The ubiquitin ligase parkin mediates resistance to intracellular pathogens

Nature

Volumn 501, Issue 7468, 2013, Pages 512-516

  Manzanillo, Paolo S ^a   Ayres, Janelle S ^b   Watson, Robert O ^a   Collins, Angela C ^c   Souza, Gianne ^a   Rae, Chris S ^d   Schneider, David S ^e   Nakamura, Ken ^f   Shiloh, Michael U ^c   Cox, Jeffery S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d University of California Berkeley   (United States)

^e STANFORD UNIVERSITY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARKIN; POLYUBIQUITIN; UBIQUITIN;

DEFENSE MECHANISM; DISEASE RESISTANCE; ENZYME; GENE; IMMUNITY; INFECTIOUS DISEASE; METAZOAN; MYCOPARASITE; PATHOGEN; TUBERCULOSIS;

ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; FEMALE; INFECTION RESISTANCE; INFECTION SENSITIVITY; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MACROPHAGE; MALE; MITOPHAGY; MOUSE; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; TUBERCULOSIS;

ANIMALS; AUTOPHAGY; BONE MARROW CELLS; DROSOPHILA MELANOGASTER; FEMALE; IMMUNITY, INNATE; LYSINE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MODELS, IMMUNOLOGICAL; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; POLYUBIQUITIN; SALMONELLA TYPHIMURIUM; SYMBIOSIS; TUBERCULOSIS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

BACTERIA (MICROORGANISMS); METAZOA; MUS; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM TUBERCULOSIS; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI;

EID: 84885576570     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12566     Document Type: Article

References (39)

1. Zhao, Z. et al. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4, 458-469 (2008).
2. Deretic, V. & Levine, B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5, 527-549 (2009).
3. Watson, R. O.,Manzanillo, P. S.& Cox, J. S. Extracellular M. tuberculosisDNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150, 803-815 (2012).
4. Wild, P. et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233 (2011).
5. Youle, R. J. & Narendra, D. P. Mechanisms of mitophagy. Nature Rev. Mol. Cell Biol. 12, 9-14 (2011).
6. Komatsu, M. et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149-1163 (2007).
7. Geisler, S. et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nature Cell Biol. 12, 119-131 (2010).
8. Pankiv, S. et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145 (2007).
9. Chopra, R. et al. Mapping of PARK2 and PACRG overlapping regulatory region reveals LD structure and functional variants in association with leprosy in unrelated Indian population groups. PLoS Genet. 9, e1003578 (2013).
10. Mira, M. T. et al. Susceptibility to leprosy is associated with PARK2 and PACRG. Nature 427, 636-640 (2004).
11. Ali, S. et al. PARK2/PACRG polymorphisms and susceptibility to typhoid and paratyphoid fever. Clin. Exp. Immunol. 144, 425-431 (2006).
12. Romagnoli, A. et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8, 1357-1370 (2012).
13. Huett, A. et al.The LRRand RINGdomain protein LRSAM1isanE3ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium. Cell Host Microbe 12, 778-790 (2012).
14. Ponpuak, M. et al. Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 32, 329-341 (2010).
15. Martin, I., Dawson, V. L. & Dawson, T. M. Recent advances in the genetics of Parkinson's disease. Annu. Rev. Genomics Hum. Genet. 12, 301-325 (2011).
16. Chen, D. et al. Parkin mono-ubiquitinates Bcl-2 and regulates autophagy. J. Biol. Chem. 285, 38214-38223 (2010).
17. Lim, K.-L. et al. Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J. Neurosci. 25, 2002-2009 (2005).
18. Newton, K. et al. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134, 668-678 (2008).
19. Kitada, T. et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608 (1998).
20. Houben, D. et al. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell. Microbiol. 14, 1287-1298 (2012).
21. Alonso, S., Pethe, K., Russell, D. G.&Purdy, G. E. Lysosomal killing ofMycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc. Natl Acad. Sci. USA 104, 6031-6036 (2007).
22. Collins, C. A. et al. Atg5-independent sequestration of ubiquitinated mycobacteria. PLoS Pathog. 5, e1000430 (2009).
23. Mar?́n, I. & Ferrú s, A. Comparative genomics of the RBR family, including the Parkinson's disease-related gene parkin and the genes of the ariadne subfamily. Mol. Biol. Evol. 19, 2039-2050 (2002).
24. Moy, R. H. & Cherry, S. Antimicrobial autophagy: a conserved innate immune response in Drosophila. J. Innate Immun. 5, 444-455 (2013).
25. Narendra, D., Kane, L. A., Hauser, D. N., Fearnley, I. M.& Youle, R. J. p62/SQSTM1is required for parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 6, 1090-1106 (2010).
26. Yano, T. et al. Autophagic control of listeria through intracellular innate immune recognition in Drosophila. Nature Immunol. 9, 908-916 (2008).
27. Voronin, D., Cook, D. A. N., Steven, A.&Taylor, M. J. Autophagy regulatesWolbachia populations across diverse symbiotic associations. Proc. Natl Acad. Sci. USA 109, E1638-E1646 (2012).
28. Zhou, R., Yazdi, A. S., Menu, P. & Tschopp, J. A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221-225 (2011).
29. Nakahira, K. et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nature Immunol. 12, 222-230 (2011).
30. Stavru, F., Bouillaud, F., Sartori, A., Ricquier, D.& Cossart, P. Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc. Natl Acad. Sci. USA 108, 3612-3617 (2011).
31. Johnson, B. N., Berger, A. K., Cortese, G. P. & LaVoie, M. J. The ubiquitin E3 ligase parkin regulates the proapoptotic function of Bax. Proc. Natl Acad. Sci. USA 109, 6283-6288 (2012).
32. Kim, K.-Y. et al. Parkin is a lipid-responsive regulator of fat uptake in mice and mutant human cells. J. Clin. Invest. 121, 3701-3712 (2011).
33. de Léséleuc, L. et al. PARK2 mediates interleukin 6 andmonocyte chemoattractant protein1production byhumanmacrophages. PLoS Negl. Trop. Dis. 7, e2015(2013).
34. Anderson, C. A. et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nature Genet. 43, 246-252 (2011).
35. Jostins, L. et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491, 119-124 (2012).
36. Goldberg, M. S. et al. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J. Biol. Chem. 278, 43628-43635 (2003).
37. Ohol, Y. M. et al. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 7, 210-220 (2010).
38. Thibault, S. T. et al. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nature Genet. 36, 283-287 (2004).
39. Ayres, J. S. & Schneider, D. S. A signaling protease required formelanization in Drosophila affects resistance and tolerance of infections. PLoS Biol. 6, e305 (2008).