Compensatory T cell responses in IRG-deficient mice prevent sustained Chlamydia trachomatis infections

PLoS Pathogens

Volumn 7, Issue 6, 2011, Pages

  Coers, Jörn ^a   Gondek, Dave C ^b   Olive, Andrew J ^b   Rohlfing, Amy ^b   Taylor, Gregory A ^a,c   Starnbach, Michael N ^b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DURHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; IMMUNITY RELATED GUANOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG; HYDROLYASE; IRG1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; CD4+ T LYMPHOCYTE; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; FLOW CYTOMETRY; GENE; IMMUNE DEFICIENCY; IMMUNITY; INTRAUTERINE INFECTION; IRGM1 GENE; IRGM3 GENE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; ADAPTIVE IMMUNITY; ANIMAL; EPITHELIUM CELL; IMMUNOLOGY; MICROBIOLOGY; MOUSE MUTANT;

ADOLESCENT; ADULT; AGED; AUTOANTIBODIES; CD4 LYMPHOCYTE COUNT; FAMILY; FEMALE; GENOTYPE; HUMANS; IMMUNOGLOBULIN G; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; MODELS, IMMUNOLOGICAL; PHENOTYPE; PROTEIN BINDING; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT; ADAPTIVE IMMUNITY; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; EPITHELIAL CELLS; HYDRO-LYASES; MICE; MICE, KNOCKOUT;

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

EID: 79959853767     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001346     Document Type: Article

References (59)

