Skip to main content
SpringerLink
Log in

Trypanosoma cruzi Journey from the Insect Vector to the Host Cell

  • Chapter
  • First Online:
Chagas Disease

Part of the book series: Birkhäuser Advances in Infectious Diseases ((BAID))

Abstract

Trypanosoma cruzi, etiological agent of Chagas disease, has evolved a complex interaction with mammalian cells and insect vector’s intestine. During its journey between these environments, it is subject to stressful changes. To overcome them, parasites use numerous strategies. Different stages contact diverse compartments of hosts and vectors thus assuring survival and multiplication. Surface proteins, some identified in particular stages of the protozoan, are critical for interaction with the milieu although their relevance is not totally understood for many. Parasite molecules allow T. cruzi to progress in the vector intestine, to duplicate and differentiate in order to become the infective stage for mammals. Surface molecules also allow parasites to advance through intracellular matrix of the mammals to reach the cells and, after recognition, invade them and adapt to survive but also to multiply and differentiate to circulating trypomastigotes thus assuring life cycle continuity. In this chapter we summarize T. cruzi pathways of humans and other reservoirs of infection as well as the participation of different T. cruzi lineages in geographical distribution and human disease. Finally, we review some of the mechanisms used by the parasite to reach, enter, and survive inside the host cell described so far.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Kollien AH, Schaub GA. The development of Trypanosoma cruzi in Triatominae. Parasitol Today. 2000;16(9):381–7.

    Article  CAS  PubMed  Google Scholar 

  2. Garcia ES, Genta FA, de Azambuja P, Schaub GA. Interactions between intestinal compounds of triatomines and T. cruzi. Trends Parasitol. 2010a;26(10):499–505.

    Article  CAS  PubMed  Google Scholar 

  3. Ferguson MA. The estructure, biosintesis and functions of glycosylphospatidyilinositol anchors, and the contributions of trypanosome research. J Cell Sci. 1999;112:2799–809.

    CAS  PubMed  Google Scholar 

  4. Opperdoes RF, Michels PA. The glicosome of the kinetoplastida. Biochimie. 1993;75(3-4):231–4.

    Article  CAS  PubMed  Google Scholar 

  5. Docampo R, Moreno SN. Acidocalcisome: a novel Ca2+ storage compartment in trypanosomatids and apiocomplexan parasites. Parasitol Today. 1999;15(11):443–8.

    Article  CAS  PubMed  Google Scholar 

  6. Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN. Acidocalcisomes – conserved from bacteria to man. Nat Rev Microbiol. 2005;3(3):251–61.

    Article  CAS  PubMed  Google Scholar 

  7. Hoare C. The trypanosomes of mammals. Oxford, England: Blackwell Scientific Publications; 1972. p. 60. Chapter 5.

    Google Scholar 

  8. Chagas C. Nova tripanozomiase humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Mem Inst Oswaldo Cruz. 1909;1:159–218. Cited in Cruz RE, Macedo AM, Barnabe C, Freitas JM, Chiari E, Veloso CM, et al. Further genetic characterization of the two Trypanosoma cruzi Berenice strains (Be-62 and Be-78) isolated from the first human case of Chagas disease (Chagas, 1909) Acta Trop. 2006; 97: 239–46.

    Article  Google Scholar 

  9. Bertelli M, Brener Z. Infection of Tissue Culture Cells with Bloodstream Trypomastigotes of Trypanosoma cruzi. J Parasitol. 1981;66(6):992–7.

    Article  Google Scholar 

  10. Brener Z. The behavior of slender and stout forms of Trypanosoma cruzi in the blood-stream of normal and immune mice. Ann Trop Med Parasitol. 1969;63(2):215–20.

    Article  CAS  PubMed  Google Scholar 

  11. Schmatz DM, Boltz RC, Murray PK. Trypanosoma cruzi: separation of broad and slender trypomastigotes using a continuous hypaque gradient. Parasitology. 1983;87(Pt 2):219–27.

    Article  PubMed  Google Scholar 

  12. Borges MM, De Andrade SG, Pilatti CG, do Prado Júnior JC, Kloetzel JK. Macrophage activation and histopathological findings in Calomys callosus and Swiss mice infected with several strains of Trypanosoma cruzi. Mem Inst Oswaldo Cruz. 1992;87(4):493–502.

    Article  CAS  PubMed  Google Scholar 

  13. Risso MG, Garbarino GB, Mocetti E, Campetella O, Gonzalez Cappa SM, Buscaglia CA, et al. Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages. J Infect Dis. 2004;189(12):2250–9.

    Article  CAS  PubMed  Google Scholar 

  14. Botero LA, Mejía AM, Triana O. Caracterización biológica y genética de dos clones pertenecientes a los grupos I y II de Trypanosoma cruzi de Colombia. Biomedica. 2007;27(Suppl 1):64–74.

    Article  PubMed  Google Scholar 

  15. Melo RC, Brener Z. Tissue tropism of different Trypanosoma cruzi strains. J Parasitol. 1978;64(3):475–82.

    Article  CAS  PubMed  Google Scholar 

  16. Alba Soto CD, Mirkin GA, Solana ME, González Cappa SM. Trypanosoma cruzi infection modulates in vivo expression of major histocompatibility complex class II molecules on antigen-presenting cells and T-cell stimulatory activity of dendritic cells in a strain-dependent manner. Infect Immun. 2003;71(3):1194–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Mirkin GA, Celentano AM, Malchiodi EL, Jones M, González Cappa SM. Different Trypanosoma cruzi strains promote neuromyopathic damage mediated by distinct T lymphocyte subsets. Clin Exp Immunol. 1997;107(2):328–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mirkin GA, Jones M, Sanz OP, Rey R, Sica RE, González Cappa SM. Experimental Chagas’ disease: electrophysiology and cell composition of the neuromyopathic inflammatory lesions in mice infected with a myotropic and a pantropic strain of Trypanosoma cruzi. Clin Immunol Immunopathol. 1994;73(1):69–79.

    Article  CAS  PubMed  Google Scholar 

  19. Andrade SG. The influence of the strain of Trypanosoma cruzi in placental infections in mice. Trans R Soc Trop Med Hyg. 1982;76(1):123–8.

    Article  CAS  PubMed  Google Scholar 

  20. Solana ME, Celentano AM, Tekiel V, Jones M, González Cappa SM. Trypanosoma cruzi: effect of parasite subpopulation on murine pregnancy outcome. J Parasitol. 2002;88(1):102–6.

    Article  PubMed  Google Scholar 

  21. Andrade SG. Caracterizaçao de cepas de Trypanosoma cruzi isoladas no Recôncavo Baiano. Rev Patol Trop. 1974;3:65–121.

