Metacaspases and their role in the life cycle of human protozoan parasites
Keywords:
caspases, apoptosis, Plasmodium, Leishmania, Trypanosoma, malaria
Abstract
Metacaspases are caspase-related cysteine-proteases that are present in organisms devoid of caspases such as plants, yeast, and protozoan parasites. Since caspases are important effector molecules in mammalian apoptosis, the possible role of metacaspases in programmed cell death has been evaluated in the organisms where they are expressed. In some species of the human protozoan parasites Trypanosoma spp. and Leishmania spp., metacaspases have been involved in programmed cell death, although a role of metacaspases in recycling processes in T. brucei has also been suggested. Metacaspases are also expressed in Plasmodium spp., however their role in these organisms is still unknown. More than one metacaspase gene is present in some of these parasites, which suggests that these proteins are physiologically redundant or have different functions depending on their localization and protein interactions. The catalytic activity of metacaspases is different from that of caspases—again noting that metacaspase genes are absent in mammals. These characteristics make metacaspases and their activating mechanisms interesting subjects of research in the development of new drug targets for the treatment of trypanosomiasis, leishmaniasis, and malaria. A summary of the literature on metacaspases is provided, and Latin American researchers are encouraged to more actively explore the metacaspase potential.Downloads
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References
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2. Lavrik IN, Golks A, Krammer PH. Caspases: pharmacological manipulation of cell death. J Clin Invest. 2005;115:2665-72.
3. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol. 2004;5:897-907.
4. MacFarlane M, Williams AC. Apoptosis and disease: a life or death decision. EMBO Rep. 2004;5:674-8.
5. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. The C. elegans cell death gene Ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell. 1993;75:641-52.
6. Kumar S, Doumanis J. The fly caspases. Cell Death Differ. 2000;7:1039-44.
7. Debrabant A, Lee N, Bertholet S, Duncan R, Nakhasi HL. Programmed cell death in trypanosomatids and other unicellular organisms. Int J Parasitol. 2003;33:257-67.
8. Koonin EV, Aravind L. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ. 2002;9:394-404.
9. Vercammen D, Declercq W, Vandenabeele P, van Breusegem F. Are metacaspases caspases? J Cell Biol. 2007;179:375-80.
10. Vercammen D, van de Cotte B, De Jaeger G, Eeckhout D, Casteels P, Vandepoele K, et al. Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem. 2004;279:45329-36.
11. Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, Herlan M, et al. A caspase-related protease regulates apoptosis in yeast. Mol Cell. 2002;9:911-7.
12. González IJ, Desponds C, Schaff C, Mottram JC, Fasel N. Leishmania major metacaspase can replace yeast metacaspase in programmed cell death and has arginine-specific cysteine peptidase activity. Int J Parasitol. 2007;37:161-72.
13. Lee N, Gannavaram S, Selvapandiyan A, Debrabant A. Characterization of metacaspases with trypsin-like activity and their putative role in the programmed cell death in the protozoan parasite Leishmania. Eukaryot Cell. 2007;6:1745-57.
14. Trzyna WC, Legras XD, Cordingley JS. A type-1 metacaspase from Acanthamoeba castellanii. Microbiol Res. 2008;163:414-23.
15. Bidle KD, Haramaty L, Barcelos E Ramos J, Falkowski P. Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc Natl Acad Sci USA. 2007;104:6049-54.
16. Okamoto OK, Hastings JW. Genome-wide analysis of redox-regulated genes in a dinoflagellate. Gene. 2003;321:73-81.
17. Herker E, Jungwirth H, Lehmann KA, Maldener C, Frohlich KU, Wissing S, et al. Chronological aging leads to apoptosis in yeast. J Cell Biol. 2004;164:501-7.
18. Bettiga M, Calzari L, Orlandi I, Alberghina L, Vai M. Involvement of the yeast metacaspase Yca1 in ubp10Delta-programmed cell death. FEMS Yeast Res. 2004;5:141-7.
19. Mazzoni C, Herker E, Palermo V, Jungwirth H, Eisenberg T, Madeo F, et al. Yeast caspase 1 links messenger RNA stability to apoptosis in yeast. EMBO Rep. 2005;6:1076-81.
20. Weinberger M, Ramachandran L, Feng L, Sharma K, Sun X, Marchetti M, et al. Apoptosis in budding yeast caused by defects in initiation of DNA replication. J Cell Sci. 2005;118:3543-53.
21. Mitsui K, Nakagawa D, Nakamura M, Okamoto T, Tsurugi K. Valproic acid induces apoptosis dependent of Yca1p at concentrations that mildly affect the proliferation of yeast. FEBS Lett. 2005;579:723-7.
