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Research Paper

Trypanosoma cruzi pathogenicity involves virulence factor expression and upregulation of bioenergetic and biosynthetic pathways

ORCID Icon, , , , , , , , , , , , , , , & ORCID Icon show all
Pages 1827-1848 | Received 02 Dec 2021, Accepted 01 Oct 2022, Published online: 25 Oct 2022

References

  • WHO. 2022. WHO. http://www.who.int/mediacentre/factsheets/fs340/es/
  • Zingales B. Trypanosoma cruzi genetic diversity: something new for something known about Chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Trop. 2018;184:38–52.
  • Atayde VD, Neira I, Cortez M, et al. Molecular basis of non-virulence of Trypanosoma cruzi clone CL-14. Int J Parasitol. 2004;34:851–860.
  • de Castro Neto AL, da Silveira JF, Mortara RA. Comparative analysis of virulence mechanisms of trypanosomatids pathogenic to humans. Front Cell Infect Microbiol. 2021;669079:11.
  • Osorio L, Ríos I, Gutiérrez B, et al. Virulence factors of Trypanosoma cruzi: who is who? Microbes Infect. 2012;14:1390–1402.
  • Yoshida N. Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An Acad Bras Cienc. 2006;78:87–111.
  • Miles MA, Toye PJ, Oswald SC, et al. The identification by isoenzyme patterns of two distinct strain-groups of Trypanosoma cruzi, circulating independently in a rural area of Brazil. Trans R Soc Trop Med Hyg. 1977;71:217–225.
  • Macedo AM, Machado CR, Oliveira RP, et al. Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of Chagas disease. Mem Inst Oswaldo Cruz. 2004;99:1–12.
  • Lima L, Espinosa-Álvarez O, Ortiz PA, et al. Genetic diversity of Trypanosoma cruzi in bats, and multilocus phylogenetic and phylogeographical analyses supporting Tcbat as an independent DTU (discrete typing unit). Acta Trop. 2015;151:166–177.
  • Henrique PM, Marques T, da Silva MV, et al. Correlation between the virulence of T. cruzi strains, complement regulatory protein expression levels, and the ability to elicit lytic antibody production. Exp Parasitol. 2016;170:66–72.
  • Revelli S, Gómez L, Wietzerbin J, et al. Levels of tumor necrosis factor alpha, gamma interferon, and interleukins 4, 6, and 10 as determined in mice infected with virulent or attenuated strains of Trypanosoma cruzi. Parasitol Res. 1999;85(2):147–150.
  • Mule SN, Costa-Martins AG, Rosa-Fernandes L, et al. PhyloQuant approach provides insights into Trypanosoma cruzi evolution using a systems-wide mass spectrometry-based quantitative protein profile. Commun Biol. 2021;4(1):324.
  • Postan M, Dvorak JA, McDaniel JP. Studies of Trypanosoma cruzi clones in inbred mice. I. A comparison of the course of infection C3H/HEN- mice with two clones isolated from a common source. Am J Trop Med Hyg. 1983;32(3):497–506.
  • Sales-Campos H, Kappel HB, Andrade CP, et al. Trypanosoma cruzi DTU TcII presents higher blood parasitism than DTU TcI in an experimental model of mixed infection. Acta Parasitol. 2015;60. DOI:10.1515/ap-2015-0060
  • Meza SKL, Kaneshima EN, de Oliveira Silva S, et al. Comparative pathogenicity in Swiss mice of Trypanosoma cruzi IV from northern Brazil and Trypanosoma cruzi II from southern Brazil. Exp Parasitol. 2014;146. DOI:10.1016/j.exppara.2014.08.014
  • Pan SC. Establishment of clones of Trypanosoma cruzi and their characterization in vitro and in vivo. Bull World Health Organ. 1982;60:101–107.
  • Luban NA, Dvorak JA. Trypanosoma cruzi: interaction with vertebrate cells in vitro. III. Selection for biological characteristics following intracellular passage. Exp Parasitol. 1974;36:143–149.
  • Camargo EP. Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid medium. Rev Soc Bras Med Trop. 1964;6:93–100.
  • Araya JE, Cornejo A, Orrego PR, et al. Calcineurin B of the human protozoan parasite Trypanosoma cruzi is involved in cell invasion. Microbes Infect. 2008;10(8):892–900.
  • Murthy VK, Dibbern KM, Campbell DA. PCR amplification of mini-exon genes differentiates Trypanosoma cruzi from Trypanosoma rangeli. Mol Cell Probes. 1992;6:237–243.
