Leishmania mexicana metacaspase is a negative regulator of amastigote proliferation in mammalian cells

Cell Death and Disease

Volumn 3, Issue 9, 2012, Pages

  Castanys Munoz E ^a   Brown, E ^a   Coombs, G H ^b   Mottram, J C ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

Caspase; Cysteine peptidase; Metacaspase; Programmed cell death

Indexed keywords

CASPASE; CASPASE 3; METACASPASE; MILTEFOSINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMASTIGOTE; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; AXENIC CULTURE; CELL CYCLE REGULATION; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; GENE DELETION; GENETIC MANIPULATION; HOST CELL; IN VITRO STUDY; IN VIVO STUDY; LEISHMANIA MEXICANA; MACROPHAGE; MAMMAL CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PARASITE SURVIVAL; PARASITE VIRULENCE; PHENOTYPE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN DEGRADATION; PROTIST LIFE CYCLE STAGE;

ANIMALS; ANTIPROTOZOAL AGENTS; CASPASES; FEMALE; LEISHMANIA MEXICANA; MACROPHAGES; MICE; MICE, INBRED BALB C; PHOSPHORYLCHOLINE;

FUNGI; LEISHMANIA MEXICANA; MAMMALIA; MUS; PROTOZOA;

EID: 84867227941     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2012.113     Document Type: Article

References (46)

