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

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Robinson, Kelly M ^a   Sieber, Karsten B ^a   Dunning Hotopp, Julie C ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL COLONIZATION; CARCINOGENESIS; CELL PROLIFERATION; CHROMOSOME ANALYSIS; CYTOPLASM; DNA INTEGRATION; ENDOSYMBIONT; GENE MUTATION; GENE SEQUENCE; GERM CELL; HORIZONTAL GENE TRANSFER; HUMAN; LONG TERMINAL REPEAT; MUTAGENESIS; NONHUMAN; PHENOTYPE; PHYLOGENY; RETROPOSON; REVIEW; SOMATIC CELL; WOLBACHIA;

ANIMALS; CHROMOSOMES; DNA, BACTERIAL; GENE TRANSFER, HORIZONTAL; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; NEOPLASMS; PHYLOGENY; SYMBIOSIS; WOLBACHIA;

EID: 84887277415     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003877     Document Type: Review

References (83)

1. Gelvin SB, (2003) Agrobacterium-mediated plant transformation: the biology behind the "gene-jockeying" tool. Microbiol Mol Biol Rev 67: 16-37.
2. Gelvin SB, (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu Rev Plant Physiol Plant Mol Biol 51: 223-256.
3. Tzfira T, Rhee Y, Chen MH, Kunik T, Citovsky V, (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54: 187-219.
4. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
5. Salzberg SL, White O, Peterson J, Eisen JA, (2001) Microbial genes in the human genome: lateral transfer or gene loss? Science 292: 1903-1906.
6. Skaar EP, Seifert HS, (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. Pleasance ED, Cheetham RK, Stephens PJ, McBride DJ, Humphray SJ, et al. (2010) A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 463: 191-196.
8. Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, et al. (2012) Landscape of somatic retrotransposition in human cancers. Science 337: 967-971.
9. Bass AJ, Lawrence MS, Brace LE, Ramos AH, Drier Y, et al. (2011) Genomic sequencing of colorectal adenocarcinomas identifies a recurrent VTI1A-TCF7L2 fusion. Nat Genet 43: 964-968.
10. Sung WK, Zheng H, Li S, Chen R, Liu X, et al. (2012) Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat Genet 44: 765-769.
11. Dunning Hotopp JC, (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. Graham LA, Lougheed SC, Ewart KV, Davies PL, (2008) Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS ONE 3: e2616 doi:10.1371/journal.pone.0002616.
14. Moran NA, Jarvik T, (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328: 624-627.
15. Altincicek B, Kovacs JL, Gerardo NM, (2012) Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol Lett 8: 253-257.
16. Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, et al. (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153: 1567-1578.
17. Acuna R, Padilla BE, Florez-Ramos CP, Rubio JD, Herrera JC, 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. Danchin EGJ, Rossoa M-N, Vieiraa P, Almeida-Englera Jd, Coutinhob PM, 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. Mayer WE, Schuster LN, Bartelmes G, Dieterich C, Sommer RJ, (2011) Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC Evol Biol 11: 13.
20. Dieterich C, Clifton SW, Schuster LN, Chinwalla A, Delehaunty K, et al. (2008) The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 40: 1193-1198.
21. Stouthamer R, Breeuwer JA, Hurst GD, (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53: 71-102.
22. Werren JH, (1997) Biology of Wolbachia. Annu Rev Entomol 42: 587-609.
23. Fast EM, Toomey ME, Panaram K, Desjardins D, Kolaczyk ED, et al. (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334: 990-992.
24. Kondo N, Nikoh N, Ijichi N, Shimada M, Fukatsu T, (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A 99: 14280-14285.
25. Nikoh N, Tanaka K, Shibata F, Kondo N, Hizume M, et al. (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18: 272-280.