22. Khan MA, Chock PB, Stadtman ER. Knockout of caspase-like gene, YCA1, abrogates apoptosis and elevates oxidized proteins in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 2005;102:17326-31.
23. Wadskog I, Maldener C, Proksch A, Madeo F, Adler L. Yeast lacking the SRO7/SOP1-encoded tumor suppressor homologue show increased susceptibility to apoptosis-like cell death on exposure to NaCl stress. Mol Biol Cell. 2004;15:1436-44.
24. Flower TR, Chesnokova LS, Froelich CA, Dixon C, Witt SN. Heat shock prevents alpha-synuclein-induced apoptosis in a yeast model of Parkinson’s disease. J Mol Biol. 2005;351:1081-100.
25. Silva RD, Sotoca R, Johansson B, Ludovico P, Sansonetty F, Silva MT, et al. Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol. 2005;58:824-34.
26. Ivanovska I, Hardwick JM. Viruses activate a genetically conserved cell death pathway in a unicellular organism. J Cell Biol. 2005;170:391-9.
27. Suarez MF, Filonova LH, Smertenko A, Savenkov EI, Clapham DH, von Arnold S, et al. Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr Biol. 2004;14:R339-40.
28. Hoeberichts FA, ten Have A, Woltering EJ. A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves. Planta. 2003;217:517-22.
29. Watanabe N, Lam E. Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J Biol Chem. 2005;280:14691-9.
30. Richie DL, Miley MD, Bhabhra R, Robson GD, Rhodes JC, Askew DS. The Aspergillus fumigatus metacaspases CasA and CasB facilitate growth under conditions of endoplasmic reticulum stress. Mol Microbiol. 2007;63:591-604.
31. Meslin B, Barnadas C, Boni V, Latour C, De Monbrison F, Kaiser K, et al. Features of apoptosis in Plasmodium falciparum erythrocytic stage through a putative role of PfMCA1 metacaspase-like protein. J Infect Dis. 2007;195:1852-9.
32. Le Chat L, Sinden RE, Dessens JT. The role of metacaspase 1 in Plasmodium berghei development and apoptosis. Mol Biochem Parasitol. 2007;153:41-7.
33. Ambit A, Fasel N, Coombs GH, Mottram JC. An essential role for the Leishmania major metacaspase in cell cycle progression. Cell Death Differ. 2008;15:113-22.
34. Kosec G, Álvarez VE, Aguero F, Sánchez D, Dolinar M, Turk V, et al. Metacaspases of Trypanosoma cruzi: possible candidates for programmed cell death mediators. Mol Biochem Parasitol. 2006;145:18-28.
35. Mottram JC, Helms MJ, Coombs GH, Sajid M. Clan CD cysteine peptidases of parasitic protozoa. Trends Parasitol. 2003;19:182-7.
36. Szallies A, Kubata BK, Duszenko M. A metacaspase of Trypanosoma brucei causes loss of respiration competence and clonal death in the yeast Saccharomyces cerevisiae. FEBS Lett. 2002;517:144-50.
37. Helms MJ, Ambit A, Appleton P, Tetley L, Coombs GH, Mottram JC. Bloodstream form Trypanosoma brucei depend upon multiple metacaspases associated with RAB11-positive endosomes. J Cell Sci. 2006;119:1105-17.
38. Figarella K, Rawer M, Uzcategui N L, Kubata BK, Lauber K, Madeo F, et al. Prostaglandin D2 induces programmed cell death in Trypanosoma brucei bloodstream form. Cell Death Differ. 2005;12:335-46.
39. Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inze D, Delledonne M, et al. Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem. 2007;282:1352-8.
40. Moss CX, Westrop GD, Juliano L, Coombs GH, Mottram JC. Metacaspase 2 of Trypanosoma brucei is a calcium-dependent cysteine peptidase active without processing. FEBS Lett. 2007;581:5635-9.
41. Jäättelä M. Programmed cell death: many ways for cells to die decently. Ann Med. 2002;34:480-8.
42. Bursch W. Multiple cell death programs: Charon’s lifts to Hades. FEMS Yeast Res. 2004;5:101-10.
43. Vaux DL, Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci USA. 1996;93:2239-44.
44. Lee N, Bertholet S, Debrabant A, Muller J, Duncan R, Nakhasi HL. Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ. 2002;9:53-64.
45. Lindoso JA, Cotrim PC, Goto H. Apoptosis of Leishmania (Leishmania) chagasi amastigotes in hamsters infected with visceral leishmaniasis. Int J Parasitol. 2004;34:1-4.
46. Wanderley JL, Benjamin A, Real F, Bonomo A, Moreira ME, Barcinski MA. Apoptotic mimicry: an altruistic behavior in host/Leishmania interplay. Braz J Med Biol Res. 2005;38:807-12.
