Unveiling the Intracellular Survival Gene Kit of Trypanosomatid Parasites


Trypanosomatids are unicellular protozoans of medical and economical relevance since they are the etiologic agents of infectious diseases in humans as well as livestock. Whereas Trypanosoma cruzi and different species of Leishmania are obligate intracellular parasites, Trypanosoma brucei and other trypanosomatids develop extracellularly throughout their entire life cycle. After their genomes have been sequenced, various comparative genomic studies aimed at identifying sequences involved with host cell invasion and intracellular survival have been described. However, for only a handful of genes, most of them present exclusively in the T. cruzi or Leishmania genomes, has there been any experimental evidence associating them with intracellular parasitism. With the increasing number of published complete genome sequences of members of the trypanosomatid family, including not only different Trypanosoma and Leishmania strains and subspecies but also trypanosomatids that do not infect humans or other mammals, we may now be able to contemplate a slightly better picture regarding the specific set of parasite factors that defines each organism's mode of living and the associated disease phenotypes. Here, we review the studies concerning T. cruzi and Leishmania genes that have been implicated with cell invasion and intracellular parasitism and also summarize the wealth of new information regarding the mode of living of intracellular parasites that is resulting from comparative genome studies that are based on increasingly larger trypanosomatid genome datasets.


Vyšlo v časopise: Unveiling the Intracellular Survival Gene Kit of Trypanosomatid Parasites. PLoS Pathog 10(12): e32767. doi:10.1371/journal.ppat.1004399
Kategorie: Review
prolekare.web.journal.doi_sk: 10.1371/journal.ppat.1004399

Souhrn

Trypanosomatids are unicellular protozoans of medical and economical relevance since they are the etiologic agents of infectious diseases in humans as well as livestock. Whereas Trypanosoma cruzi and different species of Leishmania are obligate intracellular parasites, Trypanosoma brucei and other trypanosomatids develop extracellularly throughout their entire life cycle. After their genomes have been sequenced, various comparative genomic studies aimed at identifying sequences involved with host cell invasion and intracellular survival have been described. However, for only a handful of genes, most of them present exclusively in the T. cruzi or Leishmania genomes, has there been any experimental evidence associating them with intracellular parasitism. With the increasing number of published complete genome sequences of members of the trypanosomatid family, including not only different Trypanosoma and Leishmania strains and subspecies but also trypanosomatids that do not infect humans or other mammals, we may now be able to contemplate a slightly better picture regarding the specific set of parasite factors that defines each organism's mode of living and the associated disease phenotypes. Here, we review the studies concerning T. cruzi and Leishmania genes that have been implicated with cell invasion and intracellular parasitism and also summarize the wealth of new information regarding the mode of living of intracellular parasites that is resulting from comparative genome studies that are based on increasingly larger trypanosomatid genome datasets.


Zdroje

1. StevensJR (2008) Kinetoplastid phylogenetics, with special reference to the evolution of parasitic trypanosomes. Parasite 15: 226–232.

2. TeixeiraSM, El-SayedNM, AraujoPR (2011) The genome and its implications. Adv Parasitol 75: 209–230.

3. RudenkoG, BishopD, GottesdienerK, Van der PloegLH (1989) Alpha-amanitin resistant transcription of protein coding genes in insect and bloodstream form Trypanosoma brucei. Embo J 8: 4259–4263.

4. MatthewsKR, TschudiC, UlluE (1994) A common pyrimidine-rich motif governs trans-splicing and polyadenylation of tubulin polycistronic pre-mRNA in trypanosomes. Genes Dev 8: 491–501.

5. LeBowitzJH, SmithHQ, RuscheL, BeverleySM (1993) Coupling of poly(A) site selection and trans-splicing in Leishmania. Genes Dev 7: 996–1007.

6. HajdukS, OchsenreiterT (2010) RNA editing in kinetoplastids. RNA Biol 7: 229–236.

7. SmithDF, PeacockCS, CruzAK (2007) Comparative genomics: from genotype to disease phenotype in the leishmaniases. Int J Parasitol 37: 1173–1186.

8. BrenerZ (1973) Biology of Trypanosoma cruzi. Annu Rev Microbiol 27: 347–382.

9. FernandesMC, AndrewsNW (2012) Host cell invasion by Trypanosoma cruzi: a unique strategy that promotes persistence. FEMS Microbiol Rev 36: 734–747.

10. UenoN, WilsonME (2012) Receptor-mediated phagocytosis of Leishmania: implications for intracellular survival. Trends Parasitol 28: 335–344.

11. FennK, MatthewsKR (2007) The cell biology of Trypanosoma brucei differentiation. Curr Opin Microbiol 10: 539–546.

12. HornD, McCullochR (2010) Molecular mechanisms underlying the control of antigenic variation in African trypanosomes. Curr Opin Microbiol 13: 700–705.

13. BerrimanM, GhedinE, Hertz-FowlerC, BlandinG, RenauldH, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416–422.

14. El-SayedNM, MylerPJ, BartholomeuDC, NilssonD, AggarwalG, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409–415.

15. IvensAC, PeacockCS, WortheyEA, MurphyL, AggarwalG, et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436–442.

16. WeatherlyDB, BoehlkeC, TarletonRL (2009) Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10: 255.

17. El-SayedNM, MylerPJ, BlandinG, BerrimanM, CrabtreeJ, et al. (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309: 404–409.

18. NgoH, TschudiC, GullK, UlluE (1998) Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc Natl Acad Sci U S A 95: 14687–14692.

19. LyeLF, OwensK, ShiH, MurtaSM, VieiraAC, et al. (2010) Retention and loss of RNA interference pathways in trypanosomatid protozoans. PLoS Pathog 6: e1001161.

20. KolevNG, TschudiC, UlluE (2011) RNA interference in protozoan parasites: achievements and challenges. Eukaryot Cell 10: 1156–1163.

21. DaRochaWD, OtsuK, TeixeiraSM, DonelsonJE (2004) Tests of cytoplasmic RNA interference (RNAi) and construction of a tetracycline-inducible T7 promoter system in Trypanosoma cruzi. Mol Biochem Parasitol 133: 175–186.

22. HartleyMA, KohlK, RonetC, FaselN (2013) The therapeutic potential of immune cross-talk in leishmaniasis. Clin Microbiol Infect 19: 119–130.

23. TeixeiraSM, de PaivaRM, Kangussu-MarcolinoMM, DarochaWD (2012) Trypanosomatid comparative genomics: Contributions to the study of parasite biology and different parasitic diseases. Genet Mol Biol 35: 1–17.

24. McCallLI, McKerrowJH (2014) Determinants of disease phenotype in trypanosomatid parasites. Trends Parasitol 30: 342–349.

25. KedzierskiL, MontgomeryJ, BullenD, CurtisJ, GardinerE, et al. (2004) A leucine-rich repeat motif of Leishmania parasite surface antigen 2 binds to macrophages through the complement receptor 3. J Immunol 172: 4902–4906.

26. LincolnLM, OzakiM, DonelsonJE, BeethamJK (2004) Genetic complementation of Leishmania deficient in PSA (GP46) restores their resistance to lysis by complement. Mol Biochem Parasitol 137: 185–189.

27. MatlashewskiG (2001) Leishmania infection and virulence. Med Microbiol Immunol 190: 37–42.

28. ZhangWW, MatlashewskiG (2000) Analysis of antisense and double stranded RNA downregulation of A2 protein expression in Leishmania donovani. Mol Biochem Parasitol 107: 315–319.

29. ZhangWW, MendezS, GhoshA, MylerP, IvensA, et al. (2003) Comparison of the A2 gene locus in Leishmania donovani and Leishmania major and its control over cutaneous infection. J Biol Chem 278: 35508–35515.

