Skip to main content
SpringerLink
Log in

Role of Microbiome in Carcinogenesis Process and Epigenetic Regulation of Colorectal Cancer

  • Protocol
  • First Online:
Cancer Epigenetics for Precision Medicine

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1856))

Abstract

Epigenetic changes during the development of colorectal cancer (CRC) play a significant role. Along with factors such as diet, lifestyle, and genetics, oncogenic infection, bacteria alone or whole microbiome, has been associated with this tumor type. How gut microbiome contributes to CRC pathogenesis in the host is not fully understood. Most of the epigenetic studies in CRC have been conducted in populations infected with Helicobacter pylori. In the current review, we summarize how the gut microbiota contributes in colon carcinogenesis and the potential role of epigenetic mechanism in gene regulation. We discuss microbiota-mediated initiation and progression of colon tumorigenesis and have also touched upon the role of microbial metabolites as an initiator or an inhibitor for procarcinogenic or antioncogenic activities. The hypothesis of gut microbiota associated CRC revealed the dynamic and complexity of microbial interaction in initiating the development of CRC. In the multifaceted processes of colonic carcinogenesis, gradual alteration of microbiota along with their microenvironment and the potential oncopathogenic microbes mediated modulation of cancer therapy and other factors involved in microbiome dysbiosis leading to the CRC have also been discussed. This review provides a comprehensive summary of the mechanisms of CRC development, the role of microbiome or single bacterial infection in regulating the processes of carcinogenesis, and the intervention by novel therapeutics. Epigenetic mechanism involved in CRC is also discussed.

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

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
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

Similar content being viewed by others

References

  1. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62(1):10–29

    Google Scholar 

  2. Siegel RL, Fedewa SA, Anderson WF, Miller KD, Ma J, Rosenberg PS, Jemal A (2017) Colorectal cancer incidence patterns in the United States, 1974–2013. J Natl Cancer Inst 109(8). https://doi.org/10.1093/jnci/djw322

  3. El-Shami K, Oeffinger KC, Erb NL, Willis A, Bretsch JK, Pratt-Chapman ML, Cannady RS, Wong SL, Rose J, Barbour AL, Stein KD, Sharpe KB, Brooks DD, Cowens-Alvarado RL (2015) American cancer society colorectal cancer survivorship care guidelines. CA Cancer J Clin 65(6):428–455

    Google Scholar 

  4. Kokki I, Papana A, Campbell H, Theodoratou E (2013) Estimating the incidence of colorectal cancer in South East Asia. Croat Med J 54(6):532–540

    Google Scholar 

  5. Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, Jemal A (2017) Colorectal cancer statistics, 2017. CA Cancer J Clin 67(3):177–193

    Google Scholar 

  6. Theodoratou E, Montazeri Z, Hawken S, Allum GC, Gong J, Tait V, Kirac I, Tazari M, Farrington SM, Demarsh A, Zgaga L, Landry D, Benson HE, Read SH, Rudan I, Tenesa A, Dunlop MG, Campbell H, Little J (2012) Systematic meta-analyses and field synopsis of genetic association studies in colorectal cancer. J Natl Cancer Inst 104(19):1433–1457

    Google Scholar 

  7. Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, Norat T (2011) Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS One 6(6):e20456

    Google Scholar 

  8. Mai V, McCrary QM, Sinha R, Glei M (2009) Associations between dietary habits and body mass index with gut microbiota composition and fecal water genotoxicity: an observational study in African American and Caucasian American volunteers. Nutr J 8:49

    Google Scholar 

  9. Satia-Abouta J, Galanko JA, Martin CF, Potter JD, Ammerman A, Sandler RS (2003) Associations of micronutrients with colon cancer risk in African Americans and whites: results from the North Carolina colon cancer study. Cancer Epidemiol Biomark Prev 12(8):747–754

    Google Scholar 

  10. Butler LM, Sinha R, Millikan RC, Martin CF, Newman B, Gammon MD, Ammerman AS, Sandler RS (2003) Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol 157(5):434–445

    Google Scholar 

  11. Giovannucci E (2009) Vitamin D and cancer incidence in the Harvard cohorts. Ann Epidemiol 19(2):84–88

    Google Scholar 

  12. Center MM, Jemal A, Smith RA, Ward E (2009) Worldwide variations in colorectal cancer. CA Cancer J Clin 59(6):366–378

    Google Scholar 

  13. Ferlay J, Parkin DM, Steliarova-Foucher E (2010) Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 46(4):765–781

    Google Scholar 

  14. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917

    Google Scholar 

  15. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61(5):759–767

    Google Scholar 

  16. Lane DP (1992) Cancer. p53, guardian of the genome. Nature 358(6381):15–16

    Google Scholar 

  17. Kaufmann WK, Paules RS (1996) DNA damage and cell cycle checkpoints. FASEB J 10(2):238–247

    Google Scholar 

  18. Niida H, Nakanishi M (2006) DNA damage checkpoints in mammals. Mutagenesis 21(1):3–9

    Google Scholar 

  19. Wood LD, Parsons DW, Jones S, Lin J, Sjöblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z, Croshaw R, Willis J, Dawson D, Shipitsin M, Willson JK, Sukumar S, Polyak K, Park BH, Pethiyagoda CL, Pant PV, Ballinger DG, Sparks AB, Hartigan J, Smith DR, Suh E, Papadopoulos N, Buckhaults P, Markowitz SD, Parmigiani G, Kinzler KW, Velculescu VE, Vogelstein B (2007) The genomic landscapes of human breast and colorectal cancers. Science 318(5853):1108–1113

