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Cell Stress and Chaperones

, Volume 22, Issue 1, pp 15–27 | Cite as

Ultrastructural and physiological changes induced by different stress conditions on the human parasite Trypanosoma cruzi

  • Deyanira Pérez-Morales
  • Karla Daniela Rodríguez Hernández
  • Ignacio Martínez
  • Lourdes Teresa Agredano-Moreno
  • Luis Felipe Jiménez-García
  • Bertha EspinozaEmail author
Original Paper

Abstract

Trypanosoma cruzi is the etiological agent of Chagas disease. The life cycle of this protozoan parasite is digenetic because it alternates its different developmental forms through two hosts, a vector insect and a vertebrate host. As a result, the parasites are exposed to sudden and drastic environmental changes causing cellular stress. The stress response to some types of stress has been studied in T. cruzi, mainly at the molecular level; however, data about ultrastructure and physiological state of the cells in stress conditions are scarce or null. In this work, we analyzed the morphological, ultrastructural, and physiological changes produced on T. cruzi epimastigotes when they were exposed to acid, nutritional, heat, and oxidative stress. Clear morphological changes were observed, but the physiological conditions varied depending on the type of stress. The maintenance of the physiological state was severely affected by heat shock, acidic, nutritional, and oxidative stress. According to the surprising observed growth recovery after damage by stress alterations, different adaptations from the parasite to these harsh conditions were suggested. Particular cellular death pathways are discussed.

Keywords

Trypanosoma cruzi Stress Physiological damage Apoptosis 

Notes

Acknowledgments

This work was supported by DGAPA, UNAM, grant number IN206512. PMD received a scholarship from CONACYT during her PhD studies. We thank Dr. Ruben Arroyo-Olarte for his valuable comments and the help in the English review.

