Apoptotic markers in protozoan parasites

Parasites and Vectors

Volumn 3, Issue 1, 2010, Pages

  Jiménez Ruiz, Antonio ^a   Alzate, Juan Fernando ^b   MacLeod, Ewan Thomas ^c   Lüder, Carsten Günter Kurt ^d   Fasel, Nicolas ^e   Hurd, Hilary ^f  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

^f KEELE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CELL MARKER; CYTOCHROME C; NUCLEASE; PHOSPHATIDYLSERINE;

APOPTOSIS; BLASTOCYSTIS HOMINIS; CELL ACTIVITY; CELL MEMBRANE; CELL STRUCTURE; CELL SURFACE; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; DNA DEGRADATION; DNA FRAGMENTATION; ENTAMOEBA HISTOLYTICA; ENZYME ACTIVATION; ENZYME ACTIVITY; GIARDIA LAMBLIA; LEISHMANIA; LEISHMANIA DONOVANI; LEISHMANIA INFANTUM; LEISHMANIA MAJOR; LEISHMANIA MEXICANA; MEMBRANE PERMEABILITY; METAZOON; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PROTOZOON; REVIEW; TOXOPLASMA GONDII; TRICHOMONAS VAGINALIS; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

METAZOA; PROTOZOA;

EID: 78049520841     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-3-104     Document Type: Review

References (81)

1. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. G Kroemer L Galluzzi P Vandenabeele J Abrams ES Alnemri EH Baehrecke MV Blagosklonny WS El-Deiry P Golstein DR Green M Hengartner RA Knight S Kumar SA Lipton W Malorni G Nũez ME Peter J Tschopp J Yuan M Piacentini B Zhivotovsky G Melino Nomenclature Committee on Cell Death 2009, Cell Death Differ 2009 16 3 11 10.1038/cdd.2008.150 18846107
2. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. L Galluzzi SA Aaronson J Abrams ES Alnemri DW Andrews EH Baehrecke NG Bazan MV Blagosklonny K Blomgren C Borner, et al. Cell Death Differ 2009 16 1093 1107 10.1038/cdd.2009.44 19373242
3. Apoptosis in a unicellular eukaryote (Trypanosoma cruzi): implications for the evolutionary origin and role of programmed cell death in the control of cell proliferation, differentiation and survival. JC Ameisen T Idziorek O Billaut-Mulot M Loyens JP Tissier A Potentier A Ouaissi, Cell Death Differ 1995 2 285 300 17180034
4. Apoptosis in procyclic Trypanosoma brucei rhodesiense in vitro. SC Welburn C Dale D Ellis R Beecroft TW Pearson, Cell Death Differ 1996 3 229 236 17180087
5. Programmed cell death in unicellular parasites: a prerequisite for sustained infection? G van Zandbergen CG Luder V Heussler M Duszenko, Trends Parasitol 26 477 483 10.1016/j.pt.2010.06.008 20591738
6. The major cell surface glycoprotein procyclin is a receptor for induction of a novel form of cell death in African trypanosomes in vitro. TW Pearson RP Beecroft SC Welburn S Ruepp I Roditi KY Hwa PT Englund CW Wells NB Murphy, Mol Biochem Parasitol 2000 111 333 349 10.1016/S0166-6851(00)00327-3 11163441
7. Death of a trypanosome: a selfish altruism. M Duszenko K Figarella ET Macleod SC Welburn, Trends Parasitol 2006 22 536 542 10.1016/j.pt.2006.08.010 16942915
8. Persistent ER stress induces the spliced leader RNA silencing pathway (SLS), leading to programmed cell death in Trypanosoma brucei. H Goldshmidt D Matas A Kabi S Carmi R Hope S Michaeli, PLoS Pathog 2010 6 1000731 10.1371/journal.ppat.1000731 20107599
9. Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. KA Robinson SM Beverley, Mol Biochem Parasitol 2003 128 217 228 10.1016/S0166-6851(03)00079-3 12742588
