Cell death in Leishmania induced by stress and differentiation: Programmed cell death or necrosis?

Cell Death and Differentiation

Volumn 9, Issue 10, 2002, Pages 1126-1139

  Zangger, H ^a   Mottram, J C ^b   Fasel, N ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Cysteine protease; DNA fragmentation; Host parasite interaction; Leishmania; Necrosis; Programmed cell death

Indexed keywords

CATHEPSIN L; CYSTEINE PROTEINASE; DNA FRAGMENT; GENOMIC DNA; LYSOSOME ENZYME; NITRIC OXIDE; NUCLEASE;

APOPTOSIS; ARTICLE; BIOCHEMISTRY; CELL DEATH; CELL DIFFERENTIATION; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; HEAT SHOCK; LEISHMANIA; LIFE CYCLE; MAMMAL; METAZOON; MORPHOLOGY; NICK END LABELING; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTOZOON; SERUM; STIMULATION; STRESS;

ANIMALS; APOPTOSIS; CASPASES; CELL DIFFERENTIATION; CELL NUCLEUS; CELLS, CULTURED; CHELATING AGENTS; COUMARINS; DNA; DNA FRAGMENTATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDONUCLEASES; HUMANS; IN SITU NICK-END LABELING; LEISHMANIA; LEISHMANIASIS; MICE; MICROSCOPY, ELECTRON; OLIGOPEPTIDES; STRESS;

MAMMALIA; METAZOA; PROTOZOA;

EID: 0036792472     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401071     Document Type: Article

References (73)

