Skip to main content

Implications of Lateral or Horizontal Gene Transfer from Bacteria to the Human Gastrointestinal System for Cancer Development and Treatment

  • Chapter
  • First Online:
Horizontal Gene Transfer

Abstract

The ultimate consequence of horizontal, or lateral, gene transfer, as it is usually understood, is the transient or permanent acquisition by the recipient cell(s) of new, positive or negative, functional characteristics by virtue of the incorporation of the DNA from the donor into their own genome. In reality, it is simply the manifestation of a novel gene expression repertoire(s). It has been recognized for some time that gene expression changes in human cells were primarily the result of structural alterations of their own DNA (mutations, deletions, amplification, or major rearrangements). At present, despite some degree of controversy, it is becoming an increasingly accepted notion that gene expression changes in human cells may be brought about also by their acquisition of exogenous DNA from microorganisms, particularly bacteria, present in the human microbiome. Recent published analyses of information deposited in publicly available data bases of human normal and tumor genome sequences reported a high frequency of detection of bacterial DNA integrated in the human DNA, thus providing solid evidence in support for bacteria-to-human lateral gene transfer. In addition, and most importantly, these studies also showed a much more frequent presence of bacterial DNA in human cancer samples (e.g., acute myeloid leukemia, gastric cancers) than in the DNA samples from healthy individuals, raising the possibility that the bacterial sequences might be directly or indirectly involved in the development of cancer, either by encoding protein/enzyme products with pro-carcinogenic activity or by causing epigenetic alterations that ultimately could lead to genomic instability in the host cells and, later, to carcinogenic progression. This chapter will examine the current status and landmark developments in this still growing and highly innovative research field, focusing on the role of resident bacteria in the onset and/or progression of human gastrointestinal malignancies. We will also discuss the exciting possibility of exploiting bacteria-to-human lateral gene transfer to deliver anticancer therapeutic tools to human tumors.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abreu MT (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10:131–144

    Article  CAS  PubMed  Google Scholar 

  • Abreu MT, Peek RM (2014) Gastrointestinal malignancy and the microbiome. Gastroenterology 146:1534–1546

    Article  CAS  PubMed  Google Scholar 

  • Aggarwala V et al (2017) Viral communities of the human gut: metagenomic analysis of composition and dynamics. Mob DNA 8:12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alexander JL et al (2017) Gut microbiota modulation of chemotherapy efficacy and toxicity. Nat Rev Gastroenterol Hepatol 14:356–365

    Article  CAS  PubMed  Google Scholar 

  • Allen JM et al (2018) Exercise alters gut microbiota composition and function in lean and obese humans. Med Sci Sports Exerc 50:747–757

    Article  PubMed  Google Scholar 

  • Arends MJ (2013) Pathways of colorectal carcinogenesis. Appl Immunohistochem Mol Morphol 21:97–102

    CAS  PubMed  Google Scholar 

  • Azzouz D et al (2019) Lupus nephritis is linked to disease-activity associated expansions and immunity to a gut commensal. Ann Rheum Dis:annrheumdis-2018-214856

    Google Scholar 

  • Baba Y et al (2017) Review of the gut microbiome and esophageal cancer: pathogenesis and potential clinical implications. Ann Gastroenterol Surg 1:99–104

    Article  PubMed  PubMed Central  Google Scholar 

  • Baban CK et al (2010) Bacteria as vectors for gene therapy of cancer. Bioeng Bugs 1:6

    Article  Google Scholar 

  • Baek MK (2010) Lithocholic acid upregulates uPAR and cell invasiveness via MAPK and AP-1 signaling in colon cancer cells. Cancer Lett 290:123–128

    Article  CAS  PubMed  Google Scholar 

  • Behsen J et al (2013) Probiotics: properties, examples, and specific applications. Cold Spring Harb Perspect Med 3:a010074

    Google Scholar 

  • Beiko RG et al (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102:14332–14337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benard A et al (2013) Epigenetic status of LINE-1 predicts clinical outcome in early-stage rectal cancer. Br J Cancer 109:3073–3083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bezine E et al (2014) The cytolethal distending toxin effects on Mammalian cells: a DNA damage perspective. Cell 3:592–615

    Article  CAS  Google Scholar 

  • Bhatt AP et al (2017) The role of the microbiome in cancer development and therapy. CA Cancer J Clin 67:326–344

    Article  PubMed  PubMed Central  Google Scholar 

  • Bierne H, Cossart P (2012) When bacteria target the nucleus: the emerging family of nucleomodulins. Cell Microbiol 14:622–633