    Google Scholar 

  22. Andrade SG. Influence of Trypanosoma cruzi strain on the pathogenesis of chronic myocardiopathy in mice. Mem Inst Oswaldo Cruz. 1990;85(1):17–27.

    Article  CAS  PubMed  Google Scholar 

  23. Miles MA, Toye PJ, Oswald SC, Godfrey DG. 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(3):217–25.

    Article  CAS  PubMed  Google Scholar 

  24. Morel C, Chiari E, Camargo EP, Mattei DM, Romanha AJ, Simpson L. Strains and clones of Trypanosoma cruzi can be characterized by pattern of restriction endonuclease products of kinetoplast DNA minicircles. Proc Natl Acad Sci U S A. 1980;77(11):6810–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Souto RP, Fernandes O, Macedo AM, Campbell DA, Zingales B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol. 1996;83(2):141–52.

    Article  CAS  PubMed  Google Scholar 

  26. Zingales B, Andrade SG, Briones MR, Campbell DA, Chiari E, Fernandes O, et al. Second Satellite Meeting. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz. 2009;104(7):1051–4.

    Article  CAS  PubMed  Google Scholar 

  27. Tibayrenc M. Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int J Parasitol. 1998;28(1):85–104.

    Article  CAS  PubMed  Google Scholar 

  28. Zingales B. Trypanosoma cruzi genetic diversity: something new for something known about Chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Trop. 2018;184:38. https://doi.org/10.1016/j.actatropica.2017.09.017. Review. pii: S0001-706X(17)30426-6.

    Article  CAS  PubMed  Google Scholar 

  29. Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM, Teixeira MM, et al. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect Genet Evol. 2012;12(2):240–53.

    Article  PubMed  Google Scholar 

  30. Hernández C, Cucunubá Z, Flórez C, Olivera M, Valencia C, Zambrano P, et al. Molecular diagnosis of Chagas disease in colombia: parasitic loads and discrete typing units in patients from acute and chronic phases. PLoS Negl Trop Dis. 2016;10(9):e0004997.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Ramírez JD, Guhl F, Rendón LM, Rosas F, Marin-Neto JA, Morillo CA. Chagas cardiomyopathy manifestations and Trypanosoma cruzi genotypes circulating in chronic Chagasic patients. PLoS Negl Trop Dis. 2010;4(11):e899.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Brenière SF, Waleckx E, Barnabé C. Over six thousand Trypanosoma cruzi strains classified into discrete typing units (DTUs): attempt at an inventory. PLoS Negl Trop Dis. 2016;10(8):e0004792.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Cardinal MV, Lauricella MA, Ceballos LA, Lanati L, Marcet PL, Levin MJ, et al. Molecular epidemiology of domestic and sylvatic Trypanosoma cruzi infection in rural northwestern Argentina. Int J Parasitol. 2008;38(13):1533–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Acosta N, López E, Lewis MD, Llewellyn MS, Gómez A, Román F, et al. Hosts and vectors of Trypanosoma cruzi discrete typing units in the Chagas disease endemic region of the Paraguayan Chaco. Parasitology. 2017;144(7):884–98.

    Article  PubMed  Google Scholar 

  35. Marcili A, Lima L, Valente VC, Valente SA, Batista JS, Junqueira AC, et al. Comparative phylogeography of Trypanosoma cruzi TCIIc: new hosts, association with terrestrial ecotopes, and spatial clustering. Infect Genet Evol. 2009;9(6):1265–74.

    Article  PubMed  Google Scholar 

  36. Monteiro WM, Magalhães LK, de Sá AR, Gomes ML, Toledo MJ, Borges L, et al. Trypanosoma cruzi IV causing outbreaks of acute Chagas disease and infections by different haplotypes in the Western Brazilian Amazonia. PLoS One. 2012;7(7):e41284. https://doi.org/10.1371/journal.pone.0041284.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Diosque P, Barnabé C, Padilla AM, Marco JD, Cardozo RM, Cimino RO, et al. Multilocus enzyme electrophoresis analysis of Trypanosoma cruzi isolates from a geographically restricted endemic area for Chagas’ disease in Argentina. Int J Parasitol. 2003;33(10):997–1003.

    Article  CAS  PubMed  Google Scholar 

  38. Fernández MP, Cecere MC, Lanati LA, Lauricella MA, Schijman AG, Gürtler RE, et al. Geographic variation of Trypanosoma cruzi discrete typing units from Triatoma infestans at different spatial scales. Acta Trop. 2014;140:10–8.

    Article  Google Scholar 

  39. Maffey L, Cardinal MV, Ordóñez-Krasnowski PC, Lanati LA, Lauricella MA, Schijman AG, et al. Direct molecular identification of Trypanosoma cruzi discrete typing units in domestic and peridomestic Triatoma infestans and Triatoma sordida from the Argentine Chaco. Parasitology. 2012;139(12):1570–9.

    Article  CAS  PubMed  Google Scholar 

  40. Guhl F, Ramírez JD. Retrospective molecular integrated epidemiology of Chagas disease in Colombia. Infect Genet Evol. 2013;20:148–54.

    Article  PubMed  Google Scholar 

  41. Cura CI, Lucero RH, Bisio M, Oshiro E, Formichelli LB, Burgos JM, et al. Trypanosoma cruzi discrete typing units in Chagas disease patients from endemic and non-endemic regions of Argentina. Parasitology. 2012;139(4):516–21.

    Article  CAS  PubMed  Google Scholar 

  42. Duz AL, Vieira PM, Roatt BM, Aguiar-Soares RD, Cardoso JM, Oliveira FC, et al. The TcI and TcII Trypanosoma cruzi experimental infections induce distinct immunoresponses and cardiac fibrosis in dogs. Mem Inst Oswaldo Cruz. 2014;109(8):1005–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Marin-Neto JA, Cunha-Neto E, Maciel BC, Simões MV. Pathogenesis of chronic Chagas heart disease. Circulation. 2007;115:1109–23.

    Article  PubMed  Google Scholar 

  44. Burgos JM, Begher S, Silva HM, Bisio M, Duffy T, Levin MJ, et al. Molecular identification of Trypanosoma cruzi I tropism for central nervous system in Chagas reactivation due to AIDS. Am J Trop Med Hyg. 2008;78(2):294–7.

    Article  CAS  PubMed  Google Scholar 

  45. Burgos JM, Diez M, Vigliano C, Bisio M, Risso M, Duffy T, 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(5):485–95.

    Article  CAS  PubMed  Google Scholar 

  46. Poveda C, Fresno M, Gironès N, Martins-Filho OA, Ramírez JD, Santi-Rocca J. Cytokine profiling in Chagas disease: towards understanding the association with infecting Trypanosoma cruzi discrete typing units (a BENEFIT TRIAL sub-study). PLoS One. 2014;9(3):e91154.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Mejía-Jaramillo AM, Fernández GJ, Montilla M, Nicholls RS, Triana-Chávez O. Trypanosoma cruzi strains resistant to benznidazole occurring in Colombia. Biomedica. 2012;32(2):196–205.

