Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry

Nature Immunology

Volumn 11, Issue 1, 2010, Pages 55-62

  Travassos, Leonardo H ^a   Carneiro, Leticia A M ^b   Ramjeet, Mahendrasingh ^b   Hussey, Seamus ^a,c   Kim, Yun Gi ^d   Magalhes, Joo G ^a   Yuan, Linda ^a   Soares, Fraser ^b   Chea, Evelyn ^a   Le Bourhis, Lionel ^a   Boneca, Ivo G ^e   Allaoui, Abdelmounaaim ^f   Jones, Nicola L ^c   Nũez, Gabriel ^d   Girardin, Stephen E ^b   Philpott, Dana J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e INSTITUT PASTEUR   (France)

^f UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; AUTOPHAGY RELATED 16 LIKE 1 PROTEIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CELL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RECEPTOR INTERACTING PROTEIN 2; UNCLASSIFIED DRUG; ATG16L PROTEIN, MOUSE; ATG16L1 PROTEIN, HUMAN; CARRIER PROTEIN; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; BACTERIAL IMMUNITY; CELL MEMBRANE; CONTROLLED STUDY; CROHN DISEASE; FRAMESHIFT MUTATION; GENETIC ASSOCIATION; HOMOZYGOTE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; BACTERIUM; C57BL MOUSE; CELL CULTURE; CELL LINE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; FEMALE; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; GENETICS; HELA CELL; IMMUNOBLOTTING; MALE; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; MOUSE STRAIN; MUTATION; ULTRASTRUCTURE;

ANIMALS; AUTOPHAGY; BACTERIA; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; FEMALE; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; IMMUNOBLOTTING; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MUTATION; NOD1 SIGNALING ADAPTOR PROTEIN; NOD2 SIGNALING ADAPTOR PROTEIN; TRANSFECTION;

EID: 73849121209     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1823     Document Type: Article

References (47)