    Google Scholar 

  20. Todaro M, Iovino F, Eterno V, Cammareri P, Gambara G, Espina V, Gulotta G, Dieli F, Giordano S, De Maria R, Stassi G (2010) Tumorigenic and metastatic activity of human thyroid cancer stem cells. Cancer Res 70(21):8874–8885

    Google Scholar 

  21. Fu C, Liang X, Cui W, Ober-Blöbaum J, Vazzana J, Shrikant PA, Lee KP, Clausen BE, Mellman I, Jiang A (2015) Beta-catenin in dendritic cells exerts opposite functions in cross-priming and maintenance of CD8+ T cells through regulation of IL-10. Proc Natl Acad Sci U S A 112(9):2823–2828

    Google Scholar 

  22. Spranger S, Gajewski TF (2015) A new paradigm for tumor immune escape: beta-catenin-driven immune exclusion. J Immunother Cancer 3:43

    Google Scholar 

  23. Pai SG, Carneiro BA, Mota JM, Costa R, Leite CA, Barroso-Sousa R, Kaplan JB, Chae YK, Giles FJ (2017) Wnt/beta-catenin pathway: modulating anticancer immune response. J Hematol Oncol 10(1):101

    Google Scholar 

  24. Network CGA (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487(7407):330–337

    Google Scholar 

  25. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457(7229):608–611

    Google Scholar 

  26. Kanwar SS, Nautiyal J, Majumdar AP (2010) EGFR(S) inhibitors in the treatment of gastro-intestinal cancers: what's new? Curr Drug Targets 11(6):682–698

    Google Scholar 

  27. Todaro M, Francipane MG, Medema JP, Stassi G (2010) Colon cancer stem cells: promise of targeted therapy. Gastroenterology 138(6):2151–2162

    Google Scholar 

  28. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr, Kinzler KW (2013) Cancer genome landscapes. Science 339(6127):1546–1558

    Google Scholar 

  29. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM, Bos JL (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319(9):525–532

    Google Scholar 

  30. Robbins DH, Itzkowitz SH (2002) The molecular and genetic basis of colon cancer. Med Clin North Am 86(6):1467–1495

    Google Scholar 

  31. Brennan CA, Garrett WS (2016) Gut microbiota, inflammation, and colorectal cancer. Annu Rev Microbiol 70:395–411

    Google Scholar 

  32. Sender R, Fuchs S, Milo R (2016) Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164(3):337–340

    Google Scholar 

  33. Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107–133

    Google Scholar 

  34. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, Beaumont M, Van Treuren W, Knight R, Bell JT, Spector TD, Clark AG, Ley RE (2014) Human genetics shape the gut microbiome. Cell 159(4):789–799

    Google Scholar 

  35. Bhatt AP, Redinbo MR, Bultman SJ (2017) The role of the microbiome in cancer development and therapy. CA Cancer J Clin 67(4):326–344

    Google Scholar 

  36. Marchesi JR, Dutilh BE, Hall N, Peters WH, Roelofs R, Boleij A, Tjalsma H (2011) Towards the human colorectal cancer microbiome. PLoS One 6(5):e20447

    Google Scholar 

  37. Louis P, Hold GL, Flint HJ (2014) Flint, the gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12(10):661–672

    Google Scholar 

  38. Sears CL, Garrett WS (2014) Microbes, microbiota, and colon cancer. Cell Host Microbe 15(3):317–328

    Google Scholar 

  39. Drewes JL, Housseau F, Sears CL (2016) Sporadic colorectal cancer: microbial contributors to disease prevention, development and therapy. Br J Cancer 115(3):273–280

    Google Scholar 

  40. Louis P, Flint HJ (2009) Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 294(1):1–8

    Google Scholar 

  41. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504(7480):451–455

    Google Scholar 

  42. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, Taniguchi T, Takeda K, Hori S, Ivanov II, Umesaki Y, Itoh K, Honda K (2011) Induction of colonic regulatory T cells by indigenous clostridium species. Science 331(6015):337–341

    Google Scholar 

  43. Rose DP, Connolly JM (1999) Omega-3 fatty acids as cancer chemopreventive agents. Pharmacol Ther 83(3):217–244

    Google Scholar 

  44. Piazzi G, D'Argenio G, Prossomariti A, Lembo V, Mazzone G, Candela M, Biagi E, Brigidi P, Vitaglione P, Fogliano V, D'Angelo L, Fazio C, Munarini A, Belluzzi A, Ceccarelli C, Chieco P, Balbi T, Loadman PM, Hull MA, Romano M, Bazzoli F, Ricciardiello L (2014) Eicosapentaenoic acid free fatty acid prevents and suppresses colonic neoplasia in colitis-associated colorectal cancer acting on notch signaling and gut microbiota. Int J Cancer 135(9):2004–2013