  • Thompson JD, Higgins DG, Gibson DJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids. 1994;22:4673–4680.
  • Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–1549.
  • Sreejit P, Kumar S, Verma RS. An improved protocol for primary culture of cardiomyocyte from neonatal mice. Vitr Cell Dev Biol - Anim. 2008;44:45–50.
  • Yoshida N. Surface antigens of metacyclic trypomastigotes of Trypanosoma cruzi. Infect Immun. 1983;40(2):836–839.
  • Brener Z. Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi 1962. Rev Inst Med Trop Sao Paulo. 1962;4:389–396.
  • Cummings KL, Tarleton RL. Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Mol Biochem Parasitol. 2003;129:53–59.
  • Caldas S, Santos FM, de Lana M, et al. Trypanosoma cruzi: acute and long-term infection in the vertebrate host can modify the response to benznidazole. Exp Parasitol. 2008;118(3):315–323.
  • Stordeur P, Poulin LF, Craciun L, et al. Cytokine mRNA quantification by real-time PCR. J Immunol Methods. 2002;259(1–2):55–64.
  • Moreno ML, Escobar J, Izquierdo-Álvarez A, et al. Disulfide stress: a novel type of oxidative stress in acute pancreatitis. Free Radic Biol Med. 2014;70:265–277.
  • Shevchenko A, Wilm M, Vorm O, et al. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem. 1996;68(5):850–858.
  • Alonso R, Pisa D, Marina AI, et al. Evidence for fungal infection in cerebrospinal fluid and brain tissue from patients with amyotrophic lateral sclerosis. Int J Biol Sci. 2015;11(5):546–558.
  • Tyanova S, Temu T, Cox J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 2016;11(12):2301–2319.
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Anal Biochem. 1976;72:248–254.
  • Campetella O, Martínez J, Cazzulo JJ. A major cysteine proteinase is developmentally regulated in Trypanosoma cruzi. FEMS Microbiol Lett. 1990;55(1–2):145–149.
  • Norris KA, Schrimpf JE, Szabo MJ. Identification of the gene family encoding the 160-kilodalton Trypanosoma cruzi complement regulatory protein. Infect Immun. 1997;65(2):349–357.
  • Schenkman S, Diaz C, Nussenzweig V. Attachment of Trypanosoma cruzi trypomastigotes to receptors at restricted cell surface domains. Exp Parasitol. 1991;72(1):76–86.
  • Schenkman S, Jiang MS, Hart GW, et al. A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell. 1991;65(7):1117–1125.
  • Manso Alves MJ, Abuin G, Kuwajima VY, et al. Partial inhibition of trypomastigote entry into cultured mammalian cells by monoclonal antibodies against a surface glycoprotein of Trypanosoma cruzi. Mol Biochem Parasitol. 1986;21:75–82.
  • Norris KA. Ligand-binding renders the 160 kDa Trypanosoma cruzi complement regulatory protein susceptible to proteolytic cleavage. Microb Pathog. 1996;21(4):235–248.
  • dos Cestari IS, Krarup A, Sim RB, et al. Role of early lectin pathway activation in the complement-mediated killing of Trypanosoma cruzi. Mol Immunol. 2009;47(2–3):426–437.
  • González J, Ramalho-Pinto FJ, Frevert U, et al. Proteasome activity is required for the stage-specific transformation of a protozoan parasite. J Exp Med. 1996;184(5):1909–1918.
  • Cazzulo JJ, Cazzulo Franke MC, Martínez J, et al. Some kinetic properties of a cysteine proteinase (cruzipain) from Trypanosoma cruzi. Biochim Biophys Acta (BBA)/Protein Struct Mol. 1990;1037:186–191.
  • Grellier P, Blum J, Santana J, et al. Involvement of calyculin A-sensitive phosphatase(s) in the differentiation of Trypanosoma cruzi trypomastigotes to amastigotes. Mol Biochem Parasitol. 1999;98:239–252.
  • Coura JR, Borges-Pereira J. Chagas disease: what is known and what should be improved: a systemic review. Rev Soc Bras Med Trop. 2012;45:286–296.
  • Borghesan TC, Ferreira RC, Takata CSA, et al. Molecular phylogenetic redefinition of Herpetomonas (Kinetoplastea, Trypanosomatidae), a genus of insect parasites associated with flies. Protist. 2013;164:129–152.
  • Franke de Cazzulo BM, Martínez J, North MJ, et al. Effects of proteinase inhibitors on the growth and differentiation of Trypanosoma cruzi. FEMS Microbiol Lett. 1994;124(1):81–86.