Supplementary material

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References

  1. Alvarez EV, Kosec G, SantÁnna C, Turk V, Cazzulo JJ, Turk B (2008) Autophagy is involved in nutritional stress response and differentiation in Trypanosoma cruzi. J Biol Chem 283:3454–3464CrossRefPubMedGoogle Scholar
  2. Batista DG, Pacheco MG, Kumar A, Branowska D, Ismail MA, Hu L, Boykin DW, Soeiro MN (2010) Biological, ultrastructural effect and subcellular localization of aromatic diamidines in Trypanosoma cruzi. Parasitology 137:251–259CrossRefPubMedGoogle Scholar
  3. Bera A, Singh S, Nagaraj R, Vaidya T (2003) Induction of autophagic cell death in Leishmania donovani by antimicrobial peptides. Mol Biochem Parasitol 127:23–35CrossRefPubMedGoogle Scholar
  4. Carnieri EG, Moreno SN, Docampo R (1993) Trypanothione-dependent peroxide metabolism in Trypanosoma cruzi different stages. Mol Biochem Parasitol 61:79–86CrossRefPubMedGoogle Scholar
  5. Cassola A, De Gaudenzi JG, Frasch AC (2007) Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol Microbiol 65:655–670CrossRefPubMedGoogle Scholar
  6. Castillo JL, Reynolds SE, Eleftherianos I (2011) Insect immune responses to nematode parasites. Trends Parasitol 27:537–547CrossRefPubMedGoogle Scholar
  7. Chiari E, Camargo EP (1984) Culturing and cloning of Trypanosoma cruzi. In: Morel M (ed) Genes and Antigens of Parasite. Institute Oswaldo Cruz, Río de Janeiro, BrazilGoogle Scholar
  8. Contreras VT, Salles JM, Thomas N, Morel CM, Goldenberg S (1985) In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol Biochem Parasitol 16:315–327CrossRefPubMedGoogle Scholar
  9. Cyrino LT, Araújo AP, Joazeiro PP, Vicente CP, Giorgio S (2012) In vivo and in vitro Leishmania amazonensis infection induces autophagy in macrophages. Tissue Cell 44:401–408CrossRefPubMedGoogle Scholar
  10. Das M, Mukherjee SB, Shaha C (2001) Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J Cell Sci 114:2461–2469PubMedGoogle Scholar
  11. de Souza W, Sant'Anna C, Cunha-e-Silva NL (2009) Electron microscopy and cytochemistry analysis of the endocytic pathway of pathogenic protozoa. Prog Histochem Cytochem 44(2):67--124. doi: 10.1016/j.proghi.2009.01.001. Epub 2009 Apr 5
  12. Dost CK, Saraiva J, Monesi N, Zentgraf U, Engels W, Albuquerque S (2004) Six Trypanosoma cruzi strains characterized by specific gene expression patterns. Parasitol Res 94:134–140PubMedGoogle Scholar
  13. Espinoza B, Rico T, Sosa S, Oaxaca E, Vizcano-Castillo A, Caballero ML, Martínez I (2010) Mexican Trypanosoma cruzi TCI strains with different virulence induce diverse humoral and cellular immune response in murine experimental infection. J Biomed Biotech. doi: 10.1155/2010/890672 Google Scholar
  14. Finzi JK, Chiavegatto CWM, Corat KF, López JA, Cabrera OG, Mielniczki-Pereia AA, Colli W, Alves MJM, Gadelha FR (2004) Trypanosoma cruzi response to the oxidative stress generated by hydrogen peroxide. Mol Biochem Parasitol 133:37–43CrossRefPubMedGoogle Scholar
  15. Fozo EM, Quivey RG Jr (2004) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70:929–936CrossRefPubMedPubMedCentralGoogle Scholar
  16. Grela E, Ząbek A, Grabowiecka A (2015) Interferences in the Optimization of the MTT Assay for Viability Estimation of Proteus mirabilis. Avicenna J Med Biotechnol 7:159–167PubMedPubMedCentralGoogle Scholar
  17. Hall BF (1993) Trypanosoma cruzi: mechanisms for entry into host cells. Sem Cell Biol 4:323–333CrossRefGoogle Scholar
  18. Jiménez-García LF, Segura-Valdéz ML (2004) Visualizing nuclear structure in situ by atomic force microscopy. Meth Mol Biol 242:191–199Google Scholar
  19. Kollien A, Schaub GA (1998) Trypanosoma cruzi in the rectum of the bug Triatoma infestans: effects of blood ingestion by the starved vector. Am J Trop Med Hyg 59:166–170PubMedGoogle Scholar
  20. Kollien AH, Grospietsch T, Kleffmann T, Zerbst-Boroffka I, Schaub GA (2001) Ionic composition of the rectal contents and excreta of the reduviid bug Triatoma infestans. J Insec Physiol 47:739–747CrossRefGoogle Scholar
