Open Access
Review Article
Issue
Parasite
Volume 26, 2019
Article Number 71
Number of page(s) 13
DOI https://doi.org/10.1051/parasite/2019071
Published online 11 December 2019
  1. Alcolea PJ, Alonso A, Gomez MJ, Sanchez-Gorostiaga A, Moreno-Paz M, Gonzalez-Pastor E, Torano A, Parro V, Larraga V. 2010. Temperature increase prevails over acidification in gene expression modulation of amastigote differentiation in Leishmania infantum. BMC Genomics, 11(1), 31. [CrossRef] [PubMed] [Google Scholar]
  2. Ambit A, Fasel N, Coombs GH, Mottram JC. 2008. An essential role for the Leishmania major metacaspase in cell cycle progression. Cell Death & Differentiation, 15(1), 113–122. [CrossRef] [Google Scholar]
  3. 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 & Differentiation, 9(1), 65–81. [CrossRef] [Google Scholar]
  4. Basmaciyan L, Azas N, Casanova M. 2017. Calcein+/PI- as an early apoptotic feature in Leishmania. PLoS One, 12(11), e0187756. [CrossRef] [PubMed] [Google Scholar]
  5. Basmaciyan L, Azas N, Casanova M. 2018. Different apoptosis pathways in Leishmania parasites. Cell Death Discovery, 5, 27. [Google Scholar]
  6. Basmaciyan L, Azas N, Casanova M. 2019. A potential acetyltransferase involved in Leishmania major metacaspase-dependent cell death. Parasites & Vectors, 12(1), 266. [CrossRef] [PubMed] [Google Scholar]
  7. Basmaciyan L, Berry L, Gros J, Azas N, Casanova M. 2018. Temporal analysis of the autophagic and apoptotic phenotypes in Leishmania parasites. Microbial Cell, 5(9), 404–417. [CrossRef] [Google Scholar]
  8. Basmaciyan L, Jacquet P, Azas N, Casanova M. 2019. A novel hydrolase with a pro-death activity from the protozoan parasite Leishmania major. Cell Death Discovery, 5(1), 99. [CrossRef] [PubMed] [Google Scholar]
  9. Bates PA. 2008. Leishmania sand fly interaction: progress and challenges. Current Opinion in Microbiology, 11(4), 340–344. [CrossRef] [PubMed] [Google Scholar]
  10. Besteiro S, Williams RAM, Morrison LS, Coombs GH, Mottram JC. 2006. Endosome sorting and autophagy are essential for differentiation and virulence of Leishmania major. Journal of Biological Chemistry, 281(16), 11384–11396. [CrossRef] [Google Scholar]
  11. BoseDasgupta S, Das BB, Sengupta S, Ganguly A, Roy A, Dey S, Tripathi G, Dinda B, Majumder HK. 2008. 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”. Cell Death & Differentiation, 15(10), 1629–1640. [CrossRef] [Google Scholar]
  12. Bredesen DE. 2000. Apoptosis: overview and signal transduction pathways. Journal of Neurotrauma, 17(10), 801–810. [CrossRef] [PubMed] [Google Scholar]
  13. Bröker LE, Kruyt FAE, Giaccone G. 2005. Cell death independent of caspases: a review. Clinical Cancer Research, 11(9), 3155–3162. [CrossRef] [PubMed] [Google Scholar]
  14. Bruchhaus I, Roeder T, Rennenberg A, Heussler VT. 2007. Protozoan parasites: programmed cell death as a mechanism of parasitism. Trends in Parasitology, 23(8), 376–383. [CrossRef] [PubMed] [Google Scholar]