10. Exogenous nitric oxide induces apoptosis in Toxoplasma gondii tachyzoites via a calcium signal transduction pathway. BW Peng J Lin JY Lin MS Jiang T Zhang, Parasitology 2003 126 541 550 12866791
11. Cell volume regulatory ion channels in cell proliferation and cell death. F Lang M Foller K Lang P Lang M Ritter A Vereninov I Szabo SM Huber E Gulbins, Methods Enzymol 2007 428 209 225 full-text 17875419
12. Heat-induced programmed cell death in Leishmania infantum is reverted by Bcl-X(L) expression. JF Alzate A Alvarez-Barrientos VM Gonzalez A Jimenez-Ruiz, Apoptosis 2006 11 161 171 10.1007/s10495-006-4570-z 16502255
13. Apoptosis related to chloroquine sensitivity of the human malaria parasite Plasmodium falciparum. S Picot J Burnod V Bracchi BF Chumpitazi P Ambroise-Thomas, Trans R Soc Trop Med Hyg 1997 91 590 591 10.1016/S0035-9203(97) 90039-0 9463676
14. Features of apoptosis in Plasmodium falciparum erythrocytic stage through a putative role of PfMCA1 metacaspase-like protein. B Meslin C Barnadas V Boni C Latour F De Monbrison K Kaiser S Picot, J Infect Dis 2007 195 1852 1859 10.1086/518253 17492602
15. Asexual blood stages of Plasmodium falciparum exhibit signs of secondary necrosis, but not classical apoptosis after exposure to febrile temperature (40 C). H Porter MJ Gamette DG Cortes-Hernandez JB Jensen, J Parasitol 2008 94 473 480 10.1645/GE-1343.1 18564748
16. Plasmodium falciparum: erythrocytic stages die by autophagic-like cell death under drug pressure. PR Totino CT Daniel-Ribeiro S Corte-Real Ferreira-da-Cruz M de Fatima, Exp Parasitol 2008 118 478 486 10.1016/j.exppara.2007.10.017 18226811
17. Apoptosis in the malaria protozoan, Plasmodium berghei: a possible mechanism for limiting intensity of infection in the mosquito. EM Al-Olayan GT Williams H Hurd, Int J Parasitol 2002 32 1133 1143 10.1016/S0020-7519(02)00087-5 12117496
18. Binding of recombinant annexin V to endothelial cells: effect of annexin V binding on endothelial-cell-mediated thrombin formation. WL van Heerde S Poort Veer C van 't CP Reutelingsperger PG de Groot, Biochem J 1994 302 Pt 1 305 312 8068019
19. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. SJ Martin CP Reutelingsperger AJ McGahon JA Rader RC van Schie DM LaFace DR Green, J Exp Med 1995 182 1545 1556 10.1084/jem.182.5.1545 7595224
20. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. I Vermes C Haanen H Steffens-Nakken C Reutelingsperger, J Immunol Methods 1995 184 39 51 10.1016/0022-1759(95)00072-I 7622868
21. Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. G van Zandbergen A Bollinger A Wenzel S Kamhawi R Voll M Klinger A Muller C Holscher M Herrmann D Sacks W Solbach T Laskay, Proc Natl Acad Sci USA 2006 103 13837 42 10.1073/pnas.0600843103 16945916
22. Novobiocin induces apoptosis-like cell death in topoisomerase II over-expressing arsenite resistant Leishmania donovani. G Singh KG Jayanarayan CS Dey, Mol Biochem Parasitol 2005 141 57 69 10.1016/j.molbiopara.2005.01.014 15811527
23. Miltefosine induces apoptosis-like death in Leishmania donovani promastigotes. C Paris PM Loiseau C Bories J Breard, Antimicrob Agents Chemother 2004 48 852 859 10.1128/AAC.48.3.852-859.2004 14982775
24. Leishmania donovani: intracellular ATP level regulates apoptosis-like death in luteolin induced dyskinetoplastid cells. N Sen BB Das A Ganguly B Banerjee T Sen HK Majumder, Exp Parasitol 2006 114 204 214 10.1016/j.exppara. 2006.03.013 16707127