1. Jacobson MD, Weil M and Raff MC (1997) Programmed cell death in animal development. Cell 88: 347-354
2. Greil P, Egle A and Villunger A (1998) On the role and significance of Fas (Apo-1/CD95) ligand (FasL) expression in immune privileged tissues and cancer cells using multiple myeloma as a model. Leuk. Lymphoma 31: 477-490
3. Evan G and Littlewood T (1998) A matter of life and cell death. Science 281: 1317-1322
4. Welburn SC, Barcinski MA and Williams GT (1997) Programmed cell death in Trypanosomatids. Parasitol. Today 13: 22-26
5. Ameisen JC. (1996) The origin of programmed cell death [see comments]. Science 272: 1278-1279
6. Christensen ST, Leick V, Rasmussen L and Wheatley DN (1998) Signaling in unicellular eukaryotes. Int. Rev. Cytol. 177: 181-253
7. Davis MC, Ward JG, Herrick G and Allis CD (1992) Programmed nuclear death: apoptotic-like degradation of specific nuclei in conjugating Tetrahymena. Dev. Biol. 154: 419-432
8. Madireddi MT, Coyne RS, Smothers JF, Mickey KM, Yao MC and Allis CD (1996) Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87: 75-84
9. Mpoke S and Wolfe J (1996) DNA digestion and chromatin condensation during nuclear death in Tetrahymena. Exp. Cell. Res. 225: 357-365
10. Mpoke SS and Wolfe J (1997) Differential staining of apoptotic nuclei in living cells: application to macronuclear elimination in Tetrahymena. J. Histochem. Cytochem. 45: 675-683
11. Christensen ST, Mottram JC, Staarup EM, Kristiansen K, Wheatley DN and Rasmussen L (1998) Staurosporine-induced cell death in Tetrahymena thermophila has mixed characteristics of both apoptotic and autophagic degeneration. Curr. Biol. Int. 22: 591-598
12. Kovacs P, Hegyesi H, Kohidai L, Nemes P and Csaba G (1999) Effect of C2 ceramide on the inositol phospholipid metabolism (uptake of 32P, 3H-serine and 3H-palmitic acid) and apoptosis-related morphological changes in Tetrahymena. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 122: 215-224
13. Cornillon S, Foa C, Davoust J, Buonavista N, Gross JD and Golstein P (1994) Programmed cell death in Dictyostelium. J. Cell. Sci. 107: 2691-2704
14. Cornillon S, Olie RA and Golstein P (1998) An insertional mutagenesis approach to Dictyostelium cell death. Cell Death Differ. 5: 416-425
15. Schaap P, Nebl T and Fisher PR (1996) A slow sustained increase in cytosolic Ca2+ levels mediates stalk gene induction by differentiation inducing factor in Dictyostelium. EMBO J. 15: 5177-5183
16. Olie RA, Durrieu F, Cornillon S, Loughran G, Gross J, Earnshaw WC and Golstein P (1998) Apparent caspase independence of programmed cell death in Dictyostelium. Curr. Biol. 8: 955-958
17. Verkerke-van Wijk I, Brandt R, Bosman L and Schaap P (1998) Two distinct signaling pathways mediate DIF induction of prestalk gene expression in Dictyostelium. Exp. Cell. Res. 245: 179-185
18. Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A and Levine A (1999) Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO(2) limitation and oxidative stress. Curr. Biol. 9: 1061-1064
19. Yarmolinsky MB. (1995) Programmed cell death in bacterial populations [comment]. Science 267: 836-837
20. Kobayashi I. (1998) Selfishness and death: raison d'etre of restriction, recombination and mitochondria. Trends Genet. 14: 368-374
21. Welburn SC and Maudlin I (1997) Control of Trypanosoma brucei brucei infections in tsetse, Glossina morsitans. Med. Vet. Entomol. 11: 286-289
22. Welburn SC, Maudlin I and Ellis DS (1989) Rate of trypanosome killing by lectins in midguts of different species and strains of Glossina. Med. Vet. Entomol. 3: 77-82
23. Ameisen JC, Idziorek T, Billaut-Mulot O, Loyens M, Tissier J-P, Potentier A and Ouaissi A (1995) 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. Cell Death Differ. 2: 285-300
24. Pearson TW, Beecroft RP, Welburn SC, Ruepp S, Roditi I, Hwa KY, Englund PT, Wells CW and Murphy NB (2000) The major cell surface glycoprotein procyclin is a receptor for induction of a novel form of cell death in African trypanosomes in vitro. Mol. Biochem. Parasitol. 111: 333-349
25. Welburn SC, Lillico S and Murphy NB (1999) Programmed cell death in procyclic form Trypanosoma brucei rhodesiense-identification of differentially expressed genes during con A induced death. Mem. Inst. Oswaldo Cruz 94: 229-234