  21. Lazarin-Bidóia D, Desoti VC, Ueda-Nakamura T, Dias Filho BP, Nakamura CV, Silva SO (2013) Further evidence of the trypanocidal action of eupomatenoid-5: confirmation of involvement of reactive oxygen species and mitochondria owing to a reduction in trypanothione reductase activity. Free Rad Biol Med 60:17–28CrossRefPubMedGoogle Scholar
  22. Lazarin-Bidóia D, Desoti VC, Martins SC, Ribeiro FM, Ud Din Z, Rodrigues-Filho E, Ueda-Nakamura T, Nakamura CV, de Oliveira Silva S (2016) Dibenzylideneacetones are potent trypanocidal compounds that affect the Trypanosoma cruzi redox system. Antimicrob Agents Chemother 60:890–903CrossRefPubMedPubMedCentralGoogle Scholar
  23. Machado-Silva A, Cerqueira PG, Graziell-Silva V, Gadelha FR, Peloso-Ede F, Teixeira SM, Machado CR (2016) How Trypanosoma cruzi deals with oxidative stress: antioxidant defense and DNA repair patways. Mutat Res Rev Mutat Res 767:8–22CrossRefPubMedGoogle Scholar
  24. Martins RM, Covarrubias C, Rojas RG, Silber AM, Yoshida N (2009) Use of L-proline and ATP production by Trypanosoma cruzi metacyclic forms as requirements for host cell invasion. Infec Imm 77:3023–3032CrossRefGoogle Scholar
  25. Matthews KR (2011) Controlling and coordinating development in vector-transmitted parasites. Science 331:1149–1153CrossRefPubMedGoogle Scholar
  26. Mayorga-Reyes L, Bustamante-Camilo P, Gutiérrez-Nava A, Barranco-Florido E, Azaola-Espinosa A (2009) Crecimiento, sobrevivencia y adaptación de Bifidobacterium infantis a condiciones ácidas. Revista Mexicana de Ingeniería Química 8:259–264Google Scholar
  27. Menna-Barreto RF, Corrêa JR, Cascabulho CM, Fernandes MC, Pinto AV, Soares MJ, De Castro SL (2009a) Naphthoimidazoles promote different death phenotypes in Trypanosoma cruzi. Parasitology 136:499–510CrossRefPubMedGoogle Scholar
  28. Menna-Barreto RF, Salomão K, Dantas AP, Santa-Rita RM, Soares MJ, Barbosa HS, de Castro SL (2009b) Different cell death pathways induced by drugs in Trypanosoma cruzi: an ultrastructural study. Micron 40:157–168CrossRefPubMedGoogle Scholar
  29. Mielniczki-Pereira AA, Chiavegatto CM, López JA, Colli W, Alves MJ, Gadelha FR (2007) Trypanosoma cruzi strains, Tulahuen 2 and Y, besides the difference in resistance to oxidative stress, display differential glucose-6-phosphate and 6-phosphogluconate dehydrogenases activities. Acta Trop 101:54–60CrossRefPubMedGoogle Scholar
  30. Mofarrahi M, Sigala I, Guo Y, Godin R, Davis EC, Petrof B, Sandri M, Burelle Y, Hussain SN (2012) Autophagy and skeletal muscles in sepsis. PLoS One 7:e47265CrossRefPubMedPubMedCentralGoogle Scholar
  31. Moreira ME, Del Portillo HA, Milder RV, Balanco JM, Barcinski MA (1996) Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis. J Cell Physiol 167:305–313CrossRefPubMedGoogle Scholar
  32. Názer E, Verdún RE, Sánchez DO (2012) Severe heat shock induces nucleolar accumulation of mRNAs in Trypanosoma cruzi. PLoS One 7:e43715CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nogueira NP, Saraiva FMS, Sultano PE, Cunha PRBB, Laranja GAT, Justo GA, Sabino KCC, Coelho MGP, Rossini A, Atella GC, Paes MC (2015) Proliferation and differentiation of Trypanosoma cruzi inside its vector have a new trigger: redox status. Plos One. doi: 10.1371/journal.pone.0116712 Google Scholar
  34. Nolan DP, Rolin S, Rodriguez JR, Van Den Abbeele J, Pays E (2000) Slender and stumpy bloodstream forms of Trypanosoma brucei display a differential response to extracellular acidic and proteolytic stress. Eur J Biochem 267:18–27CrossRefPubMedGoogle Scholar
  35. Olson CL, Nadeau KC, Sullivan MA, Winquist AG, Donelson JE, Walsh CT, Engmann DM (1994) Molecular and biochemical comparison of the 70-kDa heat shock proteins of Trypanosoma cruzi. J Biol Chem 269:3868–3874PubMedGoogle Scholar
  36. Pérez-Morales D, Ostoa-Saloma P, Espinoza B (2009) Trypanosoma cruzi SHSP16: characterization of an α-crystallin small heat shock protein. Exp Parasitol 123:182–189CrossRefPubMedGoogle Scholar
  37. Piacenza L, Alvarez MN, Peluffo G, Radi R (2009) Fighting the oxidative assault: the Trypanosoma cruzi journey to infection. Curr Opinion Microbiol 12:415–421CrossRefGoogle Scholar