25. Expression of alternative oxidase inhibits programmed cell death-like phenomenon in bloodstream form of Trypanosoma brucei rhodesiense. A Tsuda WH Witola K Ohashi M Onuma, Parasitol Int 2005 54 243 251 10.1016/j.parint.2005.06. 007 16115792
26. Prostaglandin-induced programmed cell death in Trypanosoma brucei involves oxidative stress. K Figarella NL Uzcategui A Beck C Schoenfeld BK Kubata F Lang M Duszenko, Cell Death Differ 2006 13 1802 1814 10.1038/sj.cdd.4401862 16456581
27. Mimicry of apoptotic cells by exposing phosphatidylserine participates in the establishment of amastigotes of Leishmania (L) amazonensis in mammalian hosts. JL Wanderley ME Moreira A Benjamin AC Bonomo MA Barcinski, J Immunol 2006 176 1834 1839 16424214
28. Toxoplasma gondii exposes phosphatidylserine inducing a TGF-beta1 autocrine effect orchestrating macrophage evasion. SH Seabra W de Souza RA Damatta, Biochem Biophys Res Commun 2004 324 744 752 10.1016/j.bbrc.2004.09.114 15474490
29. Malaria ookinetes exhibit multiple markers for apoptosis-like programmed cell death in vitro. SC Arambage KM Grant I Pardo L Ranford-Cartwright H Hurd, Parasit Vectors 2009 2 32 10.1186/1756-3305-2-32 19604379
30. Mitochondrial superoxide mediates heat-induced apoptotic-like death in Leishmania infantum. JF Alzate AA Arias D Moreno-Mateos A Alvarez-Barrientos A Jimenez-Ruiz, Mol Biochem Parasitol 2007 152 192 202 10.1016/j.molbiopara.2007. 01.006 17300844
31. Programmed cell death in the unicellular protozoan parasite Leishmania. N Lee S Bertholet A Debrabant J Muller R Duncan HL Nakhasi, Cell Death Differ 2002 9 53 64 10.1038/sj.cdd.4400952 11803374
32. Apoptotic death in Leishmania donovani promastigotes in response to respiratory chain inhibition: complex II inhibition results in increased pentamidine cytotoxicity. A Mehta C Shaha, J Biol Chem 2004 279 11798 11813 10.1074/jbc.M309341200 14679210
33. Apoptosis is induced in leishmanial cells by a novel protein kinase inhibitor withaferin A and is facilitated by apoptotic topoisomerase I-DNA complex. N Sen B Banerjee BB Das A Ganguly T Sen S Pramanik S Mukhopadhyay HK Majumder, Cell Death Differ 2007 14 358 367 10.1038/sj.cdd.4402002 16841091
34. Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis? H Zangger JC Mottram N Fasel, Cell Death Differ 2002 9 1126 1139 10.1038/sj.cdd.4401071 12232801
35. Imaging in five dimensions: time-dependent membrane potentials in individual mitochondria. LM Loew RA Tuft W Carrington FS Fay, Biophys J 1993 65 2396 2407 10.1016/S0006-3495(93)81318-3 8312478
36. Naturally occurring triggers that induce apoptosis-like programmed cell death in Plasmodium berghei ookinetes. M Ali EM Al-Olayan S Lewis H Matthews H Hurd, PLoS One 5 9 ii e12634 20844583
37. A programmed cell death pathway in the malaria parasite Plasmodium falciparum has general features of mammalian apoptosis but is mediated by clan CA cysteine proteases. J-H Ch'ng SR Kotturi AG-L Chong MJ Lear KS-W Tan, Cell Death and Disease 2010 1 26 10.1038/cddis.2010.2
38. Bilirubin inhibits Plasmodium falciparum growth through the generation of reactive oxygen species. S Kumar M Guha V Choubey P Maity K Srivastava SK Puri U Bandyopadhyay, Free Radic Biol Med 2008 44 602 613 10.1016/j.freeradbiomed. 2007.10.057 18070610
39. Drug-induced death of the asexual blood stages of Plasmodium falciparum occurs without typical signs of apoptosis. AM Nyakeriga H Perlmann M Hagstedt K Berzins M Troye-Blomberg B Zhivotovsky P Perlmann A Grandien, Microbes Infect 2006 8 1560 1568 10.1016/j.micinf.2006.01.016 16702009