47. van Zandbergen G, Bollinger A, Wenzel A, Kamhawi S, Voll R, Klinger M, et al. Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci USA. 2006;103:13837-42.
48. Vercammen D, Belenghi B, van de Cotte B, Beunens T, Gavigan JA, De Rycke R, et al. Serpin1 of Arabidopsis thaliana is a suicide inhibitor for metacaspase 9. J Mol Biol. 2006;364:625-36.
2. Lavrik IN, Golks A, Krammer PH. Caspases: pharmacological manipulation of cell death. J Clin Invest. 2005;115:2665-72.
3. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol. 2004;5:897-907.
4. MacFarlane M, Williams AC. Apoptosis and disease: a life or death decision. EMBO Rep. 2004;5:674-8.
5. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. The C. elegans cell death gene Ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell. 1993;75:641-52.
6. Kumar S, Doumanis J. The fly caspases. Cell Death Differ. 2000;7:1039-44.
7. Debrabant A, Lee N, Bertholet S, Duncan R, Nakhasi HL. Programmed cell death in trypanosomatids and other unicellular organisms. Int J Parasitol. 2003;33:257-67.
8. Koonin EV, Aravind L. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ. 2002;9:394-404.
9. Vercammen D, Declercq W, Vandenabeele P, van Breusegem F. Are metacaspases caspases? J Cell Biol. 2007;179:375-80.
10. Vercammen D, van de Cotte B, De Jaeger G, Eeckhout D, Casteels P, Vandepoele K, et al. Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem. 2004;279:45329-36.
11. Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, Herlan M, et al. A caspase-related protease regulates apoptosis in yeast. Mol Cell. 2002;9:911-7.
12. González IJ, Desponds C, Schaff C, Mottram JC, Fasel N. Leishmania major metacaspase can replace yeast metacaspase in programmed cell death and has arginine-specific cysteine peptidase activity. Int J Parasitol. 2007;37:161-72.
13. Lee N, Gannavaram S, Selvapandiyan A, Debrabant A. Characterization of metacaspases with trypsin-like activity and their putative role in the programmed cell death in the protozoan parasite Leishmania. Eukaryot Cell. 2007;6:1745-57.
14. Trzyna WC, Legras XD, Cordingley JS. A type-1 metacaspase from Acanthamoeba castellanii. Microbiol Res. 2008;163:414-23.
15. Bidle KD, Haramaty L, Barcelos E Ramos J, Falkowski P. Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc Natl Acad Sci USA. 2007;104:6049-54.
16. Okamoto OK, Hastings JW. Genome-wide analysis of redox-regulated genes in a dinoflagellate. Gene. 2003;321:73-81.
17. Herker E, Jungwirth H, Lehmann KA, Maldener C, Frohlich KU, Wissing S, et al. Chronological aging leads to apoptosis in yeast. J Cell Biol. 2004;164:501-7.
18. Bettiga M, Calzari L, Orlandi I, Alberghina L, Vai M. Involvement of the yeast metacaspase Yca1 in ubp10Delta-programmed cell death. FEMS Yeast Res. 2004;5:141-7.
19. Mazzoni C, Herker E, Palermo V, Jungwirth H, Eisenberg T, Madeo F, et al. Yeast caspase 1 links messenger RNA stability to apoptosis in yeast. EMBO Rep. 2005;6:1076-81.
20. Weinberger M, Ramachandran L, Feng L, Sharma K, Sun X, Marchetti M, et al. Apoptosis in budding yeast caused by defects in initiation of DNA replication. J Cell Sci. 2005;118:3543-53.
21. Mitsui K, Nakagawa D, Nakamura M, Okamoto T, Tsurugi K. Valproic acid induces apoptosis dependent of Yca1p at concentrations that mildly affect the proliferation of yeast. FEBS Lett. 2005;579:723-7.
22. Khan MA, Chock PB, Stadtman ER. Knockout of caspase-like gene, YCA1, abrogates apoptosis and elevates oxidized proteins in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 2005;102:17326-31.
23. Wadskog I, Maldener C, Proksch A, Madeo F, Adler L. Yeast lacking the SRO7/SOP1-encoded tumor suppressor homologue show increased susceptibility to apoptosis-like cell death on exposure to NaCl stress. Mol Biol Cell. 2004;15:1436-44.
24. Flower TR, Chesnokova LS, Froelich CA, Dixon C, Witt SN. Heat shock prevents alpha-synuclein-induced apoptosis in a yeast model of Parkinson’s disease. J Mol Biol. 2005;351:1081-100.
