Mucin Gene (PoMuc) Expression: Epigenetic Control to Shape Adaptation to a New Host

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The digenetic trematode Schistosoma mansoni is a human parasite that uses the mollusc Biomphalaria glabrata as intermediate host. Specific S. mansoni strains can infect efficiently only certain B. glabrata strains (compatible strain) while others are incompatible. Strain-specific differences in transcription of a conserved family of polymorphic mucins (SmPoMucs) in S. mansoni are the principle determinants for this compatibility. In the present study, we investigated the bases of the control of SmPoMuc expression that evolved to evade B. glabrata diversified antigen recognition molecules. We compared the DNA sequences and chromatin structure of SmPoMuc promoters of two S. mansoni strains that are either compatible (C) or incompatible (IC) with a reference snail host. We reveal that although sequence differences are observed between active promoter regions of SmPoMuc genes, the sequences of the promoters are not diverse and are conserved between IC and C strains, suggesting that genetics alone cannot explain the evolution of compatibility polymorphism. In contrast, promoters carry epigenetic marks that are significantly different between the C and IC strains. Moreover, we show that modifications of the structure of the chromatin of the parasite modify transcription of SmPoMuc in the IC strain compared to the C strain and correlate with the presence of additional combinations of SmPoMuc transcripts only observed in the IC phenotype. Our results indicate that transcription polymorphism of a gene family that is responsible for an important adaptive trait of the parasite is epigenetically encoded. These strain-specific epigenetic marks are heritable, but can change while the underlying genetic information remains stable. This suggests that epigenetic changes may be important for the early steps in the adaptation of pathogens to new hosts, and might be an initial step in adaptive evolution in general.

Vyšlo v časopise: Mucin Gene (PoMuc) Expression: Epigenetic Control to Shape Adaptation to a New Host. PLoS Pathog 9(8): e32767. doi:10.1371/journal.ppat.1003571
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003571

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Zdroje

1. MackinnonMJ, MarshK (2010) The selection landscape of malaria parasites. Science 328 ((5980)) 866–871.

2. Van ValenL (1974) Molecular evolution as predicted by natural selection. J Mol Evol 3: 89–101.

3. JemmelyNY, NiangM, PreiserPR (2010) Small variant surface antigens and Plasmodium evasion of immunity. Future Microbiol 5 ((4)) 663–682.

4. MittaG, AdemaCM, GourbalB, LokerES, TheronA (2012) Compatibility polymorphism in snail/schistosome interactions: From field to theory to molecular mechanisms. Dev Comp Immunol 37 ((1)) 1–8.

5. TheronA, CoustauC (2005) Are Biomphalaria snails resistant to Schistosoma mansoni? J Helminthol 79 ((3)) 187–191.

6. MorganJA, DejongRJ, AdeoyeGO, AnsaED, BarbosaCS, et al. (2005) Origin and diversification of the human parasite Schistosoma mansoni. Mol Ecol 14 ((12)) 3889–3902.

7. RogerE, MittaG, MoneY, BouchutA, RognonA, et al. (2008) Molecular determinants of compatibility polymorphism in the Biomphalaria glabrata/Schistosoma mansoni model: new candidates identified by a global comparative proteomics approach. Mol Biochem Parasitol 157 ((2)) 205–216.

8. RogerE, GrunauC, PierceRJ, HiraiH, GourbalB, et al. (2008) Controlled chaos of polymorphic mucins in a metazoan parasite (Schistosoma mansoni) interacting with its invertebrate host (Biomphalaria glabrata). PLoS Negl Trop Dis 2 ((11)) e330.

9. MoneY, GourbalB, DuvalD, Du PasquierL, Kieffer-JaquinodS, et al. (2010) A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis 4: e813.

10. AdemaCM, HertelLA, MillerRD, LokerES (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci U S A 94 ((16)) 8691–8696.

11. HaningtonPC, ForysMA, DragooJW, ZhangSM, AdemaCM, et al. (2010) Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc Natl Acad Sci U S A 107 ((49)) 21087–21092.

12. ZhangSM, ZengY, LokerES (2008) Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immun 14 ((3)) 175–189.

13. CosseauC, AzziH, RognonA, BoissierJ, GourbièreS, et al. (2010) Epigenetic and phenotypic variability in populations of Schistosoma mansoni – a possible kick-off for adaptive host/parasite evolution. Oikos 119: 669–678.