1. Taylor RC, Cullen SP, Martin SJ. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008; 9: 231-241. (Pubitemid 351301823)
2. Debrabant A, Lee N, Bertholet S, Duncan R, Nakhasi HL. Programmed cell death in trypanosomatids and other unicellular organisms. Int J Parasitol 2003; 33: 257-267. (Pubitemid 36369147)
3. Murray HW, Berman JD, Davies CR, Saravia NG. Advances in leishmaniasis. Lancet 2005; 366: 1561-1577. (Pubitemid 41540115)
4. Kaye P, Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Micro 2011; 9: 604-615.
5. 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. (Pubitemid 34071993)
6. Das M, Mukherjee SB, Shaha C. Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J Cell Sci 2001; 114: 2461-2469. (Pubitemid 32684800)
7. Holzmuller P, Sereno D, Cavaleyra M, Mangot I, Daulouede S, Vincendeau P et al. Nitric oxide-mediated proteasome-dependent oligonucleosomal DNA fragmentation in Leishmania amazonensis amastigotes. Infect Immun 2002; 70: 3727-3735. (Pubitemid 34666012)
8. Moreira MEC, Del Portillo HA, Milder RV, Balanco JMF, Barcinski MA. Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis. J Cell Physiol 1996; 167: 305-313. (Pubitemid 26145864)
9. Paris C, Loiseau PM, Bories C, Breard J. Miltefosine induces apoptosis-like death in Leishmania donovani promastigotes. Antimicrob Agents Chemother 2004; 48: 852-859. (Pubitemid 38280335)
10. Sen N, Das BB, Ganguly A, Mukherjee T, Tripathi G, Bandyopadhyay S et al. Camptothecin induced mitochondrial dysfunction leading to programmed cell death in unicellular hemoflagellate Leishmania donovani. Cell Death Differ 2004; 11: 924-936. (Pubitemid 39139751)
11. Verma NK, Singh G, Dey CS. Miltefosine induces apoptosis in arsenite-resistant Leishmania donovani promastigotes through mitochondrial dysfunction. Exp Parasitol 2007; 116: 1-13. (Pubitemid 46412310)
12. Zangger H, Mottram JC, Fasel N. Cell death in Leishmania induced by stress and differentiation: Programmed cell death or necrosis? Cell Death Differ 2002; 9: 1126-1139.
13. Reece SE, Pollitt LC, Colegrave N, Gardner A. The meaning of death: Evolution and ecology of apoptosis in protozoan parasites. PLoS Pathog 2011; 7: e1002320.
14. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M et al. The genome of the kinetoplastid parasite, Leishmania major. Science 2005; 309: 436-442. (Pubitemid 40994677)
15. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC et al. The genome of the African trypanosome Trypanosoma brucei. Science 2005; 309: 416-422. (Pubitemid 40994676)
16. Uren GA, O'Rourke K, Aravind L, Pisabarro TM, Seshagiri S, Koonin VE et al. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 2000; 6: 961-967.
17. 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: 45329-45336. (Pubitemid 39491515)
18. 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: 5635-5639. (Pubitemid 350179768)
19. Gonzales 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: 161-172. (Pubitemid 46074020)
20. Bozhkov PV, Suarez MF, Filonova LH, Daniel G, Zamyatnin AA Jr, Rodriguez-Nieto S et al. Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. PNAS 2005; 102: 14463-14468. (Pubitemid 41429720)
21. McLuskey K, Rudolf J, Proto WR, Isaacs NW, Coombs GH, Moss CX et al. Crystal structure of a Trypanosoma brucei metacaspase. Proc Natl Acad Sci USA 2012; 109: 7469-7474.
22. Sundstrom JF, Vaculova A, Smertenko AP, Savenkov EI, Golovko A, Minina E et al. Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat Cell Biol 2009; 11: 1347-1354.
23. Tsiatsiani L, Van BF, Gallois P, Zavialov A, Lam E, Bozhkov PV. Metacaspases. Cell Death Differ 2011; 18: 1279-1288.
24. Lee RE, Puente LG, Kaern M, Megeney LA. A non-death role of the yeast metacaspase: Yca1p alters cell cycle dynamics. PLoS ONE 2008; 3: e2956.
25. Lee RE, Brunette S, Puente LG, Megeney LA. Metacaspase Yca1 is required for clearance of insoluble protein aggregates. Proc Natl Acad Sci USA 2010; 107: 13348-13353.
26. Coll NS, Vercammen D, Smidler A, Clover C, Van BF, Dangl JL et al. Arabidopsis type I metacaspases control cell death. Science 2010; 330: 1393-1397.
27. Ambit A, Fasel N, Coombs GH, Mottram JC. An essential role for the Leishmania major metacaspase in cell cycle progression. Cell death Diff 2008; 15: 113-122. (Pubitemid 350286179)
28. Zalila H, Gonzalez IJ, El-Fadili AK, Delgado MB, Desponds C, Schaff C et al. Processing of metacaspase into a cytoplasmic catalytic domain mediating cell death in Leishmania major. Mol Microbiol 2011; 79: 222-239.
29. Lee N, Gannavaram S, Selvapandiyan A, Debrabant A. Characterization of metacaspases with trypsin-like activity and their putative role in programmed cell death in the protozoan parasite Leishmania. Eukaryot Cell 2007; 6: 1745-1757. (Pubitemid 47585564)
30. Raina P, Kaur S. Knockdown of LdMC1 and Hsp70 by antisense oligonucleotides causes cell-cycle defects and programmed cell death in Leishmania donovani. Mol Cell Biochem 2012; 359: 135-149.
31. 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. PNAS 2006; 103: 13837-13842. (Pubitemid 44413994)
32. van Zandbergen G, Luder CG, Heussler V, Duszenko M. Programmed cell death in unicellular parasites: a prerequisite for sustained infection? Trends Parasitol 2010; 26: 477-483.
33. Williams RAM, Smith TK, Cull B, Mottram JC, Coombs GH. ATG5 is essential for ATG8- dependent autophagy and mitochondrial homeostasis in Leishmania. PLoS Path 2012; 8: e1002695.
34. Jaramillo M, Gomez M-A, Larsson O, Shio M-T, Topisirovic I, Contreras I et al. Leishmania repression of host translation through mTOR cleavage is required for parasite survival and infection. Cell Host Microbe 2011; 9: 331-341.
35. Silverman JM, Chan SK, Robinson DP, Dwyer DM, Nandan D, Foster LJ et al. Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 2008; 9: R35.
36. Cameron P, McGachy A, Anderson M, Paul A, Coombs GH, Mottram JC et al. Inhibition of Lipopolysaccharide-induced macrophage IL-12 production by Leishmania mexicana amastigotes: the role of cysteine peptidases and the NF-kB signaling pathway. J Immunol 2004; 173: 3297-3304. (Pubitemid 39142038)
37. Halle M, Gomez MA, Stuible M, Shimizu H, McMaster WR, Olivier M et al. The Leishmania surface protease GP63 cleaves multiple intracellular proteins and actively participates in p38 mitogen-activated protein kinase inactivation. J Biol Chem 2009; 284: 6893-6908.
38. Contreras I, Gomez MA, Nguyen O, Shio MT, McMaster RW, Olivier M. Leishmaniainduced inactivation of the macrophage transcription factor AP-1 is mediated by the parasite metalloprotease GP63. PLoS Pathog 2010; 6: e1001148.
39. Brooks DR, Tetley L, Coombs GH, Mottram JC. Processing and trafficking of cysteine proteases in Leishmania mexicana. J Cell Sci 2000; 113: 4035-4041. (Pubitemid 32194528)
40. Ellis M, Sharma DK, Hilley JD, Coombs GH, Mottram JC. Processing and trafficking of Leishmania mexicana GP63: analysis using mutants deficient in glycosylphosphatidyl inositol protein anchoring. J Biol Chem 2002; 277: 27968-27974. (Pubitemid 34966745)
41. Proto WR, Castanys-Munoz E, Black A, Tetley L, Juliano L, Coombs GH et al. Trypanosoma brucei metacaspase 4 is a pseudopeptidase and a virulence factor. J Biol Chem 2011; 286: 39914-39925.
42. Rogers MB, Hilley JD, Dickens NJ, Wilkes JM, Bates PA, Depledge DP et al. Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res 2011; 21: 2129-2142.
43. Brooks DR, Denise H, Westrop GD, Coombs GH, Mottram JC. The stage-regulated expression of Leishmania mexicana CPB cysteine proteases is mediated by an intercistronic sequence element. J Biol Chem 2001; 276: 47081-47089.
44. Bates PA, Robertson CD, Tetley L, Coombs GH. Axenic cultivation and characterization of Leishmania mexicana amastigote-like forms. Parasitology 1992; 105: 193-202.
45. Mißlitz A, Mottram JC, Overath P, Aebischer T. Targeted integration into a rRNA locus results in uniform and high level expression of transgenes in Leishmania amastigotes. Mol Biochem Parasitol 2000; 107: 251-261. (Pubitemid 30211639)
46. Williams RAM, Tetley L, Mottram JC, Coombs GH. Cysteine peptidases CPA and CPB are vital for autophagy and differentiation in Leishmania mexicana. Mol Microbiol 2006; 61: 655-674. (Pubitemid 44324091)