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Autophagy in Immunity Against Toxoplasma gondii

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Autophagy in Infection and Immunity

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 335))

Abstract

A decisive outcome during host-pathogen interaction is governed by whether pathogen-containing vacuoles fuse with lysosomes. Fusion with lysosomes typically kills microbes. Toxoplasma gondii represents a classical example of an intracellular pathogen that survives within host cells by preventing the endosomal-lysosomal compartments from fusing with the vacuoles that contain the pathogen. Thus, T. gondii provides an excellent model to determine if the immune system can target a pathogen for lysosomal degradation. CD40, a major regulator of cell-mediated immunity, activates macrophages to kill T. gondii through a process that requires recruitment of autophagosomes around the parasitophorous vacuole, leading to lysosomal degradation of the parasite. These studies demonstrate that cell-mediated immunity can activate autophagy to kill a pathogen. CD40-induced autophagy likely contributes to resistance against T. gondii, particularly in neural tissues, the main sites affected by this pathogen.

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References

  • Andrade RM, Wessendarp M, Subauste CS (2003) CD154 activates macrophage anti-microbial activity in the absence of IFN-γ through a TNF-α-dependent mechanism. J Immunol 171:6750–6756

    CAS  PubMed  Google Scholar 

  • Andrade RM, Portillo J-AC, Wessendarp M, Subauste CS (2005a) CD40 signaling in macrophages induces anti-microbial activity against an intracellular pathogen independently of IFN-γ and reactive nitrogen intermediates. Infect Immun 73:3115–3123

    Article  CAS  PubMed  Google Scholar 

  • Andrade RM, Wessendarp M, Portillo J-AC, Yang J-Q, Gomez FJ, Durbin JE, Bishop GA, Subauste CS (2005b) TRAF6 signaling downstream of CD40 primes macrophages to acquire anti-microbial activity in response to TNF-α. J Immunol 175:6014–6021

    CAS  PubMed  Google Scholar 

  • Andrade RM, Wessendarp M, Gubbels MJ, Striepen B, Subauste CS (2006) CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes. J Clin Invest 116:2366–2377

    Article  CAS  PubMed  Google Scholar 

  • Archbarou A, Mercereau-Puijalon O, Sadak A, Fortier B, Leriche MA, Camus D, Dubremetz JF (1991) Differential targeting of dense granule proteins in the parasitophorous vacuole of Toxoplasma gondii. Parasitology 103:321–329

    Article  Google Scholar 

  • Bekpen C, Hunn JP, Rohde C, Parvanova I, Guethlein L, Dunn DM, Glowalla E, Leptin M, Howard JC (2005) The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol 6:R92

    Article  PubMed  Google Scholar 

  • Birmingham CL, Smith AC, Bakowski MA, Yoshimori T, Brumell JH (2006) Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem 281:11374–11383

    Article  CAS  PubMed  Google Scholar 

  • Bishop GA, Moore CR, Xie P, Stunz LL, Kraus ZJ (2007) TRAF proteins in CD40 signaling. Adv Exp Med Biol 597:131–151

    Article  PubMed  Google Scholar 

  • Carruthers VB, Boothroyd JC (2007) Pulling together: an integrated model of Toxoplasma cell invasion. Curr Opin Microbiol 10:83–89

    Article  CAS  PubMed  Google Scholar 

  • Carruthers VB, Sibley D (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73:114–123

    CAS  PubMed  Google Scholar 

  • Cesbron-Delauw MF (1994) Dense-granule organelles of Toxoplasma gondii: their role in the host-parasite relationship. Parasitol Today 10:293–296

    Article  CAS  PubMed  Google Scholar 

  • Checroun C, Wehrly TD, Fischer ER, Hayes SF, Celli J (2006) Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc Natl Acad Sci USA 103:14578–14583

    Article  CAS  PubMed  Google Scholar 

  • Collazo CM, Yap GS, Sempowski GD, Lusby KC, Tessarollo L, Vande Woude GF, Sher A, Taylor GA (2001) Inactivation of LRG-47 and IRG-47 reveals a family of interferon γ-inducible genes with essential, pathogen-specific roles in resistance to infection. J Exp Med 194:181–187

    Article  CAS  PubMed  Google Scholar 

  • Collazo CM, Yap G, Hieny S, Caspar P, Feng CG, Taylor GA, Sher A (2002) The function of gamma interferon-inducible GTP-binding protein IGTP in host resistance to Toxoplasma gondii is Stat1 dependent and requires expression in both hematopoietic and nonhematopoietic cellular compartments. Infect Immun 70:6933–6939