    Article  PubMed  Google Scholar 

  48. Rumi MM, Pérez Brandán C, Gil JF, D’Amato AM, Ragone PG, Lauthier JJ, et al. Benznidazole treatment in chronic children infected with Trypanosoma cruzi: serological and molecular follow-up of patients and identification of Discrete Typing Units. Acta Trop. 2013;128(1):130–6.

    Article  CAS  PubMed  Google Scholar 

  49. Zingales B, Araujo RG, Moreno M, Franco J, Aguiar PH, Nunes SL, et al. A novel ABCG-like transporter of Trypanosoma cruzi is involved in natural resistance to benznidazole. Mem Inst Oswaldo Cruz. 2015;110(3):433–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Andrade LO, Machado CR, Chiari E, Pena SD, Macedo AM. Differential tissue distribution of diverse clones of Trypanosoma cruzi in infected mice. Mol Biochem Parasitol. 1999;100(2):163–72.

    Article  CAS  PubMed  Google Scholar 

  51. Freitas JM, Andrade LO, Pires SF, Lima R, Chiari E, Santos RR, et al. The MHC Gene Region of Murine Hosts Influences the Differential Tissue Tropism of Infecting Trypanosoma cruzi Strains. PLoS One. 2009;4(4):e5113.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Alves MJ, Kawahara R, Viner R, Colli W, Mattos EC, Thaysen-Andersen M, et al. Comprehensive glycoprofiling of the epimastigote and trypomastigote stages of Trypanosoma cruzi. J Proteomics. 2017;151:182–92.

    Article  CAS  PubMed  Google Scholar 

  53. Queiroz RM, Ricart CA, Machado MO, Bastos IM, de Santana JM, de Sousa MV, et al. Insight into the exoproteome of the tissue-derived trypomastigote form of Trypanosoma cruzi. Front Chem. 2016;4:42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Kahn SJ, Wleklinski M, Ezekowitz RA, Coder D, Aruffo A, Farr A. The major surface glycoprotein of Trypanosoma cruzi amastigotes are ligands of the human serum mannose-binding protein. Infect Immun. 1996;64(7):2649–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Santos MA, Garg N, Tarleton RL. The identification and molecular characterization of Trypanosoma cruzi amastigote surface protein-1, a member of the trans-sialidase gene super-family. Mol Biochem Parasitol. 1997;86(1):1–11.

    CAS  PubMed  Google Scholar 

  56. Turner CW, Lima MF, Villalta F. Trypanosoma cruzi uses a 45-kDa mucin for adhesion to mammalian cells. Biochem Biophys Res Commun. 2002;290(1):29–34.

    Article  CAS  PubMed  Google Scholar 

  57. Alves MJM, Colli W. Adhesion to the host cell and intracellular survival. Critical review. IUBMB Life. 2007;59(4-5):274–9.

    Article  CAS  PubMed  Google Scholar 

  58. Magdesian MH, Giordano R, Ulrich H, Juliano MA, Juliano L, Schumacher RI, et al. Infection by Trypanosoma cruzi. Identification of a parasite ligand and its host cell receptor. J Biol Chem. 2001;276(22):19382–9.

    Article  CAS  PubMed  Google Scholar 

  59. Freire-de-Lima L, Fonseca LM, Oeltmann T, Mendonça-Previato L, Previato JO. The trans-sialidase, the major Trypanosoma cruzi virulence factor: three decades of studies. Glycobiology. 2015;25(11):1142–9.

    Article  CAS  PubMed  Google Scholar 

  60. Schenkman S, Jiang MS, Hart GW, Nussenzweig V. A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell. 1991a;65(7):1117–25.

    Article  CAS  PubMed  Google Scholar 

  61. Rubin-de-Celis SS, Uemura H, Yoshida N, Schenkman S. Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell Microbiol. 2006;8(12):1888–90.

    Article  PubMed  CAS  Google Scholar 

  62. Nardy AF, Freire-de-Lima CG, Pérez AR, Morrot A. Role of Trypanosoma cruzi Trans-sialidase on the Escape from Host Immune Surveillance. Front Microbiol. 2016;7:348. https://doi.org/10.3389/fmicb.2016.00348. Mini Review.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Cánepa GE, Degese MS, Budu A, Garcia CR, Buscaglia CA. Involvement of TSSA (trypomastigote small surface antigen) in Trypanosoma cruzi invasion of mammalian cells. Biochem J. 2012;444(2):211–8.

    Article  PubMed  CAS  Google Scholar 

  64. García EA, Ziliani M, Agüero F, Bernabó G, Sánchez DO, Tekiel V. TcTASV: a novel protein family in Trypanosoma cruzi identified from a subtractive trypomastigote cDNA library. PLoS Negl Trop Dis. 2010b;4(10):e841. https://doi.org/10.1371/journal.pntd.0000841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Bernabó G, Levy G, Ziliani M, Caeiro LD, Sánchez DO, Tekiel V. TcTASV-C, a protein family in Trypanosoma cruzi that is predominantly trypomastigote-stage specific and secreted to the medium. PLoS One. 2013;8(7):e71192.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Staquicini DI, Martins RM, Macedo S, Sasso GR, Atayde VD, Juliano MA, et al. Role of GP82 in the selective binding to gastric mucin during oral infection with Trypanosoma cruzi. PLoS Negl Trop Dis. 2010;4(3):e613.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Cortez C, Sobreira TJ, Maeda FY, Yoshida N. The gp82 surface molecule of Trypanosoma cruzi metacyclic forms. Subcell Biochem. 2014;74:137–50.

    Article  CAS  PubMed  Google Scholar 

  68. Correa PR, Cordero EM, Gentil LG, Bayer-Santos E, da Silveira JF. Genetic structure and expresión of the surface glycoprotein GP82, the main adhesin of Trypanosoma cruzi metacyclic trypomastigotes. Scientific World Journal. 2013;2013:156734.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  69. Yoshida N. Molecular mechanisms of Trypanosoma cruzi infection by oral route. Mem Inst Oswaldo Cruz. 2009;104(Suppl 1):101–7.

    Article  CAS  PubMed  Google Scholar 

  70. Rodrigues JPF, Santana GHT, Juliano MA, Yoshida N. Inhibition of host cell lysosome spreading by Trypanosoma cruzi metacyclic stage-specific surface molecule gp90 downregulates parasite invasion. Infect Immun. 2017;85(9):e00302–17. https://doi.org/10.1128/IAI.00302-17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Cazzulo JJ. Proteinases of Trypanosoma cruzi: patential targets for the chemotherapy of Changas desease. Curr Top Med Chem. 2002;2(11):1261–71.

