Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 41, 2015, Pages E5628-E5637

  Haldar, Arun K ^a   Foltz, Clémence ^b   Finethy, Ryan ^a   Piro, Anthony S ^a   Feeley, Eric M ^a   Pilla Moffett, Danielle M ^a   Komatsu, Masaki ^c   Frickel, Eva Maria ^b   Coers, Jörn ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^c NIIGATA UNIVERSITY   (Japan)

Author keywords

Chlamydia; GBPs; Immunity related GTPase; Interferon; Toxoplasma

Indexed keywords

GAMMA INTERFERON; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN KINASE; PROTEIN P62; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; BACTERIAL VIRULENCE; CELL VACUOLE; CELLULAR IMMUNITY; CHLAMYDIA TRACHOMATIS; CONFERENCE PAPER; CONTROLLED STUDY; HOST CELL; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MICROBIAL GROWTH; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TOXOPLASMA GONDII; UBIQUITINATION; ANIMAL; CHLAMYDIASIS; GENETICS; IMMUNE EVASION; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PATHOLOGY; TOXOPLASMA; TOXOPLASMOSIS;

ANIMALS; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; GTP-BINDING PROTEINS; IMMUNE EVASION; IMMUNITY, INNATE; MICE; MICE, KNOCKOUT; TNF RECEPTOR-ASSOCIATED FACTOR 6; TOXOPLASMA; TOXOPLASMOSIS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; VACUOLES;

EID: 84944242576     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1515966112     Document Type: Article

References (65)