    Article  CAS  PubMed  Google Scholar 

  • Bierne H et al (2012) Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2:a010272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Biteen JS et al (2016) Tools for the microbiome: nano and beyond. ACS Nano 10:6–37

    Article  CAS  PubMed  Google Scholar 

  • Bitto NJ et al (2017) Bacterial membrane vesicles transport their DNA cargo into host cells. Sci Rep 7:7072

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blaser MJ, Kirshner D (2007) The equilibria that allow bacterial persistence in human hosts. Nature 449:843–849

    Article  CAS  PubMed  Google Scholar 

  • Boto L (2014) Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc Biol Sci 281:20132450

    Article  PubMed  PubMed Central  Google Scholar 

  • Brawner KM et al (2014) Gastric microbiome and gastric cancer. Cancer J 20:211–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullman S et al (2017) Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science 358:1443–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bultman SJ (2014) Emerging roles of the microbiome in cancer. Carcinogenesis 35:249–255

    Article  CAS  PubMed  Google Scholar 

  • Burns MB, Blekhman R (2018) Integrating tumor genomics into studies of the microbiome in colorectal cancer. Gut Microbes:1–6. https://doi.org/10.1080/19490976.2018.1549421

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Burns MB et al (2018) Colorectal cancer mutational profiles correlate with defined microbial communities in the tumor microenvironment. PLoS Genet 14:e1007376

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cancer Facts and Figures (2018) American Cancer Society. Atlanta

    Google Scholar 

  • Cani PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67:1716–1725

    Article  CAS  PubMed  Google Scholar 

  • Carding S et al (2015) Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis 26:26191

    PubMed  Google Scholar 

  • Cario E (2013) Microbiota and innate immunity in intestinal inflammation and neoplasia. Curr Opin Gastroenterol 29:85–91

    Article  CAS  PubMed  Google Scholar 

  • Castellarin M et al (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22:299–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Celec P, Gardlik R (2017) Gene therapy using bacterial vectors. Front Biosci 22:81–95

    Article  CAS  Google Scholar 

  • Cervantes-Barragán L et al (2017) Lactobacillus reuteri induces gut intraepithelial CD4+ CD8αα+ T cells. Science 357:806–810

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Y et al (2014) Viral carcinogenesis: factors inducing DNA damage and virus integration. Cancers 6:2155–2186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y et al (2017) Invasive Fusobacterium nucleatum activates beta-catenin signaling in colorectal cancer via a TLR4/P-PAK1 cascade. Oncotarget 8:31802–31814

    PubMed  PubMed Central  Google Scholar 

  • Cheung SG et al (2019) Systematic review of gut microbiota and major depression. Front Psych 10:34

    Article  Google Scholar 

  • Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi IJ et al (2018) Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med 378:1085–1095

    Article  CAS  PubMed  Google Scholar 

  • Chou S et al (2015) Transferred interbacterial antagonism genes augment eukaryotic innate immune function. Nature 518:98–101

    Article  CAS  PubMed  Google Scholar 

  • Chroscinski D et al (2014) Registered report: melanoma genome sequencing reveals frequent PREX2 mutations. elife 3:e04180. https://doi.org/10.7554/eLife.04180

    Article  PubMed Central  Google Scholar 

  • Chung H et al (2012) Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149:1578–1593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Citi S (2018) Intestinal barriers protect against disease. Science 359:1097–1098

    Article  CAS  PubMed  Google Scholar 

  • Claesson MJ et al (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A 108(1):4586–4591

    Article  CAS  PubMed  Google Scholar 

  • Cohen NA, Maharshak N (2017) Novel indications for fecal microbial transplantation: update and review of the literature. Dig Dis Sci 62:1131–1145

    Article  PubMed  Google Scholar 

  • Cohen LJ et al (2017) Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature 549:48–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corning D et al (2018) The esophageal microbiome in health and disease. Curr Gastroenterol Rep 20:39

    Article  PubMed  Google Scholar 

  • Couturier-Maillard A et al (2013) NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest 123:700–711

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crisp A et al (2015) Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biol 16:50

    Article  PubMed  PubMed Central  Google Scholar 

  • Cui J et al (2015) Comprehensive characterization of the genomic alterations in human gastric cancer. Int J Cancer 137:86–95

    Article  CAS  PubMed  Google Scholar 

  • Cui M et al (2016) Circadian rhythm shapes the gut microbiota affecting host radiosensitivity. Int J Mol Sci 17:E1786

    Article  PubMed  CAS  Google Scholar 

  • Cui M et al (2017) Faecal microbiota transplantation protects against radiation-induced toxicity. EMBO Mol Med 9:448–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dahmus JD et al (2018) The gut microbiome and colorectal cancer: a review of bacterial pathogenesis. J Gastrointest Oncol 9:769–777