26. Ridgley EL, Xiong ZH and Ruben L (1999) Reactive oxygen species activate a Ca2+-dependent cell death pathway in the unicellular organism Trypanosoma brucei brucei. Biochem. J. 340: 33-40
27. Moreira ME, Del Portillo HA, Milder RV, Balanco JM and Barcinski MA (1996) Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis. J. Cell Physiol. 167: 305-313
28. Billaut-Mulot O, Fernandez-Gomez R, Loyens M and Ouaissi A (1996) Trypanosoma cruzi elongation factor 1-alpha: nuclear localization in parasites undergoing apoptosis. Gene 174: 19-26
29. Welburn SC and Murphy NB (1998) Prohibitin and RACK homologues are upregulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms. Cell Death Differ. 5: 615-622
30. Maercker C, Kortwig H, Nikiforov MA, Allis CD and Lipps HJ (1999) A nuclear protein involved in apoptotic-like DNA degradation in Stylonychia: implications for similar mechanisms in differentiating and starved cells. Mol. Biol. Cell. 10: 3003-3014
31. Aravind L, Dixit VM and Koonin EV (2001) Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 291: 1279-1284
32. Aravind L, Dixit VM and Koonin EV (1999) The domains of death: evolution of the apoptosis machinery. Trends Biochem. Sci. 24: 47-53
33. Uren AG, O'Rourke K, Aravind LA, Pisabarro MT, Seshagiri S, Koonin EV and Dixit VM (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell. 6: 961-967
34. Arnoult D, Akarid K, Grodet A, Petit PX, Estaquier J and Ameisen JC (2002) On the evolution of programmed cell death: apoptosis of the unicellular eukaryote Leishmania major involves cysteine proteinase activation and mitochondrion permeabilization. Cell Death Differ. 9: 65-81
35. Lee N, Bertholet S, Debrabant A, Muller J, Duncan R and Nakhasi HL (2002) Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ. 9: 53-64
36. Leist M and Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2: 589-598
37. Telford DJ and Stewart BW (1989) Micrococcal nuclease: its specificity and use for chromatin analysis. Int. J. Biochem. 21: 127-137
38. Ishisaka R, Kanno t, Akiyama J, Yoshioka T, Utsumi K and Utsumi T (2001) Activation of caspase-3 by lysosomal cysteine proteases and its role in 2, 2′-azobis-(2-amidinopropane)dihydrochloride (AAPH)-induced apoptosis in HL-60 cells. J. Biochem. (Tokyo) 129: 35-41
39. Mottram JC, Souza AE, Hutchison JE, Carter R, Frame MJ and Coombs GH (1996) Evidence from disruption of the Imcpb gene array of Leishmania mexicana that cysteine proteinases are virulence factors. Proc. Natl. Acad. Sci. USA 93: 6008-6013
40. Balk J, Leaver CJ and McCabe PF (1999) Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett. 463: 151-154
41. Mauel J and Ransijn A (1997) Leishmania spp.: mechanisms of toxicity of nitrogen oxidation products. Exp. Parasitol. 87: 98-111
42. Lecoeur H, Prevost M and Gougeon M (2001) Oncosis is associated with exposure of phosphatidylserine residues on the outside layer of the plasma membrane: a reconsideration of the specificity of the annexin V/propidium iodide assay. Cytometry 44: 65-72
43. Marini M and Musiani D (1998) Micromolar zinc affects endonucleolytic activity in hydrogen peroxide-mediated apoptosis. Exp. Cell. Res. 239: 393-398
44. Widlak P, Li P, Wang X and Garrard WT (2000) Cleavage preferences of the apoptotic endonuclease DFF40 (caspase-activated DNase or nuclease) on naked DNA and chromatin substrates. J. Biol. Chem. 275: 8226-8232
45. Gaido ML and Cidlowski JA (1991) Identification, purification, and characterization of a calcium-dependent endonuclease (NUC18) from apoptotic rat thymocytes. NUC18 is not histone H2B. J. Biol. Chem. 266: 18580-18585
46. Sun DY, Jiang S, Zheng LM, Ojcius DM and Young JD (1994) Separate metabolic pathways leading to DNA fragmentation and apoptotic chromatin condensation. J. Exp. Med. 179: 559-568
47. Cohen JJ and Duke RC (1984) Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J. Immunol. 132: 38-42
48. Zamzami N and Kroemer G (1999) Condensed matter in cell death. Nature 401: 127-128
49. Zhang C, Robertson MJ and Schiossman SF (1995) A triplet of nuclease proteins (NP42-50) is activated in human Jurkat cells undergoing apoptosis. Cell Immunol. 165: 161-167
50. Warbrick E. (1996) A new twist to the tale? Apoptosis. Curr. Biol. 6: 1057-1059