    Article  CAS  PubMed  Google Scholar 

  72. San Francisco J, Barría I, Gutiérrez B, Neira I, Muñoz C, Sagua H, 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.

    Article  CAS  PubMed  Google Scholar 

  73. Stoka V, Nycander M, Lenarcic B, Labriola C, Cazzulo JJ, Björk I, et al. Inhibition of cruzipain, the major cysteine proteinase of the protozoan parasite, Trypanosoma cruzi, by proteinase inhibitors of the cystatin superfamily. FEBS Lett. 1995;370(1-2):101–4.

    Article  CAS  PubMed  Google Scholar 

  74. Pinto Dìas JC, Schofield CJ. History of Chagas Disease as a public health problem in Latin America. In: Teixeira A, Vinaud M, Castro AM, editors. Emerging Chagas Disease. Sharjah: Bentham; 2009. p. 1–9. Chapter 1.

    Google Scholar 

  75. Darwin C. Journal of researches into the geology and natural history of the various countries visited by H.M.S. Beagle, under the command of captain Fitzroy, R.N. from 1832 to 1836. London: Henry Colburn; 1839.

    Google Scholar 

  76. Zeledón R, Rabinovich JE. Chagas Disease: an ecological appraisal with special enphasis on its insect vector. Annu Rev Entomol. 1981;26:101–33.

    Article  PubMed  Google Scholar 

  77. Shelock IA. Vectores. In: Brener Z, Andrade ZA, Barral-Netto M, editors. Trypanosoma cruzi e doença de Chagas, vol. 3. 2nd ed. Río de Janeiro: Wanabara Koogan SA; 2000. p. 21–40.

    Google Scholar 

  78. Garcia ES, de Azambuja P. Fisiología de Triatomíneos: desenvolvimento, reproduçao e interaçao com Trypanosoma cruzi. In: Brener Z, Andrade Z, Barral-Netto M, editors. Trypanosoma cruzi e doença de Chagas, vol. 4. 2nd ed. Río de Janeiro: Wanabara Koogan SA; 2000. p. 41–7.

    Google Scholar 

  79. García DS, Dvorak JA. Growth and development of two Trypanosoma cruzi clones in the arthropod Dipetalogaster maximun. Am J Trop Med Hyg. 1982;31(2):259–62.

    Article  PubMed  Google Scholar 

  80. Lammel EL, de Isola EL, Korn C, Gonzalez Cappa SM. Trypanosoma cruzi: comparative Studies of infectivity of parasite ingested by Triatoma infestans and those present in their feces. Acta Trop. 1981;38(2):107–14.

    CAS  PubMed  Google Scholar 

  81. Dvorak JA. A new in vitro approach to quantitation of Trypanosoma cruzi-vertebrate cell interaction. In: Proc. Symposium on New approaches in American Trypanosomiasis research. Washington, DC: PAHO/WHO; 1976. p. 109–20. Scientific Publication No 318.

    Google Scholar 

  82. de Souza W. O parasito e sua interaçao com os hospedeiros. In: Brener Z, Andrade Z, Barral-Netto M, editors. Trypanosoma cruzi e doença de Chagas, vol. 7. 2nd ed. Río de Janeiro: Wanabara Koogan SA; 2000. p. 88–126.

    Google Scholar 

  83. Enriquez GF, Bua J, Orozco MM, Wirth S, Schijman AG, Gürtler RE, et al. High levels of Trypanosoma cruzi DNA determined by qPCR and infectiousness to Triatoma infestans support dogs and cats are major sources of parasites for domestic transmission. Infect Genet Evol. 2014;25:36–43.

    Article  CAS  PubMed  Google Scholar 

  84. Gürtler RE, Cécere MC, Rubel DN, Petersen RM, Schweigmann NJ, Lauricella MA, et al. Chagas disease in north-west Argentina: infected dogs as a risk factor for the domestic transmission of Trypanosoma cruzi. Trans R Soc Trop Med Hyg. 1991;85(6):741–5.

    Article  PubMed  Google Scholar 

  85. Ramírez JD, Turriago B, Tapia-Calle G, Guhl F. Understanding the role of dogs (Canis lupus familiaris) in the transmission dynamics of Trypanosoma cruzi genotypes in Colombia. Vet Parasitol. 2013;196(1-2):216–9.

    Article  PubMed  Google Scholar 

  86. Moncayo A. Current epidemiological trends after the interruption of vectorial and transfusional transmission in the southern Cone Countries. Mem Inst Oswaldo Cruz. 2003;98(5):577–91.

    Article  PubMed  Google Scholar 

  87. Moncayo A, Silveira AC. Current epidemiological trends for Chagas disease in Latin America and future challenges in epidemiology, surveillance and health policy. Mem I Oswaldo Cruz. 2009;104(Suppl 1):17–309.

    Article  Google Scholar 

  88. Reyes M, Torres A, Esteban L, Flórez M, Angulo VM. Riesgo de transmisión de la enfermedad de Chagas por intrusión de triatominos y mamíferos silvestres en Bucaramanga, Santander, Colombia. Biomédica. 2017;37:68–78.

    Article  PubMed  Google Scholar 

  89. Argibay HD, Orozco MM, Cardinal MV, Rinas MA, Arnaiz M, Mena Segura C, et al. First finding of Trypanosoma cruzi II in vampire bats from a district free o domestic vector-born transmssion in Northeastern Argentina. Parasitology. 2016;143(11):1358–68.

    Article  CAS  PubMed  Google Scholar 

  90. Gurgel-Gonçalves R, Cura C, Schijman AG, Cuba CA. Infestation of Mauritia flexuosa palms by triatomines (Hemiptera: Reduviidae), vectors of Trypanosoma cruzi and Trypanosoma rangeli in the Brazilian savanna. Acta Trop. 2012;121(2):105–11.

    Article  PubMed  Google Scholar 

  91. Miles MA, Arias JR, de Souza AA. Chagas’ disease in the Amazon basin: V. Periurban palms as habitats of Rhodnius robustus and Rhodnius pictipes-triatomine vectors of Chagas’ disease. Mem Inst Oswaldo Cruz. 1983;78(4):391–8.

    Article  CAS  PubMed  Google Scholar 

  92. Schmunis GA. Prevention of transfusional Trypanosoma cruzi infection in Latin America. Mem Inst Oswaldo Cruz. 1999;94(Suppl 1):93–101.

    Article  PubMed  Google Scholar 

  93. Yadon ZE, Schmunis GA. Congenital Chagas disease: estimating the potential risk in the United States. Am J Trop Med Hyg. 2009;81(6):927–33.

    Article  PubMed  Google Scholar 

  94. Celentano AM, González Cappa SM. Chagas’ disease and blood transfusion: trypanocidal activity of maprotiline hydrochloride and gentian violet. Medicina. 1988;48(3):265–8.

