K63-Linked Ubiquitination Targets Toxoplasma gondii for Endo-lysosomal Destruction in IFNγ-Stimulated Human Cells

PLoS Pathogens

Volumn 12, Issue 11, 2016, Pages

  Clough, Barbara ^a   Wright, Joseph D ^a   Pereira, Pedro M ^b   Hirst, Elizabeth M ^a   Johnston, Ashleigh C ^a   Henriques, Ricardo ^b   Frickel, Eva Maria ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATG16L1 PROTEIN; GABARAP PROTEIN; GAMMA INTERFERON; LC3B PROTEIN; LYSOSOME ENZYME; MEMBRANE PROTEIN; NDP52 PROTEIN; PROTEIN P62; UNCLASSIFIED DRUG; LYSINE;

ARTICLE; AUTOPHAGY; CELL DESTRUCTION; CELL STIMULATION; CELL VIABILITY ASSAY; CONTROLLED STUDY; FIXED IMMUNOFLUORESCENCE MICROSCOPY; FLOW CYTOMETRY; GENE EXPRESSION; HOST RESISTANCE; HUMAN; HUMAN CELL; PARASITE VIRULENCE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RNA SEQUENCE; SIGNAL TRANSDUCTION; SUPERRESOLUTION STRUCTURED ILLUMINATION MICROSCOPY; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRANSMISSION ELECTRON MICROSCOPY; UBIQUITINATION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; CELL VACUOLE; FLUORESCENCE MICROSCOPY; HOST PARASITE INTERACTION; IMMUNOBLOTTING; IMMUNOLOGY; LYSOSOME; METABOLISM; PARASITOLOGY; TOXOPLASMA;

FLOW CYTOMETRY; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOBLOTTING; INTERFERON-GAMMA; LYSINE; LYSOSOMES; MICROSCOPY, FLUORESCENCE; TOXOPLASMA; TOXOPLASMOSIS; UBIQUITINATION; VACUOLES;

EID: 85002188876     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006027     Document Type: Article

References (56)

