Skip to main content
Log in

Stationary phase in Trypanosoma cruzi epimastigotes as a preadaptive stage for metacyclogenesis

  • Review
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Trypanosoma cruzi is a species of parasitic protozoa that causes American trypanosomiasis or Chagas disease. These parasites go through a complex life cycle in Triatominae insects and vertebrate hosts. Epimastigotes are replicative forms that colonize the digestive tract of the vector and can be cultured in axenic media. The growth curve of epimastigotes allows assessment of differences in cells undergoing growth rate transitions from an exponential growth to a stationary phase. Since the classical descriptions of T. cruzi, it has been noted that the growth curve of epimastigotes in culture can give rise, in the stationary phase, to nonreplicating forms of metacyclic trypomastigotes. Metacyclogenesis therefore regards to the development process by which epimastigote transform into infective metacyclic trypomastigotes. In nature, these metacyclic forms allow the spread of Chagas disease when transmitted from an infected vector to a vertebrate host. This work reviews cellular phenomena that occur during the growth rate transitions of epimastigotes in culture, which may be related to very early physiological conditions for metacyclogenesis. Many of these events have not been thoroughly investigated. Their analysis can stimulate new hypotheses and future research in an important area not fully exploited.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Atwood JA III, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, Orlando R, Tarleton RL (2005) The Trypanosoma cruzi proteome. Science 309:473–476

    Article  PubMed  CAS  Google Scholar 

  • Barreto ML, Teixeira MG, Bastos FI, Ximenes RA, Barata RB, Rodrigues LC (2011) Successes and failures in the control of infectious diseases in Brazil: social and environmental context, policies, interventions, and research needs. Lancet 377:1877–1889

    Article  PubMed  Google Scholar 

  • Bonaldo MC, Souto-Padron T, de Souza W, Goldenberg S (1988) Cell-substrate adhesion during Trypanosoma cruzi differentiation. J Cell Biol 106:1349–1358

    Article  PubMed  CAS  Google Scholar 

  • Camargo EP (1964) Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop Sao Paulo 6:93–100

    PubMed  CAS  Google Scholar 

  • Cassola A, De Gaudenzi JG, Frasch AC (2007) Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol Microbiol 65:655–670

    Article  PubMed  CAS  Google Scholar 

  • Cazzulo JJ (1992) Energy metabolism in Trypanosoma cruzi. Subcell Biochem 18:235–257

    PubMed  CAS  Google Scholar 

  • Cazzulo JJ, Franke de Cazzulo BM, Engel JC, Cannata JJB (1985) End products and enzyme levels of aerobic glucose fermentation in trypanosomatids. Mol Biochem Parasitol 16:329–343

    Article  PubMed  CAS  Google Scholar 

  • Cevallos AM, Pérez-Escobar M, Espinosa N, Herrera J, López-Villaseñor I, Hernández R (2005) The stabilization of housekeeping transcripts in Trypanosoma cruzi epimastigotes evidences a global regulation of RNA decay during stationary phase. FEMS Microbiol Lett 246:259–264

    Article  PubMed  CAS  Google Scholar 

  • Cevallos AM, Segura-Kato YX, Merchant-Larios H, Manning-Cela R, Alberto Hernández-Osorio L, Márquez-Dueñas C, Ambrosio JR, Reynoso-Ducoing O, Hernández R (2011) Trypanosoma cruzi: multiple actin isovariants are observed along different developmental stages. Exp Parasitol 127:249–259

    Article  PubMed  CAS  Google Scholar 

  • Contreras VT, Morel CM, Goldenberg S (1985a) Stage specific gene expression precedes morphological changes during Trypanosoma cruzi metacyclogenesis. Mol Biochem Parasitol 14:83–96

    Article  PubMed  CAS  Google Scholar 

  • Contreras VT, Salles JM, Thomas N, Morel CM, Goldenberg S (1985b) In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol Biochem Parasitol 16:315–327

    Article  PubMed  CAS  Google Scholar 

  • Drygin D, Rice WG, Grummt I (2010) The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu Rev Pharmacol Toxicol 250:131–156

    Google Scholar 

  • Dubner S, Schapachnik E, Riera AR, Valero E (2008) Chagas disease: state-of-the-art of diagnosis and management. Cardiol J 15:493–504

    PubMed  Google Scholar 

  • Dusanic DG (1980) In vitro production of metacyclic trypomastigotes of Trypanosoma cruzi. J Parasitol 66:1046–1049

    Article  PubMed  CAS  Google Scholar 

  • Elias MC, Marques-Porto R, Freymüller E, Schenkman S (2001) Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Mol Biochem Parasitol 112:79–90

    Article  PubMed  CAS  Google Scholar 

  • Engel JC, Franke de Cazzulo BM, Stoppani AO, Cannata JJB, Cazzulo JJ (1987) Aerobic glucose fermentation by Trypanosoma cruzi axenic culture amastigote-like forms during growth and differentiation to epimastigotes. Mol Biochem Parasitol 26:1–10

    Article  PubMed  CAS  Google Scholar 

  • Fampa P, Santos AL, Ramirez MI (2010) Trypanosoma cruzi: ubiquity expression of surface cruzipain molecules in TCI and TCII field isolates. Parasitol Res 107:443–447