    CAS  PubMed  Google Scholar 

  95. Hammond DJ, Croft SL, Hogg J, Gutteridge WE. A strategy for the prevention of the transmission of Chagas’ disease during blood transfusion. Acta Trop. 1986;43:367–78.

    CAS  PubMed  Google Scholar 

  96. Carlier Y, Torrico F, Sosa-Estani S, Russomando G, Luquetti A, Freilij H, et al. Congenital Chagas disease: recommendations for diagnosis, treatment and control of newborns, siblings and pregnant women. PLoS Negl Trop Dis. 2011;5(10):e1250.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Juiz NA, Cayo NM, Burgos M, Salvo ME, Nasser JR, Búa J, et al. Human polymorphisms in placentally expressed genes and their association with susceptibility to congenital Trypanosoma cruzi infection. Infect Dis. 2016;213(8):1299–306.

    Article  CAS  Google Scholar 

  98. Barcán L, Luna C, Clara L, Sinagra A, Valledor A, De Rissio AM, et al. Transmission of T. cruzi infection via liver transplantation to a nonreactive recipient for Chagas’ disease. Liver Transpl. 2005;11(9):1112–6.

    Article  PubMed  Google Scholar 

  99. Bocchi EA, Fiorelli A. The paradox of survival results after heart transplantation for cardiomyopathy caused by Trypanosoma cruzi. First Guidelines Group for Heart Transplantation of the Brazilian Society of Cardiology. Ann Thorac Surg. 2001;71(6):1833–8.

    Article  CAS  PubMed  Google Scholar 

  100. Casadei D, Chagas’ Disease Argentine Collaborative Transplant Consortium. Chagas’ disease and solid organ transplantation. Transplant Proc. 2010;42(9):3354–9.

    Article  PubMed  Google Scholar 

  101. Kransdorf EP, Zakowski PC, Kobashigawa JA. Chagas disease in solid organ and heart transplantation. Curr Opin Infect Dis. 2014;27(5):418–24.

    Article  PubMed  Google Scholar 

  102. Kleffmann T, Schmidt J, Schaub GA. Attachment to Trypanosoma cruzi epimastigotes to hydrophobic substrates and use of this property to separate stages and promote metacyclogenesis. J Eukaryot Microbiol. 1998;45(5):548–55.

    Article  CAS  PubMed  Google Scholar 

  103. Guarneri AA, Lorenzo MG. Triatomine physiology in the context of trypanosome infection. J Insect Physiol. 2017;97:66–76.

    Article  CAS  PubMed  Google Scholar 

  104. de Isola EL, Lammel EM, Katzin VJ, GonzalezCappa SM. Influence of organ extracts of Triatoma infestans on differentiation of Trypanosoma cruzi. J Parasitol. 1981;67(1):53–8.

    Article  PubMed  Google Scholar 

  105. Isola EL, Lammel EM, Giovanniello O, Katzin AM, González Cappa SM. Trypanosoma cruzi morphogenesis: preliminary purification of an active fraction from hemolymph and intestinal homogenate of Triatoma infestans. J Parasitol. 1986b;72(3):467–9.

    Article  CAS  PubMed  Google Scholar 

  106. Lammel EM, Barbieri MA, Wilkowsky SE, Bertini F, Isola EL. Trypanosoma cruzi: involvemente of intracellular calciun in multiplication and differentiation. Exp Parasitol. 1996;83(2):240–9.

    Article  CAS  PubMed  Google Scholar 

  107. Isola EL, Lammel EM, González Cappa SM. Trypanosoma cruzi diferenciation after interaction of epimastigote and Triatoma infestans intestine homogenate. Exp Parasitol. 1986a;62(3):329–35.

    Article  CAS  PubMed  Google Scholar 

  108. Fraidenraich D, Peña C, Isola EL, Lammel EM, Coso O, Añel AD, et al. Stimulation of Trypanosoma cruzi adenyl cyclase by an alpha D-globin fragment from Triatoma hindgat: effect on differentiation of epimastigote to trypomastigote forms. Proc Natl Acad Sci U S A. 1993;90(21):10140–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Belauzaran ML, Lammel EM, Giménez G, Wainszelbaum MJ, de Isola EL. Envolvement of protein kinase C isoenzymes in Trypanosoma cruzi metaciclogenesis induced by oleica cid. Parasitol Res. 2009;105(1):47–55.

    Article  Google Scholar 

  110. Wainszelbaum MJ, Belaunzarán ML, Lammel EM, Florin-Christensen M, Florin-Christensen J, Isola EL. Free fatty acids induce cell differenciatin to infective forms in Trypanosoma cruzi. Biochem J. 2003;375(3):705–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Isola EL, Lammel EM, González Cappa SM. Trypanosoma cruzi: differentiation to metacyclic trypomastigotes in the presence of ADP-ribosyltransferase inhibitors. Exp Parasitol. 1987;64(3):424–9.

    Article  CAS  PubMed  Google Scholar 

  112. Contreras VT, Araujo-Jorge TC, Bonaldo MC, Thomaz N, Barbosa HS, Meirelles Mde N, et al. Biological aspects of the D28c clone of Trypanosoma cruzi after metacyclogenesis in chemical defined media. Mem Inst Oswaldo Cruz. 1988;83(1):123–33.

    Article  CAS  PubMed  Google Scholar 

  113. Contreras VT, Salles JM, Thomas N, Morel CM, Goldenberg S. In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol Biochem Parasitol. 1985;16(3):315–27.

    Article  CAS  PubMed  Google Scholar 

  114. Hamedi A, Botelho L, Britto C, Fragoso SP, Umaki AC, Goldenberg S, et al. In vitro metacyclogenesis of Trypanosoma cruzi induced by starvation correlates with a transient adenilyl cyclase stimulation as well as with a constitutive upregulation of adenylyn cyclase expression. Mol Biochem Parasitol. 2015;200(1-2):9–18.

    Article  CAS  PubMed  Google Scholar 

  115. Dworak ES, Araújo SM, Gomes M, Massago M, Ferreira ÉC, Toledo MJO. Sympatry influence in the interaction of Trypanosoma cruzi with triatomine. Rev Soc Bras Med Trop. 2017;50(5):629–37.

    Article  PubMed  Google Scholar 

  116. Lammel EM, Müller LA, Isola EL, González Cappa SM. Effect of vector on infectivity of Trypanosoma cruzi. Acta Trop. 1985;42(2):149–55.

    CAS  PubMed  Google Scholar 

  117. Szumlewicz AP, Muller CA. Studies in search of a suitable experimental insect model for xenodiagnosis of hosts with Chagas’ disease. 2 Attempts to upgrade the reliability and the efficacy of xenodiagnosis in chronic Chagas’ disease. Mem Inst Oswaldo Cruz. 1987;82(2):259–72.

