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Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

Programmed cell death (PCD) is not confined to mammals and is extremely widespread, possibly universal, in multicellular animals. It is now evident that PCD also occurs in single-celled organisms and it is an important feature of host-pathogen relationships. Protists are capable of eliciting an apoptotic response in several circumstances. Studies are in course in order to establish whether these organism share some or all of the effectors and regulators common to multicellular PCD or have evolved their own divergent pathways. Trichomonads are amitochondrial protists that inhabit different ecological niches. Among them Tritrichomonas foetus, a cattle parasite and Trichomonas vaginalis, a human parasite, are the most important because they cause trichomoniasis, a sexually transmitted disease. They do not possess mitochondria, but harbor another type of membrane-bounded organelle, an unusual anaerobic energy-producing organelle called hydrogenosome. Studies of cell death in trichomonads are under way in order to establish whether the hydrogenosome could represent an alternative to mitochondria whether these organisms possess all caspase activities and which conditions lead trichomonads to cell death. In these organisms the known “mitochondrial cell death machinery” is supposed to be distinct from mitochondrial eukaryotes. The presence of a cell death program in trichomonads suggests the existence either of a dependent or independent caspase-like execution pathway in such organisms. Dramatic changes in trichomonad morphology are observed when the cells are under stress, such as after drug treatment and nutrient depletion. These changes include intense plasma membrane and nuclear envelope blebbing, nucleus fragmentation, an abnormal number of oversized vacuoles and altered hydrogenosomes. DNA fragmentation, exposure of phosphatidylserine (PS) in the outer leaflet of the plasma membrane, hydrogenosomal membrane potential dissipation, are features observed in apoptotic cells. Trichomonads also present autophagic processes, observed when altered hydrogenosomes, misshapen flagella, abnormal cellular elements and tubulin precipitates are located in autophagic vacuoles, which are limited by a double or multiple concentric membrane. In all stress situations, trichomonads form pseudocysts, cells with internalized flagella. Different forms of cell death, such as apoptosis, autophagy and necrosis have been shown to exist in trichomonads and so the possibility of the existence of different pathways to cell death in trichomonads is raised.

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References

  1. Chose O, Noel C, Gerbod D et al. A form of cell death with some features resembling apoptosis in the amitochondrial unicellular organism Trichomonas vaginalis. Exp Cell Res 2002; 276:32–39.

    Article  PubMed  CAS  Google Scholar 

  2. Benchimol M. Hydrogenosome autophagy: an ultrastructural and cytochemical study. Biol Cell 1999; 91:165–174.

    Article  PubMed  CAS  Google Scholar 

  3. Benchimol M. Hydrogenosome morphological variation induced by fibronectin and other drugs in Trichomonas vaginalis and Tritrichomonas foetus. Parasitol Res 2001; 87:215–222.

    Article  PubMed  CAS  Google Scholar 

  4. Mariante RM, Guimarães CA, Linden R et al. Hydrogen peroxide induces caspase activation and programmed cell death in the amitochondrial Tritrichomonas foetus. Histochem Cell Biol 2003; 120:129–141.

    Article  PubMed  CAS  Google Scholar 

  5. Mariante RM, Vancini R, Benchimol M. Cell death in Trichomonads: new insights. Histochem Cell Biol 2005; 5:1–12.

    Google Scholar 

  6. Benchimol M, Mariante RM, Ribeiro KC et al. Structure and Division of the Golgi complex in Trichomonas vaginalis and Tritrichomonas foetus. Eur J Cell Biol 2001; 80:593–607.

    Article  PubMed  CAS  Google Scholar 

  7. Granger BL, Warwood SJ, Benchimol M et al. Transient invagination of flagella by Tritrichomonas foetus. Parasitol Res 2000; 86:699–709.

    Article  PubMed  CAS  Google Scholar 

  8. Pereira AN, Ribeiro KC, Benchimol M. Pseudocysts in Trichomonads-new insights. Protist 2003; 154:313–327.

    Article  Google Scholar 

  9. Mauel J, Schnyder J, Baggiolini M. Intracellular parasite killing induced by electron carriers. II. Correlation between parasite killing and the induction of oxidative events in macrophages. Mol Biochem Parasitol 1984; 13:97–110.

    Article  PubMed  CAS  Google Scholar 

  10. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 1997; 326:1–16.

    PubMed  CAS  Google Scholar 

  11. Sahara S, Aoto M, Eguchi Y et al. Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature 1999; 401:168–173.

    Article  PubMed  CAS  Google Scholar 

  12. Lazebnik YA, Takahashi A, Moir RD et al. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc Natl Acad Sci USA 1995; 92:9042–9046.