  15. Carmona-Gutierrez D, Bauer MA, Zimmermann A, Aguilera A, Austriaco N, Ayscough K, Balzan R, Bar-Nun S, Barrientos A, Belenky P, Blondel M, Braun RJ, Breitenbach M, Burhans WC, Buettner S, Cavalieri D, Chang M, Cooper KF, Côrte-Real M, Costa V, Cullin C, Dawes I, Dengjel J, Dickman MB, Eisenberg T, Fahrenkrog B, Fasel N, Froehlich K-U, Gargouri A, Giannattasio S, Goffrini P, Gourlay CW, Grant CM, Greenwood MT, Guaragnella N, Heger T, Heinisch J, Herker E, Herrmann JM, Hofer S, Jiménez-Ruiz A, Jungwirth H, Kainz K, Kontoyiannis DP, Ludovico P, Manon S, Martegani E, Mazzoni C, Megeney LA, Meisinger C, Nielsen J, Nystroem T, Osiewacz HD, Outeiro TF, Park H-O, Pendl T, Petranovic D, Picot S, Polčic P, Powers T, Ramsdale M, Rinnerthaler M, Rockenfeller P, Ruckenstuhl C, Schaffrath R, Segovia M, Severin FF, Sharon A, Sigrist SJ, Sommer-Ruck C, Sousa MJ, Thevelein JM, Thevissen K, Titorenko V, Toledano MB, Tuite M, Voegtle F-N, Westermann B, Winderickx J, Wissing S, Woelfl S, Zhang ZJ, Zhao RY, Zhou B, Galluzzi L, Kroemer G, Madeo F. 2018. Guidelines and recommendations on yeast cell death nomenclature. Microbial Cell, 5(1), 4–31. [CrossRef] [Google Scholar]
  16. Casanova M, Gonzalez IJ, Sprissler C, Zalila H, Dacher M, Basmaciyan L, Späth GF, Azas N, Fasel N. 2015. Implication of different domains of the Leishmania major metacaspase in cell death and autophagy. Cell Death & Disease, 6, e1933. [CrossRef] [PubMed] [Google Scholar]
  17. Castanys-Muñoz E, Brown E, Coombs GH, Mottram JC. 2012. Leishmania mexicana metacaspase is a negative regulator of amastigote proliferation in mammalian cells. Cell Death & Disease, 3, e385. [CrossRef] [PubMed] [Google Scholar]
  18. Chowdhury S, Mukherjee T, Chowdhury SR, Sengupta S, Mukhopadhyay S, Jaisankar P, Majumder HK. 2014. Disuccinyl betulin triggers metacaspase-dependent endonuclease G-mediated cell death in unicellular protozoan parasite Leishmania donovani. Antimicrobial Agents & Chemotherapy, 58(4), 2186–2201. [CrossRef] [Google Scholar]
  19. Crauwels P, Bohn R, Thomas M, Gottwalt S, Jäckel F, Krämer S, Bank E, Tenzer S, Walther P, Bastian M, van Zandbergen G. 2015. Apoptotic-like Leishmania exploit the host’s autophagy machinery to reduce T-cell-mediated parasite elimination. Autophagy, 11(2), 285–297. [CrossRef] [PubMed] [Google Scholar]
  20. da Silva R, Sacks DL. 1987. Metacyclogenesis is a major determinant of Leishmania promastigote virulence and attenuation. Infection & Immunity, 55(11), 2802–2806. [CrossRef] [Google Scholar]
  21. Debrabant A, Nakhasi H. 2003. Programmed cell death in trypanosomatids: is it an altruistic mechanism for survival of the fittest? Kinetoplastid Biology & Disease, 2(1), 7. [CrossRef] [Google Scholar]
  22. Djavaheri-Mergny M, Maiuri MC, Kroemer G. 2010. Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1. Oncogene, 29(12), 1717–1719. [Google Scholar]
  23. Dotiwala F, Mulik S, Polidoro RB, Ansara JA, Burleigh BA, Walch M, Gazzinelli RT, Lieberman J. 2016. Killer lymphocytes use granulysin, perforin and granzymes to kill intracellular parasites. Nature Medicine, 22(2), 210–216. [CrossRef] [PubMed] [Google Scholar]
  24. Duszenko M, Figarella K, Macleod ET, Welburn SC. 2006. Death of a trypanosome: a selfish altruism. Trends in Parasitology, 22(11), 536–542. [CrossRef] [PubMed] [Google Scholar]
  25. 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 & Disease, 1, e71. [CrossRef] [PubMed] [Google Scholar]
  26. Elmore S. 2007. Apoptosis: a review of programmed cell death. Toxicologic Pathology, 35(4), 495–516. [CrossRef] [PubMed] [Google Scholar]
  27. Ersfeld K, Barraclough H, Gull K. 2005. Evolutionary relationships and protein domain architecture in an expanded calpain superfamily in kinetoplastid parasites. Journal of Molecular Evolution, 61(6), 742–757. [CrossRef] [PubMed] [Google Scholar]
  28. Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D, Alnemri ES, Altucci L, Andrews D, Annicchiarico-Petruzzelli M, Baehrecke EH, Bazan NG, Bertrand MJ, Bianchi K, Blagosklonny MV, Blomgren K, Borner C, Bredesen DE, Brenner C, Campanella M, Candi E, Cecconi F, Chan FK, Chandel NS, Cheng EH, Chipuk JE, Cidlowski JA, Ciechanover A, Dawson TM, Dawson VL, De Laurenzi V, De Maria R, Debatin K-M, Di Daniele N, Dixit VM, Dynlacht BD, El-Deiry WS, Fimia GM, Flavell RA, Fulda S, Garrido C, Gougeon M-L, Green DR, Gronemeyer H, Hajnoczky G, Hardwick JM, Hengartner MO, Ichijo H, Joseph B, Jost PJ, Kaufmann T, Kepp O, Klionsky DJ, Knight RA, Kumar S, Lemasters JJ, Levine B, Linkermann A, Lipton SA, Lockshin RA, López-Otín C, Lugli E, Madeo F, Malorni W, Marine J-C, Martin SJ, Martinou J-C, Medema JP, Meier P, Melino S, Mizushima N, Moll U, Muñoz-Pinedo C, Nuñez G, Oberst A, Panaretakis T, Penninger JM, Peter ME, Piacentini M, Pinton P, Prehn JH, Puthalakath H, Rabinovich GA, Ravichandran KS, Rizzuto R, Rodrigues CM, Rubinsztein DC, Rudel T, Shi Y, Simon H-U, Stockwell BR, Szabadkai G, Tait SW, Tang HL, Tavernarakis N, Tsujimoto Y, Vanden Berghe T, Vandenabeele P, Villunger A, Wagner EF, Walczak H, White E, Wood WG, Yuan J, Zakeri Z, Zhivotovsky B, Melino G, Kroemer G. 2015. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death & Differentiation, 22(1), 58–73. [CrossRef] [MathSciNet] [PubMed] [Google Scholar]
  29. Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, Annicchiarico-Petruzzelli M, Antonov AV, Arama E, Baehrecke EH, Barlev NA, Bazan NG, Bernassola F, Bertrand MJM, Bianchi K, Blagosklonny MV, Blomgren K, Borner C, Boya P, Brenner C, Campanella M, Candi E, Carmona-Gutierrez D, Cecconi F, Chan FK-M, Chandel NS, Cheng EH, Chipuk JE, Cidlowski JA, Ciechanover A, Cohen GM, Conrad M, Cubillos-Ruiz JR, Czabotar PE, D’Angiolella V, Dawson TM, Dawson VL, De Laurenzi V, De Maria R, Debatin K-M, DeBerardinis RJ, Deshmukh M, Di Daniele N, Di Virgilio F, Dixit VM, Dixon SJ, Duckett CS, Dynlacht BD, El-Deiry WS, Elrod JW, Fimia GM, Fulda S, García-Sáez AJ, Garg AD, Garrido C, Gavathiotis E, Golstein P, Gottlieb E, Green DR, Greene LA, Gronemeyer H, Gross A, Hajnoczky G, Hardwick JM, Harris IS, Hengartner MO, Hetz C, Ichijo H, Jäättelä M, Joseph B, Jost PJ, Juin PP, Kaiser WJ, Karin M, Kaufmann T, Kepp O, Kimchi A, Kitsis RN, Klionsky DJ, Knight RA, Kumar S, Lee SW, Lemasters JJ, Levine B, Linkermann A, Lipton SA, Lockshin RA, López-Otín C, Lowe SW, Luedde T, Lugli E, MacFarlane M, Madeo F, Malewicz M, Malorni W, Manic G, Marine J-C, Martin SJ, Martinou J-C, Medema JP, Mehlen P, Meier P, Melino S, Miao EA, Molkentin JD, Moll UM, Muñoz-Pinedo C, Nagata S, Nuñez G, Oberst A, Oren M, Overholtzer M, Pagano M, Panaretakis T, Pasparakis M, Penninger JM, Pereira DM, Pervaiz S, Peter ME, Piacentini M, Pinton P, Prehn JHM, Puthalakath H, Rabinovich GA, Rehm M, Rizzuto R, Rodrigues CMP, Rubinsztein DC, Rudel T, Ryan KM, Sayan E, Scorrano L, Shao F, Shi Y, Silke J, Simon H-U, Sistigu A, Stockwell BR, Strasser A, Szabadkai G, Tait SWG, Tang D, Tavernarakis N, Thorburn A, Tsujimoto Y, Turk B, Vanden Berghe T, Vandenabeele P, Vander Heiden MG, Villunger A, Virgin HW, Vousden KH, Vucic D, Wagner EF, Walczak H, Wallach D, Wang Y, Wells JA, Wood W, Yuan J, Zakeri Z, Zhivotovsky B, Zitvogel L, Melino G, Kroemer G. 2018. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death & Differentiation, 25(3), 486–541. [CrossRef] [Google Scholar]