26. Aikawa T, Anbutsu H, Nikoh N, Kikuchi T, Shibata F, et al. (2009) Longicorn beetle that vectors pinewood nematode carries many Wolbachia genes on an autosome. Proc Biol Sci 276: 3791-3798.
27. Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, et al. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317: 1753-1756.
28. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, et al. (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: 343-348.
29. Doudoumis V, Alam U, Aksoy E, Abd-Alla A, Tsiamis G, 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. Fenn K, Conlon C, Jones M, Quail MA, Holroyd NE, et al. (2006) Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2: e94 doi:10.1371/journal.ppat.0020094.
31. McNulty SN, Foster JM, Mitreva M, Dunning Hotopp JC, Martin J, 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. Beiko RG, Harlow TJ, Ragan MA, (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102: 14332-14337.
33. Nikoh N, McCutcheon JP, Kudo T, Miyagishima S-y, Moran NA, 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. Nikoh N, Nakabachi A, (2009) Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol 7: 12.
35. Luckey TD, (1970) Introduction to the ecology of the intestinal flora. Am J Clin Nutr 23: 1430-1432.
36. Mogensen TH, (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22: 240-273.
37. Hacker G, Redecke V, Hacker H, (2002) Activation of the immune system by bacterial CpG-DNA. Immunology 105: 245-251.
38. Sander LE, Davis MJ, Boekschoten MV, Amsen D, Dascher CC, et al. (2011) Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474: 385-389.
39. Weiner AM, (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. Kapitonov VV, Jurka J, (2003) A novel class of SINE elements derived from 5S rRNA. Mol Biol Evol 20: 694-702.
41. Roy-Engel AM, (2012) LINEs, SINEs and other retroelements: do birds of a feather flock together? Front Biosci 17: 1345-1361.
42. Hancks DC, Kazazian HH Jr, (2012) Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22: 191-203.
43. Mills RE, Bennett EA, Iskow RC, Devine SE, (2007) Which transposable elements are active in the human genome? Trends Genet 23: 183-191.
44. Konkel MK, Batzer MA, (2010) A mobile threat to genome stability: the impact of non-LTR retrotransposons upon the human genome. Semin Cancer Biol 20: 211-221.
45. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, 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. Solyom S, Ewing AD, Rahrmann EP, Doucet T, Nelson HH, et al. (2012) Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res 22: 2328-2338.
47. Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, et al. (2010) Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 141: 1253-1261.
48. de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, et al. (2012) Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 13: 607-615.
49. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S, (2007) Human papillomavirus and cervical cancer. Lancet 370: 890-907.
50. Faridi R, Zahra A, Khan K, Idrees M, (2011) Oncogenic potential of Human Papillomavirus (HPV) and its relation with cervical cancer. Virol J 8: 269.
51. Corden SA, Sant-Cassia LJ, Easton AJ, Morris AG, (1999) The integration of HPV-18 DNA in cervical carcinoma. Mol Pathol 52: 275-282.
52. Melsheimer P, Vinokurova S, Wentzensen N, Bastert G, von Knebel Doeberitz M, (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 Tine BA, Kappes JC, Banerjee NS, Knops J, Lai L, et al. (2004) Clonal selection for transcriptionally active viral oncogenes during progression to cancer. J Virol 78: 11172-11186.
54. Beasley RP, Hwang LY, Lin CC, Chien CS, (1981) Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22,707 men in Taiwan. Lancet 2: 1129-1133.
55. Moore PS, Chang Y, (2010) Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat Rev Cancer 10: 878-889.