    Article  PubMed  CAS  Google Scholar 

  13. Takahashi A, Alnemri ES, Lazebnik YA et al. Cleavage of lamin A by Mch2 alpha but not CPP32: multiple interleukin 1 beta-converting enzymerelated proteases with distinct substrate recognition properties are active in apoptosis. Proc Natl Acad Sci USA 1996; 93:8395–8400.

    Article  PubMed  CAS  Google Scholar 

  14. Mukherjee SB, Das M, Sudhandiran G et al. Increase in cytosolic Ca2+ levels through the activation of nonselective cation channels induced by oxidative stress causes mitochondrial depolarization leading to apoptosis-like death in Leishmania donovani promastigotes. J Biol Chem 2002; 277:24717–24722.

    Article  PubMed  CAS  Google Scholar 

  15. Madeiro RF, Benchimol B. The effect of drugs in T. foetus. Parasitol Res 2004; 92:159–170.

    Article  Google Scholar 

  16. Müller M. Structure. In: Honigberg BM, ed. Trichomonads parasitic in humans. New York: Springer-Verlag, 1990:5–35.

    Google Scholar 

  17. Benchimol M, De Souza W. Fine structure and cytochemistry of the hydrogenosome of Tritrichomonas foetus. J Protozool 1983; 30:422–425.

    PubMed  CAS  Google Scholar 

  18. Benchimol M, Johnson PJ, de Souza W. Morphogenesis of the hydrogenosome: an ultrastructural study. Biol Cell 1996; 87:197–205.

    Article  PubMed  CAS  Google Scholar 

  19. Johnson PJ, Lahti CJ, Bradley PJ. Biogenesis of the hydrogenosome in the anaerobic protist Trichomonas vaginalis. J Parasitol 1993; 79:664–670.

    Article  PubMed  CAS  Google Scholar 

  20. Rosa IA, Einicker-Lamas M, Bernardo RR et al. Cardiolipin in Hydrogenosomes: Evidence of Symbiotic Origin. Eukaryot Cell 2006; 5:784–787.

    Article  CAS  Google Scholar 

  21. Lindmark DG, Müller M. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus and its role in pyruvate metabolism. J Biol Chem 1973; 248:7724–7728.

    PubMed  CAS  Google Scholar 

  22. Clemens DL, Johnson PJ. Failure to detect DNA in hydrogenosomes of Trichomonas vaginalis by nick translation and immunomicroscopy. Mol Biochem Parasitol 2000; 106:307–313.

    Article  PubMed  CAS  Google Scholar 

  23. Embley TM, Horner DA, Hirt RP. Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria. TREE 1997; 12:433–441.

    Google Scholar 

  24. Dyall SD, Koehler CM, Delgadillo-Correa MG et al. Presence of a member of the mitochondrial carrier family in hydrogenosomes: Conservation of membrane-targeting pathways between hydrogenosomes and mitochondria. Mol Cell Biol 2000; 20:2488–2497.

    Article  PubMed  CAS  Google Scholar 

  25. Arnoult D, Tatischeff I, Estaquier J et al. On the evolutionary conservation of the cell death pathway: mitochondrial release of an apoptosis-inducing factor during dictyostelium discoideum cell death. Mol Biol Cell 2001; 12:3016–3030.

    PubMed  CAS  Google Scholar 

  26. Arnoult D, Akarid K, Grodet A et al. On the evolution of programmed cell death: apoptosis of the unicellular eukaryote Leishmania major involves cysteine proteinase activation and mitochondrion permeabilization. Cell Death Differ 2002; 9:65–81

    Article  PubMed  CAS  Google Scholar 

  27. Lee N, Bertholet S, Debrabant A et al. Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ 2002; 9:53–64.

    Article  PubMed  CAS  Google Scholar 

  28. Sen N, Das BB, Gaguly A et al. Camptothecin-induced imbalance in intracellular cation homeostasis regulates programmed cell death in unicellular hemoflagellate Leishmania donovan. J Biol Chem 2004; 279:52366–52375.

    Article  PubMed  CAS  Google Scholar 

  29. Brenner C, Kroemer G. Apoptosis. Mitochondria: the death signal integrators. Science 2000; 289:1150–1151.

    Article  PubMed  CAS  Google Scholar 

  30. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med 2000; 6:513–519.

    Article  PubMed  CAS  Google Scholar 

  31. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998; 281:1309–1312.