1. Randow F, MacMicking JD, James LC, Cellular Self-Defense: How Cell-Autonomous Immunity Protects Against Pathogens. Science. 2013;340: 701–706. doi: 10.1126/science.123302823661752
2. Suzuki Y, Orellana MA, Schreiber RD, Remington JS, Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science. 1988;240: 516–518. 3128869
3. Sibley LD, Ajioka JW, Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu Rev Microbiol. 2008;62: 329–351. doi: 10.1146/annurev.micro.62.081307.16292518544039
4. Sibley LD, Boothroyd JC, Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature. 1992;359: 82–85. doi: 10.1038/359082a01355855
5. Mordue DG, Sibley LD, Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J Immunol. 1997;159: 4452–4459. 9379044
6. Jones TC, Hirsch JG, The interaction between Toxoplasma gondii and mammalian cells. II. The absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J Exp Med. 1972;136: 1173–1194. 4343243
7. Joiner KA, Fuhrman SA, Miettinen HM, Kasper LH, Mellman I, Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science. 1990;249: 641–646. 2200126
8. Sibley LD, Weidner E, Krahenbuhl JL, Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature. 1985;315: 416–419. 2860567
9. Andrade RM, Wessendarp M, Gubbels MJ, Striepen B, Subauste CS, CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes. J Clin Invest. 2006;116: 2366–2377. doi: 10.1172/JCI2879616955139
10. Lees MP, Fuller SJ, McLeod R, Boulter NR, Miller CM, Zakrzewski AM, et al. P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii, by human and murine macrophages. The Journal of Immunology. 2010;184: 7040–7046. doi: 10.4049/jimmunol.100001220488797
11. Scharton-Kersten TM, Yap G, Magram J, Sher A, Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J Exp Med. 1997;185: 1261–1273. 9104813
12. Murray HW, Teitelbaum RF, L-Arginine-DependentReactive Nitrogen Intermediates and the Antimicrobial Effect of Activated Human Mononuclear Phagocytes. The Journal of Infectious Diseases. 1992;165: 513–517. 1538156
13. Selleck EM, Fentress SJ, Beatty WL, Degrandi D, Pfeffer K, Virgin HW, et al. Guanylate-binding Protein 1 (Gbp1) Contributes to Cell-autonomous Immunity against Toxoplasma gondii. PLoS Pathog. 2013;9: e1003320. doi: 10.1371/journal.ppat.100332023633952
14. Zhao Z, Fux B, Goodwin M, Dunay IR, Strong D, Miller BC, et al. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host & Microbe. 2008;4: 458–469.
15. Yap GS, Sher A, Effector Cells of Both Nonhemopoietic and Hemopoietic Origin Are Required for Interferon (IFN). Journal of Experimental Medicine. 1999;189: 1083–1091. 10190899
16. Choi J, Park S, Biering SB, Selleck E, Liu CY, Zhang X, et al. The Parasitophorous Vacuole Membrane of Toxoplasma gondii Is Targeted for Disruption by Ubiquitin-like Conjugation Systems of Autophagy. Immunity. 2014; 40(6): 924–935.
17. Ohshima J, Lee Y, Sasai M, Saitoh T, Su Ma J, Kamiyama N, et al. Role of Mouse and Human Autophagy Proteins in IFN-γ-Induced Cell-Autonomous Responses against Toxoplasma gondii. The Journal of Immunology. 2014; 192(7): 3328–3335.
18. Johnston AC, Piro A, Clough B, Siew M, Virreira Winter S, Coers J, et al. Human GBP1 does not localise to pathogen vacuoles but restricts Toxoplasma gondii. Cellular Microbiology. 2016; 18(8): 1056–1064. doi: 10.1111/cmi.12579
19. Pfefferkorn ER, Guyre PM, Inhibition of growth of Toxoplasma gondii in cultured fibroblasts by human recombinant gamma interferon. Infection and Immunity. 1984;44: 211–216. 6425215
20. Pfefferkorn ER, Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc Natl Acad Sci USA. 1984;81: 908–912. 6422465
21. Niedelman W, Gold DA, Rosowski EE, Sprokholt JK, Lim D, Farid Arenas A, et al. The Rhoptry Proteins ROP18 and ROP5 Mediate Toxoplasma gondii Evasion of the Murine, But Not the Human, Interferon-Gamma Response. PLoS Pathog. 2012;8: e1002784. doi: 10.1371/journal.ppat.100278422761577
22. Niedelman W, Sprokholt JK, Clough B, Frickel EM, Saeij JPJ, Cell Death of Gamma Interferon-Stimulated Human Fibroblasts upon Toxoplasma gondii Infection Induces Early Parasite Egress and Limits Parasite Replication. Infection and Immunity. 2013;81: 4341–4349. doi: 10.1128/IAI.00416-1324042117
23. Woodman JP, Dimier IH, Bout DT, Human endothelial cells are activated by IFN-gamma to inhibit Toxoplasma gondii replication. Inhibition is due to a different mechanism from that existing in mouse macrophages and human fibroblasts. J Immunol. 1991;147: 2019–2023. 1909738
24. Dimier IH, Bout DT, Inhibition of Toxoplasma gondii replication in IFN-gamma-activated human intestinal epithelial cells. Immunol Cell Biol. 1997;75: 511–514. doi: 10.1038/icb.1997.809429902
25. Van Grol J, Muniz-Feliciano L, Portillo J-AC, Bonilha VL, Subauste CS, CD40 induces anti-Toxoplasma gondii activity in nonhematopoietic cells dependent on autophagy proteins. Infection and Immunity. 2013;81: 2002–2011. doi: 10.1128/IAI.01145-1223509150
26. Selleck EM, Orchard RC, Lassen KG, Beatty WL, Xavier RJ, Levine B, et al. A Noncanonical Autophagy Pathway Restricts Toxoplasma gondii Growth in a Strain-Specific Manner in IFN-γ-Activated Human Cells. MBio. 2015;6: e01157–15. doi: 10.1128/mBio.01157-1526350966
27. Thurston TLM, Ryzhakov G, Bloor S, Muhlinen von N, Randow F, The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol. 2009;10: 1215–1221. doi: 10.1038/ni.180019820708
28. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science. 2011;333: 228–233. doi: 10.1126/science.120540521617041
29. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V, Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell. 2004;119: 753–766. doi: 10.1016/j.cell.2004.11.03815607973
30. Mostowy S, Sancho-Shimizu V, Hamon MA, Simeone R, Brosch R, Johansen T, et al. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. Journal of Biological Chemistry. 2011;286: 26987–26995. doi: 10.1074/jbc.M111.22361021646350
