Autophagy restricts Chlamydia trachomatis growth in human macrophages via IFNG-inducible guanylate binding proteins

Autophagy

Volumn 9, Issue 1, 2013, Pages 50-62

  Al Zeer, Munir A ^a   Al Younes, Hesham M ^b   Lauster, Daniel ^a   Lubad, Mohammad Abu ^a   Meyer, Thomas F ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b UNIVERSITY OF JORDAN   (Jordan)

Author keywords

Chlamydial inclusion; GTPase; Innate immunity; Interferon response; Intracellular bacteria

Indexed keywords

GAMMA INTERFERON; GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; AUTOPHAGY; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CELL INCLUSION; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; DEGRADATION; GENE SILENCING; LYSOSOME; MACROPHAGE; NONHUMAN; WILD TYPE;

BACTERIA (MICROORGANISMS); CHLAMYDIA; CHLAMYDIA TRACHOMATIS; MURINAE;

EID: 84872194128     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.22482     Document Type: Article

References (50)

1. Byrne GI, Krueger DA. Lymphokine-mediated inhibition of Chlamydia replication in mouse fibroblasts is neutralized by anti-gamma interferon immunoglobulin. Infect Immun 1983; 42:1152-8; PMID:6417024
2. Rank RG, Ramsey KH, Pack EA, Williams DM. Effect of gamma interferon on resolution of murine chlamydial genital infection. Infect Immun 1992; 60:4427-9; PMID:1398955
3. Ito JI, Lyons JM. Role of gamma interferon in controlling murine chlamydial genital tract infection. Infect Immun 1999; 67:5518-21; PMID:10496942
4. Morré SA, Lyons JM, Ito JI Jr. Murine models of Chlamydia trachomatis genital tract infection: use of mouse pneumonitis strain versus human strains. Infect Immun 2000; 68:7209-11; PMID:11203323; http:// dx.doi.org/10.1128/IAI.68.12.7209-7211.2000
5. Nelson DE, Virok DP, Wood H, Roshick C, Johnson RM, Whitmire WM, et al. Chlamydial IFN-γ immune evasion is linked to host infection tropism. Proc Natl Acad Sci U S A 2005; 102:10658-63; PMID:16020528; http://dx.doi.org/10. 1073/pnas.0504198102
6. Roshick C, Wood H, Caldwell HD, McClarty G. Comparison of gamma interferon-mediated antichlamydial defense mechanisms in human and mouse cells. Infect Immun 2006; 74:225-38; PMID:16368976; http://dx.doi.org/10.1128/IAI.74.1. 225-238.2006
7. Koehler L, Nettelnbreker E, Hudson AP, Ott N, Gérard HC, Branigan PJ, et al. Ultrastructural and molecular analyses of the persistence of Chlamydia trachomatis (serovar K) in human monocytes. Microb Pathog 1997; 22:133-42; PMID:9075216; http:// dx.doi.org/10.1006/mpat.1996.0103
8. Beatty WL, Morrison RP, Byrne GI. Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 1994; 58:686-99; PMID:7854252
9. Tietzel I, El-Haibi C, Carabeo RA. Human guanylate binding proteins potentiate the anti-chlamydia effects of interferon-gamma. PLoS One 2009; 4:e6499; PMID:19652711; http://dx.doi.org/10.1371/journal. pone.0006499
10. Al-Zeer MA, Al-Younes HM, Braun PR, Zerrahn J, Meyer TF. IFN-gamma-inducible Irga6 mediates host resistance against Chlamydia trachomatis via autophagy. PLoS One 2009; 4:e4588; PMID:19242543; http://dx.doi.org/10. 1371/journal.pone.0004588
11. Azenabor AA, Chaudhry AU. Chlamydia pneumoniae survival in macrophages is regulated by free Ca2+ dependent reactive nitrogen and oxygen species. J Infect 2003; 46:120-8; PMID:12634074; http:// dx.doi.org/10.1053/jinf.2002.1098
12. Beagley KW, Huston WM, Hansbro PM, Timms P. Chlamydial infection of immune cells: altered function and implications for disease. Crit Rev Immunol 2009; 29:275-305; PMID:19673684; http://dx.doi. org/10.1615/CritRevImmunol.v29. i4.10