1. Kumar Y, Valdivia RH (2009) Leading a sheltered life: Intracellular pathogens and maintenance of vacuolar compartments Cell Host Microbe 5(6):593-601.
2. Kim BH, Shenoy AR, Kumar P, Bradfield CJ, MacMicking JD (2012) IFN-inducible GTPases in host cell defense Cell Host Microbe 12(4):432-444.
3. Ling YM, et al (2006) Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages J Exp Med 203(9): 2063-2071.
4. Martens S, et al (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases PLoS Pathog 1(3):e24.
5. Meunier E, et al (2014) Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases Nature 509(7500):366-370.
6. Yamamoto M, et al (2012) A cluster of interferon-?-inducible p65 GTPases plays a critical role in host defense against Toxoplasma gondii Immunity 37(2):302-313.
7. Zhao YO, Khaminets A, Hunn JP, Howard JC (2009) Disruption of the Toxoplasma gondii parasitophorous vacuole by IFNgamma-inducible immunity-related GTPases (IRG proteins) triggers necrotic cell death PLoS Pathog 5(2):e1000288.
8. Meunier E, et al (2015) Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida Nat Immunol 16(5):476-484.
9. Kim BH, et al (2011) A family of IFN-?-inducible 65-kD GTPases protects against bacterial infection Science 332(6030):717-721.
10. Pilla DM, et al (2014) Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS Proc Natl Acad Sci USA 111(16):6046-6051.
11. Shenoy AR, et al (2012) GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals Science 336(6080):481-485.
12. Man SM, et al (2015) The transcription factor IRF1 and guanylate-binding proteins target activation of the AIM2 inflammasome by Francisella infection Nat Immunol 16(5):467-475.
13. Prakash B, Praefcke GJ, Renault L, Wittinghofer A, Herrmann C (2000) Structure of human guanylate-binding protein 1 representing a unique class of GTP-binding proteins Nature 403(6769):567-571.
14. Ghosh A, Praefcke GJ, Renault L, Wittinghofer A, Herrmann C (2006) How guanylatebinding proteins achieve assembly-stimulated processive cleavage of GTP to GMP Nature 440(7080):101-104.
15. Vöpel T, et al (2010) Mechanism of GTPase-Activity-induced self-Assembly of human guanylate binding protein 1 J Mol Biol 400(1):63-70.
16. Britzen-Laurent N, et al (2010) Intracellular trafficking of guanylate-binding proteins is regulated by heterodimerization in a hierarchical manner PLoS One 5(12):e14246.
17. Haldar AK, et al (2013) IRG and GBP host resistance factors target aberrant, "nonself" vacuoles characterized by the missing of "self" IRGM proteins PLoS Pathog 9(6): e1003414.
18. Virreira Winter S, et al (2011) Determinants of GBP recruitment to Toxoplasma gondii vacuoles and the parasitic factors that control it PLoS One 6(9):e24434.
19. Coers J, et al (2008) Chlamydia muridarum evades growth restriction by the IFNgamma-inducible host resistance factor Irgb10 J Immunol 180(9):6237-6245.
20. Bekpen C, et al (2005) The interferon-inducible p47 (IRG) GTPases in vertebrates: Loss of the cell autonomous resistance mechanism in the human lineage Genome Biol 6(11):R92.
21. Hunn JP, et al (2008) Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii EMBO J 27(19):2495-2509.
22. Taylor GA, et al (1997) The inducibly expressed GTPase localizes to the endoplasmic reticulum, independently of GTP binding J Biol Chem 272(16):10639-10645.
23. Coers J (2013) Self and non-self discrimination of intracellular membranes by the innate immune system PLoS Pathog 9(9):e1003538.
24. Haldar AK, Piro AS, Pilla DM, Yamamoto M, Coers J (2014) The E2-like conjugation enzyme Atg3 promotes binding of IRG and Gbp proteins to Chlamydia-And Toxoplasma-containing vacuoles and host resistance PLoS One 9(1):e86684.
25. Selleck EM, et al (2013) Guanylate-binding protein 1 (Gbp1) contributes to cellautonomous immunity against Toxoplasma gondii PLoS Pathog 9(4):e1003320.
26. Traver MK, et al (2011) Immunity-related gtpase M (IRGM) proteins influence the localization of guanylate-binding protein 2 (GBP2) by modulating macroautophagy J Biol Chem 286(35):30471-30480.
27. Al-Zeer MA, Al-Younes HM, Lauster D, Abu Lubad M, Meyer TF (2013) Autophagy restricts Chlamydia trachomatis growth in human macrophages via IFNG-inducible guanylate binding proteins Autophagy 9(1):50-62.
28. Boyle KB, Randow F (2013) The role of 'eat-me' signals and autophagy cargo receptors in innate immunity Curr Opin Microbiol 16(3):339-348.
29. Dupont N, et al (2009) Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy Cell Host Microbe 6(2):137-149.
30. Yoshikawa Y, et al (2009) Listeria monocytogenes ActA-mediated escape from autophagic recognition Nat Cell Biol 11(10):1233-1240.
31. Zheng YT, et al (2009) The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway J Immunol 183(9):5909-5916.
32. Mostowy S, et al (2011) p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways J Biol Chem 286(30):26987-26995.
33. Vadlamudi RK, Joung I, Strominger JL, Shin J (1996) p62, a phosphotyrosine-independent ligand of the SH2 domain of p56lck, belongs to a new class of ubiquitin-binding proteins J Biol Chem 271(34):20235-20237.