51. Debrabant A, Ghedin E and Dwyer DM (2000) Dissection of the functional domains of the Leishmania surface membrane 3′-nucleotidase/nuclease, a unique member of the class I nuclease family. J. Biol. Chem. 275: 16366-16372
52. Glaser TA, Wells SJ, Spithill TW, Pettitt JM, Humphris DC and Mukkada AJ (1990) Leishmania major and L. donovani: a method for rapid purification of amastigotes. Exp. Parasitol. 71: 343-345
53. Chandler JM, Cohen GM and MacFarlane M (1998) Different subcellular distribution of caspase-3 and caspase-7 following Fas-induced apoptosis in mouse liver. J. Biol. Chem. 273: 10815-10818
54. Mottram JC, Brooks DR and Coombs GH (1998) Roles of cysteine proteinases of trypanosomes and Leishmania in host-parasite interactions. Curr. Opin. Microbiol. 1: 455-460
55. Alves LC, St. Hilaire PM, Meldal M, Sanderson SJ, Mottram JC, Coombs GH, Juliano L and Juliano MA (2001) Identification of peptides inhibitory to recombinant cysteine proteinase, CPB, of Leishmania mexicana. Mol. Biochem. Parasitol. 114: 81-88
56. Alves LC, Judice WAS, St. Hilaire PM, Meldal M, Sanderson SJ, Mottram JC, Coombs GH, Juliano L and Juliano MA (2001) Substrate specificity of recombinant cysteine protainase, CPB, of Leishmania mexicana. Mol. Biochem. Parasitol. 116: 1-9
57. Bart G, Frame MJ, Carter A, Coombs GM and Mottram JC (1997) Cathepsin B-like cysteine proteinase-deficient mutants of Leishmania mexicana. Mol. Biochem. Parasitol. 88: 53-61
58. Frame MJ, Mottram JC and Coombs GH (2000) Analysis of the roles of cysteine proteinases of Leishmania mexicana in the host-parasite interaction. Parasitology 121: 367-377
59. Roberts LR, Adjei PN and Gores GJ (1999) Cathepsins as effector proteases in hepatocyte apoptosis. Cell. Biochem. Biophys. 30: 71-88
60. Shibata M, Kanamori S, Isahara K, Ohsawa Y, Konishi A, Kametaka S, Watanabe T, Ebisu S, Ishido K, Kominami E and Uchiyama Y (1998) Participation of cathepsins B and D in apoptosis of PC12 cells following serum deprivation. Biochem. Biophys. Res. Commun. 251: 199-203
61. Vancompernolle K, Van Herreweghe F, Pynaert G, Van de Craen M, De Vos K, Totty N, Sterling A, Fiers W, Vandenabeele P and Grooten J (1998) Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett. 438: 150-158
62. Bart G, Coombs GH and Mottram JC (1995) Isolation of Imcpc, a gene encoding a Leishmania mexicana cathepsin-B-like cysteine proteinase. Mol. Biochem. Parasitol. 73: 271-274
63. Sperando S, de Belle I and Bredesen DE (2000) An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA 97: 14376-14381
64. Das M, Mukherjee SB and Shaha C (2001) Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J. Cell Science 114: 2461-2469
65. Sereno D, Holzmuller P, Mangot I, Cuny G, Ouaissi A and Lemesre JL (2001) Antimonial-mediated DNA fragmentation in Leishmania infantum amastigotes. Antimicrob. Agents Chemother. 45: 2064-2069
66. Belli SI. (2000) Chromatin remodelling during the life cycle of trypanosomatids. Int. J. Parasitol. 30: 679-687
67. Alexander J, Coombs GH and Mottram JC (1998) Leishmania mexicana cysteine proteinase-deficient mutants have attenuated virulence for mice and potentiate a Th1 response. J. Immunol. 161: 6794-6801
68. Solioz N, Blum-Tirouvanziam U, Jacquet R, Rafati S, Corradin G, Mauel J and Fasel N (1999) The protective capacities of histone H1 against experimental murine cutaneous leishmaniasis. Vaccine 18: 850-859
69. Schlimme W, Burri M, Bender K, Betschart B and Hecker H (1993) Trypanosoma brucei brucei: differences in the nuclear chromatin of bloodstream forms and procyclic culture forms. Parasitology 107: 237-247
70. Noll TM, Desponds C, Belli SI, Glaser TA and Fasel NJ (1997) Histone H1 expression varies during the Leishmania major life cycle. Mol. Biochem. Parasitol. 84: 215-227
71. Kataoka T, Holler N, Micheau O, Martinon F, Tinel A, Hofmann K and Tschopp J (2001) Bcl-rambo, a novel Bcl-2 homologue that induces apoptosis via its unique C-terminal extension. J. Biol. Chem. 276: 19548-19554
72. BodmerJL, Holler N, Reynard S, Vinciguerra P, Schneider P, Juo P, Blenis J and Tschopp J (2000) TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat. Cell. Biol. 2: 241-243
73. Corradin S, Mauel J, Ransijn A, Sturzinger C and Vergeres G (1999) Down-regulation of MARCKS-related protein (MRP) in macrophages infected with Leishmania. J. Biol. Chem. 274: 16782-16787