  • Tomas AM, Miles MA, Kelly JM. Overexpression of cruzipain, the major cysteine proteinase of Trypanosoma cruzi, is associated with enhanced metacyclogenesis. Eur J Biochem. 1997;244(2):596–603.
  • Brunoro GVF, Caminha MA, da Silva Ferreira AT, et al. Reevaluating the Trypanosoma cruzi proteomic map: the shotgun description of bloodstream trypomastigotes. J Proteomics. 2015;115:58–65.
  • Atwood JA, Weatherly DB, Minning TA, et al. The Trypanosoma cruzi proteome. Science. 2005;309:473–476.
  • de Castro Moreira dos Santos A, Kalume DE, Camargo R, et al. Unveiling the Trypanosoma cruzi nuclear proteome. PLoS One. 2015;10(9):e0138667.
  • Coutinho JVP, Rosa-Fernandes L, Mule SN, et al. The thermal proteome stability profile of Trypanosoma cruzi in epimastigote and trypomastigote life stages. J Proteomics. 2021;248:104339.
  • Magalhães RDM, Mattos EC, Rozanski A, et al. Global changes in nitration levels and DNA binding profile of Trypanosoma cruzi histones induced by incubation with host extracellular matrix. PLoS Negl Trop Dis. 2020;14(5):e0008262.
  • Avila CC, Almeida FG, Palmisano G. Direct identification of trypanosomatids by matrix-assisted laser desorption ionization–time of flight mass spectrometry (DIT MALDI-TOF MS). J Mass Spectrom. 2016;51(8):549–557.
  • Kikuchi SA, Sodré CL, Kalume DE, et al. Proteomic analysis of two Trypanosoma cruzi zymodeme 3 strains. Exp Parasitol. 2010;126(4):540–551.
  • Herreros-Cabello A, Callejas-Hernández F, Fresno M, et al. Comparative proteomic analysis of trypomastigotes from Trypanosoma cruzi strains with different pathogenicity. Infect Genet Evol. 2019;76:104041.
  • Ribeiro KS, Vasconcellos CI, Soares RP, et al. Proteomic analysis reveals different composition of extracellular vesicles released by two Trypanosoma cruzi strains associated with their distinct interaction with host cells. J Extracell Vesicles. 2018;7(1):1463779.
  • Tavares De Oliveira M, Taciana Santos Silva K, Xavier Neves L, et al. Differential expression of proteins in genetically distinct Trypanosoma cruzi samples (TcI and TcII DTUs) isolated from chronic Chagas disease cardiac patients. Parasites Vectors. 2018;11(1):611.
  • San Francisco J, Barría I, Gutiérrez B, et al. Decreased cruzipain and gp85/trans-sialidase family protein expression contributes to loss of Trypanosoma cruzi trypomastigote virulence. Microbes Infect. 2017;19(1):55–61.
  • Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev. 2001;81(1):153–208.
  • De Sá-Freire A, Nepomuceno-Silva JL, Da Paixão JC, et al. TcArf1: a Trypanosoma cruzi ADP-ribosylation factor. Parasitol Res. 2003;91(2):166–170.
  • Cuvillier A, Redon F, Antoine JC, et al. LdARL-3A, a Leishmania promastigote-specific ADP-ribosylation factor-like protein, is essential for flagellum integrity. J Cell Sci. 2000;113(Pt 11):2065–2074.
  • Kelly FD, Sanchez MA, Landfear SM. Touching the surface: diverse roles for the flagellar membrane in kinetoplastid parasites. Microbiol Mol Biol Rev. 2020;84(2):e00079–19.
  • Arias-Del-Angel JA, Santana-Solano J, Santillán M, et al. Motility patterns of Trypanosoma cruzi trypomastigotes correlate with the efficiency of parasite invasion in vitro. Sci Rep. 2020;10(1):15894.
  • Shiratsubaki IS, Fang X, Souza ROO, et al. Genome-scale metabolic models highlight stage-specific differences in essential metabolic pathways in Trypanosoma cruzi. PLoS Negl Trop Dis. 2020;14(10):e0008728.
  • 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(2):645–654.
  • Marchese L, Nascimento JDF, Damasceno FS, et al. The uptake and metabolism of amino acids, and their unique role in the biology of pathogenic trypanosomatids. Pathogens. 2018;7(2):36.