  38. Piacenza L, Peluffo G, Alvárez MN, Martínez A, Radi R (2013) Trypanosoma cruzi antioxidant enzymes as virulent factors in Chagas Disease. Antox Redox Signal 19:723–734CrossRefGoogle Scholar
  39. Raff M (1998) Cell suicide for beginners. Nature 396:119–122CrossRefPubMedGoogle Scholar
  40. Reggiori F, Klionsky DJ (2002) Autophagy in the eukaryotic cell. Euk Cell 1:11–21CrossRefGoogle Scholar
  41. Requena JM, Jimenez-Ruiz A, Soto M, Assiego R, Santarén JF, López MC, Patarroyo ME, Alonso C (1992) Regulation of hsp70 expression in Trypanosoma cruzi by temperature and growth phase. Mol Biochem Parasitol 53:201–212CrossRefPubMedGoogle Scholar
  42. Ricci MS, Zong WX (2006) Chemotherapeutic approaches for targeting cell death pathways. Oncologist 11:342–357CrossRefPubMedPubMedCentralGoogle Scholar
  43. Sandes JM, Fontes A, Regis-da-Silva CG, de Castro MCAB, Lima-Junior CG, Silva FPL et al (2014) Trypanosoma cruzi cell death induced by the Morita-Baylis-Hillman adduct 3-Hydroxy-2-Methylene-3-(4-Nitrophenylpropanenitrile). PLoS One 9(4):e93936CrossRefPubMedPubMedCentralGoogle Scholar
  44. Santos AO, Santin AC, Yamaguchi MU, Cortez LE, Ueda-Nakamura T, Dias-Filho BP, Nakamura CV (2010) Antileishmanial activity of an essential oil from the leaves and flowers of Achillea millefolium. Ann Trop Med Parasitol 104:475–483CrossRefPubMedGoogle Scholar
  45. Souquere S, Mollet S, Kress M, Dautry F, Pierron G, Weil D (2009) Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J Cell Sci 122:3619–3626CrossRefPubMedGoogle Scholar
  46. Thammavongs B, Denou E, Missous G, Guéguen M, Panoff JM (2008) Response to environmental stress as a global phenomenon in biology: the example of microorganisms. Micro Environ 23:20–23CrossRefGoogle Scholar
  47. Vassar Stats: Statistical computational Web site. http://vassarstats.net/
  48. Veiga-Santos P, Barrias ES, Santos JF, de Barros Moreira TL, de Carvalho TM, Urbina JA, de Souza W (2012) Effects of amiodarone and posaconazole on the growth and ultrastructure of Trypanosoma cruzi. Inter. J. Antimicrobial Agents 40:61–71CrossRefGoogle Scholar
  49. Vieira LL (1998) pH and volume homeostasis in trypanosomatids: current views and perspectives. Biochim Biophys Acta 1376:221–224CrossRefPubMedGoogle Scholar
  50. Volpato H, Desoti VC, Valdez RH, Ueda-Nakamura T, Silva SO, Sarragiotto MH et al (2015) Mitochondrial Dysfunction Induced by N-Butyl-1-(4-Dimethylamino) Phenyl-1, 2,3,4-Tetrahydro-β-Carboline-3-Carboxamide Is Required for Cell Death of Trypanosoma cruzi. PLoS One 10(6):e0130652. doi: 10.1371/journal.pone.0130652 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Webster DL, Watson K (1993) Ultrastructural changes in yeast following heat shock and recovery. Yeast 9:1165–1175CrossRefPubMedGoogle Scholar
  52. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3050–3060CrossRefGoogle Scholar
  53. WHO (2015) Chagas disease. (http://www.who.int/mediacentre/factsheets/fs340/en/). Accessed on September 4th, 2015.
  54. Wilkinson SR, Taylor MC, Touitha S, Mauricio IL, Meyer D, Kelly J (2002) TcGPXII a glutathione-dependent Trypanosoma cruzi peroxidase with substrate specificity restricted to fatty acid and phospholipid hydroperoxides is localized to the endoplasmic reticulum. Biochem J 364:787–794CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wyllie AH, Kerr JFK, Currie AR (1980) Cell death. The significance of apoptosis. Inf Rev Cytol 68:251–306CrossRefGoogle Scholar

Copyright information

© Cell Stress Society International 2016

Authors and Affiliations

  • Deyanira Pérez-Morales
    • 1
  • Karla Daniela Rodríguez Hernández
    • 1
  • Ignacio Martínez
    • 1
  • Lourdes Teresa Agredano-Moreno
    • 2
  • Luis Felipe Jiménez-García
    • 2
  • Bertha Espinoza
    • 1
    Email author
  1. 1.Laboratorio de Estudios sobre Tripanosomiasis. Departamento de Inmunología, Instituto de Investigaciones BiomédicasUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMéxico
  2. 2.Departamento de Biología Celular, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMéxicoMéxico

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