31. Husnjak K, Dikic I, Ubiquitin-Binding Proteins: Decoders of Ubiquitin-Mediated Cellular Functions. Annual Reviews in Biochemistry; 2012;81: 291–322.
32. Perrin AJ, Jiang X, Birmingham CL, So NSY, Brumell JH, Recognition of Bacteria in the Cytosol of Mammalian Cells by the Ubiquitin System. Current Biology. 2004;14: 806–811. doi: 10.1016/j.cub.2004.04.03315120074
33. Yamamoto M, Standley DM, Takashima S, Saiga H, Okuyama M, Kayama H, et al. A single polymorphic amino acid on Toxoplasma gondii kinase ROP16 determines the direct and strain-specific activation of Stat3. Journal of Experimental Medicine. 2009;206: 2747–2760. doi: 10.1084/jem.2009170319901082
34. Ong Y-C, Reese ML, Boothroyd JC, Toxoplasma rhoptry protein 16 (ROP16) subverts host function by direct tyrosine phosphorylation of STAT6. Journal of Biological Chemistry. American Society for Biochemistry and Molecular Biology; 2010;285: 28731–28740. doi: 10.1074/jbc.M110.11235920624917
35. Etheridge RD, Alaganan A, Tang K, Lou HJ, Turk BE, Sibley LD, The Toxoplasma Pseudokinase ROP5Forms Complexes with ROP18 and ROP17 Kinases that Synergize to Control Acute Virulence in Mice. Cell Host & Microbe. Elsevier Inc; 2014;15: 537–550.
36. Virreira Winter S, Niedelman W, Jensen KD, Rosowski EE, Julien L, spooner E, et al. Determinants of GBP Recruitment to Toxoplasma gondii Vacuoles and the Parasitic Factors That Control It. PLoS ONE. 2011;6: e24434. doi: 10.1371/journal.pone.002443421931713
37. Saeij JPJ, Boyle JP, Coller S, Taylor S, Sibley LD, Brooke-Powell ET, et al. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science. 2006;314: 1780–1783. doi: 10.1126/science.113369017170306
38. Taylor S, Barragan A, Su C, Fux B, Fentress SJ, Tang K, et al. A Secreted Serine-Threonine Kinase Determines Virulence in the Eukaryotic Pathogen Toxoplasma gondii. Science. 2006;314: 1776–1780. doi: 10.1126/science.113364317170305
39. Butcher BA, Fox BA, Rommereim LM, Kim SG, Maurer KJ, Yarovinsky F, et al. Toxoplasma gondii rhoptry kinase ROP16 activates STAT3 and STAT6 resulting in cytokine inhibition and arginase-1-dependent growth control. PLoS Pathog. 2011;7: e1002236. doi: 10.1371/journal.ppat.100223621931552
40. Steinfeldt T, Könen-Waisman S, Tong L, Pawlowski N, Lamkemeyer T, Sibley LD, et al. Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii. PLoS Biol. 2010;8: e1000576. doi: 10.1371/journal.pbio.100057621203588
41. Zhao YO, Khaminets A, Hunn JP, Howard JC, Soldati-Favre D, Disruption of the Toxoplasma gondii Parasitophorous Vacuole by IFNγ-Inducible Immunity-Related GTPases (IRG Proteins) Triggers Necrotic Cell Death. PLoS Pathog. 2009;5: e1000288. doi: 10.1371/journal.ppat.100028819197351
42. Zhao Y, Ferguson DJP, Wilson DC, Howard JC, Sibley LD, Yap GS, Virulent Toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages. J Immunol. 2009;182: 3775–3781. doi: 10.4049/jimmunol.080419019265156
43. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, Reichmann G, et al. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog. 2005;1: e24. doi: 10.1371/journal.ppat.001002416304607
44. Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, Ferguson DJP, et al. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med. 2006;203: 2063–2071. doi: 10.1084/jem.2006131816940170
45. Yamamoto M, Okuyama M, Ma JS, Kimura T, Kamiyama N, Saiga H, et al. A Cluster of Interferon-γ-Inducible p65 GTPases Plays a Critical Role in Host Defense against Toxoplasma gondii. Immunity. 2012; 37: 302–313
46. Thurston TLM, Wandel MP, Muhlinen von N, Foeglein A, Randow F, Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature. 2012;482: 414–418. doi: 10.1038/nature1074422246324
47. Cemma M, Kim PK, Brumell JH, 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;7: 341–345. doi: 10.4161/auto.7.3.1404621079414
48. Zheng YT, Shahnazari S, Brech A, Lamark T, Johansen T, Brumell JH, The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. The Journal of Immunology. American Association of Immunologists; 2009;183: 5909–5916. doi: 10.4049/jimmunol.090044119812211
49. Haldar AK, Foltz C, Finethy R, Piro AS, Feeley EM, Pilla-Moffett DM, et al. Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins. Proc Natl Acad Sci USA. National Acad Sciences; 2015;112: E5628–37. doi: 10.1073/pnas.151596611226417105
50. Long J, Gallagher TRA, Cavey JR, Sheppard PW, Ralston SH, Layfield R, et al. Ubiquitin recognition by the ubiquitin-associated domain of p62 involves a novel conformational switch. J Biol Chem. 2008;283: 5427–5440. doi: 10.1074/jbc.M70497320018083707
51. Tan JMM, Wong ESP, Kirkpatrick DS, Pletnikova O, Ko HS, Tay S- P, et al. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet. Oxford University Press; 2008;17: 431–439. doi: 10.1093/hmg/ddm32017981811
52. Wooten MW, Geetha T, Babu JR, Seibenhener ML, Peng J, Cox N, et al. Essential role of sequestosome 1/p62 in regulating accumulation of Lys63-ubiquitinated proteins. J Biol Chem. American Society for Biochemistry and Molecular Biology; 2008;283: 6783–6789. doi: 10.1074/jbc.M70949620018174161
53. Muhlinen von N, Akutsu M, Ravenhill BJ, Foeglein A, Bloor S, Rutherford TJ, et al. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol Cell. 2012;48: 329–342. doi: 10.1016/j.molcel.2012.08.02423022382
54. Selleck EM, Orchard RC, Lassen KG, Beatty WL, Xavier RJ, Levine B, et al. A Noncanonical Autophagy Pathway Restricts Toxoplasma gondii Growth in a Strain-Specific Manner in IFN-γ-Activated Human Cells. MBio. American Society for Microbiology; 2015;6: e01157–15–14.
55. Mizushima N, Yoshimori T, Levine B, Methods in mammalian autophagy research. Cell. Elsevier; 2010;140: 313–326.
56. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4: 151–175. 18188003