40. Killing of Trypanosomatid Parasites by a Modified Bovine Host Defense Peptide, BMAP-18. LR Haines JM Thomas AM Jackson BA Eyford M Razavi CN Watson B Gowen RE Hancock TW Pearson, PLoS Negl Trop Dis 2009 3 373 10.1371/journal.pntd. 0000373 19190729
41. Prostaglandin D2 induces programmed cell death in Trypanosoma brucei bloodstream form. K Figarella M Rawer NL Uzcategui BK Kubata K Lauber F Madeo S Wesselborg M Duszenko, Cell Death Differ 2005 12 335 346 10.1038/sj.cdd.4401564 15678148
42. JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess delta psi changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. S Salvioli A Ardizzoni C Franceschi A Cossarizza, FEBS Lett 1997 411 77 82 10.1016/S0014-5793(97)00669-8 9247146
43. Miltefosine induces apoptosis in arsenite-resistant Leishmania donovani promastigotes through mitochondrial dysfunction. NK Verma G Singh CS Dey, Exp Parasitol 2007 116 1 13 10.1016/j.exppara.2006.10.007 17161839
44. Temporal dissection of Bax-induced events leading to fission of the single mitochondrion in Trypanosoma brucei. AC Esseiva AL Chanez N Bochud-Allemann JC Martinou A Hemphill A Schneider, EMBO Rep 2004 5 268 273 10.1038/sj.embor.7400095 14968134
45. Antimicrobial peptide-induced apoptotic death of Leishmania results from calcium-dependent, caspase-independent mitochondrial toxicity. MM Kulkarni WR McMaster W Kamysz BS McGwire, J Biol Chem 2009 284 15496 504 10.1074/jbc.M809079200 19357081
46. Edelfosine induces an apoptotic process in Leishmania infantum that is regulated by the ectopic expression of Bcl-XL and Hrk. JF Alzate A Arias F Mollinedo E Rico J de la Iglesia-Vicente A Jimenez-Ruiz, Antimicrob Agents Chemother 2008 52 3779 3792 10.1128/AAC.01665-07 18644968
47. Mitochondria dependent ROS-mediated programmed cell death (PCD) induced by 3,3'-Diindolylmethane (DIM) through Inhibition of FoF1-ATP synthase in unicellular protozoan parasite Leishmania donovani. A Roy A Ganguly S Bosedasgupta BB Das C Pal P Jaisankar HK Majumder, Mol Pharmacol 2008 74 1292 307 10.1124/mol.108.050161 18703668
48. Inhibition of papain-like cysteine proteases and legumain by caspase-specific inhibitors: when reaction mechanism is more important than specificity. J Rozman-Pungercar N Kopitar-Jerala M Bogyo D Turk O Vasiljeva I Stefe P Vandenabeele D Bromme V Puizdar M Fonovic M Trstenjak-Prebanda I Dolenc V Turk B Turk, Cell Death Differ 2003 10 881 888 10.1038/sj.cdd.4401247 12867995
49. Non-specific effects of methyl ketone peptide inhibitors of caspases. P Schotte W Declercq S Van Huffel P Vandenabeele R Beyaert, FEBS Lett 1999 442 117 121 10.1016/S0014-5793(98)01640-8 9923616
50. Lysosomal membrane permeabilization in cell death. P Boya G Kroemer, Oncogene 2008 27 6434 6451 10.1038/onc.2008.310 18955971
51. Cathepsin B-like and cell death in the unicellular human pathogen Leishmania. AK El-Fadili H Zangger C Desponds IJ Gonzalez H Zalila C Schaff A Ives S Masina JC Mottram N Fasel, Cell Death and Disease 2010 1 71 10.1038/cddis.2010.51
52. Design and evaluation of Trypanosoma brucei metacaspase inhibitors. M Berg P Van der Veken J Joossens V Muthusamy M Breugelmans CX Moss J Rudolf P Cos GH Coombs L Maes A Haemers JC Mottram K Augustyns, Bioorg Med Chem Lett 2010 20 2001 2006 10.1016/j.bmcl.2010.01.099 20167486
