4,535
Views
25
CrossRef citations to date
0
Altmetric
Special Focus on Autophagy in host-pathogen interactions

Autophagy: A necessary process during the Trypanosoma cruzi life-cycle

& ORCID Icon
Pages 460-469 | Received 01 Aug 2018, Accepted 24 Oct 2018, Published online: 29 Nov 2018

References

  • Simpson AGB, Stevens JR, Lukeš J. The evolution and diversity of kinetoplastid flagellates. Trends Parasitol. 2006;22:168–174.
  • Duszenko M, Ginger ML, Brennand A, et al. Autophagy in protists. Autophagy. 2011;7:127–158.
  • Schenkman S, Robbins ES, Nussenzweig V. Attachment of Trypanosoma cruzi to mammalian cells requires parasite energy, and invasion can be independent of the target cell cytoskeleton. Infect Immun. 1991;59:645–654.
  • Fernandes MC, Flannery AR, Andrews N, et al. Extracellular amastigotes of Trypanosoma cruzi are potent inducers of phagocytosis in mammalian cells. Cell Microbiol. 2013;15:977–991.
  • Bonfim-Melo A, Ferreira ÉR, Mortara RA. Rac1/WAVE2 and Cdc42/N-WASP participation in actin-dependent host cell invasion by extracellular amastigotes of Trypanosoma cruzi. Front Microbiol. 2018;9:360.
  • Maeda FY, Cortez C, Yoshida N. Cell signaling during Trypanosoma cruzi invasion. Front Immunol. 2012;3:361.
  • Yoshida N. Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An Acad Bras Cienc. 2006;78:87–111.
  • Magdesian MH, Giordano R, Ulrich H, et al. Infection by Trypanosoma cruzi. Identification of a parasite ligand and its host cell receptor. J Biol Chem. 2001;276:19382–19389.
  • Martins NO, de Souza RT, Cordero EM, et al. Molecular characterization of a novel family of Trypanosoma cruzi Surface Membrane Proteins (TcSMP) involved in mammalian host cell invasion. PLoS Negl Trop Dis. 2015;9:e0004216.
  • de Souza W, de Carvalho TMU, Barrias ES. Review on Trypanosoma cruzi: host cell interaction. Int J Cell Biol. 2010;2010:1–18.
  • de Araujo-Jorge TC, Barbosa HS, Meirelles MNL, et al. Trypanosoma cruzi recognition by macrophages and muscle cells: perspectives after a 15-year study. Mem Inst Oswaldo Cruz. 1992;87:43–56.
  • Tardieux I, Nathanson MH, Andrews NW. Role in host cell invasion of Trypanosoma cruzi-induced cytosolic-free Ca2+ transients. J Exp Med. 1994;179:1017–1022.
  • Tardieux I, Webster P, Ravesloot J, et al. Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell. 1992;71:1117–1130.
  • Rodríguez A, Samoff E, Rioult MG, et al. Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J Cell Biol. 1996;134:349–362.
  • Hissa B, de Oliveira Andrade L. Trypasonoma cruzi uses a specific subset of host cell lysosomes for cell invasion. Parasitol Int. 2015;64:135–138.
  • Romano PS, Arboit MA, Vázquez CL, et al. The autophagic pathway is a key component in the lysosomal dependent entry of Trypanosoma cruzi into the host cell. Autophagy. 2009;5:6–18.
  • Woolsey AM, Sunwoo L, Petersen CA, et al. Novel PI 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation. J Cell Sci. 2003;116:3611–3622.
  • Wilkowsky SE, Barbieri MA, Stahl PD, et al. Regulation of Trypanosoma cruzi invasion of nonphagocytic cells by the endocytically active GTPases dynamin, Rab5, and Rab7. Biochem Biophys Res Commun. 2002;291:516–521.
  • Barrias ES, Reignault LC, De Souza W, et al. Dynasore, a dynamin inhibitor, inhibits Trypanosoma cruzi entry into peritoneal macrophages. PLoS One. 2010;5:e7764.
  • Tam C, Idone V, Devlin C, et al. Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. J Cell Biol. 2010;189:1027–1038.
  • Fernandes MC, Cortez M, Flannery AR, et al. Trypanosoma cruzi subverts the sphingomyelinase-mediated plasma membrane repair pathway for cell invasion. J Exp Med. 2011;208:909–921.
  • Cortez C, Real F, Yoshida N. Lysosome biogenesis/scattering increases host cell susceptibility to invasion by Trypanosoma cruzi metacyclic forms and resistance to tissue culture trypomastigotes. Cell Microbiol. 2016;18:748–760.