56. Murakami Y, Saigo K, Takashima H, Minami M, Okanoue T, et al. (2005) Large scaled analysis of hepatitis B virus (HBV) DNA integration in HBV related hepatocellular carcinomas. Gut 54: 1162-1168.
57. Paterlini-Brechot P, Saigo K, Murakami Y, Chami M, Gozuacik D, 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. Gozuacik D, Murakami Y, Saigo K, Chami M, Mugnier C, et al. (2001) Identification of human cancer-related genes by naturally occurring Hepatitis B Virus DNA tagging. Oncogene 20: 6233-6240.
59. Saigo K, Yoshida K, Ikeda R, Sakamoto Y, Murakami Y, 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. Lopez JV, Yuhki N, Masuda R, Modi W, O'Brien SJ, (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-Covo E, Zeller RM, Martin W, (2010) Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 6: e1000834 doi:10.1371/journal.pgen.1000834.
62. Hazkani-Covo E, Covo S, (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-Brozick JE, Savul SA, Richey LE, Baysal BE, (2001) Germ line insertion of mtDNA at the breakpoint junction of a reciprocal constitutional translocation. Hum Genet 109: 216-223.
64. Shay JW, Baba T, Zhan QM, Kamimura N, Cuthbert JA, (1991) HeLaTG cells have mitochondrial DNA inserted into the c-myc oncogene. Oncogene 6: 1869-1874.
65. Borensztajn K, Chafa O, Alhenc-Gelas M, Salha S, Reghis A, 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. Turner C, Killoran C, Thomas NS, Rosenberg M, Chuzhanova NA, et al. (2003) Human genetic disease caused by de novo mitochondrial-nuclear DNA transfer. Hum Genet 112: 303-309.
67. Goldin E, Stahl S, Cooney AM, Kaneski CR, Gupta S, et al. (2004) Transfer of a mitochondrial DNA fragment to MCOLN1 causes an inherited case of mucolipidosis IV. Hum Mutat 24: 460-465.
68. Ahmed ZM, Smith TN, Riazuddin S, Makishima T, Ghosh M, et al. (2002) Nonsyndromic recessive deafness DFNB18 and Usher syndrome type IC are allelic mutations of USHIC. Hum Genet 110: 527-531.
69. Chen JM, Chuzhanova N, Stenson PD, Ferec C, Cooper DN, (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. Schon EA, DiMauro S, Hirano M, (2012) Human mitochondrial DNA: roles of inherited and somatic mutations. Nat Rev Genet 13: 878-890.
71. Caro P, Gomez J, Arduini A, Gonzalez-Sanchez M, Gonzalez-Garcia M, et al. (2010) Mitochondrial DNA sequences are present inside nuclear DNA in rat tissues and increase with age. Mitochondrion 10: 479-486.
72. Wang D, Lloyd AH, Timmis JN, (2012) Nuclear genome diversity in somatic cells is accelerated by environmental stress. Plant Signal Behav 7: 595-597.
73. Kusters JG, van Vliet AH, Kuipers EJ, (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19: 449-490.
74. Maddocks ODK, Short AJ, Donnenberg MS, Bader S, Harrison DJ, (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. Fried B, Reddy A, Mayer D, (2011) Helminths in human carcinogenesis. Cancer Lett 305: 239-249.
76. Sears CL, Islam S, Saha A, Arjumand M, Alam NH, et al. (2008) Association of enterotoxigenic Bacteroides fragilis infection with inflammatory diarrhea. Clin Infect Dis 47: 797-803.
77. Kostic AD, Ojesina AI, Pedamallu CS, Jung J, Verhaak RG, et al. (2011) PathSeq: software to identify or discover microbes by deep sequencing of human tissue. Nat Biotechnol 29: 393-396.
78. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, et al. (2011) Enterotypes of the human gut microbiome. Nature 473: 174-180.
79. Jeon S, Allen-Hoffmann BL, Lambert PF, (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. Schwabe RF, Wang TC, (2012) Cancer. Bacteria deliver a genotoxic hit. Science 338: 52-53.
81. Chang AH, Parsonnet J, (2010) Role of bacteria in oncogenesis. Clin Microbiol Rev 23: 837-857.
82. Riley DR, Sieber KB, Robinson KM, White JR, Ganesan A, 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. Salinas GF, Braza F, Brouard S, Tak PP, Baeten D, (2013) The role of B lymphocytes in the progression from autoimmunity to autoimmune disease. Clin Immunol 146: 34-45.