Role of mouse and human autophagy proteins in IFN-γ-induced cell-autonomous responses against Toxoplasma gondii

Journal of Immunology

Volumn 192, Issue 7, 2014, Pages 3328-3335

  Ohshima, Jun ^a,b,c   Lee, Youngae ^a,b   Sasai, Miwa ^a,b   Saitoh, Tatsuya ^a,b   Ma, Ji Su ^a,b,c   Kamiyama, Naganori ^a,b,c   Matsuura, Yoshiharu ^a   Pann Ghill, Suh ^d   Hayashi, Mikako ^b   Ebisu, Shigeyuki ^b   Takeda, Kiyoshi ^b,c,e   Akira, Shizuo ^a,b   Yamamoto, Masahiro ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d Ulsan National Institute of Science and Technology   (South Korea)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 5; BINDING PROTEIN; GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; P65 GUANYLATE BINDING PROTEIN; PEPTIDES AND PROTEINS; PROTEIN ATG14; PROTEIN ATG16L1; PROTEIN ATG7; PROTEIN ATG9A; PROTEIN IRGB6; PROTEIN P47; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FIBROBLAST; GENOMICS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TOXOPLASMA GONDII;

ANIMALS; AUTOPHAGY; BASE SEQUENCE; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; EMBRYO, MAMMALIAN; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; INTERFERON-GAMMA; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; TOXOPLASMA; VERO CELLS;

EID: 84897535028     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302822     Document Type: Article

References (43)