    Google Scholar 

  45. Van Raay T, Allen-Vercoe E (2017) Microbial interactions and interventions in colorectal cancer. Microbiol Spectr 5(3). https://doi.org/10.1128/microbiolspec.BAD-0004-2016

  46. Sears CL, Pardoll DM (2011) Pardoll, perspective: alpha-bugs, their microbial partners, and the link to colon cancer. J Infect Dis 203(3):306–311

    Google Scholar 

  47. Wu S, Rhee KJ, Zhang M, Franco A, Sears CL (2007) Bacteroides fragilis toxin stimulates intestinal epithelial cell shedding and gamma-secretase-dependent E-cadherin cleavage. J Cell Sci 120(Pt 11):1944–1952

    Google Scholar 

  48. Sears CL, Islam S, Saha A, Arjumand M, Alam NH, Faruque AS, Salam MA, Shin J, Hecht D, Weintraub A, Sack RB, Qadri F (2008) Association of enterotoxigenic Bacteroides fragilis infection with inflammatory diarrhea. Clin Infect Dis 47(6):797–803

    Google Scholar 

  49. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, Barnes R, Watson P, Allen-Vercoe E, Moore RA, Holt RA (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22(2):299–306

    Google Scholar 

  50. Tjalsma H, Boleij A, Marchesi JR, Dutilh BE (2012) A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 10(8):575–582

    Google Scholar 

  51. Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313(5788):848–851

    Google Scholar 

  52. Tahara T, Yamamoto E, Suzuki H, Maruyama R, Chung W, Garriga J, Jelinek J, Yamano HO, Sugai T, An B, Shureiqi I, Toyota M, Kondo Y, Estécio MR, Issa JP (2014) Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res 74(5):1311–1318

    Google Scholar 

  53. Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, Peterson SN, Snesrud EC, Borisy GG, Lazarev M, Stein E, Vadivelu J, Roslani AC, Malik AA, Wanyiri JW, Goh KL, Thevambiga I, Fu K, Wan F, Llosa N, Housseau F, Romans K, Wu X, McAllister FM, Wu S, Vogelstein B, Kinzler KW, Pardoll DM, Sears CL (2014) Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A 111(51):18321–18326

    Google Scholar 

  54. Li S, Peng C, Wang C, Zheng J, Hu Y, Li D (2017) Microbial succession and nitrogen cycling in cultured biofilms as affected by the inorganic nitrogen availability. Microb Ecol 73(1):1–15

    Google Scholar 

  55. Bromberg J, Wang TC (2009) Inflammation and cancer: IL-6 and STAT3 complete the link. Cancer Cell 15(2):79–80

    Google Scholar 

  56. Vipperla K, O'Keefe SJ (2016) Diet, microbiota, and dysbiosis: a 'recipe' for colorectal cancer. Food Funct 7(4):1731–1740

    Google Scholar 

  57. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336(6086):1268–1273

    Google Scholar 

  58. Emerit I, Garban F, Vassy J, Levy A, Filipe P, Freitas J (1996) Superoxide-mediated clastogenesis and anticlastogenic effects of exogenous superoxide dismutase. Proc Natl Acad Sci U S A 93(23):12799–12804

    Google Scholar 

  59. Huycke MM, Moore D, Joyce W, Wise P, Shepard L, Kotake Y, Gilmore MS (2001) Extracellular superoxide production by enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol 42(3):729–740

    Google Scholar 

  60. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638

    Google Scholar 

  61. Allen-Vercoe E, Jobin C (2014) Fusobacterium and Enterobacteriaceae: important players for CRC? Immunol Lett 162(2 Pt A):54–61

    Google Scholar 

  62. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214

    Google Scholar 

  63. Ivanov II, Honda K (2012) Intestinal commensal microbes as immune modulators. Cell Host Microbe 12(4):496–508

    Google Scholar 

  64. Zitvogel L, Daillère R, Roberti MP, Routy B, Kroemer G (2017) Anticancer effects of the microbiome and its products. Nat Rev Microbiol 15(8):465–478

    Google Scholar 

  65. Zitvogel L, Galluzzi L, Viaud S, Vétizou M, Daillère R, Merad M, Kroemer G (2015) Cancer and the gut microbiota: an unexpected link. Sci Transl Med 7(271):271ps1

    Google Scholar 

  66. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillère R, Hannani D, Enot DP, Pfirschke C, Engblom C, Pittet MJ, Schlitzer A, Ginhoux F, Apetoh L, Chachaty E, Woerther PL, Eberl G, Bérard M, Ecobichon C, Clermont D, Bizet C, Gaboriau-Routhiau V, Cerf-Bensussan N, Opolon P, Yessaad N, Vivier E, Ryffel B, Elson CO, Doré J, Kroemer G, Lepage P, Boneca IG, Ghiringhelli F, Zitvogel L (2013) The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 342(6161):971–976

