The Meaning of Death: Evolution and Ecology of Apoptosis in Protozoan Parasites

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The discovery that an apoptosis-like, programmed cell death (PCD) occurs in a broad range of protozoan parasites offers novel therapeutic tools to treat some of the most serious infectious diseases of humans, companion animals, wildlife, and livestock. Whilst apoptosis is an essential part of normal development, maintenance, and defence in multicellular organisms, its occurrence in unicellular parasites appears counter-intuitive and has proved highly controversial: according to the Darwinian notion of “survival of the fittest”, parasites are expected to evolve strategies to maximise their proliferation, not death. The prevailing, and untested, opinion in the literature is that parasites employ apoptosis to “altruistically” self-regulate the intensity of infection in the host/vector. However, evolutionary theory tells us that at most, this can only be part of the explanation, and other non-mutually exclusive hypotheses must also be tested. Here, we explain the evolutionary concepts that can explain apoptosis in unicellular parasites, highlight the key questions, and outline the approaches required to resolve the controversy over whether parasites “commit suicide”. We highlight the need for integration of proximate and functional approaches into an evolutionary framework to understand apoptosis in unicellular parasites. Understanding how, when, and why parasites employ apoptosis is central to targeting this process with interventions that are sustainable in the face of parasite evolution.

Vyšlo v časopise: The Meaning of Death: Evolution and Ecology of Apoptosis in Protozoan Parasites. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002320
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002320

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Zdroje

1. KerrJFWyllieAHCurrieAR 1972 Apoptosis: a basic biological phenomenon with wide ranging implications in tissue kinetics. Br J Cancer 26 239 257

2. GardnerAGrafenA 2009 Capturing the superorganism: a formal theory of group adaptation. J Evol Biol 22 659 671

3. HamiltonWD 1964 The genetical evolution of social behaviour, I & II. J Theor Biol 7 1 52

4. GordeevaAVLabasYAZvyagilskayaRA 2004 Apoptosis in unicellular organisms: mechanisms and evolution. Biochem J 69 1055 1066

5. AmeisenJC 1996 The origin of programmed cell death. Science 272 1278 1279

6. VercammenDDeclercqWVandenabeelePVan BreusegemF 2007 Are metacaspases caspases? J Cell Biol 179 375 380

7. Le ChatLSindenREDessensJT 2007 The role of metacaspase 1 in Plasmodium berghei development and apoptosis. Mol Biochem Parasitol 153 41 47

8. NguewaPAFuertesMAValladaresBAlonsoCPerezJM 2004 Programmed cell death in trypanosomatids: a way to maximize their biological fitness? Trends Parasitol 20 375 380

9. van ZandbergenGLuderCGHeusslerVDuszenkoM Programmed cell death in unicellular parasites: a prerequisite for sustained infection? Trends Parasitol 26 477 483

10. HurdHCarterV 2004 The role of programmed cell death in Plasmodium-mosquito interactions. Int J Parasitol 34 1459 1472

11. DebrabantALeeNBertholetSDunconRNakhasiHL 2003 Programmed cell death in trypanosomatids and other unicellular organisms. Int J Parasitol 33 257 267

12. MeslinBZalilaHFaselNPicotSBienvenuA-L 2011 Are protozoan metacaspases potential parasite killers? Parasit Vectors 4 26

13. WelburnSCMacleodEFigarellaKDuszenkoM 2006 Programmed cell death in African trypanosomes. Parasitology 132 s7 s18

14. SaranS 2000 Programmed cell death. Curr Sci 78 575 586

15. MeierPFinchAEvanG 2000 Apoptosis in development. Nature 407 796 801

16. KroemerGGalluzziLVandenebeelePAdbramsJAlnemriES 2009 Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16 3 11

17. SavilJFadokV 2000 Corpse clearance defines the meaning of cell death. Nature 407 784 788

18. SayanBSInceGSayanAEOzturkM 2001 NAPO as a novel marker for apoptosis. J Cell Biol 155 719 724

19. ZanggerHMottramJCFaselN 2002 Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis? Cell Death Differ 9 1126 1139

20. MoharikarSD'SouzaJSKulkarniABRaoBJ 2006 Apoptotic-like cell death pathway is induced in unicellular chlorophyte Chlamydomonas reinhardtii (chlorophyceae) cells following UV irradiation: detection and functional analyses. J Phycol 42 423 433

21. Al-OlayanEMWilliamsGTHurdH 2002 Apoptosis in the malaria protozoan, Plasmodium berghei: a possible mechanism for limiting intensity of infection in the mosquito. Int J Parasitol 32 1133 1143

22. AmeisenJCIdziorekTBillautmulotOLoyensMTissierJP 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

23. CornillonSFoaCDavoustJBuonavistaNGrossJD 1994 Programmed cell death in Dictostelium. J Cell Sci 107 2691 2704

24. FröhlichK-UMadeoF 2000 Apoptosis in yeast-a monocellular organism exhibits altruistic behaviour. FEBS Lett 473 6 9

25. SatBHazanRFisherTKhanerHGlaserG 2001 Programmed cell death in Escherichia coli: some antibiotics can trigger mazEF lethality. J Bacteriol 183 2041 2045

26. PicotSBurnodJBracchiVChumpitaziBFFAmbroise-ThomasP 1997 Apoptosis related to chloroquine sensitivity of the human malaria parasite Plasmodium falciparum. Trans R Soc Trop Med Hyg 91 590 591

27. MoreiraMECDel PortilloHAMilderRVBalancoJMBarcinskiMA 1996 Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis. J Cell Physiol 167 305 313

28. MadeoFEngelhardtSHerkerELehmannNMaldenerC 2002 Apoptosis in yeast: a new model system with applications in cell biology and medicine. Curr Genet 41 208 216

29. ArambageSGrantKPardoIRanford-CartwrightLHurdH 2009 Malaria ookinetes exhibit multiple markers for apoptosis-like programmed cell death in vitro. Parasit Vectors 2 32

30. PollittLCColegraveNKhanSSajidMReeceSE 2010 Investigating the evolution of apoptosis in malaria parasites: the importance of ecology. ParasitVectors 3 105

31. SturmAAminoRSandCvdRegenTRetzlaffS 2006 Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313 1287 1290

32. AliMAl-OlayanEMLewisSMatthewsHHurdH 2010 Naturally occurring triggers that induce apoptosis-like programmed cell death in Plasmodium berghei ookinetes. PLoS ONE 5 e12634 doi:10.1371/journal.pone.0012634

33. Ch'ngJHKotturiSRChongAGLLearMJTanKSW 2010 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. Cell Death Dis 1 e26

34. MeslinBBarnadasCBoniVLatourCDe MonbrisonF 2007 Features of apoptosis in Plasmodium falciparum erythrocytic stage through a putative role of PfMCA1 metacaspase-like protein. J Infect Dis 195 1852 1859

35. Jimenez-RuizAAlzateJMacLeodELuderCGFaselN 2010 Apoptotic markers in protozoan parasites. Parasit Vectors 3 104

36. KaczanowskiSSajidMReeceSE 2011 Evolution of apoptosis-like programmed cell death in unicellular protozoan parasites. Parasit Vectors 4 44

37. NedelcuADriscollWDurandPHerronMRashidiE 2011 On the paradigm of altruistic suicide in the unicellular world. Evolution 65 3 20

38. AmeisenJC 2002 On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ 9 367 393

39. VauxDLHaeckerGStrasserA 1994 An evolutionary perspective on apoptosis. Cell 76 777 779

40. HamiltonWD 1963 The evolution of altruistic behaviour. Am Nat 97 354 356

41. WestSAGriffinASGardnerA 2007 Evolutionary explanations for cooperation. Curr Biol 17 661 672

42. WestSAGriffinASGardnerA 2007 Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 20 415 432

43. FrankSA 1998 Foundations of social evolution. Princeton Princeton University Press

44. HardinG 1968 The tragedy of the commons. Science 162 1243 1248

45. FiegnaFYuYTNKadamSVVelicerGJ 2006 Evolution of an obligate social cheater to a superior cooperator. Nature 441 310 314

46. GrafenA 2006 Optimization of inclusive fitness. J Theor Biol 238 541 563

47. GrafenA 1985 A geometric view of relatedness. Oxford Surv Evol Biol 2 28 89

48. GardnerAWestSAWildG 2011 The genetical theory of kin selection. J Evol Biol 24 1020 1043

49. ReeceSERamiroRSNusseyDH 2009 Plastic parasites: sophisticated strategies for survival and reproduction? Evol Appl 2 11 23

50. WestSAGriffinASGardnerADiggleSP 2006 Social evolution theory for microorganisms. Nature Rev Microbiol 4 597 607

51. DuszenkoMFigarellaKMacleodETWelburnSC 2006 Death of a trypanosome: a selfish altruism. Trends Parasitol 22 536 542

52. BruchhausIRoederTRennenbergAHeusslerVT 2007 Protozoan parasites: programmed cell death as a mechanism of parasitism. Trends Parasitol 23 376 383

53. HurdHGrantKMArambageSC 2006 Apoptosis-like death as a feature of malaria infection in mosquitoes. Parasitology 132 S33 S47

54. SwiftSAllan DownieJWhiteheadNABarnardAMLSalmondGPC 2001 Quorum sensing as a population-density-dependent determinant of bacterial physiology. Advanc Microbial Physiol Academic Press 199 270

55. DyerMDayKP 2003 Regulation of the rate of asexual growth and commitment to sexual development by diffusible factors from in vitro cultures of Plasmodium faliciparum. Am J Trop Med Hyg 68 403 409

56. ReeceSEAliESchneiderPBabikerHA 2010 Stress, drugs and the evolution of reproductive restraint in malaria parasites. Proc Biol Sci: 277 3123 3129

57. ReeceSEDrewDRGardnerA 2008 Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453 609 615

58. PollittLCMacGregorPMatthewsKRReeceSE 2011 Malaria and trypanosome transmission: different parasites, same rules? Trends Parasitol 27 197 203

59. PollittLCMideoNDrewDRColegraveNSchneiderP 2011 Competition and the Evolution of Reproductive Restraint in Malaria Parasites. Amer Nat 177 358 367

60. RoussetFRozeD 2007 Constraints on the origin and maintenance of genetic kin recognition. Evolution 61 2320 2330

61. CrozierRH 1986 Genetic clonal recognition abilities in marine invertebrates must be maintained by selection for something else. Evolution 40 1100 1101

62. GardnerAWestSA 2007 Social evolution: The decline and fall of genetic kin recognition. Cur Biol 17 810 812

63. AckermannMStecherBFreedNESonghetPHardtW-D 2008 Self-destructive cooperation mediated by phenotypic noise. Nature 454 987 990

64. DurandPMRashidiAMichodRE 2011 How an organism dies affects the fitness of its neighbours. Am Nat 177 : 177 224 232

65. SegoviaMHaramatyLBergesJAFalkowskiPG 2003 Cell death in the unicellular chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol 132 99 105

66. GardnerAKummerliR 2008 Social evolution: this microbe will self destruct. Curr Biol 18 R1021 R1023

67. GrafenA 2002 A first formal link between the price equation and an optimization program. J Theor Biol 217 75 91

68. MutaiBKWaitumbiJN Apoptosis stalks Plasmodium falciparum maintained in continuous culture condition. Malar J 9 Suppl 3 S6

69. AravindLDixitVMKooninEV 1999 The domains of death: evolution of the apoptosis machinery. Trends Biochem Sci 24 47 53

70. AtkinsonHJBabbittPCSajidM 2009 The global cysteine peptidase landscape in parasites. Trends Parasitol 25 573 581

71. WuYMWangXYLiuXWangYF 2003 Data-mining approaches reveal hidden families of proteases in the genome of malaria parasite. Genome Res 13 601 616

72. AbrahamMCShahamS 2004 Death without caspases, caspases without death. Trends Cell Biol 14 184 193

73. LeistMJäätteläM 2001 Four deaths and a funeral: from caspases to alternative mechanisms. Nature Rev Mol Cell Biol 2 589 598