    Article  CAS  PubMed  Google Scholar 

  118. Alves MJ, Colli W. Role of the gp85/trans-sialidase superfamily of glycoproteins in the interaction of Trypanosoma cruzi with host structures. Subcell Biochem. 2008;47:58–69.

    Article  PubMed  Google Scholar 

  119. Maeda FY, Cortez C, Izidoro MA, Juliano L, Yoshida N. Fibronectin-degrading activity of Trypanosoma cruzi cysteine proteinase plays a role in host cell invasion. Infect Immun. 2014;82(12):5166–74.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Nde PN, Simmons KJ, Kleshchenko YY, Pratap S, Lima MF, Villalta F. Silencing of the laminin gamma-1 gene blocks Trypanosoma cruzi infection. Infect Immun. 2006;74(3):1643–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Coimbra VC, Yamamoto D, Khusal KG, Atayde VD, Fernandes MC, Mortara RA, et al. Enucleated L929 cells support invasion, differentiation, and multiplication of Trypanosoma cruzi parasites. Infect Immun. 2007;75(8):3700–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Epting CL, Coates BM, Engman DM. Molecular mechanisms of host cell invasion by Trypanosoma cruzi. Exp Parasitol. 2010;126(3):283–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Burleigh BA, Andrews NW. The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Annu Rev Microbiol. 1995;49:175–200.

    Article  CAS  PubMed  Google Scholar 

  124. Milei J, Sánchez J, Storino R, Yu ZX, Denduchis B, Ferrans VJ. Antibodies to laminin and immunohistochemical localization of laminin in chronic chagasic cardiomyopathy: a review. Mol Cell Biochem. 1993;129(2):161–70.

    Article  CAS  PubMed  Google Scholar 

  125. Ferreira V, Molina MC, Valck C, Rojas A, Aguilar L, Ramírez G, et al. Role of calreticulin from parasites in its interaction with vertebrate hosts. Mol Immunol. 2004;40(17):1279–91.

    Article  CAS  PubMed  Google Scholar 

  126. Johnson CA, Kleshchenko YY, Ikejiani AO, Udoko AN, Cardenas TC, Pratap S, et al. Thrombospondin-1 interacts with Trypanosoma cruzi surface calreticulin to enhance cellular infection. PLoS One. 2012;7(7):e40614. https://doi.org/10.1371/journal.pone.0040614.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Kleshchenko YY, Moody TN, Furtak VA, Ochieng J, Lima MF, Villalta F. Human galectin-3 promotes Trypanosoma cruzi adhesion to human coronary artery smooth muscle cells. Infect Immun. 2004;72(11):6717–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Moody TN, Ochieng J, Villalta F. Novel mechanism that Trypanosoma cruzi uses to adhere to the extracellular matrix mediated by human galectin-3. FEBS Lett. 2000;470(3):305–8.

    Article  CAS  PubMed  Google Scholar 

  129. Sato S, Hughes RC. Control of Mac-2 surface expression on murine macrophage cell lines. Eur J Immunol. 1994;24(1):216–21.

    Article  CAS  PubMed  Google Scholar 

  130. Grellier P, Vendeville S, Joyeau R, Bastos IM, Drobecq H, Frappier F, et al. Trypanosoma cruzi prolyl oligopeptidase Tc80 is involved in nonphagocytic mammalian cell invasion by trypomastigotes. J Biol Chem. 2001;276(50):47078–86.

    Article  CAS  PubMed  Google Scholar 

  131. Teixeira AA, de Vasconcelos Vde C, Colli W, Alves MJ, Giordano RJ. Trypanosoma cruzi binds to cytokeratin through conserved peptide motifs found in the laminin-G-like domain of the gp85/trans-sialidase proteins. PLoS Negl Trop Dis. 2015;9(9):e0004099.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Weston D, Patel B, Van Voorhis WC. Virulence in Trypanosoma cruzi infection correlates with the expression of a distinct family of sialidase superfamily genes. Mol Biochem Parasitol. 1999;98(1):105–16.

    Article  CAS  PubMed  Google Scholar 

  133. Ruiz RC, Favoreto S, Dorta ML, Oshiro MEM, Ferreira AT, Manque PM, et al. Infectivity of Trypanosoma cruzi strains is associated with differential expresión of surface glycoproteins with differential CA2 signaling activity. Biochem J. 1998;330:505–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Alves MJ, Abuin G, Kuwajima VY, Colli W. Partial inhibition of trypomastigote entry into cultured mammalian cells by monoclonal antibodies against a surface glycoprotein of Trypanosoma cruzi. Mol Biochem Parasitol. 1986;21(1):75–82.

    Article  CAS  PubMed  Google Scholar 

  135. Freitas LM, dos Santos SL, Rodrigues-Luiz GF, Mendes TAO, Rodrigues TS, Gazzinelli RT, et al. Genomic analices, gene expresison and antigenic profile of the trans-sialidase superfamily of Trypanosoma cruzi reveal an undetected level of complexity. PLoS One. 2011;6:e25914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Mattos EC, Tonelli RR, Colli W, Alves MJ. The Gp85 surface glycoproteins from Trypanosoma cruzi. Subcell Biochem. 2014;74:151–80.

    Article  CAS  PubMed  Google Scholar 

  137. Tonelli RR, Giordano RJ, Barbu EM, Torrecilhas AC, Kobayashi GS, Langley RR, 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Zingales B, Carniol C, de Lederkremer RM, Colli W. Direct sialic acid transfer from a protein donor to glycolipids of trypomastigote forms of Trypanosoma cruzi. Mol Biochem Parasitol. 1987;26(1-2):135–44.

    Article  CAS  PubMed  Google Scholar 

  139. Campetella O, Sánchez D, Cazzulo JJ, Frasch AC. A superfamily of Trypanosoma cruzi surface antigens. Parasitol Today. 1992;8(11):378–81.

    Article  CAS  PubMed  Google Scholar 

  140. Frasch AC. Trans-sialidase, SAPA amino acid repeats and the relationship between Trypanosoma cruzi and the mammalian host. Parasitology. 1994;108(Suppl):S37–44.

    Article  PubMed  Google Scholar 

  141. Affranchino JL, Ibañez CF, Luquetti AO, Rassi A, Reyes MB, Macina RA, et al. Identification of a Trypanosoma cruzi antigen that is shed during the acute phase of Chagas’ disease. Mol Biochem Parasitol. 1989;34(3):221–8.

    Article  CAS  PubMed  Google Scholar 

  142. Tambourgi DV, Kipnis TL, da Silva WD, Joiner KA, Sher A, Heath S, et al. A partial cDNA clone of trypomastigote decay-accelerating factor (T-DAF), a developmentally regulated complement inhibitor of Trypanosoma cruzi, has genetic and functional similarities to the human complement inhibitor DAF. Infect Immun. 1993;61(9):3656–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Hall BF, Webster P, Ma AK, Joiner KA, Andrews NW. Desialylation of lysosomal membrane glycoproteins by Trypanosoma cruzi: a role for the surface neuraminidase in facilitating parasite entry into the host cell cytoplasm. J Exp Med. 1992;176(2):313–25.