    Google Scholar 

  67. Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, Poirier-Colame V, Roux A, Becharef S, Formenti S, Golden E, Cording S, Eberl G, Schlitzer A, Ginhoux F, Mani S, Yamazaki T, Jacquelot N, Enot DP, Bérard M, Nigou J, Opolon P, Eggermont A, Woerther PL, Chachaty E, Chaput N, Robert C, Mateus C, Kroemer G, Raoult D, Boneca IG, Carbonnel F, Chamaillard M, Zitvogel L (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350(6264):1079–1084

    Google Scholar 

  68. Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML, Chang EB, Gajewski TF (2015) Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350(6264):1084–1089

    Google Scholar 

  69. Modi SR, Collins JJ, Relman DA (2014) Relman, antibiotics and the gut microbiota. J Clin Invest 124(10):4212–4218

    Google Scholar 

  70. Pitt JM, Vétizou M, Gomperts Boneca I, Lepage P, Chamaillard M, Zitvogel L (2016) Enhancing the clinical coverage and anticancer efficacy of immune checkpoint blockade through manipulation of the gut microbiota. Oncoimmunology 6(1):e1132137

    Google Scholar 

  71. Kawahara T, Takahashi T, Oishi K, Tanaka H, Masuda M, Takahashi S, Takano M, Kawakami T, Fukushima K, Kanazawa H, Suzuki T (2015) Consecutive oral administration of Bifidobacterium longum MM-2 improves the defense system against influenza virus infection by enhancing natural killer cell activity in a murine model. Microbiol Immunol 59(1):1–12

    Google Scholar 

  72. Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, Gaskins HR, O'Keefe SJ (2013) Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr 98(1):111–120

    Google Scholar 

  73. Bordonaro M, Lazarova DL, Sartorelli AC (2008) Butyrate and Wnt signaling: a possible solution to the puzzle of dietary fiber and colon cancer risk? Cell Cycle 7(9):1178–1183

    Google Scholar 

  74. Donaldson GP, Lee SM, Mazmanian SK (2016) Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 14(1):20–32

    Google Scholar 

  75. Windey K, De Preter V, Verbeke K (2012) Relevance of protein fermentation to gut health. Mol Nutr Food Res 56(1):184–196

    Google Scholar 

  76. Toden S, Bird AR, Topping DL, Conlon MA (2007) High red meat diets induce greater numbers of colonic DNA double-strand breaks than white meat in rats: attenuation by high-amylose maize starch. Carcinogenesis 28(11):2355–2362

    Google Scholar 

  77. Xu R, Wang Q, Li L (2015) A genome-wide systems analysis reveals strong link between colorectal cancer and trimethylamine N-oxide (TMAO), a gut microbial metabolite of dietary meat and fat. BMC Genomics 16(Suppl 7):S4

    Google Scholar 

  78. Toprak NU, Yagci A, Gulluoglu BM, Akin ML, Demirkalem P, Celenk T, Soyletir G (2006) A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin Microbiol Infect 12(8):782–786

    Google Scholar 

  79. Draht MX, Riedl RR, Niessen H, Carvalho B, Meijer GA, Herman JG, van Engeland M, Melotte V, Smits KM (2012) Promoter CpG island methylation markers in colorectal cancer: the road ahead. Epigenomics 4(2):179–194

    Google Scholar 

  80. Lee S, Oh T, Chung H, Rha S, Kim C, Moon Y, Hoehn BD, Jeong D, Lee S, Kim N, Park C, Yoo M, An S (2012) Identification of GABRA1 and LAMA2 as new DNA methylation markers in colorectal cancer. Int J Oncol 40(3):889–898

    Google Scholar 

  81. You JS, Jones PA (2012) Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell 22(1):9–20

    Google Scholar 

  82. Khare S, Verma M (2012) Epigenetics of colon cancer. Methods Mol Biol 863:177–185

    Google Scholar 

  83. Verma M (2015) Cancer epigenetics: risk assessment, diagnosis, treatment, and prognosis. Preface. Methods Mol Biol 1238:v–vi

    Google Scholar 

  84. Takane K, Midorikawa Y, Yagi K, Sakai A, Aburatani H, Takayama T, Kaneda A (2014) Aberrant promoter methylation of PPP1R3C and EFHD1 in plasma of colorectal cancer patients. Cancer Med 3(5):1235–1245

    Google Scholar 

  85. Valenzuela MA, Canales J, Corvalán AH, Quest AF (2015) Helicobacter pylori-induced inflammation and epigenetic changes during gastric carcinogenesis. World J Gastroenterol 21(45):12742–12756

    Google Scholar 

  86. Kumar D, Verma M (2009) Methods in cancer epigenetics and epidemiology. Methods Mol Biol 471:273–288

    Google Scholar 

  87. Deb M, Sengupta D, Kar S, Rath SK, Roy S, Das G, Patra SK (2016) Epigenetic drift towards histone modifications regulates CAV1 gene expression in colon cancer. Gene 581(1):75–84

