Apoptotic marker expression in the absence of cell death in staurosporine-treated leishmania donovani

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 3, 2013, Pages 1252-1261

  Foucher, Aude L ^a,b   Rachidi, Najma ^a   Gharbi, Sarah ^b   Blisnick, Thierry ^c   Bastin, Philippe ^c   Pemberton, Iain K ^b   Späth, Gerald F ^a  

^a INSTITUT PASTEUR   (France)

^b Photeomix   (France)

^c Unité de Biologie Cellulaire des Trypanosomes   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMPHOTERICIN B; BINDING PROTEIN; CASEIN KINASE I; CASPASE; LIPOCORTIN 5; MILTEFOSINE; PHOSPHOTRANSFERASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE INHIBITOR; STAUROSPORINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL DEATH; DISSOCIATION; ENZYME ASSAY; ENZYME INHIBITION; IN VITRO STUDY; LEISHMANIA DONOVANI; MOUSE; NONHUMAN; PARASITE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN FAMILY;

AMINO ACID SEQUENCE; AMPHOTERICIN B; ANNEXIN A5; ANTIPROTOZOAL AGENTS; APOPTOSIS; BENZAMIDES; BIOLOGICAL MARKERS; CASEIN KINASE I; CELL CYCLE CHECKPOINTS; HUMANS; IMIDAZOLES; LEISHMANIA DONOVANI; MOLECULAR SEQUENCE DATA; PHOSPHORYLCHOLINE; PHOSPHOTRANSFERASES; PROTEIN BIOSYNTHESIS; PROTEIN KINASE INHIBITORS; PROTOZOAN PROTEINS; STAUROSPORINE; SUBSTRATE SPECIFICITY;

EID: 84874024381     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01983-12     Document Type: Article

References (45)