    Article  PubMed  PubMed Central  Google Scholar 

  • Das A et al (2016) Xenobiotic metabolism and gut microbiomes. PLoS One 11:e0163099

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dejea CM et al (2018) Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science 359:592–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desphande NP et al (2018) Signatures within the esophageal microbiome are associated with host genetics, age, and disease. Microbiome 6:227

    Article  Google Scholar 

  • Di Pilato V et al (2016) The esophageal microbiota in health and disease. Ann N Y Acad Sci 1381:21–33

    Article  PubMed  Google Scholar 

  • Ding SZ et al (2010) Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis. PLoS One 5:e9875

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ding C et al (2018) Intestinal microbiota: a novel perspective in colorectal cancer biotherapeutics. Onco Targets Ther 11:4797–4810

    Article  PubMed  PubMed Central  Google Scholar 

  • Dominguez Bello MG et al (2018) Preserving microbial diversity. Science 362:33–34

    Article  CAS  Google Scholar 

  • Dominguez-Bello MG et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107:11971–11975

    Article  PubMed  PubMed Central  Google Scholar 

  • Donaldson GP et al (2018) Gut microbiota utilize immunoglobulin A for mucosal colonization. Science 360:795–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doran KS et al (2013) Concepts and mechanisms: crossing host barriers. Cold Spring Harb Perspect Med 3:a010090

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duning Hotopp JC et al (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756

    Article  CAS  Google Scholar 

  • Dunning Hotopp JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27:157–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunning Hotopp JC (2018) Grafting or pruning in the animal tree: lateral gene transfer and gene loss? BMC Genomics 19:470

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dziki L et al (2017) Modulation of colorectal cancer risk by polymorphisms in 51Gln/His, 64Ile/Val, and 148Asp/Glu of APEX gene; 23Gly/Ala of XPA gene; and 689Ser/Arg of ERCC4 gene. Gastroenterol Res Pract 2017:3840243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faith JJ et al (2013) The long-term stability of the human gut microbiota. Science 341:1237439

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Falony G et al (2016) Population-level analysis of gut microbiome variation. Science 352:560–564

    Article  CAS  PubMed  Google Scholar 

  • Fearon ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6:479–507

    Article  CAS  PubMed  Google Scholar 

  • Fernández MF et al (2018) Breast cancer and its relationship with the microbiota. Int J Environ Res Public Health 15:E1747. https://doi.org/10.3390/ijerph15081747

    Article  CAS  PubMed  Google Scholar 

  • Fine B et al (2009) Activation of the PI3K pathway in cancer through inhibition of PTEN by exchange factor P-REX2a. Science 325:1261–1265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischbach MA (2018) Microbiome: focus on causation and mechanism. Cell 174:785–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flemer B et al (2017) Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut 66:633–643

    Article  CAS  PubMed  Google Scholar 

  • Flint HJ et al (2017) The impact of nutrition on intestinal bacterial communities. Curr Opin Microbiol 38:59–65

    Article  CAS  PubMed  Google Scholar 

  • Foster JA et al (2012) Measuring the microbiome: perspectives on advances in DNA-based techniques for exploring microbial life. Brief Bioinform 13:420–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank DN et al (2007) Molecular–phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104:13780–13785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fulbright LE et al (2017) The microbiome and the hallmarks of cancer. PLoS Pathog 13:e1006480

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gevers D et al (2014) The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 15:382–392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert JA et al (2018) Current understanding of the human microbiome. Nat Med 24:392–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goel A, Boland CR (2012) Epigenetics of colorectal cancer. Gastroenterology 143:1442–1460

    Article  CAS  PubMed  Google Scholar 

  • Golombos DM et al (2018) The role of gut microbiome in the pathogenesis of prostate Cancer: a prospective, pilot study. Urology 111:122–128

    Article  PubMed  Google Scholar 

  • González-Sarrías A (2010) NF-kappaB-dependent anti-inflammatory activity of urolithins, gut microbiota ellagic acid-derived metabolites, in human colonic fibroblasts. Br J Nutr 104:503–512

    Article  PubMed  CAS  Google Scholar 

  • Goodman B, Gardner H (2018) The microbiome and cancer. J Pathol 244:667–676

    Article  PubMed  Google Scholar 

  • Goodrich GM et al (2014) Conducting a microbiome study. Cell 158:250–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gopalakrishnan V et al (2018) Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359:97–103

    Article  CAS  PubMed  Google Scholar 

  • Goubet AG et al (2018) The impact of the intestinal microbiota in therapeutic responses against cancer. C R Biol 341:284–289