    Google Scholar 

  88. Deb M, Sengupta D, Rath SK, Kar S, Parbin S, Shilpi A, Pradhan N, Bhutia SK, Roy S, Patra SK (2015) Clusterin gene is predominantly regulated by histone modifications in human colon cancer and ectopic expression of the nuclear isoform induces cell death. Biochim Biophys Acta 1852(8):1630–1645

    Google Scholar 

  89. Gezer U, Yörüker EE, Keskin M, Kulle CB, Dharuman Y, Holdenrieder S (2015) Histone methylation marks on circulating nucleosomes as novel blood-based biomarker in colorectal cancer. Int J Mol Sci 16(12):29654–29662

    Google Scholar 

  90. Benard A, Goossens-Beumer IJ, van Hoesel AQ, de Graaf W, Horati H, Putter H, Zeestraten EC, van de Velde CJ, Kuppen PJ (2014) Histone trimethylation at H3K4, H3K9 and H4K20 correlates with patient survival and tumor recurrence in early-stage colon cancer. BMC Cancer 14:531

    Google Scholar 

  91. Li H, Myeroff L, Kasturi L, Krumroy L, Schwartz S, Willson JK, Stanbridge E, Casey G, Markowitz S (2002) Chromosomal autonomy of hMLH1 methylation in colon cancer. Oncogene 21(9):1443–1449

    Google Scholar 

  92. Patai ÁV, Valcz G, Hollósi P, Kalmár A, Péterfia B, Patai Á, Wichmann B, Spisák S, Barták BK, Leiszter K, Tóth K, Sipos F, Kovalszky I, Péter Z, Miheller P, Tulassay Z, Molnár B (2015) Comprehensive DNA methylation analysis reveals a common ten-gene methylation signature in colorectal adenomas and carcinomas. PLoS One 10(8):e0133836

    Google Scholar 

  93. Rawłuszko-Wieczorek AA, Horbacka K, Krokowicz P, Misztal M, Jagodziński PP (2014) Prognostic potential of DNA methylation and transcript levels of HIF1A and EPAS1 in colorectal cancer. Mol Cancer Res 12(8):1112–1127

    Google Scholar 

  94. Chen SP, Chiu SC, Wu CC, Lin SZ, Kang JC, Chen YL, Lin PC, Pang CY, Harn HJ (2009) The association of methylation in the promoter of APC and MGMT and the prognosis of Taiwanese CRC patients. Genet Test Mol Biomarkers 13(1):67–71

    Google Scholar 

  95. Ines C, Donia O, Rahma B, Ben Ammar A, Sameh A, Khalfallah T, Abdelmajid BH, Sabeh M, Saadia B (2014) Implication of K-ras and p53 in colorectal cancer carcinogenesis in Tunisian population cohort. Tumour Biol 35(7):7163–7175

    Google Scholar 

  96. Knösel T, Altendorf-Hofmann A, Lindner L, Issels R, Hermeking H, Schuebbe G, Gibis S, Siemens H, Kampmann E, Kirchner T (2014) Loss of p16(INK4a) is associated with reduced patient survival in soft tissue tumours, and indicates a senescence barrier. J Clin Pathol 67(7):592–598

    Google Scholar 

  97. Li YX, Lu Y, Li CY, Yuan P, Lin SS (2014) Role of CDH1 promoter methylation in colorectal carcinogenesis: a meta-analysis. DNA Cell Biol 33(7):455–462

    Google Scholar 

  98. Nazemalhosseini Mojarad E, Kuppen PJ, Aghdaei HA, Zali MR (2013) The CpG island methylator phenotype (CIMP) in colorectal cancer. Gastroenterol Hepatol Bed Bench 6(3):120–128

    Google Scholar 

  99. Ogino S, Cantor M, Kawasaki T, Brahmandam M, Kirkner GJ, Weisenberger DJ, Campan M, Laird PW, Loda M, Fuchs CS (2006) CpG island methylator phenotype (CIMP) of colorectal cancer is best characterised by quantitative DNA methylation analysis and prospective cohort studies. Gut 55(7):1000–1006

    Google Scholar 

  100. Paul S, Ramalingam S, Subramaniam D, Baranda J, Anant S, Dhar A (2014) Histone demethylases in colon cancer. Curr Colorectal Cancer Rep 10(4):417–424

    Google Scholar 

  101. Aherne ST, Madden SF, Hughes DJ, Pardini B, Naccarati A, Levy M, Vodicka P, Neary P, Dowling P, Clynes M (2015) Circulating miRNAs miR-34a and miR-150 associated with colorectal cancer progression. BMC Cancer 15:329

    Google Scholar 

  102. Chen X, Shi K, Wang Y, Song M, Zhou W, Tu H, Lin Z (2015) Clinical value of integrated-signature miRNAs in colorectal cancer: miRNA expression profiling analysis and experimental validation. Oncotarget 6(35):37544–37556

    Google Scholar 

  103. Hur K, Toiyama Y, Takahashi M, Balaguer F, Nagasaka T, Koike J, Hemmi H, Koi M, Boland CR, Goel A (2013) MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis. Gut 62(9):1315–1326