    Article  PubMed  CAS  Google Scholar 

  32. Loeffler M, Kroemer G. The mitochondrion in cell death control: certainties and incognita. Exp Cell Res 2000; 256:19–26.

    Article  PubMed  CAS  Google Scholar 

  33. Ferri KF, Kroemer GK. Organelle-specific initiation of cell death pathways. Nat Cell Biol 2001; 3: E255–E263.

    Article  PubMed  CAS  Google Scholar 

  34. Lindmark DG, Müller M. Superoxide dismutase in the anaerobic flagellates, Tritrichomonas foetus and Monocercomonas sp. J Biol Chem 1974; 249:4634–4637.

    PubMed  CAS  Google Scholar 

  35. Page-Sharp M, Behm CA, Smith GD. Tritrichomonas foetus and Trichomonas vaginalis: the pattern of inactivation of hydrogenase activity by oxygen and activities of catalase and ascorbate peroxidase. Microbiology 1996; 142:207–211.

    Article  PubMed  CAS  Google Scholar 

  36. Ryley JF. Studies on the metabolism of the protozoa. 5. Metabolism of the parasitic flagellate Tritrichomonas foetus. Biochem J 1955; 59:361–369.

    PubMed  CAS  Google Scholar 

  37. Müller M. Biochemical cytology of trichomonad flagellates. I. Subcellular localization of hydrolases, dehydrogenases and catalase in Tritrichomonas foetus. J Cell Biol 1973; 57:453–474.

    Article  PubMed  Google Scholar 

  38. Benchimol M, Almeida JCA, de Souza W. Further studies on the organization of the hydrogenosome in Tritrichomonas foetus. Tissue Cell 1996; 28:287–299.

    Article  PubMed  CAS  Google Scholar 

  39. Sesso A, Fujiwara DT, Jaeger M et al. Structural elements common to mitosis and apoptosis. Tissue Cell 1999; 31:357–371.

    Article  PubMed  CAS  Google Scholar 

  40. Mancini M, Machamer CE, Roy S et al. Caspase-2 is localized at the Golgi complex and cleaves golgin-160 during apoptosis. J Cell Biol 2000; 149:603–612.

    Article  PubMed  CAS  Google Scholar 

  41. Lane JD, Lucocq J, Pryde J et al. Caspase-mediated cleavage of the stacking protein GRASP65 is required for Golgi fragmentation during apoptosis. J Cell Biol 2002; 156:495–509.

    Article  PubMed  CAS  Google Scholar 

  42. Chiu R, Novikov L, Mukherjee S et al. A caspase cleavage fragment of p115 induces fragmentation of the Golgi apparatus and apoptosis. J Cell Biol 2002; 159:637–648.

    Article  PubMed  CAS  Google Scholar 

  43. Ribeiro KC, Monteiro-Leal LH, Benchimol M. Contributions of the axostyle and flagella to the closed mitosis of Tritrichomonas foetus and Trichomonas vaginalis. J Euk Microbiol 2000; 47:481–492.

    Article  PubMed  CAS  Google Scholar 

  44. Ribeiro KC, Vetö Arnholdt AC, Benchimol M. Tritrichomonas foetus: induced synchrony by hydroxyurea. Parasitol Res 2002; 88:627–631.

    Article  PubMed  Google Scholar 

  45. Edinger AL, Thompson CB Death by design: apoptosis, necrosis and autophagy. Cur Opin Cell Biol 2004; 16:663–669.

    Article  CAS  Google Scholar 

  46. Kitanaka C, Kuchino Y. Caspase-independent programmed cell death with necrotic morphology. Cell Death Differ 1999; 6:508–515.

    Article  PubMed  CAS  Google Scholar 

  47. Lockshin RA, Zakeri Z. Apoptosis, autophagy and more. Int J Biochem Cell Biol 2004; 36: 2405–2419.

    Article  PubMed  CAS  Google Scholar 

  48. Benchimol M, Almeida AJC, Lins U et al. Electron microscopy study of the effect of zinc in Tritrichomonas foetus. Antimicrob Agents Chemoth 1993; 2722–2726.

    Google Scholar 

  49. Sperandio S, de Belle I, Bredesen DE. An alternative non-apoptotic form of programmed cell death. Proc Natl Acad Sci 2000; 96:14376–14391.

    Article  Google Scholar 

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Correspondence to Marlene Benchimol .

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© 2008 Landes Bioscience and Springer Science+Business Media

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Benchimol, M. (2008). Cell Death in Trichomonads. In: Programmed Cell Death in Protozoa. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/978-0-387-76717-8_9

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