53. Leishmania major metacaspase can replace yeast metacaspase in programmed cell death and has arginine-specific cysteine peptidase activity. IJ Gonzalez C Desponds C Schaff JC Mottram N Fasel, Int J Parasitol 2007 37 161 172 10.1016/j.ijpara.2006.10.004 17107676
54. Metacaspase 2 of Trypanosoma brucei is a calcium-dependent cysteine peptidase active without processing. CX Moss GD Westrop L Juliano GH Coombs JC Mottram, FEBS Lett 2007 581 5635 5639 10.1016/j.febslet.2007.11.009 18005666
55. Data-mining approaches reveal hidden families of proteases in the genome of malaria parasite. Y Wu X Wang X Liu Y Wang, Genome Res 2003 13 601 616 10.1101/gr.913403 12671001
56. Are metacaspases caspases? D Vercammen W Declercq P Vandenabeele F Van Breusegem, J Cell Biol 2007 179 375 380 10.1083/jcb.200705193 17967946
57. Characterization of metacaspases with trypsin-like activity and their putative role in programmed cell death in the protozoan parasite Leishmania. N Lee S Gannavaram A Selvapandiyan A Debrabant, Eukaryot Cell 2007 6 1745 1757 10.1128/EC.00123-07 17715367
58. The role of metacaspase 1 in Plasmodium berghei development and apoptosis. L Le Chat RE Sinden JT Dessens, Mol Biochem Parasitol 2007 153 41 47 10.1016/j.molbiopara.2007.01.016 17335919
59. Erratum to "Apoptosis in the malaria protozoan, Plasmodium berghei: a possible mechanism for limiting intensity of infection in the mosquito". E Al-Olayan G Williams H Hurd, International Journal for Parasitology 2003 33 105 10.1016/S0020-7519(02)00250-3 (Pubitemid 36126412)
60. Altered expression, polymerisation and cellular distribution of alpha-/beta-tubulins and apoptosis-like cell death in arsenite resistant Leishmania donovani promastigotes. KG Jayanarayan CS Dey, Int J Parasitol 2004 34 915 925 10.1016/j.ijpara.2004.03.009 15217730
61. Nitric oxide-mediated proteasome-dependent oligonucleosomal DNA fragmentation in Leishmania amazonensis amastigotes. P Holzmuller D Sereno M Cavaleyra I Mangot S Daulouede P Vincendeau JL Lemesre, Infect Immun 2002 70 3727 3735 10.1128/IAI.70.7.3727-3735.2002 12065515
62. Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. M Das SB Mukherjee C Shaha, J Cell Sci 2001 114 2461 2469 11559754
63. Antimonial-mediated DNA fragmentation in Leishmania infantum amastigotes. D Sereno P Holzmuller I Mangot G Cuny A Ouaissi JL Lemesre, Antimicrob Agents Chemother 2001 45 2064 2069 10.1128/AAC.45.7.2064-2069.2001 11408224
64. Reactive oxygen species and imbalance of calcium homeostasis contributes to curcumin induced programmed cell death in Leishmania donovani. R Das A Roy N Dutta HK Majumder, Apoptosis 2008 13 867 882 10.1007/s10495-008-0224-7 18506627
65. Camptothecin-induced imbalance in intracellular cation homeostasis regulates programmed cell death in unicellular hemoflagellate Leishmania donovani. N Sen BB Das A Ganguly T Mukherjee S Bandyopadhyay HK Majumder, J Biol Chem 2004 279 52366 52375 10.1074/jbc.M406705200 15355995 (Pubitemid 39656613)
66. Cooperation between Apoptotic and Viable Metacyclics Enhances the Pathogenesis of Leishmaniasis. JL Wanderley Silva LH da Pinto P Deolindo L Soong VM Borges DB Prates AP de Souza A Barral Balanco JM de Freitas MT do Nascimento EM Saraiva MA Barcinski, PLoS ONE 2009 4 5733 10.1371/journal.pone.0005733 19478944
67. Reactive oxygen species activate a Ca2+-dependent cell death pathway in the unicellular organism Trypanosoma brucei brucei. EL Ridgley ZH Xiong L Ruben, Biochem J 1999 340 Pt 1 33 40 10.1042/0264-6021:3400033 10229656