    Google Scholar 

  104. Earle JS, Luthra R, Romans A, Abraham R, Ensor J, Yao H, Hamilton SR (2010) Association of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. J Mol Diagn 12(4):433–440

    Google Scholar 

  105. Hamfjord J, Stangeland AM, Hughes T, Skrede ML, Tveit KM, Ikdahl T, Kure EH (2012) Differential expression of miRNAs in colorectal cancer: comparison of paired tumor tissue and adjacent normal mucosa using high-throughput sequencing. PLoS One 7(4):e34150

    Google Scholar 

  106. Migliore C, Martin V, Leoni VP, Restivo A, Atzori L, Petrelli A, Isella C, Zorcolo L, Sarotto I, Casula G, Comoglio PM, Columbano A, Giordano S (2012) MiR-1 downregulation cooperates with MACC1 in promoting MET overexpression in human colon cancer. Clin Cancer Res 18(3):737–747

    Google Scholar 

  107. Anton R, Chatterjee SS, Simundza J, Cowin P, Dasgupta R (2011) A systematic screen for micro-RNAs regulating the canonical Wnt pathway. PLoS One 6(10):e26257

    Google Scholar 

  108. ElSharawy A, Röder C, Becker T, Habermann JK, Schreiber S, Rosenstiel P, Kalthoff H (2016) Concentration of circulating miRNA-containing particles in serum enhances miRNA detection and reflects CRC tissue-related deregulations. Oncotarget 7(46):75353–75365

    Google Scholar 

  109. Kanaan Z, Rai SN, Eichenberger MR, Barnes C, Dworkin AM, Weller C, Cohen E, Roberts H, Keskey B, Petras RE, Crawford NP, Galandiuk S (2012) Differential microRNA expression tracks neoplastic progression in inflammatory bowel disease-associated colorectal cancer. Hum Mutat 33(3):551–560

    Google Scholar 

  110. Wang X, Wang J, Ma H, Zhang J, Zhou X (2012) Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer. Med Oncol 29(2):919–927

    Google Scholar 

  111. Xi Y, Formentini A, Chien M, Weir DB, Russo JJ, Ju J, Kornmann M, Ju J (2006) Prognostic values of microRNAs in colorectal cancer. Biomark Insights 2:113–121

    Google Scholar 

  112. Vinci S, Gelmini S, Mancini I, Malentacchi F, Pazzagli M, Beltrami C, Pinzani P, Orlando C (2013) Genetic and epigenetic factors in regulation of microRNA in colorectal cancers. Methods 59(1):138–146

    Google Scholar 

  113. Bandres E, Agirre X, Bitarte N, Ramirez N, Zarate R, Roman-Gomez J, Prosper F, Garcia-Foncillas J (2009) Epigenetic regulation of microRNA expression in colorectal cancer. Int J Cancer 125(11):2737–2743

    Google Scholar 

  114. Okayama H, Schetter AJ, Harris CC (2012) MicroRNAs and inflammation in the pathogenesis and progression of colon cancer. Dig Dis 30(Suppl 2):9–15

    Google Scholar 

  115. Xiong B, Cheng Y, Ma L, Zhang C (2013) MiR-21 regulates biological behavior through the PTEN/PI-3 K/Akt signaling pathway in human colorectal cancer cells. Int J Oncol 42(1):219–228

    Google Scholar 

  116. Kjaer-Frifeldt S, Hansen TF, Nielsen BS, Joergensen S, Lindebjerg J, Soerensen FB, dePont Christensen R, Jakobsen A, Danish Colorectal Cancer Group (2012) The prognostic importance of miR-21 in stage II colon cancer: a population-based study. Br J Cancer 107(7):1169–1174

    Google Scholar 

  117. Vogt M, Munding J, Grüner M, Liffers ST, Verdoodt B, Hauk J, Steinstraesser L, Tannapfel A, Hermeking H (2011) Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch 458(3):313–322

    Google Scholar 

  118. Kim NH, Kim HS, Kim NG, Lee I, Choi HS, Li XY, Kang SE, Cha SY, Ryu JK, Na JM, Park C, Kim K, Lee S, Gumbiner BM, Yook JI, Weiss SJ (2011) p53 and microRNA-34 are suppressors of canonical Wnt signaling. Sci Signal 4(197):ra71

    Google Scholar 

  119. Mudduluru G, Ceppi P, Kumarswamy R, Scagliotti GV, Papotti M, Allgayer H (2011) Regulation of Axl receptor tyrosine kinase expression by miR-34a and miR-199a/b in solid cancer. Oncogene 30(25):2888–2899

    Google Scholar 

  120. Tsuchida A, Ohno S, Wu W, Borjigin N, Fujita K, Aoki T, Ueda S, Takanashi M, Kuroda M (2011) miR-92 is a key oncogenic component of the miR-17-92 cluster in colon cancer. Cancer Sci 102(12):2264–2271

    Google Scholar 

  121. Motoyama K, Inoue H, Takatsuno Y, Tanaka F, Mimori K, Uetake H, Sugihara K, Mori M (2009) Over- and under-expressed microRNAs in human colorectal cancer. Int J Oncol 34(4):1069–1075