25. Silva RD, Sotoca R, Johansson B, Ludovico P, Sansonetty F, Silva MT, et al. Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol. 2005;58:824-34.
26. Ivanovska I, Hardwick JM. Viruses activate a genetically conserved cell death pathway in a unicellular organism. J Cell Biol. 2005;170:391-9.
27. Suarez MF, Filonova LH, Smertenko A, Savenkov EI, Clapham DH, von Arnold S, et al. Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr Biol. 2004;14:R339-40.
28. Hoeberichts FA, ten Have A, Woltering EJ. A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves. Planta. 2003;217:517-22.
29. Watanabe N, Lam E. Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J Biol Chem. 2005;280:14691-9.
30. Richie DL, Miley MD, Bhabhra R, Robson GD, Rhodes JC, Askew DS. The Aspergillus fumigatus metacaspases CasA and CasB facilitate growth under conditions of endoplasmic reticulum stress. Mol Microbiol. 2007;63:591-604.
31. Meslin B, Barnadas C, Boni V, Latour C, De Monbrison F, Kaiser K, et al. Features of apoptosis in Plasmodium falciparum erythrocytic stage through a putative role of PfMCA1 metacaspase-like protein. J Infect Dis. 2007;195:1852-9.
32. Le Chat L, Sinden RE, Dessens JT. The role of metacaspase 1 in Plasmodium berghei development and apoptosis. Mol Biochem Parasitol. 2007;153:41-7.
33. Ambit A, Fasel N, Coombs GH, Mottram JC. An essential role for the Leishmania major metacaspase in cell cycle progression. Cell Death Differ. 2008;15:113-22.
34. Kosec G, Álvarez VE, Aguero F, Sánchez D, Dolinar M, Turk V, et al. Metacaspases of Trypanosoma cruzi: possible candidates for programmed cell death mediators. Mol Biochem Parasitol. 2006;145:18-28.
35. Mottram JC, Helms MJ, Coombs GH, Sajid M. Clan CD cysteine peptidases of parasitic protozoa. Trends Parasitol. 2003;19:182-7.
36. Szallies A, Kubata BK, Duszenko M. A metacaspase of Trypanosoma brucei causes loss of respiration competence and clonal death in the yeast Saccharomyces cerevisiae. FEBS Lett. 2002;517:144-50.
37. Helms MJ, Ambit A, Appleton P, Tetley L, Coombs GH, Mottram JC. Bloodstream form Trypanosoma brucei depend upon multiple metacaspases associated with RAB11-positive endosomes. J Cell Sci. 2006;119:1105-17.
38. Figarella K, Rawer M, Uzcategui N L, Kubata BK, Lauber K, Madeo F, et al. Prostaglandin D2 induces programmed cell death in Trypanosoma brucei bloodstream form. Cell Death Differ. 2005;12:335-46.
39. Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inze D, Delledonne M, et al. Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem. 2007;282:1352-8.
40. Moss CX, Westrop GD, Juliano L, Coombs GH, Mottram JC. Metacaspase 2 of Trypanosoma brucei is a calcium-dependent cysteine peptidase active without processing. FEBS Lett. 2007;581:5635-9.
41. Jäättelä M. Programmed cell death: many ways for cells to die decently. Ann Med. 2002;34:480-8.
42. Bursch W. Multiple cell death programs: Charon’s lifts to Hades. FEMS Yeast Res. 2004;5:101-10.
43. Vaux DL, Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci USA. 1996;93:2239-44.
44. Lee N, Bertholet S, Debrabant A, Muller J, Duncan R, Nakhasi HL. Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ. 2002;9:53-64.
45. Lindoso JA, Cotrim PC, Goto H. Apoptosis of Leishmania (Leishmania) chagasi amastigotes in hamsters infected with visceral leishmaniasis. Int J Parasitol. 2004;34:1-4.
46. Wanderley JL, Benjamin A, Real F, Bonomo A, Moreira ME, Barcinski MA. Apoptotic mimicry: an altruistic behavior in host/Leishmania interplay. Braz J Med Biol Res. 2005;38:807-12.
47. van Zandbergen G, Bollinger A, Wenzel A, Kamhawi S, Voll R, Klinger M, et al. Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci USA. 2006;103:13837-42.
48. Vercammen D, Belenghi B, van de Cotte B, Beunens T, Gavigan JA, De Rycke R, et al. Serpin1 of Arabidopsis thaliana is a suicide inhibitor for metacaspase 9. J Mol Biol. 2006;364:625-36.
How to Cite
1.
González IJ. Metacaspases and their role in the life cycle of human protozoan parasites. biomedica [Internet]. 2009 Sep. 1 [cited 2024 May 21];29(3):485-93. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/6
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