68. Molecular factors and biochemical pathways induced by febrile temperature in intraerythrocytic Plasmodium falciparum parasites. MS Oakley S Kumar V Anantharaman H Zheng B Mahajan JD Haynes JK Moch R Fairhurst TF McCutchan L Aravind, Infect Immun 2007 75 2012 2025 10.1128/IAI.01236-06 17283083
69. The caspase-independent algorithm of programmed cell death in Leishmania induced by baicalein: the role of LdEndoG, LdFEN-1 and LdTatD as a DNA 'degradesome'. S Bosedasgupta BB Das S Sengupta A Ganguly A Roy S Dey G Tripathi B Dinda HK Majumder, Cell Death Differ 2008 15 1629 40 10.1038/cdd.2008.85 18566607
70. Conservation of the pro-apoptotic nuclease activity of endonuclease G in unicellular trypanosomatid parasites. S Gannavaram C Vedvyas A Debrabant, J Cell Sci 2008 121 99 109 10.1242/jcs.014050 18073240
71. Leishmania infantum expresses a mitochondrial nuclease homologous to EndoG that migrates to the nucleus in response to an apoptotic stimulus. E Rico JF Alzate AA Arias D Moreno J Clos F Gago I Moreno M Dominguez A Jimenez-Ruiz, Mol Biochem Parasitol 2009 163 28 38 10.1016/j.molbiopara.2008.09.007 18940204
72. Investigating the evolution of apoptosis in malaria parasites: the importance of ecology. LC Pollit N Colegrave SM Khan M Sajid SE Reece, Parasit Vectors 2010 3 105
73. Quercetin induces apoptosis of Trypanosoma brucei gambiense and decreases the proinflammatory response of human macrophages. M Mamani-Matsuda J Rambert D Malvy H Lejoly-Boisseau S Daulouede D Thiolat S Coves P Courtois P Vincendeau MD Mossalayi, Antimicrob Agents Chemother 2004 48 924 929 10.1128/AAC.48.3.924- 929.2004 14982785
74. A form of cell death with some features resembling apoptosis in the amitochondrial unicellular organism Trichomonas vaginalis. O Chose C Noel D Gerbod C Brenner E Viscogliosi A Roseto, Exp Cell Res 2002 276 32 39 10.1006/excr.2002.5496 11978006
75. Programmed cell death in a human intestinal parasite, Blastocystis hominis. AM Nasirudeen KS Tan M Singh EH Yap, Parasitology 2001 123 235 246 10.1017/S0031182001008332 11578087 (Pubitemid 32881848)
76. Metronidazole induces programmed cell death in the protozoan parasite Blastocystis hominis. AM Nasirudeen YE Hian M Singh KS Tan, Microbiology 2004 150 33 43 10.1099/mic.0.26496-0 14702395
77. Staurosporine-induced programmed cell death in Blastocystis occurs independently of caspases and cathepsins and is augmented by calpain inhibition. J Yin J Howe KS Tan, Microbiology 156 1284 1293 10.1099/mic.0.034025-0 20056704
78. Programmed cell death in Blastocystis hominis occurs independently of caspase and mitochondrial pathways. AM Nasirudeen KS Tan, Biochimie 2005 87 489 497 10.1016/j.biochi.2005.03.003 15913879
79. Caspase-3-like protease influences but is not essential for DNA fragmentation in Blastocystis undergoing apoptosis. AM Nasirudeen KS Tan, Eur J Cell Biol 2004 83 477 482 10.1078/0171-9335-00411 15540464
80. Programmed cell death in Entamoeba histolytica induced by the aminoglycoside G418. JD Villalba C Gomez O Medel V Sanchez JC Carrero M Shibayama DG Ishiwara, Microbiology 2007 153 3852 3863 10.1099/mic.0.2007/ 008599-0 17975094 (Pubitemid 350168264)
81. Oxidative stress-induced cell cycle blockage and a protease-independent programmed cell death in microaerophilic Giardia lamblia. E Ghosh A Ghosh AN Ghosh T Nozaki S Ganguly, Drug Des Devel Ther 2009 3 103 110 19920926