34. Itakura E, Mizushima N (2011) p62 targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding J Cell Biol 192(1):17-27.
35. Deng L, et al (2000) Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain Cell 103(2):351-361.
36. Linares JF, et al (2013) K63 polyubiquitination and activation of mTOR by the p62-TRAF6 complex in nutrient-Activated cells Mol Cell 51(3):283-296.
37. Sanz L, Diaz-Meco MT, Nakano H, Moscat J (2000) The atypical PKC-interacting protein p62 channels NF-kappaB activation by the IL-1-TRAF6 pathway EMBO J 19(7): 1576-1586.
38. Rogov V, Dötsch V, Johansen T, Kirkin V (2014) Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy Mol Cell 53(2):167-178.
39. Seibenhener ML, et al (2004) Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation Mol Cell Biol 24(18):8055-8068.
40. Neumann B, et al (2010) Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes Nature 464(7289):721-727.
41. Chen C, et al (2006) The hypothetical protein CT813 is localized in the Chlamydia trachomatis inclusion membrane and is immunogenic in women urogenitally infected with C.trachomatis Infect Immun 74(8):4826-4840.
42. Khaminets A, et al (2010) Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole Cell Microbiol 12(7):939-961.
43. Zhao Y, et al (2009) Virulent Toxoplasma gondii evade immunity-related GTPasemediated parasite vacuole disruption within primed macrophages J Immunol 182(6): 3775-3781.
44. Coers J, Starnbach MN, Howard JC (2009) Modeling infectious disease in mice: Coadaptation and the role of host-specific IFNgamma responses PLoS Pathog 5(5): e1000333.
45. Fentress SJ, et al (2010) Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence Cell Host Microbe 8(6):484-495.
46. Steinfeldt T, et al (2010) Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii PLoS Biol 8(12):e1000576.
47. Hermanns T, Muller UB, Konen-Waisman S, Howard JC, Steinfeldt T (2015) The Toxoplasma gondii rhoptry protein ROP18 is an Irga6-specific kinase and regulated by the dense granule protein GRA7 Cell Microbiol, 10.1111/cmi.12499.
48. Ohshima J, et al (2014) Role of mouse and human autophagy proteins in IFN-?-induced cell-Autonomous responses against Toxoplasma gondii J Immunol 192(7):3328-3335.
49. Tietzel I, El-Haibi C, Carabeo RA (2009) Human guanylate binding proteins potentiate the anti-chlamydia effects of interferon-gamma PLoS One 4(8):e6499.
50. Manzanillo PS, et al (2013) The ubiquitin ligase parkin mediates resistance to intracellular pathogens Nature 501(7468):512-516.
51. Huett A, et al (2012) The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium Cell Host Microbe 12(6):778-790.
52. Kim JY, Ozato K (2009) The sequestosome 1/p62 attenuates cytokine gene expression in activated macrophages by inhibiting IFN regulatory factor 8 and TNF receptor-Associated factor 6/NF-kappaB activity J Immunol 182(4):2131-2140.
53. O'Connor C, et al (2010) p62/sequestosome-1 associates with and sustains the expression of retroviral restriction factor TRIM5alpha J Virol 84(12):5997-6006.
54. Zhang Z, et al (2013) The E3 ubiquitin ligase TRIM21 negatively regulates the innate immune response to intracellular double-stranded DNA Nat Immunol 14(2):172-178.
55. Al-Zeer MA, Al-Younes HM, Braun PR, Zerrahn J, Meyer TF (2009) IFN-gamma-inducible Irga6 mediates host resistance against Chlamydia trachomatis via autophagy PLoS One 4(2):e4588.
56. Choi J, et al (2014) The parasitophorous vacuole membrane of Toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy Immunity 40(6):924-935.
57. Zhao Z, et al (2008) Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens Cell Host Microbe 4(5):458-469.
58. Degrandi D, et al (2007) Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense J Immunol 179(11):7729-7740.
59. Komatsu M, et al (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice Cell 131(6):1149-1163.
60. Coers J, et al (2011) Compensatory T cell responses in IRG-deficient mice prevent sustained Chlamydia trachomatis infections PLoS Pathog 7(6):e1001346.
61. Lamothe B, et al (2008) The RING domain and first zinc finger of TRAF6 coordinate signaling by interleukin-1, lipopolysaccharide, and RANKL J Biol Chem 283(36): 24871-24880.
62. Kim SK, Karasov A, Boothroyd JC (2007) Bradyzoite-specific surface antigen SRS9 plays a role in maintaining Toxoplasma gondii persistence in the brain and in host control of parasite replication in the intestine Infect Immun 75(4):1626-1634.
63. Pernas L, et al (2014) Toxoplasma effector MAF1 mediates recruitment of host mitochondria and impacts the host response PLoS Biol 12(4):e1001845.
64. Wang Y, et al (2011) Development of a transformation system for Chlamydia trachomatis: Restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector PLoS Pathog 7(9):e1002258.
65. Martens S, et al (2004) Mechanisms regulating the positioning of mouse p47 resistance GTPases LRG-47 and IIGP1 on cellular membranes: Retargeting to plasma membrane induced by phagocytosis J Immunol 173(4):2594-2606.