1. Mizushima, N., Levine, B., Cuervo, A.M. & Klionsky, D.J. Autophagy fghts disease through cellular self-digestion. Nature 451, 1069-1075 (2008).
2. Reggiori, F. & Klionsky, D.J. Autophagosomes: biogenesis from scratch? Curr. Opin. Cell Biol. 17, 415-422 (2005).
3. Hussey, S., Travassos, L.H. & Jones, N.L. Autophagy as an Emerging dimension to adaptive and innate immunity. Semin. Immunol. 21, 233-241 (2009).
4. Marx, J. Autophagy: is it cancer's friend or foe? Science 312, 1160-1161 (2006).
5. Hara, T. et al. Suppression of basal autophagy in nEural cells causes nEurodegenerative disease in mice. Nature 441, 885-889 (2006).
6. Nakagawa, I. et al. Autophagy defends cells against invading group A Streptococcus. Science 306, 1037-1040 (2004).
7. Birmingham, C.L. et al. Listeria monocytogenes evades kILling by autophagy during colonization of host cells. Autophagy 3, 442-451 (2007).
8. Ogawa, M. et al. Escape of intracellular Shigella from autophagy. Science 307, 727-731 (2005).
9. Gutierrez, M.G. et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766 (2004).
10. Birmingham, C.L. & Brumell, J.H. Autophagy recognizes intracellular Salmonella Enterica serovar Typhimurium in damaged vacuoles. Autophagy 2, 156-158 (2006).
11. Carneiro, L., Magalhaes, J., Tattoli, I., PhILpott, D. & Travassos, L. Nod-like proteins in infammation and disease. J. Pathol. 214, 136-148 (2008).
12. Martinon, F. & Tschopp, J. NLRs join TLRs as innate sensors of pathogens. Trends Immunol. 26, 447-454 (2005).
13. Meylan, E., Tschopp, J. & Karin, M. Intracellular pattern Recognition receptors in the host response. Nature 442, 39-44 (2006).
14. ChamaILlard, M. et al. An essential role for NOD1 in host Recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat. Immunol. 4, 702-707 (2003).
15. Girardin, S.E. et al. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300, 1584-1587 (2003).
16. Girardin, S.E. et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278, 8869-8872 (2003).
17. Girardin, S.E. et al. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278, 41702-41708 (2003).
18. Inohara, N. et al. Host Recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278, 5509-5512 (2003).
19. Inohara, N. et al. An induced proximity model for NF-κB activation in the Nod1/RICK and RIP signaling pathways. J. Biol. Chem. 275, 27823-27831 (2000).
20. Abbott, D.W., WILkins, A., Asara, J.M. & Cantley, L.C. The Crohn's disease protein, NOD2, requires RIP2 in order to induce ubiquitinylation of a novel site on NEMO. Curr. Biol. 14, 2217-2227 (2004).
21. Hugot, J.P. et al. Association of NOD2 leucine-rich repeat variants with susceptibILity to Crohn's disease. Nature 411, 599-603 (2001).
22. Rioux, J.D. et al. Genome-wide association study identifes new susceptibILity loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 39, 596-604 (2007).
23. Hampe, J. et al. A genome-wide association scan of nonsynonymous SNPs identifes a susceptibILity variant for Crohn disease in ATG16L1. Nat. Genet. 39, 207-211 (2007).
24. Fritz, J.H. et al. Nod1-mediated innate Immune Recognition of peptidoglycan contributes to the onset of adaptive immunity. Immunity 26, 445-459 (2007).
25. Magalhaes, J.G. et al. Nod2-dependent Th2 polarization of antigen-specifc immunity. J. Immunol. 181, 7925-7935 (2008).
26. Delgado, M.A., Elmaoued, R.A., Davis, A.S., Kyei, G. & Deretic, V. Toll-like receptors control autophagy. EMBO J. 27, 1110-1121 (2008).
27. Klionsky, D.J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175 (2008).
28. Mizushima, N., Ohsumi, Y. & Yoshimori, T. Autophagosome formation in mammalian cells. Cell Struct. Funct. 27, 421-429 (2002).
29. Magalhaes, J.G. et al. Murine Nod1 but not its human orthologue mediates innate Immune detection of tracheal cytotoxin. EMBO Rep. 6, 1201-1207 (2005).
30. Opitz, B. et al. Listeria monocytogenes activated p38 MAPK and induced IL-8 secretion in a nucleotide-binding oligomerization domain 1-dependent manner in endothelial cells. J. Immunol. 176, 484-490 (2006).
31. Travassos, L.H. et al. Nod1 participates in the innate Immune response to Pseudomonas aeruginosa. J. Biol. Chem. 280, 36714-36718 (2005).
32. Viala, J. et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5, 1166-1174 (2004).
33. Carneiro, L.A. et al. Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 5, 123-136 (2009).
34. Opitz, B. et al. Nod1-mediated endothelial cell activation by ChlamydophILa pneumoniae. Circ. Res. 96, 319-326 (2005).
35. Kim, S., La Motte-Mohs, R.N., Rudolph, D., Zuniga-Pfucker, J.C. & Mak, T.W. The role of nuclear factor-κB essential modulator (NEMO) in B cell development and survival. Proc. Natl. Acad. Sci. USA 100, 1203-1208 (2003).
36. Barnich, N., Aguirre, J.E., Reinecker, H.C., Xavier, R. & Podolsky, D.K. Membrane recruitment of NOD2 in intestinal epithelial cells is essential for nuclear factor-κB activation in muramyl dipeptide Recognition. J. Cell Biol. 170, 21-26 (2005).
37. Lecine, P. et al. The NOD2-RICK complex signals from the plasma membrane. J. Biol. Chem. 282, 15197-15207 (2007).
38. TILl, A. et al. A role for membrane-bound CD147 in NOD2-mediated Recognition of bacterial cytoinvasion. J. Cell Sci. 121, 487-495 (2008).
39. Fujita, N. et al. The Atg16L complex specifes the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 19, 2092-2100 (2008).
40. Kuballa, P., Huett, A., Rioux, J.D., Daly, M.J. & Xavier, R.J. Impaired autophagy of an intracellular pathogen induced by a Crohn's disease associated ATG16L1 variant. PLoS ONE 3, e3391 (2008).
41. Xu, Y. et al. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 27, 135-144 (2007).
42. Kaneko, T. et al. PGRP-LC and PGRP-LE have essential yet distinct functions in the DrosophILa Immune response to monomeric DAP-type peptidoglycan. Nat. Immunol. 7, 715-723 (2006).
43. Zaidman-Remy, A. et al. The DrosophILa amidase PGRP-LB modulates the Immune response to bacterial infection. Immunity 24, 463-473 (2006).
44. Yano, T. et al. Autophagic control of listeria through intracellular innate Immune Recognition in DrosophILa. Nat. Immunol. 9, 908-916 (2008).
45. Hofus, D. et al. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137, 773-783 (2009).
46. Allaoui, A., Mounier, J., Prevost, M.C., Sansonetti, P.J. & Parsot, C. icsB: a Shigella fexneri virulence gene necessary for the lysis of protrusions during intercellular spread. Mol. Microbiol. 6, 1605-1616 (1992).
47. Jounai, N. et al. The Atg5 Atg12 conjugate associates with innate antiviral Immune responses. Proc. Natl. Acad. Sci. USA 104, 14050-14055 (2007).