    Article  PubMed  Google Scholar 

  • Graillot V et al (2016) Genotoxicity of cytolethal distending toxin (CDT) on isogenic human colorectal cell lines: potential promoting effects for colorectal carcinogenesis. Front Cell Infect Microbiol 6:34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Greathouse KL et al (2018) Interaction between the microbiome and TP53 in human lung cancer. Genome Biol 19:123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Groth AC et al (2000) A phage integrase directs efficient site-specific integration in human cells. Proc Natl Acad Sci U S A 97:5995–6000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagland HR, Søreide K (2015) Cellular metabolism in colorectal carcinogenesis: influence of lifestyle, gut microbiome and metabolic pathways. Cancer Lett 356:273–280

    Article  CAS  PubMed  Google Scholar 

  • Hancks DC, Kazazian HH (2012) Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22:191–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He S et al (2016) Upregulation of PREX2 promotes the proliferation and migration of hepatocellular carcinoma cells via PTEN-AKT signaling. Oncol Lett 11:2223–2228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemminki K, Boffetta P (2004) Multiple primary cancers as clues to environmental and heritable causes of cancer and mechanisms of carcinogenesis. IARC Sci Publ 157:289–297

    Google Scholar 

  • Hodgetts T et al (2018) The microbiome and its publics: a participatory approach for engaging publics with the microbiome and its implications for health and hygiene. EMBO Rep 19:e45786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang W et al (2017) Widespread of horizontal gene transfer in the human genome. BMC Genomics 18:274

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huerta-Cepas J et al (2007) The human phylome. Genome Biol 8:R109

    Article  PubMed  PubMed Central  Google Scholar 

  • IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2012) Biological agents. Volume 100 B. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 100:1–441

    PubMed Central  Google Scholar 

  • Jiang H et al (2015) Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun 48:186–194

    Article  PubMed  Google Scholar 

  • Jin C et al (2019) Commensal microbiota promote lung cancer development via γδT cells. Cell 176:998–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jobin C (2018) Precision medicine using microbiota. Science 359:32–34

    Article  CAS  PubMed  Google Scholar 

  • Johnson et al (2015) Prebiotics modulate the effects of antibiotics on gut microbial diversity and functioning in vitro. Nutrients 7:4480–4497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones RB et al (2018) Inter-niche and inter-individual variation in gut microbial community assessment using stool, rectal swab, and mucosal samples. Sci Rep 8:4139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaakush NO (2018) Microbiome and esophageal adenocarcinoma. Cancer Res 78:1574

    Article  CAS  Google Scholar 

  • Kelly D, Mulder IE (2012) Microbiome and immunological interactions. Nutr Rev 70(1):S18–S30

    Article  PubMed  Google Scholar 

  • Kelly DL et al (2016) The microbiome and cancer: implications for oncology nursing science. Cancer Nurs 39:E56–E62

    Article  PubMed  Google Scholar 

  • Kesselring R et al (2016) IRAK-M expression in tumor cells supports colorectal cancer progression through reduction of antimicrobial defense and stabilization of STAT3. Cancer Cell 29:684–696

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi S (2002) Epidemiology of Helicobacter pylori and gastric cancer. Gastric Cancer 5:6–15

    Article  PubMed  Google Scholar 

  • Kim E et al (2016) Rapidly cycling Lgr5+ stem cells are exquisitely sensitive to extrinsic dietary factors that modulate colon cancer risk. Cell Death Dis 7:e2460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim W-J et al (2018) Uropathogenic Escherichia coli invades bladder epithelial cells by activating kinase networks in host cells. J Biol Chem 293:16518–16527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koga T et al (2002) Experimental Helicobacter pylori gastric infection in miniature pigs. J Med Microbiol 51:238–246

    Article  CAS  PubMed  Google Scholar 

  • Kominek J et al (2019) Eukaryotic acquisition of a bacterial operon. Cell 176:1356–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koppel N et al (2017) Chemical transformation of xenobiotics by the human gut microbiota. Science 356:eaag2770

    Article  PubMed  CAS  Google Scholar 

  • Kostic AD et al (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 22:292–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kostic AD et al (2013) Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14:207–215

    Article  CAS  Google Scholar 

  • Kowarsky M et al (2017) Numerous uncharacterized and highly divergent microbes which colonize humans are revealed by circulating cell-free DNA. Proc Natl Acad Sci U S A 114:9623–9628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krautkramer KA et al (2016) Diet-microbiota interactions mediate global epigenetic programming in multiple host tissues. Mol Cell 64:982–992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kroemer G, Zitvogel L (2018) Cancer immunotherapy in 2017: the breakthrough of the microbiota. Nat Rev Immunol 18:87–88