13. Jendro MC, Fingerle F, Deutsch T, Liese A, Köhler L, Kuipers JG, et al. Chlamydia trachomatis-infected macrophages induce apoptosis of activated T cells by secretion of tumor necrosis factor-alpha in vitro. Med Microbiol Immunol 2004; 193:45-52; PMID:12750883; http://dx.doi.org/10.1007/s00430-003- 0182-1
14. Redecke V, Dalhoff K, Bohnet S, Braun J, Maass M. Interaction of Chlamydia pneumoniae and human alveolar macrophages: infection and inflammatory response. Am J Respir Cell Mol Biol 1998; 19:721-7; PMID:9806736
15. Wyrick PB. Intracellular survival by Chlamydia. Cell Microbiol 2000; 2:275-82; PMID:11207584; http:// dx.doi.org/10.1046/j.1462-5822.2000.00059.x
16. Wyrick PB, Brownridge EA. Growth of Chlamydia psittaci in macrophages. Infect Immun 1978; 19:1054-60; PMID:565338
17. MacMicking JD. IFN-inducible GTPases and immunity to intracellular pathogens. Trends Immunol 2004; 25:601-9; PMID:15489189; http://dx.doi. org/10.1016/j.it.2004.08.010
18. Cheng YS, Patterson CE, Staeheli P. Interferon-induced guanylate-binding proteins lack an N(T)KXD consensus motif and bind GMP in addition to GDP and GTP. Mol Cell Biol 1991; 11:4717-25; PMID:1715024
19. Kim BH, Shenoy AR, Kumar P, Das R, Tiwari S, MacMicking JD. A family of IFN-γ-inducible 65-kD GTPases protects against bacterial infection. Science 2011; 332:717-21; PMID:21551061; http://dx.doi. org/10.1126/science. 1201711
20. Nguyen TT, Hu Y, Widney DP, Mar RA, Smith JB. Murine GBP-5, a new member of the murine guanylate-binding protein family, is coordinately regulated with other GBPs in vivo and in vitro. J Interferon Cytokine Res 2002; 22:899-909; PMID:12396730; http://dx.doi.org/10.1089/107999002760274926
21. Vestal DJ, Gorbacheva VY, Sen GC. Different subcellular localizations for the related interferon-induced GTPases, MuGBP-1 and MuGBP-2: implications for different functions? J Interferon Cytokine Res 2000; 20:991-1000; PMID:11096456; http://dx.doi. org/10.1089/10799900050198435
22. Rupper AC, Cardelli JA. Induction of guanylate binding protein 5 by gamma interferon increases susceptibility to Salmonella enterica serovar Typhimurium-induced pyroptosis in RAW 264.7 cells. Infect Immun 2008; 76:2304-15; PMID:18362138; http://dx.doi. org/10.1128/IAI.01437-07
23. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3:542-5; PMID:17611390
24. Germain M, Nguyen AP, Le Grand JN, Arbour N, Vanderluit JL, Park DS, et al. MCL-1 is a stress sensor that regulates autophagy in a developmentally regulated manner. EMBO J 2011; 30:395-407; PMID:21139567; http://dx.doi.org/10. 1038/ emboj.2010.327
25. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152:657-68; PMID:11266458; http://dx.doi.org/10. 1083/jcb.152.4.657
26. Mizushima N, Yoshimori T, Ohsumi Y. Role of the Apg12 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 2003; 35:553-61; PMID:12672448; http://dx.doi.org/10.1016/S1357-2725(02)00343-6
27. Rottenberg ME, Gigliotti-Rothfuchs A, Wigzell H. The role of IFN-γ in the outcome of chlamydial infection. Curr Opin Immunol 2002; 14:444-51; PMID:12088678; http://dx.doi.org/10.1016/S0952- 7915(02)00361-8
28. Al-Younes HM, Brinkmann V, Meyer TF. Interaction of Chlamydia trachomatis serovar L2 with the host autophagic pathway. Infect Immun 2004; 72:4751-62; PMID:15271937; http://dx.doi.org/10.1128/IAI.72.8.4751-4762.2004
29. van Ooij C, Apodaca G, Engel J. Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect Immun 1997; 65:758-66; PMID:9009339
30. Al-Younes HM, Rudel T, Meyer TF. Characterization and intracellular trafficking pattern of vacuoles containing Chlamydia pneumoniae in human epithelial cells. Cell Microbiol 1999; 1:237-47; PMID:11207556; http://dx.doi.org/10.1046/j.1462-5822.1999.00024.x
31. Friis RR. Interaction of L cells and Chlamydia psittaci: entry of the parasite and host responses to its development. J Bacteriol 1972; 110:706-21; PMID:4336694
32. Ouellette SP, Dorsey FC, Moshiach S, Cleveland JL, Carabeo RA. Chlamydia species-dependent differences in the growth requirement for lysosomes. PLoS One 2011; 6:e16783; PMID:21408144; http://dx.doi. org/10.1371/journal.pone.0016783
33. Yasir M, Pachikara ND, Bao X, Pan Z, Fan H. Regulation of chlamydial infection by host autophagy and vacuolar ATPase-bearing organelles. Infect Immun 2011; 79:4019-28; PMID:21807906; http://dx.doi. org/10.1128/IAI.05308-11
34. 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; 159:4452-9; PMID:9379044
35. 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; PMID:16304607; http://dx.doi.org/10.1371/journal. ppat.0010024
36. Yap GS, Ling Y, Zhao Y. Autophagic elimination of intracellular parasites: convergent induction by IFN-gamma and CD40 ligation? Autophagy 2007; 3:163-5; PMID:17204853
37. Colombo MI, Gutierrez MG, Romano PS. The two faces of autophagy: Coxiella and Mycobacterium. Autophagy 2006; 2:162-4; PMID:16874070
38. 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; 119:753-66; PMID:15607973; http://dx.doi. org/10.1016/j.cell.2004.11.038
39. Singh SB, Davis AS, Taylor GA, Deretic V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 2006; 313:1438-41; PMID:16888103; http://dx.doi.org/10.1126/science. 1129577
40. Voth DE, Heinzen RA. Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol 2007; 9:829-40; PMID:17381428; http:// dx.doi.org/10.1111/j.1462-5822.2007.00901.x
41. Redd T, Thompson HA. Secretion of proteins by Coxiella burnetii. Microbiology 1995; 141:363-9; PMID:7704266; http://dx.doi. org/10.1099/13500872- 141-2-363
42. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6:463-77; PMID:15068787; http://dx.doi.org/10.1016/S1534-5807(04)00099-1
43. Anderson SL, Carton JM, Lou J, Xing L, Rubin BY. Interferon-induced guanylate binding protein-1 (GBP-1) mediates an antiviral effect against vesicular stomatitis virus and encephalomyocarditis virus. Virology 1999; 256:8-14; PMID:10087221; http:// dx.doi.org/10.1006/viro.1999.9614
44. Taylor GA, Feng CG, Sher A. Control of IFN-gamma-mediated host resistance to intracellular pathogens by immunity-related GTPases (p47 GTPases). Microbes Infect 2007; 9:1644-51; PMID:18023232; http:// dx.doi.org/10.1016/j.micinf.2007. 09.004
45. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, et al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8:1124-32; PMID:16998475; http://dx.doi. org/10.1038/ncb1482
46. Braun PR, Al-Younes H, Gussmann J, Klein J, Schneider E, Meyer TF. Competitive inhibition of amino acid uptake suppresses chlamydial growth: involvement of the chlamydial amino acid transporter BrnQ. J Bacteriol 2008; 190:1822-30; PMID:18024516; http://dx.doi.org/10.1128/JB.01240-07
47. Chang YP, Chen CL, Chen SO, Lin YS, Tsai CC, Huang WC, et al. Autophagy facilitates an IFN-γ response and signal transduction. Microbes Infect 2011; 13:888-94; PMID:21664983; http://dx.doi. org/10.1016/j.micinf.2011.05.008
48. Weichhart T. Mammalian target of rapamycin: a signaling kinase for every aspect of cellular life. Methods Mol Biol 2012; 821:1-14; PMID:22125056; http://dx.doi. org/10.1007/978-1-61779-430-8-1
49. Kuballa P, Nolte WM, Castoreno AB, Xavier RJ. Autophagy and the immune system. Annu Rev Immunol 2012; 30:611-46; PMID:22449030; http://dx.doi. org/10.1146/annurev-immunol-020711-074948
50. Wiznerowicz M, Trono D. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 2003; 77:8957- 61; PMID:12885912; http://dx.doi.org/10.1128/ JVI.77.16.8957-8951.2003