3,333
Views
26
CrossRef citations to date
0
Altmetric
Special Focus on Autophagy in host-pathogen interactions

The role of host autophagy machinery in controlling Toxoplasma infection

ORCID Icon
Pages 438-447 | Received 25 May 2018, Accepted 26 Aug 2018, Published online: 29 Sep 2018

References

  • Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004;363:1965–1976.
  • Dubey JP, Lindsay DS, Speer CA. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev. 1998;11:267–299.
  • Jeffers V, Tampaki Z, Kim K, et al. A latent ability to persist: differentiation in Toxoplasma gondii. Cell Mol Life Sci CMLS. 2018;75:2355–2373.
  • Xiao J, Yolken RH. Strain hypothesis of Toxoplasma gondii infection on the outcome of human diseases. Acta Physiol. 2015;213:828–845.
  • Howe DK, Sibley LD. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis. 1995;172:1561–1566.
  • Su C, Khan A, Zhou P, et al. Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages. Proc Natl Acad Sci U S A. 2012;109:5844–5849.
  • Sibley LD, Boothroyd JC. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature. 1992;359:82–85.
  • Sasai M, Pradipta A, Yamamoto M. Host immune responses to Toxoplasma gondii. Int Immunol. 2018;30:113–119.
  • Dupont CD, Christian DA, Hunter CA. Immune response and immunopathology during toxoplasmosis. Semin Immunopathol. 2012;34:793–813.
  • Gazzinelli RT, Wysocka M, Hayashi S, et al. Parasite-induced IL-12 stimulates early IFN-gamma synthesis and resistance during acute infection with Toxoplasma gondii. J Immunol Baltim Md. 1994;153:2533–2543.
  • Dunay IR, Diefenbach A. Group 1 innate lymphoid cells in Toxoplasma gondii infection. Parasite Immunol. 2018;40:e12516.
  • Könen-Waisman S, Howard JC. Cell-autonomous immunity to Toxoplasma gondii in mouse and man. Microbes Infect. 2007;9:1652–1661.
  • Kang H, Remington JS, Suzuki Y. Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-gamma, TNF-alpha, and inducible nitric oxide synthase. J Immunol Baltim Md. 2000;164:2629–2634.
  • Sher A, Tosh K, Jankovic D. Innate recognition of Toxoplasma gondii in humans involves a mechanism distinct from that utilized by rodents. Cell Mol Immunol. 2017;14:36–42.
  • Bekpen C, Hunn JP, Rohde C, et al. The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol. 2005;6:R92.
  • Morisaki JH, Heuser JE, Sibley LD. Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J Cell Sci. 1995;108(Pt 6):2457–2464.
  • 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 Baltim Md. 1997;159:4452–4459.
  • Sturge CR, Yarovinsky F. Complex immune cell interplay in the gamma interferon response during Toxoplasma gondii infection. Infect Immun. 2014;82:3090–3097.
  • Scharton-Kersten TM, Wynn TA, Denkers EY, et al. In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J Immunol Baltim Md. 1996;157:4045–4054.
  • Suzuki Y, Orellana MA, Schreiber RD, et al. Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science. 1988;240:516–518.
  • Cerávolo IP, Chaves AC, Bonjardim CA, et al. Replication of Toxoplasma gondii, but not Trypanosoma cruzi, is regulated in human fibroblasts activated with gamma interferon: requirement of a functional JAK/STAT pathway. Infect Immun. 1999;67:2233–2240.
  • 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 U S A. 1984;81:908–912.
  • Janssen R, Van Wengen A, Verhard E, et al. Divergent role for TNF-alpha in IFN-gamma-induced killing of Toxoplasma gondii and Salmonella typhimurium contributes to selective susceptibility of patients with partial IFN-gamma receptor 1 deficiency. J Immunol Baltim Md. 2002;169:3900–3907.
  • Reichmann G, Walker W, Villegas EN, et al. The CD40/CD40 ligand interaction is required for resistance to toxoplasmic encephalitis. Infect Immun. 2000;68:1312–1318.
  • Subauste CS, Wessendarp M. CD40 restrains in vivo growth of Toxoplasma gondii independently of gamma interferon. Infect Immun. 2006;74:1573–1579.
  • Subauste CS, Wessendarp M, Sorensen RU, et al. CD40-CD40 ligand interaction is central to cell-mediated immunity against Toxoplasma gondii: patients with hyper IgM syndrome have a defective type 1 immune response that can be restored by soluble CD40 ligand trimer. J Immunol Baltim Md. 1999;162:6690–6700.
  • Yarovinsky F. Innate immunity to Toxoplasma gondii infection. Nat Rev Immunol. 2014;14:109–121.
  • Kim B-H, Shenoy AR, Kumar P, et al. IFN-inducible GTPases in host cell defense. Cell Host Microbe. 2012;12:432–444.
  • Etheridge RD, Alaganan A, Tang K, et al. The Toxoplasma pseudokinase ROP5 forms complexes with ROP18 and ROP17 kinases that synergize to control acute virulence in mice. Cell Host Microbe. 2014;15:537–550.
  • Hermanns T, Müller UB, Könen-Waisman S, et al. The Toxoplasma gondii rhoptry protein ROP18 is an Irga6-specific kinase and regulated by the dense granule protein GRA7. Cell Microbiol. 2016;18:244–259.
  • Hakimi M-A, Olias P, Sibley LD. Toxoplasma effectors targeting host signaling and transcription. Clin Microbiol Rev. 2017;30:615–645.
  • Melo MB, Jensen KDC, Saeij JPJ. Toxoplasma gondii effectors are master regulators of the inflammatory response. Trends Parasitol. 2011;27:487–495.
  • Yin Z, Pascual C, Klionsky DJ. Autophagy: machinery and regulation. Microb Cell. 2016;3:588–596.
  • Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy. Nat Cell Biol. 2013;15:713–720.
  • Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13:722–737.
  • Shibutani ST, Saitoh T, Nowag H, et al. Autophagy and autophagy-related proteins in the immune system. Nat Immunol. 2015;16:1014–1024.
  • Tsukada M, Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 1993;333:169–174.
  • Díaz-Troya S, Pérez-Pérez ME, Florencio FJ, et al. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy. 2008;4:851–865.
  • Kihara A, Noda T, Ishihara N, et al. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol. 2001;152:519–530.
  • Wild P, McEwan DG, Dikic I. The LC3 interactome at a glance. J Cell Sci. 2014;127:3885–3889.
  • Kabeya Y. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci. 2004;117:2805–2812.
  • Schaaf MBE, Keulers TG, Vooijs MA, et al. LC3/GABARAP family proteins: autophagy-(un)related functions. FASEB J Off Publ Fed Am Soc Exp Biol. 2016;30:3961–3978.
  • Lai S-C, Devenish RJ. LC3-associated phagocytosis (LAP): connections with host autophagy. Cells. 2012;1:396–408.
  • Sanjuan MA, Dillon CP, Tait SWG, et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature. 2007;450:1253–1257.
  • Martinez J, Malireddi RKS, Lu Q, et al. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat Cell Biol. 2015;17:893–906.
  • Nguyen TN, Padman BS, Usher J, et al. Atg8 family LC3/GABARAP proteins are crucial for autophagosome-lysosome fusion but not autophagosome formation during PINK1/Parkin mitophagy and starvation. J Cell Biol. 2016;215:857–874.
  • Harrison RE, Bucci C, Vieira OV, et al. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol. 2003;23:6494–6506.
  • Howard JC, Hunn JP, Steinfeldt T. The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr Opin Microbiol. 2011;14:414–421.
  • Ling YM, Shaw MH, Ayala C, et al. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med. 2006;203:2063–2071.