    Article  CAS  PubMed  Google Scholar 

  • Kumar H et al (2014) Gut microbiota as an epigenetic regulator: pilot study based on whole-genome methylation analysis. MBio 5:e02113–e02114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lacroix B, Citovsky V (2016) Transfer of DNA from bacteria to eukaryotes. MBio 7:e00863–e00816

    Article  PubMed  PubMed Central  Google Scholar 

  • Lander ES, International Human Genome Sequencing Consortium et al (2001) Initial sequencing and analysis of human genome. Nature 409:860–921

    Article  CAS  PubMed  Google Scholar 

  • Lee E-S et al (2017) Dysbiosis of gut microbiome and its impact on epigenetic regulation. J Clin Epigenetics 3:14

    Google Scholar 

  • Lemichez E, Barbieri JT (2013) General aspects and recent advances on bacterial protein toxins. Cold Spring Harb Perspect Med 3:a013573

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lerner A et al (2017) Transglutaminases in dysbiosis as potential environmental drivers of autoimmunity. Front Microbiol 8:66

    PubMed  PubMed Central  Google Scholar 

  • Lichtenstein P et al (2000) Environmental and heritable factors in the causation of cancer--analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 343:78–85

    Article  CAS  PubMed  Google Scholar 

  • Lissanu Deribe Y (2016) Mechanistic insights into the role of truncating PREX2 mutations in melanoma. Mol Cell Oncol 3:e1160174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu W et al (2016) Merkel cell polyomavirus infection and Merkel cell carcinoma. Curr Opin Virol 20:20–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llosa M et al (2012) New perspectives into bacterial DNA transfer to human cells. Trends Microbiol 20:355–359

    Article  CAS  PubMed  Google Scholar 

  • Louis P et al (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12:661–672

    Article  CAS  PubMed  Google Scholar 

  • Lu R et al (2017) Presence of Salmonella AvrA in colorectal tumor and its precursor lesions in mouse intestine and human specimens. Oncotarget 8:55104–55115

    PubMed  PubMed Central  Google Scholar 

  • Luckey TD (1972) Introduction to intestinal microecology. Am J Clin Nutr 25:1292–1294

    Article  CAS  PubMed  Google Scholar 

  • Ma C et al (2018) Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science 360(6391):eaan5931

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maier L et al (2018) Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555:623–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maisonneuve C et al (2018) The impact of the gut microbiome on colorectal cancer. Annu Rev Cancer Biol 2:229–249

    Article  Google Scholar 

  • Malinowski B et al (2019) The role of Tannerella forsythia and Porphyromonas gingivalis in pathogenesis of esophageal cancer. Infect Agent Cancer 14:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall BJ, Warren JR (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1:1311–1315

    Article  CAS  PubMed  Google Scholar 

  • Maruvada P et al (2017) The human microbiome and obesity: moving beyond associations. Cell Host Microbe 22:589–599

    Article  CAS  PubMed  Google Scholar 

  • Matson V et al (2018) The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359:104–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCoy AN et al (2013) Fusobacterium is associated with colorectal adenomas. PLoS One 8:e53653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Metcalf JA et al (2014) Antibacterial gene transfer across the tree of life. elife 3:e04266. https://doi.org/10.7554/eLife.04266

    Article  PubMed Central  Google Scholar 

  • Mira-Pascual L et al (2015) Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal biomarkers. J Gastroenterol 50:167–179

    Article  CAS  PubMed  Google Scholar 

  • Mitarai N et al (2016) Population dynamics of phage and bacteria in spatially structured habitats using phage λ and Escherichia coli. J Bacteriol 198:1783–1793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohanan V et al (2018) C1orf106 is a colitis risk gene that regulates stability of epithelial adherens junctions. Science 359:1161–1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moosavi S (2014) Location-specific effect of microbiota and MyD88-dependent signaling on Wnt/β-catenin pathway and intestinal stem cells. Gut Microbes 5:11–14

    Article  Google Scholar 

  • Moreira D, Lopez-Garcia P (2017) Protist evolution: stealing genes to gut it out. Curr Biol 27:R223–R225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morishita Y, Shimizu T (1983) Promoting effect of intestinal Pseudomonas aeruginosa on gastric tumorigenesis in rats with N-methyl-N′-nitro-N-nitrosoguanidine. Cancer Lett 17:347–352

    Article  CAS  PubMed  Google Scholar 

  • Moss SF (2017) The clinical evidence linking Helicobacter pylori to gastric cancer. Cell Mol Gastroenterol Hepatol 3:183–191

    Article  PubMed  Google Scholar 

  • Mughini-Gras L et al (2018) Increased colon cancer risk after severe Salmonella infection. PLoS One 13:e0189721