  • Barrias ES, de Carvalho TMU, De Souza W. Trypanosoma cruzi: entry into mammalian host cells and parasitophorous vacuole formation. Front Immunol. 2013;4:186.
  • Andrade LO, Andrews NW. Lysosomal fusion is essential for the retention of Trypanosoma cruzi inside host cells. J Exp Med. 2004;200:1135–1143.
  • Andrade LO, Andrews NW. The Trypanosoma cruzi–host-cell interplay: location, invasion, retention. Nat Rev Microbiol. 2005;3:819–823.
  • Fernandes MC, Andrews NW. Host cell invasion by Trypanosoma cruzi : a unique strategy that promotes persistence. FEMS Microbiol Rev. 2012;36:734–747.
  • Cueto JA, Vanrell MC, Salassa BN, et al. Soluble N-ethylmaleimide-sensitive factor attachment protein receptors required during Trypanosoma cruzi parasitophorous vacuole development. Cell Microbiol. 2017;19:e12713.
  • Nakatogawa H, Suzuki K, Kamada Y, et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–467.
  • Yang Z, Huang J, Geng J, et al. Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. Mol Biol Cell. 2006;17:5094–5104.
  • Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3–12.
  • Axe EL, Walker SA, Manifava M, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol. 2008;182:685–701.
  • Simonsen A, Tooze SA. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol. 2009;186:773–782.
  • Hayashi-Nishino M, Fujita N, Noda T, et al. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol. 2009;11:1433–1437.
  • Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280–293.
  • Baba M, Takeshige K, Baba N, et al. Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J Cell Biol. 1994;124:903–913.
  • Yang Z, Klionsky DJ. Permeases recycle amino acids resulting from autophagy. Autophagy. 2007;3:149–150.
  • Itakura E, Kishi C, Inoue K, et al. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell. 2008;19:5360–5372.
  • Mizushima N, Kuma A, Kobayashi Y, et al. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci. 2003;116:1679–1688.
  • Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000;19:5720–5728.
  • Tanida I, Ueno T, Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol. 2004;36:2503–2518.
  • Yamamoto A, Tagawa Y, Yoshimori T, et al. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct. 1998;23:33–42.
  • Cheong H, Yorimitsu T, Reggiori F, et al. Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell. 2005;16:3438–3453.
  • Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem. 1998;273:3963–3966.
  • Blommaart EF, Krause U, Schellens JP, et al. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem. 1997;243:240–246.
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2016;12:1–222.
  • Bauckman KA, Owusu-Boaitey N, Mysorekar IU. Selective autophagy: xenophagy. Methods. 2015;75:120–127.
  • Pareja MEM, Colombo MI. Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms. Front Cell Infect Microbiol. 2013;3:54.
  • Gutierrez MG, Munafó DB, Berón W, et al. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci. 2004;117:2687–2697.
  • Nakagawa I, Amano A, Mizushima N, et al. Autophagy defends cells against invading group A Streptococcus. Science. 2004;306:1037–1040.
  • Heckmann BL, Boada-Romero E, Cunha LD, et al. LC3-associated phagocytosis and inflammation. J Mol Biol. 2017;429:3561–3576.
  • Lai S, Devenish RJ. LC3-associated phagocytosis (LAP): connections with host autophagy. Cells. 2012;1:396–408.
  • Veiga-Santos P, Desoti VC, Miranda N, et al. The natural compounds piperovatine and piperlonguminine induce autophagic cell death on Trypanosoma cruzi. Acta Trop. 2013;125:349–356.
  • Fernandes MC, Da Silva EN, Pinto AV, et al. A novel triazolic naphthofuranquinone induces autophagy in reservosomes and impairment of mitosis in Trypanosoma cruzi. Parasitology. 2012;139:26–36.
  • Dos Anjos DO, Sobral Alves ES, Gonçalves VT, et al. Effects of a novel β-lapachone derivative on Trypanosoma cruzi: parasite death involving apoptosis, autophagy and necrosis. Int J Parasitol Drugs Drug Resist. 2016;6:207–219.
  • Lazarin-Bidóia D, Desoti VC, Martins SC, et al. Dibenzylideneacetones are potent trypanocidal compounds that affect the Trypanosoma cruzi redox system. Antimicrob Agents Chemother. 2016;60:890–903.