    Article  CAS  PubMed  Google Scholar 

  144. Risso MG, Pitcovsky TA, Caccuri RL, Campetella O, Leguizamón MS. Immune system pathogenesis is prevented by the neutralization of the systemic trans-sialidase from Trypanosoma cruzi during severe infections. Parasitology. 2007;134(Pt 4):503–10.

    Article  CAS  PubMed  Google Scholar 

  145. Vercelli CA, Hidalgo AM, Hyon SH, Argibay PF. Trypanosoma cruzi trans-sialidase inhibits human lymphocyte proliferation by nonapoptotic mechanisms: implications in pathogenesis and transplant immunology. Transplant Proc. 2005;37(10):4594–7.

    Article  CAS  PubMed  Google Scholar 

  146. Ruiz Díaz P, Mucci J, Meira MA, Bogliotti Y, Musikant D, Leguizamón MS, et al. Trypanosoma cruzi trans-sialidase prevents elicitation of Th1 cell response via interleukin 10 and downregulates Th1 effector cells. Infect Immun. 2015;83(5):2099–108.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  147. Barrias ES, de Carvalho TM, De Souza W. Trypanosoma cruzi: entry into mammalian host cells and parasitophorous vacuole formation. Front Immunol. 2013;4:186.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. Caradonna KL, Burleigh BA. Mechanisms of host cell invasion by Trypanosoma cruzi. Review. Adv Parasitol. 2011;76:33–61.

    Article  PubMed  Google Scholar 

  149. 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. 1991b;59(2):645–54.

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Andrews NW. Lysosome recruitment during host cell invasion by Trypanosoma cruzi. Trends Cell Biol. 1995;5(3):133–7.

    Article  CAS  PubMed  Google Scholar 

  151. Tardieux I, Webster P, Ravesloot J, Boron W, Lunn JA, Heuser JE, et al. Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell. 1992;71(7):1117–30.

    Article  CAS  PubMed  Google Scholar 

  152. Fernandes MC, Cortez M, Flannery AR, Tam C, Mortara RA, Andrews NW. Trypanosoma cruzi subverts the sphingomyelinase-mediated plasma membrane repair pathway for cell invasion. J Exp Med. 2011;208(5):909–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Rodríguez A, Samoff E, Rioult MG, Chung A, Andrews NW. Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J Cell Biol. 1996;134(2):349–62.

    Article  PubMed  Google Scholar 

  154. Caler EV, Chakrabarti S, Fowler KT, Rao S, Andrews NW. The exocytosis-regulatory protein synaptotagmin VII mediates cell invasion by Trypanosoma cruzi. J Exp Med. 2001;193(9):1097–104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Chakrabarti S, Kobayashi KS, Flavell RA, Marks CB, Miyake K, Liston DR, et al. Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J Cell Biol. 2003;162(4):543–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Rodríguez A, Rioult MG, Ora A, Andrews NW. A trypanosome-soluble factor induces IP3 formation, intracellular Ca2+ mobilization and microfilament rearrangement in host cells. J Cell Biol. 1995;129(5):1263–73.

    Article  PubMed  Google Scholar 

  157. Tardieux I, Nathanson MH, Andrews NW. Role in host cell invasion of Trypanosoma cruzi-induced cytosolic-free Ca2+ transients. J Exp Med. 1994;179(3):1017–22.

    Article  CAS  PubMed  Google Scholar 

  158. Fernandes MC, Cortez M, Geraldo Yoneyama KA, Straus AH, Yoshida N, Mortara RA. Novel strategy in Trypanosoma cruzi cell invasion: implication of cholesterol and host cell microdomains. Int J Parasitol. 2007;37(13):1431–41.

    Article  CAS  PubMed  Google Scholar 

  159. Andrews NW. Lysosomes and the plasma membrane: trypanosomes reveal a secret relationship. Review. J Cell Biol. 2002;158(3):389–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Reddy A, Caler EV, Andrews NW. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell. 2001;106(2):157–69.

    Article  CAS  PubMed  Google Scholar 

  161. McNeil PL, Steinhardt RA. Plasma membrane disruption: repair, prevention, adaptation. Review. Annu Rev Cell Dev Biol. 2003;19:697–731.

    Article  CAS  PubMed  Google Scholar 

  162. Woolsey AM, Burleigh BA. Host cell actin polymerization is required for cellular retention of Trypanosoma cruzi and early association with endosomal/lysosomal compartments. Cell Microbiol. 2004;6(9):829–38.

    Article  CAS  PubMed  Google Scholar 

  163. Woolsey AM, Sunwoo L, Petersen CA, Brachmann SM, Cantley LC, Burleigh BA. Novel PI 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation. J Cell Sci. 2003;116(17):3611–22.

    Article  CAS  PubMed  Google Scholar 

  164. Wilkowsky SE, Barbieri MA, Stahl PD, Isola EL. Regulation of Trypanosoma cruzi invasion of nonphagocytic cells by the endocytically active GTPases dynamin, Rab5, and Rab7. Biochem Biophys Res Commun. 2002;291(3):516–21.

    Article  CAS  PubMed  Google Scholar 

  165. Romano PS, Arboit MA, Vázquez CL, Colombo MI. The autophagic pathway is a key component in the lysosomal dependent entry of Trypanosoma cruzi into the host cell. Autophagy. 2009;5(1):6–18.

    Article  CAS  PubMed  Google Scholar 

  166. Martins RM, Alves RM, Macedo S, Yoshida N. Starvation and rapamycin differentially regulate host cell lysosome exocytosis and invasion by Trypanosoma cruzi metacyclic forms. Cell Microbiol. 2011;13(7):943–54.

    Article  CAS  PubMed  Google Scholar 

  167. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004;15(3):1101–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Romano PS, Cueto JA, Casassa AF, Vanrell MC, Gottlieb RA, Colombo MI. Molecular and cellular mechanisms involved in the Trypanosoma cruzi/host cell interplay. IUBMB Life. 2012;64(5):387–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Wilkowsky SE, Barbieri MA, Stahl P, Isola EL. Trypanosoma cruzi: phosphatidylinositol 3-kinase and protein kinase B activation is associated with parasite invasion. Exp Cell Res. 2001;264(2):211–8.