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Munro MJ et al (2018) Cancer stem cells in colorectal cancer: a review. J Clin Pathol 71:110–116

    Article  CAS  PubMed  Google Scholar 

  • Naito T et al (2017) Lipopolysaccharide from crypt-specific core microbiota modulates the colonic epithelial proliferation-to-differentiation balance. MBio 8:e01680–e01617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakata K et al (2017) Commensal microbiota-induced microRNA modulates intestinal epithelial permeability through the small GTPase ARF4. J Biol Chem 292:15426–15433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nardone G, Compare D (2015) The human gastric microbiota: is it time to rethink the pathogenesis of stomach diseases? United European Gastroenterol J 3:255–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narihiro T, Kanagata Y (2017) Genomics and metagenomics in microbial ecology: recent advances and challenges. Microbes Environ 32:1–4

    Article  PubMed  PubMed Central  Google Scholar 

  • Navarro F, Muniesa M (2017) Phages in the human body. Front Microbiol 8:566

    PubMed  PubMed Central  Google Scholar 

  • Nguyen S et al (2017) Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. MBio 8:e01874–e01817

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ni J et al (2017) A role for bacterial urease in gut dysbiosis and Crohn’s disease. Sci Transl Med 9:eaah6888

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Niederreiter L et al (2018) Food, microbiome and colorectal cancer. Dig Liver Dis 50:647–652

    Article  PubMed  Google Scholar 

  • Nistal E et al (2015) Factors determining colorectal cancer: the role of the intestinal microbiota. Front Oncol 5:220

    Article  PubMed  PubMed Central  Google Scholar 

  • Noto JM, Peek RM (2017) The gastric microbiome, its interaction with Helicobacter pylori, and its potential role in the progression to stomach cancer. PLoS Pathog 13:e1006573

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Connell Motherway M et al (2019) A Bifidobacterial pilus-associated protein promotes colonic epithelial proliferation. Mol Microbiol 111:287–301

    Article  PubMed  CAS  Google Scholar 

  • Ochman H et al (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  CAS  PubMed  Google Scholar 

  • Park SY et al (2009) Comparison of CpG island hypermethylation and repetitive DNA hypomethylation in premalignant stages of gastric cancer, stratified for Helicobacter pylori infection. J Pathol 219:410–416

    Article  CAS  PubMed  Google Scholar 

  • Paul B et al (2015) Influences of diet and the gut microbiome on epigenetic modulation in cancer and other diseases. Clin Epigenetics 7:112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perduca V et al (2018) Mutational and epigenetic signatures in cancer tissue linked to environmental exposures and lifestyle. Curr Opin Oncol 30:61–67

    Article  CAS  PubMed  Google Scholar 

  • Peters BA et al (2017) Oral microbiome composition reflects prospective risk for esophageal cancers. Cancer Res 77:6777–6787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porayath C et al (2018) Characterization of the bacteriophages binding to human matrix molecules. Int J Biol Macromol 110:608–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raza MH et al (2019) Microbiota in cancer development and treatment. J Cancer Res Clin Oncol 45:49–63

    Article  CAS  Google Scholar 

  • Reticker-Flynn NE, Engleman EG (2019) A gut punch fights cancer and infection. Nature 565:573–574

    Article  CAS  PubMed  Google Scholar 

  • Riley DR et al (2013) Bacteria-human somatic cell lateral gene transfer is enriched in cancer samples. PLoS Comput Biol 9:e1003107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson KM, Dunning Hotopp JC (2014) Mobile elements and viral integrations prompt considerations for bacterial DNA integration as a novel carcinogen. Cancer Lett 352:137–144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson KM et al (2013) A review of bacteria-animal lateral gene transfer may inform our understanding of diseases like cancer. PLoS Genet 9:e1003877

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rosadi F et al (2016) Bacterial protein toxins in human cancers. Pathog Dis 74:ftv105

    Article  PubMed  CAS  Google Scholar 

  • Rosner JL (2014) Ten times more microbial cells than body cells in humans? Microbe 9:47

    Google Scholar 

  • Routy B et al (2018a) The gut microbiota influences anticancer immunosurveillance and general health. Nat Rev Clin Oncol 15:382–396

    Article  CAS  PubMed  Google Scholar 

  • Routy B et al (2018b) Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359:91–97

    Article  CAS  PubMed  Google Scholar 

  • Roy S, Trinchieri G (2017) Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer 17:271–285

    Article  CAS  PubMed  Google Scholar 

  • Rubinstein MR et al (2013) Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 14:195–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salzberg SL (2017) Horizontal gene transfer is not a hallmark of the human genome. Genome Biol 18:85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Salzberg SL et al (2001) Microbial gene in the human genome: lateral transfer or gene loss? Science 292:1903–1906