  • Braga MV, Magaraci F, Lorente SO, et al. Effects of inhibitors of Delta24(25)-sterol methyl transferase on the ultrastructure of epimastigotes of Trypanosoma cruzi. Microsc Microanal. 2005;11:506–515.
  • Santa-Rita RM, Lira R, Barbosa HS, et al. Anti-proliferative synergy of lysophospholipid analogues and ketoconazole against Trypanosoma cruzi (Kinetoplastida: trypanosomatidae): cellular and ultrastructural analysis. J Antimicrob Chemother. 2005;55:780–784.
  • Michels PAM, Bringaud F, Herman M, et al. Metabolic functions of glycosomes in trypanosomatids. Biochim Biophys Acta. 2006;1763:1463–1477.
  • Herman M, Gillies S, Michels PA, et al. Autophagy and related processes in trypanosomatids: insights from genomic and bioinformatic analyses. Autophagy. 2006;2:107–118.
  • Alvarez VE, Kosec G, Sant’Anna C, et al. Autophagy is involved in nutritional stress response and differentiation in Trypanosoma cruzi. J Biol Chem. 2008;283:3454–3464.
  • Vanrell MC, Losinno AD, Cueto JA, et al. The regulation of autophagy differentially affects Trypanosoma cruzi metacyclogenesis. PLoS Negl Trop Dis. 2017;11:e0006049.
  • Eisenberg T, Knauer H, Schauer A, et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol. 2009;11:1305–1314.
  • Schoijet AC, Sternlieb T, Alonso GD. The phosphatidylinositol 3-kinase class III complex containing TcVps15 and TcVps34 participates in autophagy in Trypanosoma cruzi. J Eukaryot Microbiol. 2017;64:308–321.
  • Li F-J, He CY. Acidocalcisome is required for autophagy in Trypanosoma brucei. Autophagy. 2014;10:1978–1988.
  • Dorn BR, Dunn WA, Progulske-Fox A. Bacterial interactions with the autophagic pathway. Cell Microbiol. 2002;4:1–10.
  • Berón W, Gutierrez MG, Rabinovitch M, et al. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun. 2002;70:5816–5821.
  • Amer AO, Swanson MS. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol. 2005;7:765–778.
  • Gutierrez MG, Vázquez CL, Munafó DB, et al. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol. 2005;7:981–993.
  • Romano PS, Gutierrez MG, Berón W, et al. The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell Microbiol. 2007;9:891–909.
  • Vanrell MC, Cueto JA, Barclay JJ, et al. Polyamine depletion inhibits the autophagic response modulating Trypanosoma cruzi infectivity. Autophagy. 2013;9:1080–1093.
  • Romano PS, Cueto JA, Casassa AF, et al. Molecular and cellular mechanisms involved in the Trypanosoma cruzi/host cell interplay. IUBMB Life. 2012;64:387–396.
  • Martins RM, Alves RM, Macedo S, et al. Starvation and rapamycin differentially regulate host cell lysosome exocytosis and invasion by Trypanosoma cruzi metacyclic forms. Cell Microbiol. 2011;13:943–954.
  • Owen KA, Casanova JE. Salmonella manipulates autophagy to “serve and protect.” Cell Host Microbe. 2015;18:517–519.
  • Onizuka Y, Takahashi C, Uematsu A, et al. Inhibition of autolysosome formation in host autophagy by Trypanosoma cruzi infection. Acta Trop. 2017;170:57–62.
  • Krieger V, Liebl D, Zhang Y, et al. Reorganization of the endosomal system in Salmonella-infected cells: the ultrastructure of Salmonella-induced tubular compartments. PLoS Pathog. 2014;10:e1004374.
  • López de Armentia MM, Gauron MC, Colombo MI. Staphylococcus aureus alpha-toxin induces the formation of dynamic tubules labeled with LC3 within host cells in a Rab7 and Rab1b-dependent manner. Front Cell Infect Microbiol. 2017;7:431.
  • Castillo EF, Dekonenko A, Arko-Mensah J, et al. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc Natl Acad Sci. 2012;109:E3168–E3176.
  • Cooper AM, Dalton DK, Stewart TA, et al. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med. 1993;178:2243–2247.
  • Knop J. Immunologic effects of interferon. J Invest Dermatol. 1990;95:72S–74S.
  • Gutierrez MG, Master SS, Singh SB, et al. Autophagy is a defense mechanism inhibiting BCG and mycobacterium tuberculosis survival in infected macrophages. Cell. 2004;119:753–766.
  • Deretic V, Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe. 2009;5:527–549.