1. Rahman M, Ahmed BN, Faiz MA, Chowdhury MZ, Islam QT, Sayeedur R, Rahman MR, Hossain M, Bangali AM, Ahmad Z, Islam MN, Mascie- Taylor CG, Berman J, Arana B. 2011. Phase IV trial of miltefosine in adults and children for treatment of visceral leishmaniasis (kala-azar) in Bangladesh. Am. J. Trop. Med. Hyg. 85:66-69.
2. Perez-Victoria JM, Bavchvarov BI, Torrecillas IR, Martinez-Garcia M, Lopez-Martin C, Campillo M, Castanys S, Gamarro F. 2011. Sitamaquine overcomes ABC-mediated resistance to miltefosine and antimony in Leishmania. Antimicrob. Agents Chemother. 55:3838 -3844.
3. Doerig C. 2004. Protein kinases as targets for anti-parasitic chemotherapy. Biochim. Biophys. Acta 1697:155-168.
4. Chow C, Cloutier S, Dumas C, Chou MN, Papadopoulou B. 2011. Promastigote to amastigote differentiation of Leishmania is markedly delayed in the absence of PERK eIF2alpha kinase-dependent eIF2alpha phosphorylation. Cell. Microbiol. 13:1059 -1077.
5. Madeira da Silva L, Beverley SM. 2010. Expansion of the target of rapamycin (TOR) kinase family and function in Leishmania shows that TOR3 is required for acidocalcisome biogenesis and animal infectivity. Proc. Natl. Acad. Sci. U.S.A. 107:11965-11970.
6. Dujardin JC, Gonzalez-Pacanowska D, Croft SL, Olesen OF, Spath GF. 2010. Collaborative actions in anti-trypanosomatid chemotherapy with partners from disease endemic areas. Trends Parasitol. 26:395- 403.
7. Grant KM, Dunion MH, Yardley V, Skaltsounis AL, Marko D, Eisenbrand G, Croft SL, Meijer L, Mottram JC. 2004. Inhibitors of Leishmania mexicana CRK3 cyclin-dependent kinase: chemical library screen and antileishmanial activity. Antimicrob. Agents Chemother. 48:3033-3042.
8. Allocco JJ, Donald R, Zhong T, Lee A, Tang YS, Hendrickson RC, Liberator P, Nare B. 2006. Inhibitors of casein kinase 1 block the growth of Leishmania major promastigotes in vitro. Int. J. Parasitol. 36:1249- 1259.
9. Malki-Feldman L, Jaffe CL. 2009. Leishmania major: effect of protein kinase A and phosphodiesterase activity on infectivity and proliferation of promastigotes. Exp. Parasitol. 123:39-44.
10. Schmidt-Arras D, Leclercq O, Gherardini PF, Helmer-Citterich M, Faigle W, Loew D, Spath GF. 2011. Adaptation of a 2D in-gel kinase assay to trace phosphotransferase activities in the human pathogen Leishmania donovani. J. Proteomics 74:1644 -1651.
11. Hem S, Gherardini PF, Osorio y Fortea J, Hourdel V, Morales MA, Watanabe R, Pescher P, Kuzyk MA, Smith D, Borchers CH, Zilberstein D, Helmer-Citterich M, Namane A, Spath GF. 2010. Identification of Leishmania-specific protein phosphorylation sites by LC-ESI-MS/MS and comparative genomics analyses. Proteomics 10:3868 -3883.
12. Becker S, Jaffe CL. 1997. Effect of protein kinase inhibitors on the growth, morphology, and infectivity of Leishmania promastigotes. Parasitol. Res. 83:273-280.
13. Arnoult D, Akarid K, Grodet A, Petit PX, Estaquier J, 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.
14. Sen N, Banerjee B, Das BB, Ganguly A, Sen T, Pramanik S, Mukhopadhyay S, Majumder HK. 2007. Apoptosis is induced in leishmanial cells by a novel protein kinase inhibitor withaferin A and is facilitated by apoptotic topoisomerase I-DNA complex. Cell Death Differ. 14:358 -367.
15. Kulkarni MM, McMaster WR, Kamysz W, McGwire BS. 2009. Antimicrobial peptide-induced apoptotic death of leishmania results from calcium- dependent, caspase-independent mitochondrial toxicity. J. Biol. Chem. 284:15496 -15504.
16. Weingartner A, Kemmer G, Muller FD, Zampieri RA, Gonzaga Dos Santos M, Schiller J, Pomorski TG. 2012. Leishmania promastigotes lack phosphatidylserine but bind annexin V upon permeabilization or miltefosine treatment. PLoS One 7:e42070. doi:10.1371/journal.pone.0042070.
17. de Freitas Balanco JM, Moreira ME, Bonomo A, Bozza PT, Amarante-Mendes G, Pirmez C, Barcinski MA. 2001. Apoptotic mimicry by an obligate intracellular parasite downregulates macrophage microbicidal activity. Curr. Biol. 11:1870 -1873.
18. Saar Y, Ransford A, Waldman E, Mazareb S, Amin-Spector S, Plumblee J, Turco SJ, Zilberstein D. 1998. Characterization of developmentallyregulated activities in axenic amastigotes of Leishmania donovani. Mol. Biochem. Parasitol. 95:9 -20.
19. Goyard S, Segawa H, Gordon J, Showalter M, Duncan R, Turco SJ, Beverley SM. 2003. An in vitro system for developmental and genetic studies of Leishmania donovani phosphoglycans. Mol. Biochem. Parasitol. 130:31- 42.
20. Absalon S, Blisnick T, Bonhivers M, Kohl L, Cayet N, Toutirais G, Buisson J, Robinson D, Bastin P. 2008. Flagellum elongation is required for correct structure, orientation and function of the flagellar pocket in Trypanosoma brucei. J. Cell Sci. 121:3704 -3716.
21. Morales MA, Pescher P, Spath GF. 2010. Leishmania major MPK7 protein kinase activity inhibits intracellular growth of the pathogenic amastigote stage. Eukaryot. Cell 9:22-30.
22. El-Fadili AK, Zangger H, Desponds C, Gonzalez IJ, Zalila H, Schaff C, Ives A, Masina S, Mottram JC, Fasel N. 2010. Cathepsin B-like and cell death in the unicellular human pathogen Leishmania. Cell Death Dis. 1:e71.
23. Wemmer KA, Marshall WF. 2004. Flagellar motility: all pull together. Curr. Biol. 14:R992-R993.
24. Bengs F, Scholz A, Kuhn D, Wiese M. 2005. LmxMPK9, a mitogenactivated protein kinase homologue affects flagellar length in Leishmania mexicana. Mol. Microbiol. 55:1606 -1615.
25. Erdmann M, Scholz A, Melzer IM, Schmetz C, Wiese M. 2006. Interacting protein kinases involved in the regulation of flagellar length. Mol. Biol. Cell 17:2035-2045.
26. Portman N, Lacomble S, Thomas B, McKean PG, Gull K. 2009. Combining RNA interference mutants and comparative proteomics to identify protein components and dependences in a eukaryotic flagellum. J. Biol. Chem. 284:5610 -5619.
27. Forestier CL, Machu C, Loussert C, Pescher P, Spath GF. 2011. Imaging host cell-Leishmania interaction dynamics implicates parasite motility, lysosome recruitment, and host cell wounding in the infection process. Cell Host Microbe 9:319 -330.
28. Crissman HA, Gadbois DM, Tobey RA, Bradbury EM. 1991. Transformed mammalian cells are deficient in kinase-mediated control of progression through the G1 phase of the cell cycle. Proc. Natl. Acad. Sci. U.S.A. 88:7580 -7584.
29. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, Faraoni R, Floyd M, Hunt JP, Lockhart DJ, Milanov ZV, Morrison MJ, Pallares G, Patel HK, Pritchard S, Wodicka LM, Zarrinkar PP. 2008. A quantitative analysis of kinase inhibitor selectivity. Nat. Biotechnol. 26:127-132.
30. Parsons M, Worthey EA, Ward PN, Mottram JC. 2005. Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi.BMCGenomics 6:127.
31. Kaczanowski S, Sajid M, Reece SE. 2011. Evolution of apoptosis-like programmed cell death in unicellular protozoan parasites. Parasit. Vectors 4:44.
32. Smirlis D, Duszenko M, Ruiz AJ, Scoulica E, Bastien P, Fasel N, Soteriadou K. 2010. Targeting essential pathways in trypanosomatids gives insights into protozoan mechanisms of cell death. Parasit. Vectors 3:107.
33. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, Beck A, Beverley SM, Bianchettin G, Borzym K, Bothe G, Bruschi CV, Collins M, Cadag E, Ciarloni L, Clayton C, Coulson RM, Cronin A, Cruz AK, Davies RM, De Gaudenzi J, Dobson DE, Duesterhoeft A, Fazelina G, Fosker N, Frasch AC, Fraser A, Fuchs M, Gabel C, Goble A, Goffeau A, Harris D, Hertz-Fowler C, Hilbert H, Horn D, Huang Y, Klages S, Knights A, Kube M, Larke N, Litvin L, Lord A, Louie T, Marra M, Masuy D, Matthews K, Michaeli S, Mottram JC, Muller-Auer S, Munden H, Nelson S, Norbertczak H, Oliver K, O'Neil S, Pentony M, Pohl TM, Price C, Purnelle B, Quail MA, Rabbinowitsch E, Reinhardt R, Rieger M, Rinta J, Robben J, Robertson L, Ruiz JC, Rutter S, Saunders D, Schafer M, Schein J, Schwartz DC, Seeger K, Seyler A, Sharp S, Shin H, Sivam D, Squares R, Squares S, Tosato V, Vogt C, Volckaert G, Wambutt R, Warren T, Wedler H, Woodward J, Zhou S, Zimmermann W, Smith DF, Blackwell JM, Stuart KD, Barrell B, Myler PJ. 2005. The genome of the kinetoplastid parasite, Leishmania major. Science 309:436-442.
34. Imbert L, Ramos RG, Libong D, Abreu S, Loiseau PM, Chaminade P. 2012. Identification of phospholipid species affected by miltefosine action in Leishmania donovani cultures using LC-ELSD, LC-ESI/MS, and multivariate data analysis. Anal. Bioanal Chem. 402:1169 -1182.
35. Gonzalez IJ, Desponds C, Schaff C, Mottram JC, Fasel N. 2007. Leishmania major metacaspase can replace yeast metacaspase in programmed cell death and has arginine-specific cysteine peptidase activity. Int. J. Parasitol. 37:161-172.
36. Lee N, Bertholet S, Debrabant A, Muller J, Duncan R, Nakhasi HL. 2002. Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ. 9:53- 64.
37. Zalila H, Gonzalez IJ, El-Fadili AK, Delgado MB, Desponds C, Schaff C, Fasel N. 2011. Processing of metacaspase into a cytoplasmic catalytic domain mediating cell death in Leishmania major. Mol. Microbiol. 79: 222-239.
38. Hassan P, Fergusson D, Grant KM, Mottram JC. 2001. The CRK3 protein kinase is essential for cell cycle progression of Leishmania mexicana. Mol. Biochem. Parasitol. 113:189 -198.
39. Diaz-Gonzalez R, Kuhlmann FM, Galan-Rodriguez C, Madeira da Silva L, Saldivia M, Karver CE, Rodriguez A, Beverley SM, Navarro M, Pollastri MP. 2011. The susceptibility of trypanosomatid pathogens to PI3/mTOR kinase inhibitors affords a new opportunity for drug repurposing. PLoS Negl. Trop. Dis. 5:e1297. doi:10.1371/journal.pntd.0001297.
40. Kurokawa M, Kornbluth S. 2009. Caspases and kinases in a death grip. Cell 138:838-854.
41. Emoto Y, Manome Y, Meinhardt G, Kisaki H, Kharbanda S, Robertson M, Ghayur T, Wong WW, Kamen R, Weichselbaum R, et al. 1995. Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO J. 14:6148-6156.
42. Widmann C, Gibson S, Johnson GL. 1998. Caspase-dependent cleavage of signaling proteins during apoptosis. A turn-off mechanism for antiapoptotic signals. J. Biol. Chem. 273:7141-7147.
43. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF. 2001. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3:339 -345.
44. Zambon AC, Zhang L, Minovitsky S, Kanter JR, Prabhakar S, Salomonis N, Vranizan K, Dubchak I, Conklin BR, Insel PA. 2005. Gene expression patterns define key transcriptional events in cell-cycle regulation by cAMP and protein kinase A. Proc. Natl. Acad. Sci. U.S.A. 102: 8561-8566.
45. Zhang L, Zambon AC, Vranizan K, Pothula K, Conklin BR, Insel PA. 2008. Gene expression signatures of cAMP/protein kinase A (PKA)- promoted, mitochondrial-dependent apoptosis. Comparative analysis of wild-type and cAMP-deathless S49 lymphoma cells. J. Biol. Chem. 283: 4304-4313.