    Article  CAS  PubMed  Google Scholar 

  • Savidge TC (2016) Epigenetic regulation of enteric neurotransmission by gut bacteria. Front Cell Neurosci 9:503

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt TSB et al (2018) The human gut microbiome: from association to modulation. Cell 172:1198–1215

    Article  CAS  PubMed  Google Scholar 

  • Schwarzenbach H et al (2011) Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer 11:426–437

    Article  CAS  PubMed  Google Scholar 

  • Sekirov I et al (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904

    Article  CAS  PubMed  Google Scholar 

  • Sender R et al (2016a) Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:337–340

    Article  CAS  PubMed  Google Scholar 

  • Sender R et al (2016b) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14:e1002533

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shan J et al (2018) Bacteriophages are more virulent to bacteria with human cells than they are in bacterial culture; insights from HT-29 cells. Sci Rep 8:5091

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sieber KB et al (2016) Modeling the integration of bacterial rRNA fragments into the human cancer genome. BMC Bioinf 17:134

    Article  CAS  Google Scholar 

  • Sieber KB et al (2017) Lateral gene transfer between prokaryotes and eukaryotes. Exp Cell Res 358:421–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegel RL et al (2017) Colorectal cancer mortality rates in adults aged 20 to 54 years in the United States, 1970-2014. JAMA 318:572–574

    Article  PubMed  PubMed Central  Google Scholar 

  • Siegel RL et al (2018) Cancer statistics. CA Cancer J Clin 68:7–30

    Article  PubMed  Google Scholar 

  • Sivaprakasam S et al (2017) Cell-surface and nuclear receptors in the colon as targets for bacterial metabolites and its relevance to colon health. Nutrients 9:E856

    Article  PubMed  CAS  Google Scholar 

  • Snider EJ et al (2018) Barrett’s esophagus is associated with a distinct oral microbiome. Clin Transl Gastroenterol 9:135

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Solyom S et al (2012) Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res 22:2328–2338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song EJ et al (2018) Progress of analytical tools and techniques for human gut microbiome research. J Microbiol 10:693–705

    Article  Google Scholar 

  • Stecher B et al (2012) Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc Natl Acad Sci U S A 109:1269–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strandwitz P et al (2019) GABA-modulating bacteria of the human gut microbiota. Nat Microbiol 4:396–403

    Article  PubMed  CAS  Google Scholar 

  • Sun J (2010) Enteric bacteria and cancer stem cells. Cancers 3:285–297

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Kato I (2016) Gut microbiota, inflammation and colorectal cancer. Genes Dis 3:130–143

    Article  PubMed  PubMed Central  Google Scholar 

  • Suzuki K et al (2015) Horizontal DNA transfer from bacteria to eukaryotes and a lesson from experimental transfers. Res Microbiol 166:753–763

    Article  CAS  PubMed  Google Scholar 

  • Tanoue T et al (2019) A defined commensal consortium elicits CD8 T cells and anti-cancer immunity. Nature 565:600–605

    Article  CAS  PubMed  Google Scholar 

  • Tetz G, Tetz V (2018) Bacteriophages as new human viral pathogens. Microorganisms 6:E54

    Article  PubMed  CAS  Google Scholar 

  • Thierry AR et al (2016) Origins, structures, and functions of circulating DNA in oncology. Cancer Metastasis Rev 35:347–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tilg H et al (2018) The intestinal microbiota in colorectal cancer. Cancer Cell 33:954–964

    Article  CAS  PubMed  Google Scholar 

  • Touchefeu Y et al (2014) Systematic review: the role of the gut microbiota in chemotherapy- or radiation-induced gastrointestinal mucositis: current evidence and potential clinical applications. Aliment Pharmacol Ther 40:409–421

    CAS  PubMed  Google Scholar 

  • Toyofuku M et al (2019) Types and origins of bacterial membrane vesicles. Nat Rev Microbiol 17:13–24

    Article  CAS  PubMed  Google Scholar 

  • Tuan J, Chen Y-X (2016) Dietary and lifestyle factors associated with colorectal cancer risk and interactions with microbiota: Fiber, red or processed meat and alcoholic drinks. Gastrointest Tumors 3:17–24

    Article  CAS  Google Scholar 

  • Turnbaugh P et al (2007) The human microbiome project. Nature 449:804–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vakil N, Megraud F (2007) Eradication therapy for Helicobacter pylori. Gastroenterology 133:985–1001

    Article  CAS  PubMed  Google Scholar 

  • van Elsland D, Neefjes J (2018) Bacterial infections and cancer. EMBO Rep 19:e46632

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Venturelli OS et al (2018) Deciphering microbial interactions in synthetic human gut microbiome communities. Mol Syst Biol 14:e8157

    Article  PubMed  PubMed Central  Google Scholar 

  • Vieira M et al (2018) Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science 359:1156–1161

    Article  PubMed Central  CAS  Google Scholar 

  • Wang Y et al (2017) The intestinal microbiota regulates body composition through NFIL3 and the circadian clock. Science 357:912–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wegmann U et al (2017) Use of genetically modified bacteria for drug delivery in humans: revisiting the safety aspect. Sci Rep 7:2294

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weinstock GM (2012) Genomic approaches to studying the human microbiota. Nature 489:250–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenger SL et al (1981) Incorporation of bacteriophage DNA into the genome of cultured human lymphocytes. In Vitro 17:695–700

    Article  CAS  PubMed  Google Scholar 

  • Werawatganon D (2014) Simple animal model of Helicobacter pylori infection. World J Gastroenterol 20:6420–6424

    Article  PubMed  PubMed Central  Google Scholar 

  • White MK et al (2014) Viruses and human cancers: a long road of discovery of molecular paradigms. Clin Microbiol Rev 27:463–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson MR et al (2019) The human gut bacterial genotoxin colibactin alkylates DNA. Science 363:eaar7785

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wroblewski LE et al (2016) The role of the microbiome in gastrointestinal cancer. Gastroenterol Clin N Am 45:543–556

    Article  Google Scholar 

  • Wu J, Chen ZJ (2014) Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 32:461–488

    Article  CAS  PubMed  Google Scholar 

  • Wu S et al (2018a) Evaluating intrinsic and non-intrinsic cancer risk factors. Nat Commun 9:3490

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu X et al (2018b) Effects of the intestinal microbial metabolite butyrate on the development of colorectal cancer. J Cancer 9:2510–2517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiao HW et al (2018) Hydrogen-water ameliorates radiation-induced gastrointestinal toxicity via MyD88’s effects on the gut microbiota. Exp Mol Med 50:e433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J et al (2017) Emerging trends in microbiome analysis: from single-cell functional imaging to microbiome. Engineering 3:66–70

    Article  CAS  Google Scholar 

  • Yang T et al (2013) Microbiota impact on the epigenetic regulation of colorectal cancer. Trends Mol Med 19:714–725

    Article  CAS  PubMed  Google Scholar 

  • Yang L et al (2014) Microbiome in reflux disorders and esophageal adenocarcinoma. Cancer J 20:207–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J et al (2016) PREX2 promotes the proliferation, invasion and migration of pancreatic cancer cells by modulating the PI3K signaling pathway. Oncol Lett 12:1139–1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y et al (2017) Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating toll-like receptor 4 signaling to nuclear factor-κB, and up-regulating expression of microRNA-21. Gastroenterology 152:851–866

    Article  CAS  PubMed  Google Scholar 

  • Yilmaz B et al (2019) Microbial network disturbances in relapsing refractory Crohn’s disease. Nat Med 25:323–336

    Article  CAS  PubMed  Google Scholar 

  • Yu YN et al (2015) Berberine may rescue Fusobacterium nucleatum-induced colorectal tumorigenesis by modulating the tumor microenvironment. Oncotarget 6:32013–32026

    Google Scholar 

  • Yu G et al (2017a) Molecular characterization of the human stomach microbiota in gastric cancer patients. Front Cell Infect Microbiol 7:302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu T et al (2017b) Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 170:548–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zackular JP et al (2014) The human gut microbiome as a screening tool for colorectal cancer. Cancer Prev Res 7:1112–1121

    Article  CAS  Google Scholar 

  • Zheng P et al (2016) Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism. Mol Psychiatry 21:786–796

    Article  CAS  PubMed  Google Scholar 

  • Zierer J et al (2018) The fecal metabolome as a functional readout of the gut microbiome. Nat Genet 50:790–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zitvogel L (2016) Microbiome and anticancer immunosurveillance. Cell 165:276–287

    Article  CAS  PubMed  Google Scholar 

  • Zitvogel L et al (2017) Anticancer effects of the microbiome and its products. Nat Rev Microbiol 15:465–478

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. Notario .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Abril, A.G., Lanzi, P.G., Notario, V. (2019). Implications of Lateral or Horizontal Gene Transfer from Bacteria to the Human Gastrointestinal System for Cancer Development and Treatment. In: Villa, T., Viñas, M. (eds) Horizontal Gene Transfer. Springer, Cham. https://doi.org/10.1007/978-3-030-21862-1_16

Download citation

Publish with us

Policies and ethics