1. Belland R, Ojcius DM, Byrne GI, (2004) Chlamydia. Nat Rev Microbiol 2: 530-531.
2. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, et al. (2004) Global data on visual impairment in the year 2002. Bull World Health Organ 82: 844-851.
3. World Health Organization (2003) World Health Report, Shaping the future. World Health Organization Geneva.
4. Beatty WL, Morrison RP, Byrne GI, (1994) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58: 686-699.
5. Mpiga P, Ravaoarinoro M, (2006) Chlamydia trachomatis persistence: an update. Microbiol Res 161: 9-19.
6. Monack DM, Mueller A, Falkow S, (2004) Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2: 747-765.
7. Brown NF, Wickham ME, Coombes BK, Finlay BB, (2006) Crossing the line: selection and evolution of virulence traits. PLoS Pathog 2: e42.
8. Ito JI Jr, Harrison HR, Alexander ER, Billings LJ, (1984) Establishment of genital tract infection in the CF-1 mouse by intravaginal inoculation of a human oculogenital isolate of Chlamydia trachomatis. J Infect Dis 150: 577-582.
9. Perry LL, Su H, Feilzer K, Messer R, Hughes S, et al. (1999) Differential sensitivity of distinct Chlamydia trachomatis isolates to IFN-gamma-mediated inhibition. J Immunol 162: 3541-3548.
10. Roshick C, Wood H, Caldwell HD, McClarty G, (2006) Comparison of gamma interferon-mediated antichlamydial defense mechanisms in human and mouse cells. Infect Immun 74: 225-238.
11. Thomas SM, Garrity LF, Brandt CR, Schobert CS, Feng GS, et al. (1993) IFN-gamma-mediated antimicrobial response. Indoleamine 2,3-dioxygenase-deficient mutant host cells no longer inhibit intracellular Chlamydia spp. or Toxoplasma growth. J Immunol 150: 5529-5534.
12. Burian K, Endresz V, Deak J, Kormanyos Z, Pal A, et al. (2010) Transcriptome analysis indicates an enhanced activation of adaptive and innate immunity by chlamydia-infected murine epithelial cells treated with interferon gamma. J Infect Dis 202: 1405-1414.
13. Desvignes L, Ernst JD, (2009) Interferon-gamma-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 31: 974-985.
14. Peng K, Monack DM, (2010) Indoleamine 2,3-dioxygenase 1 is a lung-specific innate immune defense mechanism that inhibits growth of Francisella tularensis tryptophan auxotrophs. Infect Immun 78: 2723-2733.
15. Nelson DE, Virok DP, Wood H, Roshick C, Johnson RM, et al. (2005) Chlamydial IFN-gamma immune evasion is linked to host infection tropism. Proc Natl Acad Sci U S A 102: 10658-10663.
16. 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: e4588.
17. Bernstein-Hanley I, Balsara ZR, Ulmer W, Coers J, Starnbach MN, et al. (2006) Genetic analysis of susceptibility to Chlamydia trachomatis in mouse. Genes Immun 7: 122-129.
18. Bernstein-Hanley I, Coers J, Balsara ZR, Taylor GA, Starnbach MN, et al. (2006) The p47 GTPases Igtp and Irgb10 map to the Chlamydia trachomatis susceptibility locus Ctrq-3 and mediate cellular resistance in mice. Proc Natl Acad Sci U S A 103: 14092-14097.
19. Coers J, Bernstein-Hanley I, Grotsky D, Parvanova I, Howard JC, et al. (2008) Chlamydia muridarum evades growth restriction by the IFN-gamma-inducible host resistance factor Irgb10. J Immunol 180: 6237-6245.
20. Miyairi I, Tatireddigari VR, Mahdi OS, Rose LA, Belland RJ, et al. (2007) The p47 GTPases Iigp2 and Irgb10 regulate innate immunity and inflammation to murine Chlamydia psittaci infection. J Immunol 179: 1814-1824.
21. Caldwell HD, Wood H, Crane D, Bailey R, Jones RB, et al. (2003) Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J Clin Invest 111: 1757-1769.
22. MacMicking JD, (2005) Immune control of phagosomal bacteria by p47 GTPases. Curr Opin Microbiol 8: 74-82.
23. Martens S, Howard J, (2006) The interferon-inducible GTPases. Annu Rev Cell Dev Biol 22: 559-589.
24. Taylor GA, (2007) IRG proteins: key mediators of interferon-regulated host resistance to intracellular pathogens. Cell Microbiol 9: 1099-1107.
25. Feng CG, Zheng L, Jankovic D, Bafica A, Cannons JL, et al. (2008) The immunity-related GTPase Irgm1 promotes the expansion of activated CD4+ T cell populations by preventing interferon-gamma-induced cell death. Nat Immunol 9: 1279-1287.
26. Gondek DC, Roan NR, Starnbach MN, (2009) T cell responses in the absence of IFN-gamma exacerbate uterine infection with Chlamydia trachomatis. J Immunol 183: 1313-1319.
27. Roan NR, Gierahn TM, Higgins DE, Starnbach MN, (2006) Monitoring the T cell response to genital tract infection. Proc Natl Acad Sci U S A 103: 12069-12074.
28. Henry SC, Daniell XG, Burroughs AR, Indaram M, Howell DN, et al. (2009) Balance of Irgm protein activities determines IFN-gamma-induced host defense. J Leukoc Biol 85: 877-885.
29. Jayarapu K, Kerr M, Ofner S, Johnson RM, (2010) Chlamydia-specific CD4 T cell clones control Chlamydia muridarum replication in epithelial cells by nitric oxide-dependent and-independent mechanisms. J Immunol 185: 6911-6920.
30. Joyner JL, Douglas JM Jr, Foster M, Judson FN, (2002) Persistence of Chlamydia trachomatis infection detected by polymerase chain reaction in untreated patients. Sex Transm Dis 29: 196-200.
31. Mardh PA, (2004) Tubal factor infertility, with special regard to chlamydial salpingitis. Curr Opin Infect Dis 17: 49-52.
32. Intemann CD, Thye T, Niemann S, Browne EN, Amanua Chinbuah M, et al. (2009) Autophagy gene variant IRGM-261T contributes to protection from tuberculosis caused by Mycobacterium tuberculosis but not by M. africanum strains. PLoS Pathog 5: e1000577.
33. Lapaquette P, Glasser AL, Huett A, Xavier RJ, Darfeuille-Michaud A, (2010) Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly. Cell Microbiol 12: 99-113.
34. Singh SB, Davis AS, Taylor GA, Deretic V, (2006) Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313: 1438-1441.
35. Singh SB, Ornatowski W, Vergne I, Naylor J, Delgado M, et al. (2010) Human IRGM regulates autophagy and cell-autonomous immunity functions through mitochondria. Nat Cell Biol 12: 1154-1165.
36. Hunn JP, Koenen-Waisman S, Papic N, Schroeder N, Pawlowski N, et al. (2008) Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. EMBO J 27: 2495-2509.
37. Papic N, Hunn JP, Pawlowski N, Zerrahn J, Howard JC, (2008) Inactive and active states of the interferon-inducible resistance GTPase, Irga6, in vivo. J Biol Chem 283: 32143-32151.
38. Hunn JP, Howard JC, (2010) The mouse resistance protein Irgm1 (LRG-47): a regulator or an effector of pathogen defense? PLoS Pathog 6: e1001008.
39. Boehm U, Klamp T, Groot M, Howard JC, (1997) Cellular responses to interferon-gamma. Annu Rev Immunol 15: 749-795.
40. Ellis TN, Beaman BL, (2004) Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology 112: 2-12.
41. Mikhak Z, Farsidjani A, Luster AD, (2009) Endotoxin augmented antigen-induced Th1 cell trafficking amplifies airway neutrophilic inflammation. J Immunol 182: 7946-7956.
42. Strehl B, Seifert U, Kruger E, Heink S, Kuckelkorn U, et al. (2005) Interferon-gamma, the functional plasticity of the ubiquitin-proteasome system, and MHC class I antigen processing. Immunol Rev 207: 19-30.
43. Afanasyeva M, Georgakopoulos D, Belardi DF, Bedja D, Fairweather D, et al. (2005) Impaired up-regulation of CD25 on CD4+ T cells in IFN-gamma knockout mice is associated with progression of myocarditis to heart failure. Proc Natl Acad Sci U S A 102: 180-185.
44. Fonteneau JF, Larsson M, Bhardwaj N, (2002) Interactions between dead cells and dendritic cells in the induction of antiviral CTL responses. Curr Opin Immunol 14: 471-477.
45. Lan RY, Selmi C, Gershwin ME, (2008) The regulatory, inflammatory, and T cell programming roles of interleukin-2 (IL-2). J Autoimmun 31: 7-12.
46. Ganusov VV, Milutinovic D, De Boer RJ, (2007) IL-2 regulates expansion of CD4+ T cell populations by affecting cell death: insights from modeling CFSE data. J Immunol 179: 950-957.
47. Malek TR, Bayer AL, (2004) Tolerance, not immunity, crucially depends on IL-2. Nat Rev Immunol 4: 665-674.
48. Pei Y, Zhu P, Dang Y, Wu J, Yang X, et al. (2008) Nuclear export of NF90 to stabilize IL-2 mRNA is mediated by AKT-dependent phosphorylation at Ser647 in response to CD28 costimulation. J Immunol 180: 222-229.
49. Willerford DM, Chen J, Ferry JA, Davidson L, Ma A, et al. (1995) Interleukin-2 receptor alpha chain regulates the size and content of the peripheral lymphoid compartment. Immunity 3: 521-530.
50. Coers J, Starnbach MN, Howard JC, (2009) Modeling infectious disease in mice: co-adaptation and the role of host-specific IFNgamma responses. PLoS Pathog 5: e1000333.
51. Daubener W, MacKenzie CR, (1999) IFN-gamma activated indoleamine 2,3-dioxygenase activity in human cells is an antiparasitic and an antibacterial effector mechanism. Adv Exp Med Biol 467: 517-524.
52. Daubener W, Spors B, Hucke C, Adam R, Stins M, et al. (2001) Restriction of Toxoplasma gondii growth in human brain microvascular endothelial cells by activation of indoleamine 2,3-dioxygenase. Infect Immun 69: 6527-6531.
53. MacKenzie CR, Langen R, Takikawa O, Daubener W, (1999) Inhibition of indoleamine 2,3-dioxygenase in human macrophages inhibits interferon-gamma-induced bacteriostasis but does not abrogate toxoplasmastasis. Eur J Immunol 29: 3254-3261.
54. Spekker K, Czesla M, Ince V, Heseler K, Schmidt SK, et al. (2009) Indoleamine 2,3-dioxygenase is involved in defense against Neospora caninum in human and bovine cells. Infect Immun 77: 4496-4501.
55. Beatty WL, Belanger TA, Desai AA, Morrison RP, Byrne GI, (1994) Tryptophan depletion as a mechanism of gamma interferon-mediated chlamydial persistence. Infect Immun 62: 3705-3711.
56. Kane CD, Vena RM, Ouellette SP, Byrne GI, (1999) Intracellular tryptophan pool sizes may account for differences in gamma interferon-mediated inhibition and persistence of chlamydial growth in polarized and nonpolarized cells. Infect Immun 67: 1666-1671.
57. Rottenberg ME, Gigliotti-Rothfuchs A, Wigzell H, (2002) The role of IFN-gamma in the outcome of chlamydial infection. Curr Opin Immunol 14: 444-451.
58. Collazo CM, Yap GS, Sempowski GD, Lusby KC, Tessarollo L, et al. (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.
59. Taylor GA, Collazo CM, Yap GS, Nguyen K, Gregorio TA, et al. (2000) Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc Natl Acad Sci U S A 97: 751-755.