  30. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, Gottlieb E, Green DR, Hengartner MO, Kepp O, Knight RA, Kumar S, Lipton SA, Lu X, Madeo F, Malorni W, Mehlen P, Nuñez G, Peter ME, Piacentini M, Rubinsztein DC, Shi Y, Simon H-U, Vandenabeele P, White E, Yuan J, Zhivotovsky B, Melino G, Kroemer G. 2012. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death and Differentiation, 19(1), 107–120. [CrossRef] [PubMed] [Google Scholar]
  31. Gannavaram S, Vedvyas C, Debrabant A. 2008. Conservation of the pro-apoptotic nuclease activity of endonuclease G in unicellular trypanosomatid parasites. Journal of Cell Science, 121(1), 99–109. [CrossRef] [PubMed] [Google Scholar]
  32. Genes CM, de Lucio H, González VM, Sánchez-Murcia PA, Rico E, Gago F, Fasel N, Jiménez-Ruiz A. 2016. A functional BH3 domain in an aquaporin from Leishmania infantum. Cell Death Discovery, 2, 16043. [CrossRef] [PubMed] [Google Scholar]
  33. Genes CM, de Lucio H, Sánchez-Murcia PA, Gago F, Jiménez-Ruiz A. 2016. Pro-death activity of a BH3 domain in an aquaporin from the protozoan parasite Leishmania. Cell Death & Disease, 7(7), e2318–e2318. [CrossRef] [PubMed] [Google Scholar]
  34. Goll DE, Thompson VF, Li H, Wei W, Cong J. 2003. The calpain system. Physiological Reviews, 83(3), 731–801. [CrossRef] [PubMed] [Google Scholar]
  35. González 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. International Journal for Parasitology, 37(2), 161–172. [CrossRef] [PubMed] [Google Scholar]
  36. Holzmuller P, Sereno D, Cavaleyra M, Mangot I, Daulouede S, Vincendeau P, Lemesre J-L. 2002. Nitric oxide-mediated proteasome-dependent oligonucleosomal DNA fragmentation in Leishmania amazonensis amastigotes. Infection and Immunity, 70(7), 3727–3735. [CrossRef] [PubMed] [Google Scholar]
  37. Jeong H-S, Choi HY, Lee E-R, Kim J-H, Jeon K, Lee H-J, Cho S-G. 2011. Involvement of caspase-9 in autophagy-mediated cell survival pathway. Biochimica et Biophysica Acta, 1813(1), 80–90. [CrossRef] [PubMed] [Google Scholar]
  38. Jiménez-Ruiz A, Alzate JF, Macleod ET, Lüder CGK, Fasel N, Hurd H. 2010. Apoptotic markers in protozoan parasites. Parasites & Vectors, 3, 104. [CrossRef] [PubMed] [Google Scholar]
  39. Kerr JF, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer, 26(4), 239–257. [CrossRef] [PubMed] [Google Scholar]
  40. Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D, Vandenabeele P, Zhivotovsky B, Blagosklonny MV, Malorni W, Knight RA, Piacentini M, Nagata S, Melino G. 2005. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death & Differentiation, 12(S2), 1463–1467. [CrossRef] [PubMed] [Google Scholar]
  41. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nuñez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G, Nomenclature Committee on Cell Death 2009. 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death and Differentiation, 16(1), 3–11. [CrossRef] [PubMed] [Google Scholar]
  42. Lamkanfi M, Festjens N, Declercq W, Vanden Berghe T, Vandenabeele P. 2007. Caspases in cell survival, proliferation and differentiation. Cell Death & Differentiation, 14(1), 44–55. [CrossRef] [Google Scholar]
  43. Lee N, Bertholet S, Debrabant A, Muller J, Duncan R, Nakhasi HL. 2002. Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death & Differentiation, 9(1), 53–64. [CrossRef] [Google Scholar]
  44. Lee N, Gannavaram S, Selvapandiyan A, Debrabant A. 2007. Characterization of metacaspases with trypsin-like activity and their putative role in programmed cell death in the protozoan parasite Leishmania. Eukaryotic Cell, 6(10), 1745–1757. [Google Scholar]
  45. Levine B, Klionsky DJ. 2004. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Developmental Cell, 6(4), 463–477. [CrossRef] [PubMed] [Google Scholar]
  46. Li LY, Luo X, Wang X. 2001. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature, 412(6842), 95–99. [Google Scholar]
  47. Lüder CG, Campos-Salinas J, Gonzalez-Rey E, van Zandbergen G. 2010. Impact of protozoan cell death on parasite-host interactions and pathogenesis. Parasites & Vectors, 3, 116. [CrossRef] [PubMed] [Google Scholar]
  48. Mariño G, Niso-Santano M, Baehrecke EH, Kroemer G. 2014. Self-consumption: the interplay of autophagy and apoptosis. Nature Reviews. Molecular Cell Biology, 15(2), 81–94. [CrossRef] [PubMed] [Google Scholar]
  49. Martin R, Gonzalez I, Fasel N. 2014. Leishmania metacaspase: an arginine-specific peptidase. Methods in Molecular Biology, 1133, 189–202. [CrossRef] [Google Scholar]
  50. Martin SJ. 1995. 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. Journal of Experimental Medicine, 182(5), 1545–1556. [CrossRef] [Google Scholar]
  51. McNicoll F, Drummelsmith J, Müller M, Madore É, Boilard N, Ouellette M, Papadopoulou B. 2006. A combined proteomic and transcriptomic approach to the study of stage differentiation in Leishmania infantum. Proteomics, 6(12), 3567–3581. [CrossRef] [PubMed] [Google Scholar]
  52. Meslin B, Beavogui AH, Fasel N, Picot S. 2011. Plasmodium falciparum metacaspase PfMCA-1 triggers a z-VAD-fmk inhibitable protease to promote cell death. PLoS One, 6(8), e23867. [CrossRef] [PubMed] [Google Scholar]
  53. Oliva C, Sánchez-Murcia PA, Rico E, Bravo A, Menéndez M, Gago F, Jiménez-Ruiz A. 2017. Structure-based domain assignment in Leishmania infantum EndoG: characterization of a pH-dependent regulatory switch and a C-terminal extension that largely dictates DNA substrate preferences. Nucleic Acids Research, 45(15), 9030–9045. [CrossRef] [PubMed] [Google Scholar]
  54. Padmanabhan PK, Samant M, Cloutier S, Simard MJ, Papadopoulou B. 2012. Apoptosis-like programmed cell death induces antisense ribosomal RNA (rRNA) fragmentation and rRNA degradation in Leishmania. Cell Death & Differentiation, 19(12), 1972–1982. [CrossRef] [Google Scholar]
  55. Paris C, Loiseau PM, Bories C, Bréard J. 2004. Miltefosine induces apoptosis-like death in Leishmania donovani promastigotes. Antimicrobial Agents and Chemotherapy, 48(3), 852–859. [CrossRef] [PubMed] [Google Scholar]
  56. Parrish J, Li L, Klotz K, Ledwich D, Wang X, Xue D. 2001. Mitochondrial endonuclease G is important for apoptosis in C. elegans. Nature, 412(6842), 90–94. [Google Scholar]
  57. Peña MS, Cabral GC, Fotoran WL, Perez KR, Stolf BS. 2017. Metacaspase-binding peptide inhibits heat shock-induced death in Leishmania (L.) amazonensis. Cell Death & Disease, 8(3), e2645–e2645. [CrossRef] [PubMed] [Google Scholar]
  58. Perrin BJ, Huttenlocher A. 2002. Calpain. The International Journal of Biochemistry & Cell Biology, 34(7), 722–725. [CrossRef] [PubMed] [Google Scholar]
  59. Proto WR, Coombs GH, Mottram JC. 2013. Cell death in parasitic protozoa: regulated or incidental? Nature Reviews Microbiology, 11(1), 58–66. [CrossRef] [PubMed] [Google Scholar]
  60. Raina P, Kaur S. 2012. Knockdown of LdMC1 and Hsp70 by antisense oligonucleotides causes cell-cycle defects and programmed cell death in Leishmania donovani. Molecular and Cellular Biochemistry, 359(1–2), 135–149. [CrossRef] [PubMed] [Google Scholar]
  61. Rico E, Alzate JF, Arias AA, Moreno D, Clos J, Gago F, Moreno I, Domínguez M, Jiménez-Ruiz A. 2009. Leishmania infantum expresses a mitochondrial nuclease homologous to EndoG that migrates to the nucleus in response to an apoptotic stimulus. Molecular and Biochemical Parasitology, 163(1), 28–38. [CrossRef] [PubMed] [Google Scholar]
  62. Rico E, Oliva C, Gutierrez KJ, Alzate JF, Genes CM, Moreno D, Casanova E, Gigante A, Perez-Perez M-J, Camarasa M-J, Clos J, Gago F, Jimenez-Ruiz A. 2014. Leishmania infantum EndoG is an endo/exo-nuclease essential for parasite survival. PLoS One, 9(2), e89526. [CrossRef] [PubMed] [Google Scholar]
  63. Shaha C. 2006. Apoptosis in Leishmania species & its relevance to disease pathogenesis. Indian Journal of Medical Research, 123(3), 233–244. [Google Scholar]
  64. 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. Parasites & Vectors, 3, 107. [CrossRef] [PubMed] [Google Scholar]
  65. Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV. 2011. Metacaspases. Cell Death & Differentiation, 18(8), 1279–1288. [CrossRef] [Google Scholar]
  66. van Loo G, Schotte P, van Gurp M, Demol H, Hoorelbeke B, Gevaert K, Rodriguez I, Ruiz-Carrillo A, Vandekerckhove J, Declercq W, Beyaert R, Vandenabeele P. 2001. Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation. Cell Death & Differentiation, 8(12), 1136–1142. [CrossRef] [Google Scholar]
  67. van Zandbergen G, Bollinger A, Wenzel A, Kamhawi S, Voll R, Klinger M, Müller A, Hölscher C, Herrmann M, Sacks D, Solbach W, Laskay T. 2006. Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proceedings of the National Academy of Sciences of the United States of America, 103(37), 13837–13842. [CrossRef] [PubMed] [Google Scholar]
  68. Vercammen D, Declercq W, Vandenabeele P, Van Breusegem F. 2007. Are metacaspases caspases? Journal of Cell Biology, 179(3), 375–380. [CrossRef] [Google Scholar]
  69. Vergnes B, Gourbal B, Girard I, Sundar S, Drummelsmith J, Ouellette M. 2007. A proteomics screen implicates HSP83 and a small kinetoplastid calpain-related protein in drug resistance in Leishmania donovani clinical field isolates by modulating drug-induced programmed cell death. Molecular & Cellular Proteomics, 6(1), 88–101. [CrossRef] [Google Scholar]
  70. Wanderley JLM, Pinto da Silva LH, Deolindo P, Soong L, Borges VM, Prates DB, de Souza APA, Barral A, Balanco JMdF, Nascimento MTCd, Saraiva EM, Barcinski MA. 2009. Cooperation between Apoptotic and Viable Metacyclics Enhances the Pathogenesis of Leishmaniasis. PLoS One, 4(5), e5733. [CrossRef] [PubMed] [Google Scholar]
  71. Weingärtner A, Kemmer G, Müller 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(8), e42070. [CrossRef] [PubMed] [Google Scholar]
  72. Welburn SC, Barcinski MA, Williams GT. 1997. Programmed cell death in trypanosomatids. Parasitology Today, 13(1), 22–26. [CrossRef] [Google Scholar]
  73. Zalila H, González 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. Molecular Microbiology, 79(1), 222–239. [CrossRef] [PubMed] [Google Scholar]
  74. Zangger H, Mottram JC, Fasel N. 2002. Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis? Cell Death & Differentiation, 9(10), 1126–1139. [CrossRef] [Google Scholar]

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.