  • Martens S, Parvanova I, Zerrahn J, et al. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog. 2005;1:e24.
  • Zhao Z, Fux B, Goodwin M, et al. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe. 2008;4:458–469.
  • Ohshima J, Lee Y, Sasai M, et al. Role of mouse and human autophagy proteins in IFN-γ-induced cell-autonomous responses against Toxoplasma gondii. J Immunol Baltim Md. 2014;192:3328–3335.
  • Choi J, Park S, Biering SB, et al. The parasitophorous vacuole membrane of Toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy. Immunity. 2014;40:924–935.
  • Sasai M, Sakaguchi N, Ma JS, et al. Essential role for GABARAP autophagy proteins in interferon-inducible GTPase-mediated host defense. Nat Immunol. 2017;18:899–910.
  • Khaminets A, Hunn JP, Könen-Waisman S, et al. Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cell Microbiol. 2010;12:939–961.
  • Kim B-H, Shenoy AR, Kumar P, et al. A family of IFN- -Inducible 65-kD GTPases protects against bacterial infection. Science. 2011;332:717–721.
  • Liu E, Van Grol J, Subauste CS. Atg5 but not Atg7 in dendritic cells enhances IL-2 and IFN-γ production by Toxoplasma gondii-reactive CD4+ T cells. Microbes Infect. 2015;17:275–284.
  • Haldar AK, Piro AS, Pilla DM, et al. The E2-like conjugation enzyme Atg3 promotes binding of IRG and Gbp proteins to chlamydia- and toxoplasma-containing vacuoles and host resistance. PloS One. 2014;9:e86684.
  • Park S, Choi J, Biering SB, et al. Targeting by autophaGy proteins (TAG): targeting of IFNG-inducible GTPases to membranes by the LC3 conjugation system of autophagy. Autophagy. 2016;12:1153–1167.
  • Choi J, Biering SB, Hwang S. Quo vadis? Interferon-inducible GTPases go to their target membranes via the LC3-conjugation system of autophagy. Small GTPases. 2017;8:199–207.
  • Pilla-Moffett D, Barber MF, Taylor GA, et al. Interferon-inducible GTPases in host resistance, inflammation and disease. J Mol Biol. 2016;428:3495–3513.
  • Johnston AC, Piro A, Clough B, et al. Human GBP1 does not localize to pathogen vacuoles but restricts Toxoplasma gondii. Cell Microbiol. 2016;18:1056–1064.
  • Portillo J-AC, Okenka G, Reed E, et al. 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. 2010;5:e14472.
  • Andrade RM, Wessendarp M, Gubbels M-J, et al. 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.
  • Van Grol J, Muniz-Feliciano L, Portillo J-AC, et al. CD40 induces anti-toxoplasma gondii activity in nonhematopoietic cells dependent on autophagy proteins. Infect Immun. 2013;81:2002–2011.
  • Liu E, Lopez Corcino Y, Portillo J-AC, et al. Identification of signaling pathways by which CD40 stimulates autophagy and antimicrobial activity against Toxoplasma gondii in macrophages. Infect Immun. 2016;84:2616–2626.
  • Russell RC, Tian Y, Yuan H, et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol. 2013;15:741–750.
  • Muniz-Feliciano L, Van Grol J, Portillo J-AC, et al. Toxoplasma gondii-induced activation of EGFR prevents autophagy protein-mediated killing of the parasite. PLoS Pathog. 2013;9:e1003809.
  • Mizushima N, Ohsumi Y, Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct Funct. 2002;27:421–429.
  • Martinez J, Almendinger J, Oberst A, et al. Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci. 2011;108:17396–17401.
  • Portillo J-AC, Muniz-Feliciano L, Lopez Corcino Y, et al. Toxoplasma gondii induces FAK-Src-STAT3 signaling during infection of host cells that prevents parasite targeting by autophagy. PLOS Pathog. 2017;13:e1006671.
  • You L, Wang Z, Li H, et al. The role of STAT3 in autophagy. Autophagy. 2015;11:729–739.
  • Coppens I, Romano JD. Hostile intruder: toxoplasma holds host organelles captive. PLoS Pathog. 2018;14:e1006893.
  • Sinai AP, Webster P, Joiner KA. Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci. 1997;110(Pt 17):2117–2128.
  • Coppens I, Dunn JD, Romano JD, et al. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell. 2006;125:261–274.
  • Romano JD, Nolan SJ, Porter C, et al. The parasite Toxoplasma sequesters diverse Rab host vesicles within an intravacuolar network. J Cell Biol. 2017;216:4235–4254.
  • Romano JD, Sonda S, Bergbower E, et al. Toxoplasma gondii salvages sphingolipids from the host Golgi through the rerouting of selected Rab vesicles to the parasitophorous vacuole. Mol Biol Cell. 2013;24:1974–1995.
  • Nolan SJ, Romano JD, Coppens I. Host lipid droplets: an important source of lipids salvaged by the intracellular parasite Toxoplasma gondii. PLoS Pathog. 2017;13:e1006362.
  • Hu X, Binns D, Reese ML. The coccidian parasites Toxoplasma and neospora dysregulate mammalian lipid droplet biogenesis. J Biol Chem. 2017;292:11009–11020.
  • Wang Y, Weiss LM, Orlofsky A. Host cell autophagy is induced by Toxoplasma gondii and contributes to parasite growth. J Biol Chem. 2009;284:1694–1701.
  • Pernas L, Bean C, Boothroyd JC, et al. Mitochondria restrict growth of the intracellular parasite Toxoplasma gondii by limiting its uptake of fatty acids. Cell Metab. 2018;27(4):886–897.e4.
  • Selleck EM, Orchard RC, Lassen KG, 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.
  • Lee Y, Sasai M, Ma JS, et al. p62 plays a specific role in interferon-γ-induced presentation of a Toxoplasma vacuolar antigen. Cell Rep. 2015;13:223–233.
  • Virreira Winter S, Niedelman W, Jensen KD, et al. Determinants of GBP recruitment to Toxoplasma gondii vacuoles and the parasitic factors that control it. PLoS ONE. 2011;6:e24434.
  • Haldar AK, Foltz C, Finethy R, et al. Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins. Proc Natl Acad Sci U S A. 2015;112:E5628–5637.
  • Clough B, Frickel E-M. The Toxoplasma parasitophorous vacuole: an evolving host-parasite frontier. Trends Parasitol. 2017;33:473–488.
  • Man SM, Place DE, Kuriakose T, et al. Interferon-inducible guanylate-binding proteins at the interface of cell-autonomous immunity and inflammasome activation. J Leukoc Biol. 2017;101:143–150.
  • Gorfu G, Cirelli KM, Melo MB, et al. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to toxoplasma gondii. mBio. 2014;5:e01117-13-e01117-13.
  • Ewald SE, Chavarria-Smith J, Boothroyd JC. NLRP1 is an inflammasome sensor for Toxoplasma gondii. Infect Immun. 2014;82:460–468.
  • Harris J, Lang T, Thomas JPW, et al. Autophagy and inflammasomes. Mol Immunol. 2017;86:10–15.
  • Münz C. Autophagy beyond intracellular MHC class II antigen presentation. Trends Immunol. 2016;37:755–763.
  • Rubinsztein DC, Bento CF, Deretic V. Therapeutic targeting of autophagy in neurodegenerative and infectious diseases. J Exp Med. 2015;212:979–990.
  • Galluzzi L, Bravo-San Pedro JM, Levine B, et al. Pharmacological modulation of autophagy: therapeutic potential and persisting obstacles. Nat Rev Drug Discov. 2017;16:487–511.
  • Steele S, Brunton J, Kawula T. The role of autophagy in intracellular pathogen nutrient acquisition. Front Cell Infect Microbiol. 2015;5:51.