    Google Scholar 

  122. Xu XM, Qian JC, Deng ZL, Cai Z, Tang T, Wang P, Zhang KH, Cai JP (2012) Expression of miR-21, miR-31, miR-96 and miR-135b is correlated with the clinical parameters of colorectal cancer. Oncol Lett 4(2):339–345

    Google Scholar 

  123. Li XM, Wang AM, Zhang J, Yi H (2011) Down-regulation of miR-126 expression in colorectal cancer and its clinical significance. Med Oncol 28(4):1054–1057

    Google Scholar 

  124. Wu J, Qian J, Li C, Kwok L, Cheng F, Liu P, Perdomo C, Kotton D, Vaziri C, Anderlind C, Spira A, Cardoso WV, Lü J (2010) miR-129 regulates cell proliferation by downregulating Cdk6 expression. Cell Cycle 9(9):1809–1818

    Google Scholar 

  125. Koga Y, Yasunaga M, Takahashi A, Kuroda J, Moriya Y, Akasu T, Fujita S, Yamamoto S, Baba H, Matsumura Y (2010) MicroRNA expression profiling of exfoliated colonocytes isolated from feces for colorectal cancer screening. Cancer Prev Res (Phila) 3(11):1435–1442

    Google Scholar 

  126. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink JA, Bolijn A, Meijer GA, Agami R (2008) Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 68(14):5795–5802

    Google Scholar 

  127. Ma Q, Yang L, Wang C, Yu YY, Zhou B, Zhou ZG (2011) Differential expression of colon cancer microRNA in microarray study. Sichuan Da Xue Xue Bao Yi Xue Ban 42(3):344–348

    Google Scholar 

  128. Faltejskova P, Svoboda M, Srutova K, Mlcochova J, Besse A, Nekvindova J, Radova L, Fabian P, Slaba K, Kiss I, Vyzula R, Slaby O (2012) Identification and functional screening of microRNAs highly deregulated in colorectal cancer. J Cell Mol Med 16(11):2655–2666

    Google Scholar 

  129. Mosakhani N, Sarhadi VK, Borze I, Karjalainen-Lindsberg ML, Sundström J, Ristamäki R, Osterlund P, Knuutila S (2012) MicroRNA profiling differentiates colorectal cancer according to KRAS status. Genes Chromosomes Cancer 51(1):1–9

    Google Scholar 

  130. Singh U, Malik MA, Goswami S, Shukla S, Kaur J (2016) Epigenetic regulation of human retinoblastoma. Tumour Biol 37(11):14427–14441

    Google Scholar 

  131. Wu P, Cao Z, Wu S (2016) New progress of epigenetic biomarkers in urological cancer. Dis Markers 2016:9864047

    Google Scholar 

  132. Wu Y, Hao X, Feng Z, Liu Y (2015) Genetic polymorphisms in miRNAs and susceptibility to colorectal cancer. Cell Biochem Biophys 71(1):271–278

    Google Scholar 

  133. Slattery ML, Herrick JS, Pellatt DF, Mullany LE, Stevens JR, Wolff E, Hoffman MD, Wolff RK, Samowitz W (2016) Site-specific associations between miRNA expression and survival in colorectal cancer cases. Oncotarget 7(37):60193–60205

    Google Scholar 

  134. Noguchi T, Toiyama Y, Kitajima T, Imaoka H, Hiro J, Saigusa S, Tanaka K, Inoue Y, Mohri Y, Toden S, Kusunoki M (2016) miRNA-503 promotes tumor progression and is associated with early recurrence and poor prognosis in human colorectal cancer. Oncology 90(4):221–231

    Google Scholar 

  135. Pichler M, Winter E, Stotz M, Eberhard K, Samonigg H, Lax S, Hoefler G (2012) Down-regulation of KRAS-interacting miRNA-143 predicts poor prognosis but not response to EGFR-targeted agents in colorectal cancer. Br J Cancer 106(11):1826–1832

    Google Scholar 

  136. Zhang Y, Zhang XR, Park JL, Kim JH, Zhang L, Ma JL, Liu WD, Deng DJ, You WC, Kim YS, Pan KF (2016) Genome-wide DNA methylation profiles altered by helicobacter pylori in gastric mucosa and blood leukocyte DNA. Oncotarget 7(24):37132–37144

    Google Scholar 

  137. Papastergiou V, Karatapanis S, Georgopoulos SD (2016) Helicobacter pylori and colorectal neoplasia: is there a causal link? World J Gastroenterol 22(2):649–658

    Google Scholar 

  138. Shmuely H, Melzer E, Braverman M, Domniz N, Yahav J (2014) Helicobacter pylori infection is associated with advanced colorectal neoplasia. Scand J Gastroenterol 49(4):516–517

    Google Scholar 

  139. Brew R, Erikson JS, West DC, Kinsella AR, Slavin J, Christmas SE (2000) Interleukin-8 as an autocrine growth factor for human colon carcinoma cells in vitro. Cytokine 12(1):78–85

    Google Scholar 

  140. Choi W, Lee J, Lee JY, Lee SM, Kim DW, Kim YJ (2016) Classification of colon cancer patients based on the methylation patterns of promoters. Genomics Inform 14(2):46–52

    Google Scholar 

  141. Laghi L, Randolph AE, Chauhan DP, Marra G, Major EO, Neel JV, Boland CR (1999) JC virus DNA is present in the mucosa of the human colon and in colorectal cancers. Proc Natl Acad Sci U S A 96(13):7484–7489

    Google Scholar 

  142. Lin PY, Fung CY, Chang FP, Huang WS, Chen WC, Wang JY, Chang D (2008) Prevalence and genotype identification of human JC virus in colon cancer in Taiwan. J Med Virol 80(10):1828–1834

    Google Scholar 

  143. Sinagra E, Raimondo D, Gallo E, Stella M, Cottone M, Orlando A, Rossi F, Orlando E, Messina M, Tomasello G, Lo Monte AI, La Rocca E, Rizzo AG (2014) Could JC virus provoke metastasis in colon cancer? World J Gastroenterol 20(42):15745–15749

    Google Scholar 

  144. Theodoropoulos G, Panoussopoulos D, Papaconstantinou I, Gazouli M, Perdiki M, Bramis J, Lazaris AC (2005) Assessment of JC polyoma virus in colon neoplasms. Dis Colon Rectum 48(1):86–91

    Google Scholar 

  145. Brown JM, Hazen SL (2017) Targeting of microbe-derived metabolites to improve human health: the next frontier for drug discovery. J Biol Chem 292(21):8560–8568

    Google Scholar 

  146. Fleming SE, Fitch MD, Chansler MW (1989) High-fiber diets: influence on characteristics of cecal digesta including short-chain fatty acid concentrations and pH. Am J Clin Nutr 50(1):93–99

    Google Scholar 

  147. Kaczmarczyk MM, Miller MJ, Freund GG (2012) The health benefits of dietary fiber: beyond the usual suspects of type 2 diabetes mellitus, cardiovascular disease and colon cancer. Metabolism 61(8):1058–1066

    Google Scholar 

  148. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, Flint HJ (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66(4):1654–1661

    Google Scholar 

  149. Peters U, Sinha R, Chatterjee N, Subar AF, Ziegler RG, Kulldorff M, Bresalier R, Weissfeld JL, Flood A, Schatzkin A, Hayes RB, Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial Project Team (2003) Dietary fibre and colorectal adenoma in a colorectal cancer early detection programme. Lancet 361(9368):1491–1495

    Google Scholar 

  150. Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17(2):259–275

    Google Scholar 

  151. Clarke TC, Black LI, Stussman BJ, Barnes PM, Nahin RL (2015) Trends in the use of complementary health approaches among adults: United States, 2002-2012. Natl Health Stat Report 79:1–16

    Google Scholar 

  152. Sanders ME (2008) Probiotics: definition, sources, selection, and uses. Clin Infect Dis 46(Suppl 2):S58–S61 discussion S144-51

    Google Scholar 

  153. Parker EA, Roy T, D'Adamo CR, Wieland LS (2018) Probiotics and gastrointestinal conditions: an overview of evidence from the Cochrane collaboration. Nutrition 45:125–134.e11

    Google Scholar 

Download references

Acknowledgments

A part of the work presented in this chapter has been supported by grants to Dr. Majumdar by NIH/NCI (1R21CA175916), the Department of Veteran Affairs (I101BX001927), and the Metropolitan Detroit Research and Education Fund (MDREF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Veterans Affairs Medical Center, Research Service, Detroit, MI, USA

    Lulu Farhana & Adhip P. N. Majumdar

  2. Department of Internal Medicine, Wayne State University, Detroit, MI, USA

    Lulu Farhana & Adhip P. N. Majumdar

  3. Elizabeth City State University, Elizabeth City, NC, USA

    Hirendra Nath Banerjee

  4. Epidemiology and Genomics Research Program, National Cancer Institute, Rockville, MD, USA

    Mukesh Verma

  5. Karmanos Cancer Institute, Wayne State University-School of Medicine, Detroit, MI, USA

    Adhip P. N. Majumdar

Authors
  1. Lulu Farhana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hirendra Nath Banerjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mukesh Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adhip P. N. Majumdar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adhip P. N. Majumdar .

Editor information

Editors and Affiliations

  1. Kelly Government Solutions, Bethesda, MD, USA

    Ramona G. Dumitrescu

  2. Division of Cancer Control and Population Sciences, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA

    Mukesh Verma

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Farhana, L., Banerjee, H.N., Verma, M., Majumdar, A.P.N. (2018). Role of Microbiome in Carcinogenesis Process and Epigenetic Regulation of Colorectal Cancer. In: Dumitrescu, R., Verma, M. (eds) Cancer Epigenetics for Precision Medicine . Methods in Molecular Biology, vol 1856. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-8751-1_3

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-8751-1_3

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-8750-4

  • Online ISBN: 978-1-4939-8751-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation