A Review of Bacteria-Animal Lateral Gene Transfer May Inform Our Understanding of Diseases like Cancer

English version České info

Lateral gene transfer (LGT) from bacteria to animals occurs more frequently than was appreciated prior to the advent of genome sequencing. In 2007, LGT from bacterial Wolbachia endosymbionts was detected in ∼33% of the sequenced arthropod genomes using a bioinformatic approach. Today, Wolbachia/host LGT is thought to be widespread and many other cases of bacteria-animal LGT have been described. In insects, LGT may be more frequently associated with endosymbionts that colonize germ cells and germ stem cells, like Wolbachia endosymbionts. We speculate that LGT may occur from bacteria to a wide variety of eukaryotes, but only becomes vertically inherited when it occurs in germ cells. As such, LGT may happen routinely in somatic cells but never become inherited or fixed in the population. Lack of inheritance of such mutations greatly decreases our ability to detect them. In this review, we propose that such noninherited bacterial DNA integration into chromosomes in human somatic cells could induce mutations leading to cancer or autoimmune diseases in a manner analogous to mobile elements and viral integrations.

Vyšlo v časopise: A Review of Bacteria-Animal Lateral Gene Transfer May Inform Our Understanding of Diseases like Cancer. PLoS Genet 9(10): e32767. doi:10.1371/journal.pgen.1003877
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003877

Souhrn

Zdroje

1. GelvinSB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67 : 16–37.

2. GelvinSB (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu Rev Plant Physiol Plant Mol Biol 51 : 223–256.

3. TzfiraT, RheeY, ChenMH, KunikT, CitovskyV (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54 : 187–219.

4. LanderES, LintonLM, BirrenB, NusbaumC, ZodyMC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409 : 860–921.

5. SalzbergSL, WhiteO, PetersonJ, EisenJA (2001) Microbial genes in the human genome: lateral transfer or gene loss? Science 292 : 1903–1906.

6. SkaarEP, SeifertHS (2002) The misidentification of bacterial genes as human cDNAs: was the human D-1 tumor antigen gene acquired from bacteria? Genomics 79 : 625–627.

7. PleasanceED, CheethamRK, StephensPJ, McBrideDJ, HumphraySJ, et al. (2010) A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 463 : 191–196.

8. LeeE, IskowR, YangL, GokcumenO, HaseleyP, et al. (2012) Landscape of somatic retrotransposition in human cancers. Science 337 : 967–971.

9. BassAJ, LawrenceMS, BraceLE, RamosAH, DrierY, et al. (2011) Genomic sequencing of colorectal adenocarcinomas identifies a recurrent VTI1A-TCF7L2 fusion. Nat Genet 43 : 964–968.

10. SungWK, ZhengH, LiS, ChenR, LiuX, et al. (2012) Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat Genet 44 : 765–769.

11. Dunning HotoppJC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27 : 157–163.

12. Dunning Hotopp JC (2013) Lateral gene transfer in multicellular organisms. In: Gophna U, editor. Lateral gene transfer in evolution. Springer Science. pp. 161–179.

13. GrahamLA, LougheedSC, EwartKV, DaviesPL (2008) Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS ONE 3: e2616 doi:10.1371/journal.pone.0002616

14. MoranNA, JarvikT (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328 : 624–627.

15. AltincicekB, KovacsJL, GerardoNM (2012) Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol Lett 8 : 253–257.

16. HusnikF, NikohN, KogaR, RossL, DuncanRP, et al. (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153 : 1567–1578.

17. AcunaR, PadillaBE, Florez-RamosCP, RubioJD, HerreraJC, et al. (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci U S A 109 : 4197–4202.

18. DanchinEGJ, RossoaM-N, VieiraaP, Almeida-EngleraJd, CoutinhobPM, et al. (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci U S A 107 : 17651–17656.

19. MayerWE, SchusterLN, BartelmesG, DieterichC, SommerRJ (2011) Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC Evol Biol 11 : 13.

20. DieterichC, CliftonSW, SchusterLN, ChinwallaA, DelehauntyK, et al. (2008) The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 40 : 1193–1198.

21. StouthamerR, BreeuwerJA, HurstGD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53 : 71–102.

22. WerrenJH (1997) Biology of Wolbachia. Annu Rev Entomol 42 : 587–609.

23. FastEM, ToomeyME, PanaramK, DesjardinsD, KolaczykED, et al. (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334 : 990–992.

24. KondoN, NikohN, IjichiN, ShimadaM, FukatsuT (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A 99 : 14280–14285.

25. NikohN, TanakaK, ShibataF, KondoN, HizumeM, et al. (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18 : 272–280.

26. AikawaT, AnbutsuH, NikohN, KikuchiT, ShibataF, et al. (2009) Longicorn beetle that vectors pinewood nematode carries many Wolbachia genes on an autosome. Proc Biol Sci 276 : 3791–3798.

27. Dunning HotoppJC, ClarkME, OliveiraDC, FosterJM, FischerP, et al. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317 : 1753–1756.

28. WerrenJH, RichardsS, DesjardinsCA, NiehuisO, GadauJ, et al. (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327 : 343–348.

29. DoudoumisV, AlamU, AksoyE, Abd-AllaA, TsiamisG, et al. (2012) Tsetse-Wolbachia symbiosis: comes of age and has great potential for pest and disease control. J Invertebr Pathol 112 Suppl 1: S94–S103.

30. FennK, ConlonC, JonesM, QuailMA, HolroydNE, et al. (2006) Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2: e94 doi:10.1371/journal.ppat.0020094

31. McNultySN, FosterJM, MitrevaM, Dunning HotoppJC, MartinJ, et al. (2010) Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS ONE 5: e11029 doi:10.1371/journal.pone.0011029

32. BeikoRG, HarlowTJ, RaganMA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102 : 14332–14337.

33. NikohN, McCutcheonJP, KudoT, MiyagishimaS-y, MoranNA, et al. (2010) Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 6: e1000827 doi:10.1371/journal.pgen.1000827

34. NikohN, NakabachiA (2009) Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol 7 : 12.

35. LuckeyTD (1970) Introduction to the ecology of the intestinal flora. Am J Clin Nutr 23 : 1430–1432.

36. MogensenTH (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22 : 240–273.

37. HackerG, RedeckeV, HackerH (2002) Activation of the immune system by bacterial CpG-DNA. Immunology 105 : 245–251.

38. SanderLE, DavisMJ, BoekschotenMV, AmsenD, DascherCC, et al. (2011) Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474 : 385–389.

39. WeinerAM (1980) An abundant cytoplasmic 7S RNA is complementary to the dominant interspersed middle repetitive DNA sequence family in the human genome. Cell 22 : 209–218.

40. KapitonovVV, JurkaJ (2003) A novel class of SINE elements derived from 5S rRNA. Mol Biol Evol 20 : 694–702.

41. Roy-EngelAM (2012) LINEs, SINEs and other retroelements: do birds of a feather flock together? Front Biosci 17 : 1345–1361.

42. HancksDC, KazazianHHJr (2012) Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22 : 191–203.

43. MillsRE, BennettEA, IskowRC, DevineSE (2007) Which transposable elements are active in the human genome? Trends Genet 23 : 183–191.

44. KonkelMK, BatzerMA (2010) A mobile threat to genome stability: the impact of non-LTR retrotransposons upon the human genome. Semin Cancer Biol 20 : 211–221.

45. MikiY, NishishoI, HoriiA, MiyoshiY, UtsunomiyaJ, et al. (1992) Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res 52 : 643–645.

46. SolyomS, EwingAD, RahrmannEP, DoucetT, NelsonHH, et al. (2012) Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res 22 : 2328–2338.

47. IskowRC, McCabeMT, MillsRE, ToreneS, PittardWS, et al. (2010) Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 141 : 1253–1261.

48. de MartelC, FerlayJ, FranceschiS, VignatJ, BrayF, et al. (2012) Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 13 : 607–615.

49. SchiffmanM, CastlePE, JeronimoJ, RodriguezAC, WacholderS (2007) Human papillomavirus and cervical cancer. Lancet 370 : 890–907.

50. FaridiR, ZahraA, KhanK, IdreesM (2011) Oncogenic potential of Human Papillomavirus (HPV) and its relation with cervical cancer. Virol J 8 : 269.

51. CordenSA, Sant-CassiaLJ, EastonAJ, MorrisAG (1999) The integration of HPV-18 DNA in cervical carcinoma. Mol Pathol 52 : 275–282.

52. MelsheimerP, VinokurovaS, WentzensenN, BastertG, von Knebel DoeberitzM (2004) DNA aneuploidy and integration of human papillomavirus type 16 E6/E7 oncogenes in intraepithelial neoplasia and invasive squamous cell carcinoma of the cervix uteri. Clin Cancer Res 10 : 3059–3063.

53. Van TineBA, KappesJC, BanerjeeNS, KnopsJ, LaiL, et al. (2004) Clonal selection for transcriptionally active viral oncogenes during progression to cancer. J Virol 78 : 11172–11186.

54. BeasleyRP, HwangLY, LinCC, ChienCS (1981) Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22,707 men in Taiwan. Lancet 2 : 1129–1133.

55. MoorePS, ChangY (2010) Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat Rev Cancer 10 : 878–889.

56. MurakamiY, SaigoK, TakashimaH, MinamiM, OkanoueT, et al. (2005) Large scaled analysis of hepatitis B virus (HBV) DNA integration in HBV related hepatocellular carcinomas. Gut 54 : 1162–1168.

57. Paterlini-BrechotP, SaigoK, MurakamiY, ChamiM, GozuacikD, et al. (2003) Hepatitis B virus-related insertional mutagenesis occurs frequently in human liver cancers and recurrently targets human telomerase gene. Oncogene 22 : 3911–3916.

58. GozuacikD, MurakamiY, SaigoK, ChamiM, MugnierC, et al. (2001) Identification of human cancer-related genes by naturally occurring Hepatitis B Virus DNA tagging. Oncogene 20 : 6233–6240.

59. SaigoK, YoshidaK, IkedaR, SakamotoY, MurakamiY, et al. (2008) Integration of hepatitis B virus DNA into the myeloid/lymphoid or mixed-lineage leukemia (MLL4) gene and rearrangements of MLL4 in human hepatocellular carcinoma. Hum Mutat 29 : 703–708.

60. LopezJV, YuhkiN, MasudaR, ModiW, O'BrienSJ (1994) Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. J Mol Evol 39 : 174–190.

61. Hazkani-CovoE, ZellerRM, MartinW (2010) Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 6: e1000834 doi:10.1371/journal.pgen.1000834

62. Hazkani-CovoE, CovoS (2008) Numt-mediated double-strand break repair mitigates deletions during primate genome evolution. PLoS Genet 4: e1000237 doi:10.1371/journal.pgen.1000237

63. Willett-BrozickJE, SavulSA, RicheyLE, BaysalBE (2001) Germ line insertion of mtDNA at the breakpoint junction of a reciprocal constitutional translocation. Hum Genet 109 : 216–223.

64. ShayJW, BabaT, ZhanQM, KamimuraN, CuthbertJA (1991) HeLaTG cells have mitochondrial DNA inserted into the c-myc oncogene. Oncogene 6 : 1869–1874.

65. BorensztajnK, ChafaO, Alhenc-GelasM, SalhaS, ReghisA, et al. (2002) Characterization of two novel splice site mutations in human factor VII gene causing severe plasma factor VII deficiency and bleeding diathesis. Br J Haematol 117 : 168–171.

66. TurnerC, KilloranC, ThomasNS, RosenbergM, ChuzhanovaNA, et al. (2003) Human genetic disease caused by de novo mitochondrial-nuclear DNA transfer. Hum Genet 112 : 303–309.

67. GoldinE, StahlS, CooneyAM, KaneskiCR, GuptaS, et al. (2004) Transfer of a mitochondrial DNA fragment to MCOLN1 causes an inherited case of mucolipidosis IV. Hum Mutat 24 : 460–465.

68. AhmedZM, SmithTN, RiazuddinS, MakishimaT, GhoshM, et al. (2002) Nonsyndromic recessive deafness DFNB18 and Usher syndrome type IC are allelic mutations of USHIC. Hum Genet 110 : 527–531.

69. ChenJM, ChuzhanovaN, StensonPD, FerecC, CooperDN (2005) Meta-analysis of gross insertions causing human genetic disease: novel mutational mechanisms and the role of replication slippage. Hum Mutat 25 : 207–221.

70. SchonEA, DiMauroS, HiranoM (2012) Human mitochondrial DNA: roles of inherited and somatic mutations. Nat Rev Genet 13 : 878–890.

71. CaroP, GomezJ, ArduiniA, Gonzalez-SanchezM, Gonzalez-GarciaM, et al. (2010) Mitochondrial DNA sequences are present inside nuclear DNA in rat tissues and increase with age. Mitochondrion 10 : 479–486.

72. WangD, LloydAH, TimmisJN (2012) Nuclear genome diversity in somatic cells is accelerated by environmental stress. Plant Signal Behav 7 : 595–597.

73. KustersJG, van VlietAH, KuipersEJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19 : 449–490.

74. MaddocksODK, ShortAJ, DonnenbergMS, BaderS, HarrisonDJ (2009) Attaching and effacing Escherichia coli downregulate DNA mismatch repair protein in vitro and are associated with colorectal adenocarcinomas in humans. PLoS ONE 4: e5517 doi:10.1371/journal.pone.0005517

75. FriedB, ReddyA, MayerD (2011) Helminths in human carcinogenesis. Cancer Lett 305 : 239–249.

76. SearsCL, IslamS, SahaA, ArjumandM, AlamNH, et al. (2008) Association of enterotoxigenic Bacteroides fragilis infection with inflammatory diarrhea. Clin Infect Dis 47 : 797–803.

77. KosticAD, OjesinaAI, PedamalluCS, JungJ, VerhaakRG, et al. (2011) PathSeq: software to identify or discover microbes by deep sequencing of human tissue. Nat Biotechnol 29 : 393–396.

78. ArumugamM, RaesJ, PelletierE, Le PaslierD, YamadaT, et al. (2011) Enterotypes of the human gut microbiome. Nature 473 : 174–180.

79. JeonS, Allen-HoffmannBL, LambertPF (1995) Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J Virol 69 : 2989–2997.

80. SchwabeRF, WangTC (2012) Cancer. Bacteria deliver a genotoxic hit. Science 338 : 52–53.

81. ChangAH, ParsonnetJ (2010) Role of bacteria in oncogenesis. Clin Microbiol Rev 23 : 837–857.

82. RileyDR, SieberKB, RobinsonKM, WhiteJR, GanesanA, et al. (2013) Bacteria-human somatic cell lateral gene transfer is enriched in cancer samples. PLoS Comput Biol 9: e1003107 doi:10.1371/journal.pcbi.1003107

83. SalinasGF, BrazaF, BrouardS, TakPP, BaetenD (2013) The role of B lymphocytes in the progression from autoimmunity to autoimmune disease. Clin Immunol 146 : 34–45.