    Article  CAS  PubMed  Google Scholar 

  • Coppens I, Dunn JD, Romano JD, Pypaert M, Zhang H, Boothroyd JC, Joiner KA (2006) Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125:261–274

    Article  CAS  PubMed  Google Scholar 

  • Deckert-Schluter M, Bluethmann H, Rang A, Hof H, Schluter D (1998) Crucial role of TNF receptor type 1 (p55), but not of TNF receptor type 2 (p75), in murine toxoplasmosis. J Immunol 160:3427–3436

    CAS  PubMed  Google Scholar 

  • Djavaheri-Mergny M, Amelotti M, Mathieu J, Besancon F, Bauvy C, Souquere S, Pierron G, Codogno P (2006) NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem 281:30373–30382

    Article  CAS  PubMed  Google Scholar 

  • Dunn WAJ (1994) Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends Cell Biol 110:1923–1933

    Google Scholar 

  • Durandy A, de Saint Basile G, Lisowska-Grospierre B, Gauchat JF, Forveille M, Kroczek RA, Bonnefoy JY, Fischer A (1995) Undetectable CD40 ligand expression on T cells and low B cell responses to CD40 binding agonists in human newborns. J Immunol 154:1560–1568

    CAS  PubMed  Google Scholar 

  • Gavrielescu LC, Butcher BA, del Rio L, Taylor GA, Denkers EY (2004) STAT1 is essential for antimicrobial effector function but dispensable for gamma interferon production during Toxoplasma gondii infection. Infect Immun 72:1257–1264

    Article  Google Scholar 

  • Gazzinelli RT, Hakim FT, Hieny S, Shearer GM, Sher A (1991) Synergistic role of CD4+ and CD8+ T lymphocytes in IFN-γ production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. J Immunol 146:286–292

    CAS  PubMed  Google Scholar 

  • Gazzinelli RT, Eltoum I, Wynn TA, Sher A (1993) Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-α and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation. J Immunol 151:3672–3681

    CAS  PubMed  Google Scholar 

  • Gazzinelli RT, Brezin A, Li Q, Nussenblatt RB, Chan CC (1994) Toxoplasma gondii: acquired ocular toxoplasmosis in the murine model, protective role of TNF-α and IFN-γ. Exp Parasitol 78:217–229

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MC, Deretic V (2004) Autophagy is defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119:753–766

    Article  CAS  PubMed  Google Scholar 

  • Hakansson S, Charron AJ, Sibley LD (2001) Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole. EMBO J 20:3132–3144

    Article  CAS  PubMed  Google Scholar 

  • Han P, McDonald T, Hodge G (2004) Potential immaturity of the T-cell and antigen-presenting cell interaction in cord blood with particular emphasis on the CD40-CD40 ligand costimulatory pathway. Immunology 113:26–34

    Article  CAS  PubMed  Google Scholar 

  • Hayashi S, Chan C-C, Gazzinelli RT, Pham NTH, Cheung MK, Roberge FG (1996a) Protective role of nitric oxide in ocular toxoplasmosis. Br J Ophthalmol 80:644–648

    Article  CAS  PubMed  Google Scholar 

  • Hayashi S, Chan CC, Gazzinelli R, Roberge FG (1996b) Contribution of nitric oxide to the host parasite equilibrium in toxoplasmosis. J Immunol 156:1476–1481

    CAS  PubMed  Google Scholar 

  • Ishida TK, Mizushima SI, Azuma S, Kobayashi N, Tojo T, Suzuki K, Aizawa S, Watanabe T, Mosialos G, Kieff E, Yamamoto T, Inoue J (1996) Identification of TRAF6, a novel tumor necrosis factor receptor-associated factor protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J Biol Chem 271:28745–28748

    Article  CAS  PubMed  Google Scholar 

  • Israelski DM, Remington JS (1993) Toxoplasmosis in the non-AIDS immunocompromised host. Curr Clin Top Infect Dis 13:322–356

    CAS  PubMed  Google Scholar 

  • Janssen R, van Wengen A, Verhard E, de Boer T, Zomerdijk T, Ottenhoff THM, van Dissel JT (2002) Divergent role for TNF-α in IFN-γ-induced killing of Toxoplasma gondii and Salmonella typhimurium contributes to selective susceptibility of patients with partial IFN-γ receptor 1 deficiency. J Immunol 169:3900–3907

    CAS  PubMed  Google Scholar 

  • Joiner KA, Fuhrman SA, Mietinnen H, Kasper LH, Mellman I (1990) Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor transfected fibroblasts. Science 249:641–646

    Article  CAS  PubMed  Google Scholar 

  • Joiner KA, Roos DS (2002) Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. J Cell Biol 157:557–563

    Article  CAS  PubMed  Google Scholar 

  • Julien P, Cron RQ, Dabbagh K, Cleary A, Chen L, Tran P, Stepick-Biek P, Lewis DB (2003) Decreased CD154 expression by neonatal CD4+ T cells is due to limitations in both proximal and distal events of T cell activation. Int Immunol 15:1461–1472

    Article  Google Scholar 

  • Kaur K, Chowdhury S, Greenspan NS, Schreiber JR (2007) Decreased expression of tumor necrosis factor family receptors involved in humoral immune responses in preterm neonates. Blood 110:2948–2954

    Article  CAS  PubMed  Google Scholar 

  • Kravetz JD, Federman DG (2005) Toxoplasmosis in pregnancy. Am J Med 118:212–216

    Article  PubMed  Google Scholar 

  • Kroncke KD, Fehsel K, Kolb-Bachofen V (1998) Inducible nitric oxide synthase in human disease. Clin Exp Immunol 113:147–156

    Article  CAS  PubMed  Google Scholar 

  • Leiva LE, Junprasert J, Hollenbaugh D, Sorensen RU (1998) Central nervous system toxoplasmosis with an increased proportion of circulating γδ T cells in a patient with hyper IgM syndrome. J Clin Immunol 18:283–290

    Article  CAS  PubMed  Google Scholar 

  • Levine B, Klionsky DJ (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6:463–477

    Article  CAS  PubMed  Google Scholar 

  • Lieberman LA, Banica M, Reiner SL, Hunter CA (2004) STAT1 plays a critical role in the regulation of antimicrobial effector mechanisms, but not in the development of Th1-type responses during toxoplasmosis. J Immunol 172:457–463

    CAS  PubMed  Google Scholar 

  • Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, Ferguson DJP, Yap G (2006) Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med 203:2063–2071

    Article  CAS  PubMed  Google Scholar 

  • Lingelbach K, Joiner KA (1998) The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci 111:1467–1475

    CAS  PubMed  Google Scholar 

  • Lu LF, Cook WJ, Lin LL, Noelle RJ (2003) CD40 signaling through a newly identified tumor necrosis factor receptor-associated factor 2 (TRAF2) binding site. J Biol Chem 278:45414–45418

    Article  CAS  PubMed  Google Scholar 

  • Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, Reichmann G, Howard JC (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathogens 1:187–201

    Article  CAS  Google Scholar 

  • Martin AM, Liu T, Lynn BC, Sinai AP (2007) The Toxoplasma gondii parasitophorous vacuole membrane: transactions across the border. J Eukaryot Microbiol 54:25–28

    Article  CAS  PubMed  Google Scholar 

  • McCannel CA, Holland GN, Helm CJ, et al (1996) Causes of uveitis in the general practice of ophthalmology. Am J Ophthalmol 121:35–46

    CAS  PubMed  Google Scholar 

  • Mizushima N, Ohsumi Y, Yoshimori T (2002) Autophagosome formation in mammalian cells. Cell Struct Funct 27:421–429

    Article  PubMed  Google Scholar 

  • Montoya JG, Kovacs JA, Remington JS (2005) Toxoplasma gondii. In: Mandell GL, Bennett JE, Dolin R (eds) Principles and practice of infectious diseases. Elsevier Churchill Livingstone, Philadelphia, pp 3170–3198

    Google Scholar 

  • Mordue DG, Sibley LD (1997) Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanisms of entry. J Immunol 159:4452–4459

    CAS  PubMed  Google Scholar 

  • Mukundan L, Bishop GA, Head KZ, Zhang L, Wahl L, Suttles J (2005) TNF receptor-associated factor 6 is an essential mediator of CD40-activated proinflammatory pathways in monocytes and macrophages. J Immunol 174:1081–1090

    CAS  PubMed  Google Scholar 

  • Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, Nara A, Funao J, Nakata M, Tsuda K, Hamada S, Yoshimori T (2004) Autophagy defends cells against invading Group A Streptococcus. Science 306:1037–1040

    Article  CAS  PubMed  Google Scholar 

  • Navia BA, Petito CK, Gold JW, Cho ES, Jordan BD, Price RW (1986) Cerebral toxoplasmosis complicating the acquired immune deficiency syndrome: clinical and neuropathological findings in 27 patients. Ann Neurol 19:224–238

    Article  CAS  PubMed  Google Scholar 

  • Nonoyama S, Penix LA, Edwards CP Lewis D, Ito S, Aruffo A, Wilson CB, Ochs HD (1995) Diminished expression of CD40 ligand by activated neonatal T cells. J Clin Invest 95:66–75

    Article  CAS  PubMed  Google Scholar 

  • Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C (2004) Escape of intracellular Shigella from autophagy. Science 307:727–731

    Article  PubMed  Google Scholar 

  • Orvedahl A, Alexander D, Talloczy Z, Sun Q, Wei Y, Zhang W, Burns D, Leib DA, Levine B (2007) HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1:23–35

    Article  CAS  PubMed  Google Scholar 

  • Pullen SS, Miller HG, Everdeen DS, Dang TT, Crute JJ, Kehry MR (1998) CD40-tumor necrosis factor receptor-associated factor (TRAF) interactions: regulation of CD40 signaling through multiple TRAF binding sites and TRAF hetero-oligomerization. Biochemistry 37:11836–11845

    Article  CAS  PubMed  Google Scholar 

  • Reichmann G, Walker W, Villegas EN, Craig L, Cai G, Alexander J, Hunter CA (2000) The CD40/CD40 ligand interaction is required for resistance to toxoplasmic encephalitis. Infect Immun 68:1312–1318

    Article  CAS  PubMed  Google Scholar 

  • Rich KA, Burkett C, Webster P (2003) Cytoplasmic bacteria can be targets for autophagy. Cell Microbiol 5:455–468

    Article  CAS  PubMed  Google Scholar 

  • Robben PM, LaRegina M, Kuziel WA, Sibley LD (2005) Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J Exp Med 201:1761–1769

    Article  CAS  PubMed  Google Scholar 

  • Roberts F, Roberts CW, Ferguson DJP, McLeod R (2000) Inhibition of nitric oxide production exacerbates chronic ocular toxoplasmosis. Parasite Immunol 22:1–5

    Article  CAS  PubMed  Google Scholar 

  • Scharton-Kersten T, Yap G, Magram J, Sher A (1997) Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J Exp Med 185:1261–1273

    Article  CAS  PubMed  Google Scholar 

  • Schluter D, Lohler J, Deckert M, Hof H, Schwendemann G (1991) Toxoplasma encephalitis of immunocompetent and nude mice: immunohistochemical characterisation of Toxoplasma antigen, infiltrates and major histocompatibility complex gene products. J Neuroimmunol 31:185–198

    Article  CAS  PubMed  Google Scholar 

  • Singh SB, Davis AS, Taylor GA, Deretic V (2006) Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313:1438–1441

    Article  CAS  PubMed  Google Scholar 

  • Subauste CS, Wessendarp M (2000) Human dendritic cells discriminate between viable and killed Toxoplasma gondii tachyzoites: Dendritic cell activation after infection with viable parasites results in CD28 and CD40 ligand signaling that controls IL-12-dependent and -independent T cell production of IFN-γ. J Immunol 165:1498–1505

    CAS  PubMed  Google Scholar 

  • Subauste CS, Wessendarp M (2006) CD40 restrains the in vivo growth of Toxoplasma gondii independently of gamma interferon. Infect Immun 74:1573–1579

    Article  CAS  PubMed  Google Scholar 

  • Subauste CS, Wessendarp M, Sorensen RU, Leiva L (1999) 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 which can be restored by soluble CD40L trimer. J Immunol 162:6690–6700

    CAS  PubMed  Google Scholar 

  • Subauste CS, Wessendarp M, Smulian AG, Frame PT (2001) Role of CD40 ligand signaling in defective type-1 cytokine response in HIV infection. J Infect Dis 183:1722–1731

    Article  CAS  PubMed  Google Scholar 

  • Subauste CS, Wessendarp M, Portillo J-AC, Andrade RM, Hinds LM, Gomez FJ, Smulian AG, Grubbs PA, Haglund LA (2004) Pathogen-specific induction of CD154 is impaired in CD4+ T cells from HIV-infected individuals. J Infect Dis 189:61–70

    Article  CAS  PubMed  Google Scholar 

  • Subauste CS, Andrade RM, Wessendarp M (2007a) CD40-TRAF6 and autophagy-dependent anti-microbial activity in macrophages. Autophagy 3:245–248

    CAS  PubMed  Google Scholar 

  • Subauste CS, Subauste A, Wessendarp M (2007b) Role of CD40-dependent down-regulation of CD154 in impaired induction of CD154 in CD4+ T cells from HIV-1-infected patients. J Immunol 178:1645–1653

    CAS  PubMed  Google Scholar 

  • Suzuki Y, Orellana MA, Schreiber RD, Remington JS (1988) Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science 240:516–518

    Article  CAS  PubMed  Google Scholar 

  • Suzuki Y, Conley FK, Remington JS (1989) Importance of endogenous IFN-γ for prevention of toxoplasmic encephalitis in mice. J Immunol 143:2045–2050

    CAS  PubMed  Google Scholar 

  • Talloczy Z, Jiang W, Virgin HW, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B (2002) Regulation of starvation- and virus-induced autophagy by the eIF2α signaling pathway. Proc Natl Acad Sci USA 99:190–195

    Article  CAS  PubMed  Google Scholar 

  • van Kooten C, Banchereau J (2000) CD40-CD40 ligand. J Leuk Biol 67:2–17

    CAS  Google Scholar 

  • Yano T, Mita S, Ohmori H, Oshima Y, Fujimoto Y, Ueda R, Takada H, Goldman WE, Fukase K, Silverman N, Yoshimori T, Kurata S (2008) Autophagic control of Listeria through intracellular innate immune recognition in Drosophila. Nat Immunol 9:908–916

    Article  CAS  PubMed  Google Scholar 

  • Yap GS, Scharton-Kersten T, Charest H, Sher A (1998) Decreased resistance of TNF receptor p55- and p75-deficient mice to chronic toxoplasmosis despite normal activation of inducible nitric oxide synthase in vivo. J Immunol 160:1340–1345

    CAS  PubMed  Google Scholar 

  • Zhang R, Fichtenbaum CJ, Hildeman DA, Lifson JD, Chougnet C (2004) CD40 ligand dysregulation in HIV: HIV glycoprotein 120 inhibits signaling cascades upstream of CD40 ligand transcription. J Immunol 172:2678–2686

    CAS  PubMed  Google Scholar 

  • Zhao Z, Fux B, Goodwin M, Dunay IR, Strong D, Miller BC, Cadwell K, Delgado MA, Ponpuak M, Green KG, Schmidt RE, Mizushima N, Deretic V, Sibley LD, Virgin HW (2008) Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4:458–469

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The original work by the author was supported by the National Institutes of Health, the American Heart Association (Ohio Valley Affiliate), the Juvenile Diabetes Research Foundation International, the Research to Prevent Blindness Foundation and the Ohio Lions Eye Research Foundation.

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Authors and Affiliations

  1. Department of Ophthalmology and Visual Sciences, Case Western Reserve University School of Medicine, Cleveland, OH, 44106, USA

    Carlos S. Subauste

  2. Department of Medicine, Division of Infectious Diseases and HIV Medicine, Case Western Reserve University School of Medicine, Cleveland, OH, 44106, USA

    Carlos S. Subauste

  3. Department of Pathology, Case Western Reserve University School of Medicine, Cleveland, OH, 44106, USA

    Carlos S. Subauste

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  1. Carlos S. Subauste
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Correspondence to Carlos S. Subauste .

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Editors and Affiliations

  1. Southwestern Medical Center, University of Texas, Harry Hines Blvd. 5323, Dallas, 75390-9113, U.S.A.

    Beth Levine

  2. Research Inst. Microbial Diseases, Osaka University, Yamadaoka 3-1, Suita, Osaka, 565-0871, Japan

    Tamotsu Yoshimori

  3. Health Sciences Center, University of New Mexico, Camino de Salud NE., 915, Albuquerque, 87131, U.S.A.

    Vojo Deretic

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Subauste, C.S. (2009). Autophagy in Immunity Against Toxoplasma gondii . In: Levine, B., Yoshimori, T., Deretic, V. (eds) Autophagy in Infection and Immunity. Current Topics in Microbiology and Immunology, vol 335. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00302-8_12

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