1. Yarovinsky, F., and A. Sher. 2006. Toll-like receptor recognition of Toxoplasma gondii. Int. J. Parasitol. 36: 255-259.
2. Boothroyd, J. C. 2009. Toxoplasma gondii: 25 years and 25 major advances for the field. Int. J. Parasitol. 39: 935-946.
3. Hunter, C. A., and L. D. Sibley. 2012. Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat. Rev. Microbiol. 10: 766-778.
4. Israelski, D. M., and J. S. Remington. 1993. Toxoplasmosis in patients with cancer. Clin. Infect. Dis. 17(Suppl. 2): S423-S435.
5. Suzuki, Y., M. A. Orellana, R. D. Schreiber, and J. S. Remington. 1988. Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science 240: 516-518.
6. Kim, B. H., A. R. Shenoy, P. Kumar, C. J. Bradfield, and J. D. MacMicking. 2012. IFN-inducible GTPases in host cell defense. Cell Host Microbe 12: 432-444.
7. Taylor, G. A., C. G. Feng, and A. Sher. 2004. p47 GTPases: regulators of immunity to intracellular pathogens. Nat. Rev. Immunol. 4: 100-109.
8. MacMicking, J. D. 2012. Interferon-inducible effector mechanisms in cellautonomous immunity. Nat. Rev. Immunol. 12: 367-382.
9. Collazo, C. M., G. S. Yap, G. D. Sempowski, K. C. Lusby, L. Tessarollo, G. F. Vande Woude, A. Sher, and G. A. Taylor. 2001. Inactivation of LRG-47 and IRG-47 reveals a family of interferon gamma-inducible genes with essential, pathogen-specific roles in resistance to infection. J. Exp. Med. 194: 181-188.
10. Degrandi, D., E. Kravets, C. Konermann, C. Beuter-Gunia, V. Klümpers, S. Lahme, E. Wischmann, A. K. Mausberg, S. Beer-Hammer, and K. Pfeffer. 2013. Murine guanylate binding protein 2 (mGBP2) controls Toxoplasma gondii replication. Proc. Natl. Acad. Sci. USA 110: 294-299.
11. Taylor, G. A., C. M. Collazo, G. S. Yap, K. Nguyen, T. A. Gregorio, L. S. Taylor, B. Eagleson, L. Secrest, E. A. Southon, S.W. Reid, et al. 2000. Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc. Natl. Acad. Sci. USA 97: 751-755.
12. Yamamoto, M., M. Okuyama, J. S. Ma, T. Kimura, N. Kamiyama, H. Saiga, J. Ohshima, M. Sasai, H. Kayama, T. Okamoto, et al. 2012. A cluster of interferon-γ-inducible p65 GTPases plays a critical role in host defense against Toxoplasma gondii. Immunity 37: 302-313.
13. Selleck, E. M., S. J. Fentress, W. L. Beatty, D. Degrandi, K. Pfeffer, H. W. Virgin, IV, J. D. Macmicking, and L. D. Sibley. 2013. Guanylate-binding protein 1 (Gbp1) contributes to cell-autonomous immunity against Toxoplasma gondii. PLoS Pathog. 9: e1003320.
14. Deretic, V. 2012. Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr. Opin. Immunol. 24: 21-31.
15. Kim, B. H., A. R. Shenoy, P. Kumar, R. Das, S. Tiwari, and J. D. MacMicking. 2011. A family of IFN-γ-inducible 65-kD GTPases protects against bacterial infection. Science 332: 717-721.
16. Mizushima, N., T. Yoshimori, and Y. Ohsumi. 2011. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27: 107-132.
17. Zhao, Z., B. Fux, M. Goodwin, I. R. Dunay, D. Strong, B. C. Miller, K. Cadwell, M. A. Delgado, M. Ponpuak, K. G. Green, et al. 2008. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4: 458-469.
18. Hwang, S., N. S. Maloney, M. W. Bruinsma, G. Goel, E. Duan, L. Zhang, B. Shrestha, M. S. Diamond, A. Dani, S. V. Sosnovtsev, et al. 2012. Nondegradative role of Atg5-Atg12/Atg16L1 autophagy protein complex in antiviral activity of interferon gamma. Cell Host Microbe 11: 397-409.
19. Pfefferkorn, E. R., and P. M. Guyre. 1984. Inhibition of growth of Toxoplasma gondii in cultured fibroblasts by human recombinant gamma interferon. Infect. Immun. 44: 211-216.
20. Mali, P., L. Yang, K. M. Esvelt, J. Aach, M. Guell, J. E. DiCarlo, J. E. Norville, and G. M. Church. 2013. RNA-guided human genome engineering via Cas9. Science 339: 823-826.
21. Cong, L., F. A. Ran, D. Cox, S. Lin, R. Barretto, N. Habib, P. D. Hsu, X. Wu, W. Jiang, L. A. Marraffini, and F. Zhang. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823.
22. Komatsu, M., S. Waguri, T. Chiba, S. Murata, J. Iwata, I. Tanida, T. Ueno, M. Koike, Y. Uchiyama, E. Kominami, and K. Tanaka. 2006. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441: 880-884.
23. Saitoh, T., N. Fujita, M. H. Jang, S. Uematsu, B. G. Yang, T. Satoh, H. Omori, T. Noda, N. Yamamoto, M. Komatsu, et al. 2008. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456: 264-268.
24. Saitoh, T., N. Fujita, T. Hayashi, K. Takahara, T. Satoh, H. Lee, K. Matsunaga, S. Kageyama, H. Omori, T. Noda, et al. 2009. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl. Acad. Sci. USA 106: 20842-20846.
25. Kageyama, S., H. Omori, T. Saitoh, T. Sone, J. L. Guan, S. Akira, F. Imamoto, T. Noda, and T. Yoshimori. 2011. The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol. Biol. Cell 22: 2290-2300.
26. Carette, J. E., M. Raaben, A. C. Wong, A. S. Herbert, G. Obernosterer, N. Mulherkar, A. I. Kuehne, P. J. Kranzusch, A. M. Griffin, G. Ruthel, et al. 2011. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477: 340-343.
27. Fujita, N., T. Itoh, H. Omori, M. Fukuda, T. Noda, and T. Yoshimori. 2008. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 19: 2092-2100.
28. Weidberg, H., E. Shvets, T. Shpilka, F. Shimron, V. Shinder, and Z. Elazar. 2010. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J. 29: 1792-1802.
29. Itakura, E., and N. Mizushima. 2009. Atg14 and UVRAG: mutually exclusive subunits of mammalian Beclin 1-PI3K complexes. Autophagy 5: 534-536.
30. Kabeya, Y., N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19: 5720-5728.
31. Nordmann, A., L. Wixler, Y. Boergeling, V. Wixler, and S. Ludwig. 2012. A new splice variant of the human guanylate-binding protein 3 mediates anti-influenza activity through inhibition of viral transcription and replication. FASEB J. 26: 1290-1300.
32. Matsunaga, K., E. Morita, T. Saitoh, S. Akira, N. T. Ktistakis, T. Izumi, T. Noda, and T. Yoshimori. 2010. Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J. Cell Biol. 190: 511-521.
33. Obara, K., and Y. Ohsumi. 2011. Atg14: a key player in orchestrating autophagy. Int. J. Cell Biol. 2011: 713435.
34. Orsi, A., M. Razi, H. C. Dooley, D. Robinson, A. E. Weston, L. M. Collinson, and S. A. Tooze. 2012. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol. Biol. Cell 23: 1860-1873.
35. Ling, Y. M., M. H. Shaw, C. Ayala, I. Coppens, G. A. Taylor, D. J. Ferguson, and G. S. Yap. 2006. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J. Exp. Med. 203: 2063-2071.
36. Portillo, J. A., G. Okenka, E. Reed, A. Subauste, J. Van Grol, K. Gentil, M. Komatsu, K. Tanaka, G. Landreth, B. Levine, and C. S. Subauste. 2010. The CD40-autophagy pathway is needed for host protection despite IFN-Γ-dependent immunity and CD40 induces autophagy via control of P21 levels. PLoS ONE 5: e14472.
37. Gupta, S. L., J. M. Carlin, P. Pyati, W. Dai, E. R. Pfefferkorn, and M. J. Murphy, Jr. 1994. Antiparasitic and antiproliferative effects of indoleamine 2, 3-dioxygenase enzyme expression in human fibroblasts. Infect. Immun. 62: 2277-2284.
38. Pfefferkorn, E. R. 1984. Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl. Acad. Sci. USA 81: 908-912.
39. Dimier, I. H., and D. T. Bout. 1997. Inhibition of Toxoplasma gondii replication in IFN-gamma-activated human intestinal epithelial cells. Immunol. Cell Biol. 75: 511-514.
40. Dimier, I. H., and D. T. Bout. 1998. Interferon-gamma-activated primary enterocytes inhibit Toxoplasma gondii replication: a role for intracellular iron. Immunology 94: 488-495.
41. Könen-Waisman, S., and J. C. Howard. 2007. Cell-autonomous immunity to Toxoplasma gondii in mouse and man. Microbes Infect. 9: 1652-1661.
42. Niedelman, W., J. K. Sprokholt, B. Clough, E. M. Frickel, and J. P. Saeij. 2013. Cell death of gamma interferon-stimulated human fibroblasts upon Toxoplasma gondii infection induces early parasite egress and limits parasite replication. Infect. Immun. 81: 4341-4349.
43. Shenoy, A. R., D. A. Wellington, P. Kumar, H. Kassa, C. J. Booth, P. Cresswell, and J. D. MacMicking. 2012. GBP5 Promotes NLRP3 inflammasome assembly and immunity in mammals. Science. 336: 481-485.