  • Martins RM, Covarrubias C, Rojas RG, et al. Use of L-proline and ATP production by Trypanosoma cruzi metacyclic forms as requirements for host cell invasion. Infect Immun. 2009;77(7):3023–3032.
  • Mantilla BS, Paes LS, Pral EMF, et al. Role of Δ1-pyrroline-5-carboxylate dehydrogenase supports mitochondrial metabolism and host-cell invasion of Trypanosoma cruzi. J Biol Chem. 2015;290(12):7767–7790.
  • Chang SL. Studies on hemoflagellates: iV. Observations concerning some biochemical activities in culture, and respiration of three species of Leishmanias and Trypanosoma Cruzi. J Infect Dis. 1948;82(2):109–118.
  • Ryley JF. Studies on the metabolism of the Protozoa. 7. Comparative carbohydrate metabolism of eleven species of trypanosome. Biochem J. 1956;62(2):215–222.
  • Cáceres O, Fernandes JF. Glucose metabolism, growth and differentiation of Trypanosoma cruzi. Rev Bras Biol. 1976;36(2):397–410.
  • Cazzulo JJ. Intermediate metabolism in Trypanosoma cruzi. J Bioenerg Biomembr. 1994;26(2):157–165.
  • Zhang Z, Tan M, Xie Z, et al. Identification of lysine succinylation as a new post-translational modification. Nat Chem Biol. 2011;7(1):58–63.
  • Colak G, Xie Z, Zhu AY, et al. Identification of lysine succinylation substrates and the succinylation regulatory enzyme CobB in Escherichia coli. Mol Cell Proteomics. 2013;12(12):3509–3520.
  • Fernández-Veledo S, Ceperuelo-Mallafré V, Vendrell J. Rethinking succinate: an unexpected hormone-like metabolite in energy homeostasis. Trends Endocrinol Metab. 2021;32(9):680–692.
  • Li X, Hu X, Wan Y, et al. Systematic identification of the lysine succinylation in the protozoan parasite Toxoplasma gondii. J Proteome Res. 2014;13(12):6087–6095.
  • Quiñones W, Acosta H, Gonçalves CS, et al. Structure, properties, and function of glycosomes in Trypanosoma cruzi. Front Cell Infect Microbiol. 2020;10:25.
  • Mattos EC, Canuto G, Manchola NC, et al. Reprogramming of Trypanosoma cruzi metabolism triggered by parasite interaction with the host cell extracellular matrix. PLoS Negl Trop Dis. 2019;13(2):e0007103.
  • Piras R, Piras MM, Henriquez D. The effect of inhibitors of macromolecular biosynthesis on the in vitro infectivity and morphology of Trypanosoma cruzi trypomastigotes. Mol Biochem Parasitol. 1982;6(2):83–92.
  • Piras MM, Piras R, Henriquez D. Changes in morphology and infectivity of cell culture-derived trypomastigotes of Trypanosoma cruzi. Mol Biochem Parasitol. 1982;6(2):67–81.
  • Lima MF, Kierszenbaum F. Biochemical requirements for intracellular invasion by Trypanosoma cruzi: protein synthesis. J Protozool. 1982;29(4):566–570.
  • Trocoli Torrecilhas AC, Tonelli RR, Pavanelli WR, et al. Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes Infect. 2009;11:29–39.
  • Garcia-Silva MR, Cabrera-Cabrera F, Cura Das Neves RF, et al. Gene expression changes induced by Trypanosoma cruzi shed microvesicles in mammalian host cells: relevance of tRNA-derived halves. Biomed Res Int. 2014;2014:305239.
  • 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(11):e0004216.
  • Moreira LR, Serrano FR, Osuna A. Extracellular vesicles of Trypanosoma cruzi tissue-culture cell-derived trypomastigotes: induction of physiological changes in non-parasitized culture cells. PLoS Negl Trop Dis. 2019;13(2):e0007163.
  • Zago MP, Hosakote YM, Koo SJ, et al. TcI isolates of Trypanosoma cruzi exploit the antioxidant network for enhanced intracellular survival in macrophages and virulence in mice. Infect Immun. 2016;84(6):1842–1856.
  • Uttaro AD. Acquisition and biosynthesis of saturated and unsaturated fatty acids by trypanosomatids. Mol Biochem Parasitol. 2014;196(1):61–70.
  • de Souza W, Rodrigues JCF. Sterol biosynthesis pathway as target for anti-trypanosomatid drugs. Interdiscip Perspect Infect Dis. 2009;2009:649502.
  • Linn TC, Pettit FH, Reed LJ. Alpha-keto acid dehydrogenase complexes. X. Regulation of the activity of the pyruvate dehydrogenase complex from beef kidney mitochondria by phosphorylation and dephosphorylation. Proc Natl Acad Sci, USA. 1969;62(1):234–241.
  • Reed LJ. A trail of research from lipoic acid to α-Keto acid dehydrogenase complexes. J Biol Chem. 2001;276(42):38329–38336.
  • Vacchina P, Lambruschi DA, Uttaro AD. Lipoic acid metabolism in Trypanosoma cruzi as putative target for chemotherapy. Exp Parasitol. 2018;186:17–23.
  • Walker DM, Oghumu S, Gupta G, et al. Mechanisms of cellular invasion by intracellular parasites. Cell Mol Life Sci. 2014;71(7):1245–1263.
  • Borst P, Sabatini R. Base J: discovery, biosynthesis, and possible functions. Annu Rev Microbiol. 2008;62:235–251.
  • Ekanayake DK, Minning T, Weatherly B, et al. Epigenetic regulation of transcription and virulence in Trypanosoma cruzi by O-linked thymine glucosylation of DNA. Mol Cell Biol. 2011;31:1690–1700.
  • Mesías AC, Garg NJ, Zago MP. Redox balance keepers and possible cell functions managed by redox homeostasis in Trypanosoma cruzi. Front Cell Infect Microbiol. 2019;9:435.
  • Piacenza L, Zago MP, Peluffo G, et al. Enzymes of the antioxidant network as novel determiners of Trypanosoma cruzi virulence. Int J Parasitol. 2009;39(13):1455–1464.
  • Irigoín F, Cibils L, Comini MA, et al. Insights into the redox biology of Trypanosoma cruzi: trypanothione metabolism and oxidant detoxification. Free Radic Biol Med. 2008;45:733–742.
  • Machado-Silva A, Cerqueira PG, Grazielle-Silva V, et al. How Trypanosoma cruzi deals with oxidative stress: antioxidant defence and DNA repair pathways. Mutat Res Rev Mutat Res. 2016;767:8–22.
  • Ismail SO, Paramchuk W, Skeiky YAW, et al. Molecular cloning and characterization of two iron superoxide dismutase cDnas from Trypanosoma cruzi. Mol Biochem Parasitol. 1997;86(2):187–197.
  • Piñeyro MD, Arcari T, Robello C, et al. Tryparedoxin peroxidases from Trypanosoma cruzi: high efficiency in the catalytic elimination of hydrogen peroxide and peroxynitrite. Arch Biochem Biophys. 2011;507(2):287–295.
  • Carnes J, Anupama A, Balmer O, et al. Genome and phylogenetic analyses of Trypanosoma evansi reveal extensive similarity to T. brucei and multiple independent origins for dyskinetoplasty. PLoS Negl Trop Dis. 2015;9(1):e3404.
  • Wilkinson SR, Obado SO, Mauricio IL, et al. Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum. Proc Natl Acad Sci, USA. 2002;99(21):13453–13458.
  • Lopez JA, Carvalho TU, De Souza W, et al. Evidence for a trypanothione-dependent peroxidase system in Trypanosoma cruzi. Free Radic Biol Med. 2000;28:767–772.
  • Arias DG, Marquez VE, Chiribao ML, et al. Redox metabolism in Trypanosoma cruzi: functional characterization of tryparedoxins revisited. Free Radic Biol Med. 2013;63:65–77.
  • Piñeyro MD, Parodi-Talice A, Arcari T, et al. Peroxiredoxins from Trypanosoma cruzi: virulence factors and drug targets for treatment of Chagas disease? Gene. 2008;408(1–2):45–50.
  • Ariyanayagam MR, Fairlamb AH. Ovothiol and trypanothione as antioxidants in trypanosomatids. Mol Biochem Parasitol. 2001;115(2):189–198.
  • Ariyanayagam MR, Oza SL, Mehlert A, et al. Bis(glutathionyl) spermine and other novel trypanothione analogues in Trypanosoma cruzi. J Biol Chem. 2003;278(30):27612–27619.
  • Lander N, Chiurillo MA, Bertolini MS, et al. Calcium-sensitive pyruvate dehydrogenase phosphatase is required for energy metabolism, growth, differentiation, and infectivity of Trypanosoma cruzi. J Biol Chem. 2018;293(45):17402–17417.
  • Negreiros RS, Lander N, Chiurillo MA, et al. Mitochondrial pyruvate carrier subunits are essential for pyruvate-driven respiration, infectivity, and intracellular replication of Trypanosoma cruzi. MBio. 2021;12(2). e00540-21. DOI:10.1128/mBio.00540-21.
  • Macedo CM, Saraiva FMDS, Paula JIO, et al. The potent trypanocidal effect of LQB303, a novel Redox-Active Phenyl-Tert-Butyl-Nitrone derivate that causes mitochondrial collapse in Trypanosoma cruzi. Front Microbiol. 2021;12:617564.
  • Barros-Alvarez X, Gualdron-Lopez M, Acosta H, et al. Glycosomal targets for anti-trypanosomatid drug discovery. Curr Med Chem. 2014;21(15):1679–1706.
  • de Pádua RAP, Kia AM, Costa-Filho AJ, et al. Characterisation of the fumarate hydratase repertoire in Trypanosoma cruzi. Int J Biol Macromol. 2017;102:42–51.
  • Hashem Y, Des Georges A, Fu J, et al. High-resolution cryo-electron microscopy structure of the Trypanosoma brucei ribosome. Nature. 2013;494(7437):385–389.
  • Vicens Q, Bochler A, Jobe A, et al. Interaction networks of ribosomal expansion segments in kinetoplastids. Subcell Biochem. 2021;96:433–450.
  • Bochler A, Querido JB, Prilepskaja T, et al. Structural differences in translation initiation between pathogenic trypanosomatids and their mammalian hosts. Cell Rep. 2020;33(12):108534.
  • Dc-Rubin SSC, Schenkman S. Trypanosoma cruzi trans-sialidase as a multifunctional enzyme in Chagas’ disease. Cell Microbiol. 2012;14:1522–1530.
  • Schauer R, Kamerling JP. The chemistry and biology of trypanosomal Trans-Sialidases: virulence factors in Chagas disease and sleeping sickness. Chembiochem. 2011;12(15):2246–2264.
  • Campetella O, Buscaglia CA, Mucci J, et al. Parasite-host glycan interactions during Trypanosoma cruzi infection: Trans-Sialidase rides the show. Biochim Biophys Acta - Mol Basis Dis. 2020;1866(5):165692.
  • Giorgi ME, de Lederkremer RM. The glycan structure of T. cruzi mucins depends on the host. Insights on the chameleonic galactose. Molecules. 2020;25(17):3913.
  • Norris KA, Bradt B, Cooper NR, et al. Characterization of a Trypanosoma cruzi C3 binding protein with functional and genetic similarities to the human complement regulatory protein, decay-accelerating factor. J Immunol. 1991;147(7):2240–2247.
  • Arroyo-Olarte RD, Martínez I, Cruz-Rivera M, et al. Complement system contributes to modulate the infectivity of susceptible TcI strains of Trypanosoma cruzi. Mem Inst Oswaldo Cruz. 2018;113(4):e170332.
  • Cestari I, Ramirez MI. Inefficient complement system clearance of Trypanosoma cruzi metacyclic trypomastigotes enables resistant strains to invade eukaryotic cells. PLoS One. 2010;5(3):e9721.
  • Tonelli RR, Giordano RJ, Barbu EM, et al. Role of the gp85/trans-Sialidases in Trypanosoma cruzi tissue tropism: preferential binding of a conserved peptide motif to the vasculature In vivo. PLoS Negl Trop Dis. 2010;4(11):e864.
  • Muñoz-San Martín C, Zulantay I, Saavedra M, et al. Discrete typing units of Trypanosoma cruzi detected by real-time PCR in Chilean patients with chronic Chagas cardiomyopathy. Acta Trop. 2018;185:280–284.
  • Calvopina M, Segovia G, Cevallos W, et al. Fatal acute Chagas disease by Trypanosoma cruzi DTU TcI, Ecuador. BMC Infect Dis. 2020;20(1):143.
  • Burgos JM, Diez M, Vigliano C, et al. Molecular identification of Trypanosoma cruzi discrete typing units in end-stage chronic Chagas heart disease and reactivation after heart transplantation. Clin Infect Dis. 2010;51:485–495.
  • Zafra G, Mantilla JC, Jácome J, et al. Direct analysis of genetic variability in Trypanosoma cruzi populations from tissues of Colombian chagasic patients. Hum Pathol. 2011;42:1159–1168.
  • Ramírez JD, Guhl F, Rendón LM, et al. Chagas cardiomyopathy manifestations and Trypanosoma cruzi genotypes circulating in chronic chagasic patients. PLoS Negl Trop Dis. 2010;4(11):e899.