    Article  PubMed  Google Scholar 

  • Fraidenraich D, Peña C, Isola EL, Lammel EM, Coso O, Añel AD, Pongor S, Baralle F, Torres HN, Flawia MM (1993) Stimulation of Trypanosoma cruzi adenylyl cyclase by an alpha D-globin fragment from Triatoma hindgut: effect on differentiation of epimastigote to trypomastigote forms. Proc Natl Acad Sci U S A 90:10140–10144

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg S, Rodríguez Ávila A (2011) Aspects of Trypanosoma cruzi stage differentiation. Adv Parasitol 75:285–305

    Article  PubMed  Google Scholar 

  • Henríquez DA, Perez N, Pance A, Bradley C (1993) Mechanisms of protein degradation in Trypanosoma cruzi. Biol Res 26:151–157

    PubMed  Google Scholar 

  • Kollien AH, Schaub GA (1998) Trypanosoma cruzi in the rectum of the bug Triatoma infestans: effects of blood ingestion by the starved vector. AmJTrop Med Hyg 59:166–170

    CAS  Google Scholar 

  • Martínez-Calvillo S, Vizuet-de-Rueda JC, Florencio-Martínez LE, Manning-Cela RG, Figueroa-Angulo EE (2010) Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010:525241

    Article  PubMed  Google Scholar 

  • Martínez-Díaz RA, Escario JA, Nogal-Ruiz JJ, Gómez-Barrio A (2001) Biological characterization of Trypanosoma cruzi strains. Mem Inst Oswaldo Cruz 96:53–59

    Article  PubMed  Google Scholar 

  • Nepomuceno-Mejía T, Lara-Martínez R, Cevallos AM, López-Villaseñor I, Jiménez-García LF, Hernández R (2010) The Trypanosoma cruzi nucleolus: a morphometrical analysis of cultured epimastigotes in the exponential and stationary phases. FEMS Microbiol Lett 313:41–46

    Article  PubMed  Google Scholar 

  • Parodi-Talice A, Monteiro-Goes V, Arrambide N, Avila AR, Duran R, Correa A, Dallagiovanna B, Cayota A, Krieger M, Goldenberg S, Robello C (2007) Proteomic analysis of metacyclic trypomastigotes undergoing Trypanosoma cruzi metacyclogenesis. J Mas Spectom 42:1422–1432

    Article  CAS  Google Scholar 

  • Rangel-Aldao R, Allende O, Triana F, Piras R, Henriquez D, Piras M (1987) Possible role of cAMP in the differentiation of Trypanosoma cruzi. Mol Biochem Parasitol 22:39–43

    Article  PubMed  CAS  Google Scholar 

  • Snapp EL, Landfear SM (1997) Cytoskeletal association is important for differential targeting of glucose transporter isoforms in Leishmania. J Cell Biol 139:1775–1783

    Article  PubMed  CAS  Google Scholar 

  • Soares MJ, Souto-Padrón T, Bonaldo MC, Goldenberg S, de Souza W (1989) A stereological study of the differentiation process in Trypanosoma cruzi. Parasitol Res 75:522–527

    Article  PubMed  CAS  Google Scholar 

  • Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731–745

    Article  PubMed  CAS  Google Scholar 

  • Tanowitz HB, Kirchhoff LV, Simon D, Morris SA, Weiss LM, Wittner M (1992) Chagas’ disease. Clin Microbiol Rev 5:400–419

    PubMed  CAS  Google Scholar 

  • Tanowitz HB, Weiss LM, Montgomery SP (2011) Chagas disease has now gone global. PLoS Negl Trop Dis 5:e1136

    Article  PubMed  Google Scholar 

  • Tonelli RR, da Augusto LS, Castilho BA, Schenkman S (2011) Protein synthesis attenuation by phosphorylation of eIF2α is required for the differentiation of Trypanosoma cruzi into infective forms. PLoS One 6(11):e27904

    Article  PubMed  CAS  Google Scholar 

  • Tyler KM, Engman DM (2000) Flagellar elongation induced by glucose limitation is preadaptive for Trypanosoma cruzi differentiation. Cell Motil Cytoskeleton 46:269–278

    Article  PubMed  CAS  Google Scholar 

  • Urbina JA, Osorno CE, Rojas A (1989) The central role of phosphoenol pyruvate carboxykinase in the energy metabolism of Trypanosoma cruzi. Studies using 3-mercaptopicolinic acid. Mem Inst Oswaldo Cruz 84(Supl II):59

    Google Scholar 

  • Uribina JA (1994) Intermediary metabolism of Trypanosoma cruzi. Parasitol Today 10:107–110

    Article  Google Scholar 

Download references

Acknowledgments

We thank Juliana Herrera López and Patricia de la Torre for technical support and Luis Felipe Jiménez-García and Reyna Lara-Martínez for their qualified assistance with the electron microscope. Tomás Nepomuceno-Mejía was a recipient of a graduate scholarship from CONACyT México. This work was also partly supported by Grants IN228810-3 from DGAPA PAPIIT UNAM and Grant 99062 from CONACYT-Mexico to Roberto Hernández.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roberto Hernández.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hernández, R., Cevallos, A.M., Nepomuceno-Mejía, T. et al. Stationary phase in Trypanosoma cruzi epimastigotes as a preadaptive stage for metacyclogenesis. Parasitol Res 111, 509–514 (2012). https://doi.org/10.1007/s00436-012-2974-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-2974-y

Keywords