 · United States
NIDDK NIH HHS · U01 R01 DK060049 · United States
NIDDK NIH HHS · R01 DK097485 · United States
NIDDK NIH HHS · R01 DK092405 · United States
NIDDK NIH HHS · U01 DK062432 · United States
NIDDK NIH HHS · R01 DK083756 · United States
NIAID NIH HHS · R01 AI092084 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com