    Article  CAS  PubMed  Google Scholar 

  170. Chuenkova MV, Furnari FB, Cavenee WK, Pereira MA. Trypanosoma cruzi trans-sialidase: a potent and specific survival factor for human Schwann cells by means of phosphatidylinositol 3-kinase/Akt signaling. Proc Natl Acad Sci U S A. 2001;98(17):9936–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Andrade LO, Andrews NW. Lysosomal fusion is essential for the retention of Trypanosoma cruzi inside host cells. J Exp Med. 2004;200(9):1135–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Kierszenbaum F, Knecht E, Budzko DB, Pizzimenti MC. Phagocytosis: a defense mechanism against infection with Trypanosoma cruzi. J Immunol. 1974;112(5):1839–44.

    CAS  PubMed  Google Scholar 

  173. Muñoz-Fernández MA, Fernández MA, Fresno M. Activation of human macrophages for the killing of intracellular Trypanosoma cruzi by TNF-alpha and IFN-gamma through a nitric oxide-dependent mechanism. Immunol Lett. 1992;33(1):35–40.

    Article  PubMed  Google Scholar 

  174. Piacenza L, Alvarez MN, Peluffo G, Radi R. Fighting the oxidative assault: the Trypanosoma cruzi journey to infection. Curr Opin Microbiol. 2009;12(4):415–21. https://doi.org/10.1016/j.mib.2009.06.011.

    Article  CAS  PubMed  Google Scholar 

  175. Celentano AM, González Cappa SM. In vivo macrophage function in experimental infection with Trypanosoma cruzi subpopulations. Acta Trop. 1993;55(3):171–80.

    Article  CAS  PubMed  Google Scholar 

  176. Zago MP, Hosakote YM, Koo SJ, Dhiman M, Piñeyro MD, Parodi-Talice A, 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):1842–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Kipnis TL, Calich VL, da Silva WD. Active entry of bloodstream forms of Trypanosoma cruzi into macrophages. Parasitology. 1979;78(1):89–98.

    Article  CAS  PubMed  Google Scholar 

  178. Andrews NW. From lysosomes into the cytosol: the intracellular pathway of Trypanosoma cruzi. Braz J Med Biol Res. 1994;27(2):471–5.

    CAS  PubMed  Google Scholar 

  179. Ley V, Robbins ES, Nussenzweig V, Andrews NW. The exit of Trypanosoma cruzi from the phagosome is inhibited by raising the pH of acidic compartments. J Exp Med. 1990;171(2):401–13.

    Article  CAS  PubMed  Google Scholar 

  180. Andrews NW, Abrams CK, Slatin SL, Griffiths G. A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell. 1990;61(7):1277–87.

    Article  CAS  PubMed  Google Scholar 

  181. Manning-Cela R, Cortés A, González-Rey E, Van Voorhis WC, Swindle J, González A. LYT1 protein is required for efficient in vitro infection by Trypanosoma cruzi. Infect Immun. 2001;69(6):3916–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Tomlinson S, Vandekerckhove F, Frevert U, Nussenzweig V. The induction of Trypanosoma cruzi trypomastigote to amastigote transformation by low pH. Parasitology. 1995;110(Pt 5):547–54.

    Article  PubMed  Google Scholar 

  183. Tonelli RR, Silber AM, Almeida-de-Faria M, Hirata IY, Colli W, Alves MJ. L-proline is essential for the intracellular differentiation of Trypanosoma cruzi. Cell Microbiol. 2004;6(8):733–41.

    Article  CAS  PubMed  Google Scholar 

  184. Grellier P, Blum J, Santana J, Bylèn E, Mouray E, Sinou V, et al. Involvement of calyculin A-sensitive phosphatase(s) in the differentiation of Trypanosoma cruzi trypomastigotes to amastigotes. Mol Biochem Parasitol. 1999;98(2):239–52.

    Article  CAS  PubMed  Google Scholar 

  185. Costales J, Rowland EC. A role for protease activity and host-cell permeability during the process of Trypanosoma cruzi egress from infected cells. J Parasitol. 2007;93(6):1350–9.

    Article  CAS  PubMed  Google Scholar 

  186. Clark RK, Kuhn RE. Trypanosoma cruzi does not induce apoptosis in murine fibroblasts. Parasitology. 1999;118(2):167–75.

    Article  PubMed  Google Scholar 

  187. de Souza EM, Araújo-Jorge TC, Bailly C, Lansiaux A, Batista MM, Oliveira GM, et al. Host and parasite apoptosis following Trypanosoma cruzi infection in in vitro and in vivo models. Cell Tissue Res. 2003;314(2):223–35.

    Article  PubMed  Google Scholar 

  188. Mortara RA. Trypanosoma cruzi: amastigotes and trypomastigotes interact with different structures on the surface of HeLa cells. Exp Parasitol. 1991;73(1):1–14.

    Article  CAS  PubMed  Google Scholar 

  189. Ley V, Andrews NW, Robbins ES, Nussenzweig V. Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. J Exp Med. 1988;168(2):649–59.

    Article  CAS  PubMed  Google Scholar 

  190. Mortara RA, Andreoli WK, Taniwaki NN, Fernandes AB, Silva CV, Fernandes MC, et al. Mammalian cell invasion and intracellular trafficking by Trypanosoma cruzi infective forms. An Acad Bras Cienc. 2005;77(1):77–94.

    Article  PubMed  Google Scholar 

  191. Perlowagora-Szumlewics A, Moreira CJ. In vivo differentiation of Trypanosoma cruzi--1. Experimental evidence of the influence of vector species on metacyclogenesis. Mem Inst Oswaldo Cruz. 1994;89(4):603–18.

    Article  Google Scholar 

  192. Previato JO, Andrade AF, Pessolani MC, Mendonça-Previato L. Incorporation of sialic acid into Trypanosoma cruzi macromolecules. A proposal for a new metabolic route. Mol Biochem Parasitol. 1985;16(1):85–96.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Microbiología, Parasitología e Inmunología. Facultad de Medicina, Instituto de Microbiología y Parasitología Médica (IMPaM-UBA/CONICET), Universidad de Buenos Aires, Buenos Aires, Argentina

    Catalina D. Alba Soto & Stella Maris González Cappa

Authors
  1. Catalina D. Alba Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stella Maris González Cappa
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Servicio de Parasitología y Enfermedad de Chagas, Hospital de Niños “Ricardo Gutiérrez”, Buenos Aires, Argentina

    Jaime Marcelo Altcheh

  2. Servicio de Parasitología y Enfermedad de Chagas, Hospital de Niños “Ricardo Gutiérrez”, Buenos Aires, Argentina

    Hector Freilij

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Alba Soto, C.D., González Cappa, S.M. (2019). Trypanosoma cruzi Journey from the Insect Vector to the Host Cell. In: Altcheh, J., Freilij, H. (eds) Chagas Disease. Birkhäuser Advances in Infectious Diseases. Springer, Cham. https://doi.org/10.1007/978-3-030-00054-7_2

Download citation

Publish with us

Policies and ethics

Search

Navigation