14. UmlaufD, FraserP, NaganoT (2008) The role of long non-coding RNAs in chromatin structure and gene regulation: variations on a theme. Biol Chem 389 ((4)) 323–331.

15. DillonN (2008) The impact of gene location in the nucleus on transcriptional regulation. Dev Cell 15 ((2)) 182–186.

16. LeeJS, SmithE, ShilatifardA (2010) The language of histone crosstalk. Cell 142 ((5)) 682–685.

17. PalC, MiklosI (1999) Epigenetic inheritance, genetic assimilation and speciation. J Theor Biol 200 ((1)) 19–37.

18. CortesA, CrowleyVM, VaqueroA, VossTS (2012) A view on the role of epigenetics in the biology of malaria parasites. PLoS Pathog 8 ((12)) e1002943.

19. SalminenMO, CarrJK, BurkeDS, McCutchanFE (1995) Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 11 ((11)) 1423–1425.

20. MartinDP, LemeyP, LottM, MoultonV, PosadaD, et al. (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26 ((19)) 2462–2463.

21. SmithJ (1992) Analyzing the mosaic structure of genes. J Mol Evol 34 ((126–129)).

22. PosadaD, CrandallKA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98 ((24)) 13757–13762.

23. GibbsMJ, ArmstrongJS, GibbsAJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16 ((7)) 573–582.

24. De MendoncaRL, BoutonD, BertinB, EscrivaH, NoelC, et al. (2002) A functionally conserved member of the FTZ-F1 nuclear receptor family from Schistosoma mansoni. Eur J Biochem 269 ((22)) 5700–5711.

25. BechN, BeltranS, PortelaJ, RognonA, AllienneJF, et al. (2010) Follow-up of the genetic diversity and snail infectivity of a Schistosoma mansoni strain from field to laboratory. Infect Genet Evol 10 ((7)) 1039–1045.

26. DuboisF, CabyS, OgerF, CosseauC, CapronM, et al. (2009) Histone deacetylase inhibitors induce apoptosis, histone hyperacetylation and up-regulation of gene transcription in Schistosoma mansoni. Mol Biochem Parasitol 168 ((1)) 7–15.

27. AzziA, CosseauC, GrunauC (2009) Schistosoma mansoni: developmental arrest of miracidia treated with histone deacetylase inhibitors. Exp Parasitol 121 ((3)) 288–291.

28. GeyerKK, Rodriguez LopezCM, ChalmersIW, MunshiSE, TruscottM, et al. (2011) Cytosine methylation regulates oviposition in the pathogenic blood fluke Schistosoma mansoni. Nat Commun 2: 424.

29. RaddatzG, GuzzardoPM, OlovaN, FantappieMR, RamppM, et al. (2013) Dnmt2-dependent methylomes lack defined DNA methylation patterns. Proc Natl Acad Sci U S A 110 ((21)) 8627–8631.

30. Jablonka E, Lamb M (2005) Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. MIT Press, Cambridge.

31. BossdorfO, RichardsCL, PigliucciM (2008) Epigenetics for ecologists. Ecol Lett 11 ((2)) 106–115.

32. DanchinE, CharmantierA, ChampagneFA, MesoudiA, PujolB, et al. (2011) Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet 12 ((7)) 475–486.

33. JablonkaE, LambMJ, AvitalE (1998) ‘Lamarckian’ mechanisms in darwinian evolution. Trends Ecol Evol 13 ((5)) 206–210.

34. PigliucciM, MurrenCJ, SchlichtingCD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209 ((Pt 12)) 2362–2367.

35. LuijsterburgMS, WhiteMF, van DrielR, DameRT (2008) The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes. Crit Rev Biochem Mol Biol 43 ((6)) 393–418.

36. RappRA, WendelJF (2005) Epigenetics and plant evolution. New Phytol 168 ((1)) 81–91.

37. Grant-DowntonRT, DickinsonHG (2006) Epigenetics and its implications for plant biology 2. The ‘epigenetic epiphany’: epigenetics, evolution and beyond. Ann Bot 97 ((1)) 11–27.

38. RichardsEJ (2006) Inherited epigenetic variation–revisiting soft inheritance. Nat Rev Genet 7 ((5)) 395–401.

39. BossdorfO, ZhangY (2011) A truly ecological epigenetics study. Mol Ecol 20 ((8)) 1572–1574.

40. BoykoA, KovalchukI (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49 ((1)) 61–72.

41. JablonkaE, RazG (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84 ((2)) 131–176.

42. Gomez-DiazE, JordaM, PeinadoMA, RiveroA (2012) Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog 8 ((11)) e1003007.

43. VerhoevenKJ, Van DijkPJ, BiereA (2010) Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages. Mol Ecol 19 ((2)) 315–324.

44. UchidaS, HaraK, KobayashiA, OtsukiK, YamagataH, et al. (2011) Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 69 ((2)) 359–372.

45. CrowleyVM, Rovira-GraellsN, Ribas de PouplanaL, CortesA (2011) Heterochromatin formation in bistable chromatin domains controls the epigenetic repression of clonally variant Plasmodium falciparum genes linked to erythrocyte invasion. Mol Microbiol 80 ((2)) 391–406.

46. KulakovaL, SingerSM, ConradJ, NashTE (2006) Epigenetic mechanisms are involved in the control of Giardia lamblia antigenic variation. Mol Microbiol 61 ((6)) 1533–1542.

47. PruccaCG, SlavinI, QuirogaR, EliasEV, RiveroFD, et al. (2008) Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature 456 ((7223)) 750–754.

48. RudenkoG (2011) African trypanosomes: the genome and adaptations for immune evasion. Essays Biochem 51: 47–62.

49. ScherfA, Lopez-RubioJJ, RiviereL (2008) Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62: 445–470.

50. OsipovichO, OltzEM (2010) Regulation of antigen receptor gene assembly by genetic-epigenetic crosstalk. Semin Immunol 22 ((6)) 313–322.

51. BergmanY, CedarH (2010) Epigenetic control of recombination in the immune system. Semin Immunol 22 ((6)) 323–329.

52. OhnoS, WolfU, AtkinNB (1968) Evolution from fish to mammals by gene duplication. Hereditas 59 ((1)) 169–187.

53. RodinSN, ParkhomchukDV, RiggsAD (2005) Epigenetic changes and repositioning determine the evolutionary fate of duplicated genes. Biochemistry (Mosc) 70 ((5)) 559–567.

54. TheronA, PagesJR, RognonA (1997) Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snail as related to host susceptibility and sporocyst regulatory processes. Exp Parasitol 85 ((1)) 1–9.

55. PortelaJ, GrunauC, CosseauC, BeltranS, DantecC, et al. (2010) Whole-genome in-silico subtractive hybridization (WISH)–using massive sequencing for the identification of unique and repetitive sex-specific sequences: the example of Schistosoma mansoni. BMC Genomics 11: 387.

56. RogerE, GourbalB, GrunauC, PierceRJ, GalinierR, et al. (2008) Expression analysis of highly polymorphic mucin proteins (Sm PoMuc) from the parasite Schistosoma mansoni. Mol Biochem Parasitol 157 ((2)) 217–227.

57. ReeseMG (2001) Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem 26 ((1)) 51–56.

58. KohanyO, GentlesAJ, HankusL, JurkaJ (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7: 474.

59. RozasJ, Sanchez-DelBarrioJC, MesseguerX, RozasR (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 ((18)) 2496–2497.

60. RonquistF, TeslenkoM, van der MarkP, AyresDL, DarlingA, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61 ((3)) 539–542.

61. HuelsenbeckJP, LargetB, AlfaroME (2004) Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Mol Biol Evol 21 ((6)) 1123–1133.

62. Nei (1987) Molecular Evolutionary Genetics. New York: Columbia University Press.

63. CockerhamCC, WeirBS (1984) Covariances of relatives stemming from a population undergoing mixed self and random mating. Biometrics 40 ((1)) 157–164.

64. BelkhirK, DawsonKJ, BonhommeF (2006) A comparison of rarefaction and bayesian methods for predicting the allelic richness of future samples on the basis of currently available samples. J Hered 97 ((5)) 483–492.

65. RoussetF (1996) Equilibrium values of measures of population subdivision for stepwise mutation processes. Genetics 142 ((4)) 1357–1362.

66. SlatkinM (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139 ((1)) 457–462.

67. CosseauC, AzziA, SmithK, FreitagM, MittaG, et al. (2009) Native chromatin immunoprecipitation (N-ChIP) and ChIP-Seq of Schistosoma mansoni: Critical experimental parameters. Mol Biochem Parasitol 166 ((1)) 70–76.

68. GrunauC, ClarkSJ, RosenthalA (2001) Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acids Res 29 ((13)) E65–65.