30. MizbaniA, TaslimiY, ZahedifardF, TaheriT, RafatiS (2011) Effect of A2 gene on infectivity of the nonpathogenic parasite Leishmania tarentolae. Parasitol Res 109: 793–799.

31. TeixeiraSM, RussellDG, KirchhoffLV, DonelsonJE (1994) A differentially expressed gene family encoding “amastin,” a surface protein of Trypanosoma cruzi amastigotes. J Biol Chem 269: 20509–20516.

32. RochetteA, McNicollF, GirardJ, BretonM, LeblancE, et al. (2005) Characterization and developmental gene regulation of a large gene family encoding amastin surface proteins in Leishmania spp. Mol Biochem Parasitol 140: 205–220.

33. JacksonAP (2010) The evolution of amastin surface glycoproteins in trypanosomatid parasites. Mol Biol Evol 27: 33–45.

34. MottaMC, MartinsAC, de SouzaSS, Catta-PretaCM, SilvaR, et al. (2013) Predicting the proteins of Angomonas deanei, Strigomonas culicis and their respective endosymbionts reveals new aspects of the trypanosomatidae family. PLoS ONE 8: e60209.

35. CruzMC, Souza-MeloN, da SilvaCV, DarochaWD, BahiaD, et al. (2012) Trypanosoma cruzi: role of delta-amastin on extracellular amastigote cell invasion and differentiation. PLoS ONE 7: e51804.

36. Dc-RubinSS, SchenkmanS (2012) T rypanosoma cruzi trans-sialidase as a multifunctional enzyme in Chagas' disease. Cell Microbiol 14: 1522–1530.

37. MontagnaG, CremonaML, ParisG, AmayaMF, BuschiazzoA, et al. (2002) The trans-sialidase from the african trypanosome Trypanosoma brucei. Eur J Biochem 269: 2941–2950.

38. TiralongoE, MartensenI, GrotzingerJ, TiralongoJ, SchauerR (2003) Trans-sialidase-like sequences from Trypanosoma congolense conserve most of the critical active site residues found in other trans-sialidases. Biol Chem 384: 1203–1213.

39. WagnerG, Eiko YamanakaL, MouraH, Denardin LuckemeyerD, SchlindweinAD, et al. (2013) The Trypanosoma rangeli trypomastigote surfaceome reveals novel proteins and targets for specific diagnosis. J Proteomics 82: 52–63.

40. Rubin-de-CelisSS, UemuraH, YoshidaN, SchenkmanS (2006) Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell Microbiol 8: 1888–1898.

41. YoshidaN (2006) Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An Acad Bras Cienc 78: 87–111.

42. Acosta-SerranoA, AlmeidaIC, Freitas-JuniorLH, YoshidaN, SchenkmanS (2001) The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles. Mol Biochem Parasitol 114: 143–150.

43. BartholomeuDC, CerqueiraGC, LeaoAC, daRochaWD, PaisFS, et al. (2009) Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucleic Acids Res 37: 3407–3417.

44. dos SantosSL, FreitasLM, LoboFP, Rodrigues-LuizGF, MendesTA, et al. (2012) The MASP family of Trypanosoma cruzi: changes in gene expression and antigenic profile during the acute phase of experimental infection. PLoS Negl Trop Dis 6: e1779.

45. StocoPH, WagnerG, Talavera-LopezC, GerberA, ZahaA, et al. (2014) Genome of the Avirulent Human-infective Trypanosome – Trypanosoma rangeli. PLoS Negl Trop Dis 8: e3176.

46. PeacockCS, SeegerK, HarrisD, MurphyL, RuizJC, et al. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39: 839–847.

47. RogersMB, HilleyJD, DickensNJ, WilkesJ, BatesPA, et al. (2011) Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res 21: 2129–2142.

48. RealF, VidalRO, CarazzolleMF, MondegoJM, CostaGG, et al. (2013) The Genome Sequence of Leishmania (Leishmania) amazonensis: Functional Annotation and Extended Analysis of Gene Models. DNA Res 20: 567–581.

49. RaymondF, BoisvertS, RoyG, RittJF, LegareD, et al. (2012) Genome sequencing of the lizard parasite Leishmania tarentolae reveals loss of genes associated to the intracellular stage of human pathogenic species. Nucleic Acids Res 40: 1131–1147.

50. FranzenO, OchayaS, SherwoodE, LewisMD, LlewellynMS, et al. (2011) Shotgun sequencing analysis of Trypanosoma cruzi I Sylvio X10/1 and comparison with T. cruzi VI CL Brener. PLoS Negl Trop Dis 5: e984.

51. FranzenO, Talavera-LopezC, OchayaS, ButlerCE, MessengerLA, et al. (2012) Comparative genomic analysis of human infective Trypanosoma cruzi lineages with the bat-restricted subspecies T. cruzi marinkellei. BMC Genomics 13: 531.

52. NagamuneK, Acosta-SerranoA, UemuraH, BrunR, Kunz-RenggliC, et al. (2004) Surface sialic acids taken from the host allow trypanosome survival in tsetse fly vectors. J Exp Med 199: 1445–1450.

53. MendesTA, LoboFP, RodriguesTS, Rodrigues-LuizGF, daRochaWD, et al. (2013) Repeat-enriched proteins are related to host cell invasion and immune evasion in parasitic protozoa. Mol Biol Evol 30: 951–963.

54. HughesAL (2004) The evolution of amino acid repeat arrays in Plasmodium and other organisms. J Mol Evol 59: 528–535.

55. PaisFS, DaRochaWD, AlmeidaRM, LeclercqSY, PenidoML, et al. (2008) Molecular characterization of ribonucleoproteic antigens containing repeated amino acid sequences from Trypanosoma cruzi. Microbes Infect 10: 716–725.

56. GotoY, CarterD, GuderianJ, InoueN, KawazuS, et al. (2010) Upregulated expression of B-cell antigen family tandem repeat proteins by Leishmania amastigotes. Infect Immun 78: 2138–2145.

57. MaedaFY, CortezC, YoshidaN (2012) Cell signaling during Trypanosoma cruzi invasion. Front Immunol 3: 361.

58. OrregoPR, OlivaresH, CorderoEM, BressanA, CortezM, et al. (2014) A cytoplasmic new catalytic subunit of Calcineurin in Trypanosoma cruzi and its molecular and functional characterization. PLoS Negl Trop Dis 8: e2676.

59. GrantKM, DunionMH, YardleyV, SkaltsounisAL, MarkoD, et al. (2004) Inhibitors of Leishmania mexicana CRK3 cyclin-dependent kinase: chemical library screen and antileishmanial activity. Antimicrob Agents Chemother 48: 3033–3042.

60. NascimentoM, ZhangWW, GhoshA, HoustonDR, BerghuisAM, et al. (2006) Identification and characterization of a protein-tyrosine phosphatase in Leishmania: Involvement in virulence. J Biol Chem 281: 36257–36268.

61. RaltonJE, NadererT, PirainoHL, BashtannykTA, CallaghanJM, et al. (2003) Evidence that intracellular beta1-2 mannan is a virulence factor in Leishmania parasites. J Biol Chem 278: 40757–40763.

62. GaramiA, MehlertA, IlgT (2001) Glycosylation defects and virulence phenotypes of Leishmania mexicana phosphomannomutase and dolicholphosphate-mannose synthase gene deletion mutants. Mol Cell Biol 21: 8168–8183.

63. AtwoodJA3rd, WeatherlyDB, MinningTA, BundyB, CavolaC, et al. (2005) The Trypanosoma cruzi proteome. Science 309: 473–476.

64. BermanJD, GallaleeJV, BestJM, HillT (1987) Uptake, distribution, and oxidation of fatty acids by Leishmania mexicana amastigotes. J Parasitol 73: 555–560.

65. SchenkmanS, JiangMS, HartGW, NussenzweigV (1991) A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell 65: 1117–1125.

66. RamirezMI, Ruiz RdeC, ArayaJE, Da SilveiraJF, YoshidaN (1993) Involvement of the stage-specific 82-kilodalton adhesion molecule of Trypanosoma cruzi metacyclic trypomastigotes in host cell invasion. Infect Immun 61: 3636–3641.

67. MagdesianMH, TonelliRR, FesselMR, SilveiraMS, SchumacherRI, et al. (2007) A conserved domain of the gp85/trans-sialidase family activates host cell extracellular signal-regulated kinase and facilitates Trypanosoma cruzi infection. Exp Cell Res 313: 210–218.

68. YoshidaN, MortaraRA, AraguthMF, GonzalezJC, RussoM (1989) Metacyclic neutralizing effect of monoclonal antibody 10D8 directed to the 35- and 50-kilodalton surface glycoconjugates of Trypanosoma cruzi. Infect Immun 57: 1663–1667.

69. KulkarniMM, OlsonCL, EngmanDM, McGwireBS (2009) Trypanosoma cruzi GP63 proteins undergo stage-specific differential posttranslational modification and are important for host cell infection. Infect Immun 77: 2193–2200.

70. GrellierP, VendevilleS, JoyeauR, BastosIM, DrobecqH, et al. (2001) Trypanosoma cruzi prolyl oligopeptidase Tc80 is involved in nonphagocytic mammalian cell invasion by trypomastigotes. J Biol Chem 276: 47078–47086.

71. MeirellesMN, JulianoL, CarmonaE, SilvaSG, CostaEM, et al. (1992) Inhibitors of the major cysteinyl proteinase (GP57/51) impair host cell invasion and arrest the intracellular development of Trypanosoma cruzi in vitro. Mol Biochem Parasitol 52: 175–184.

72. CalerEV, Vaena de AvalosS, HaynesPA, AndrewsNW, BurleighBA (1998) Oligopeptidase B-dependent signaling mediates host cell invasion by Trypanosoma cruzi. Embo j 17: 4975–4986.

73. Manning-CelaR, CortesA, Gonzalez-ReyE, Van VoorhisWC, SwindleJ, et al. (2001) LYT1 protein is required for efficient in vitro infection by Trypanosoma cruzi. Infect Immun 69: 3916–3923.

74. AlvarezMN, PeluffoG, PiacenzaL, RadiR (2011) Intraphagosomal peroxynitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi: consequences for oxidative killing and role of microbial peroxiredoxins in infectivity. J Biol Chem 286: 6627–6640.

75. BrittinghamA, MorrisonCJ, McMasterWR, McGwireBS, ChangKP, et al. (1995) Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. J Immunol 155: 3102–3111.

76. SpathGF, EpsteinL, LeaderB, SingerSM, AvilaHA, et al. (2000) Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc Natl Acad Sci U S A 97: 9258–9263.

77. VinetAF, JananjiS, TurcoSJ, FukudaM, DescoteauxA (2011) Exclusion of synaptotagmin V at the phagocytic cup by Leishmania donovani lipophosphoglycan results in decreased promastigote internalization. Microbiology 157: 2619–2628.

78. HuynhC, SacksDL, AndrewsNW (2006) A Leishmania amazonensis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes. J Exp Med 203: 2363–2375.

79. MiguelDC, FlanneryAR, MittraB, AndrewsNW (2013) Heme uptake mediated by LHR1 is essential for Leishmania amazonensis virulence. Infect Immun 81: 3620–3626.

80. FariaMS, ReisFC, Azevedo-PereiraRL, MorrisonLS, MottramJC, et al. (2011) Leishmania inhibitor of serine peptidase 2 prevents TLR4 activation by neutrophil elastase promoting parasite survival in murine macrophages. J Immunol 186: 411–422.

81. DolaiS, YadavRK, PalS, AdakS (2009) Overexpression of mitochondrial Leishmania major ascorbate peroxidase enhances tolerance to oxidative stress-induced programmed cell death and protein damage. Eukaryot Cell 8: 1721–1731.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 12

Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa