Comparison of human gut microbiota in control subjects and patients with colorectal carcinoma in adenoma: Terminal restriction fragment length polymorphism and next-generation sequencing analyses

Oncology Reports

Volumn 35, Issue 1, 2016, Pages 325-333

  Kasai, Chika ^a   Sugimoto, Kazushi ^b   Moritani, Isao ^a   Tanaka, Junichiro ^a   Oya, Yumi ^a   Inoue, Hidekazu ^a   Tameda, Masahiko ^b   Shiraki, Katsuya ^b   Ito, Masaaki ^c   Takei, Yoshiyuki ^b   Takase, Kojiro ^a  

^a Mie Pref General Medical Center   (Japan)

^b MIE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Department of Cardiology and Nephrology ^*  (Japan)

Author keywords

Colorectal cancer; Microbiota; Next generation sequencing; Terminal restriction fragment length polymorphism

Indexed keywords

ACTINOMYCES; ACTINOMYCES ODONTOLYTICUS; ADENOMA; ADULT; AGED; ARTICLE; ATOPOBIUM; BACTERIUM; BACTEROIDES; BACTEROIDES FRAGILES; BIFIDOBACTERIUM; CLINICAL ARTICLE; CLOSTRIDIUM; CLOSTRIDIUM NEXILE; COLON ADENOMA; COLONOSCOPY; COLORECTAL CANCER; COLORECTAL CARCINOMA; COMPARATIVE STUDY; CONTROLLED STUDY; DNA EXTRACTION; EUBACTERIUM COPROSTANOLIGENS; FECES ANALYSIS; FEMALE; FUSOBACTERIUM; FUSOBACTERIUM VARIUM; GENUS; HAEMOPHILUS; HAEMOPHILUS PARAINFLUENZAE; HUMAN; INTESTINE FLORA; JAPAN; JAPANESE (PEOPLE); LACTOBACILLALES; MALE; MICROBIAL COMMUNITY; MICROBIAL POPULATION DYNAMICS; NEXT GENERATION SEQUENCING; PREVOTELLA; PREVOTELLA STERCOREA; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SLACKIA; STREPTOCOCCUS GORDONII; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISM; VEILLONELLA DISPAR; CLASSIFICATION; COLORECTAL TUMOR; DNA SEQUENCE; FECES; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MIDDLE AGED; NORMAL HUMAN; PROCEDURES;

RIBOSOME DNA; RNA 16S;

ADENOMA; ADULT; BACTERIA; COLORECTAL NEOPLASMS; DNA, RIBOSOMAL; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HEALTHY VOLUNTEERS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; JAPAN; MALE; MIDDLE AGED; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84954065775     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2015.4398     Document Type: Article

References (57)

1. Savage DC: Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31: 107-133, 1977.
2. Mitsuoka T and Hayakawa K: The fecal flora in man. I. Composition of the fecal flora of various age groups. Zentralbl Bakteriol Orig A 223: 333-342, 1973 (In German).
3. Zoetendal EG, Akkermans AD and De Vos WM: Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64: 3854-3859, 1998.
4. Rajilić-Stojanović M, Heilig HG, Tims S, Zoetendal EG and de Vos WM: Long-term monitoring of the human intestinal microbiota composition. Environ Microbiol 15: 1146-1159, 2013.
5. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N and Pace NR: Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104: 13780-13785, 2007.
6. Martinez C, Antolin M, Santos J, Torrejon A, Casellas F, Borruel N, Guarner F and Malagelada JR: Unstable composition of the fecal microbiota in ulcerative colitis during clinical remission. Am J Gastroenterol 103: 643-648, 2008.
7. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, et al: Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 13: R79, 2012.
8. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER and Gordon JI: An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031, 2006.
9. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P and Flint HJ: Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes 32: 1720-1724, 2008.
10. Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C and Hardt PD: Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 18: 190-195, 2010.
11. Irrazábal T, Belcheva A, Girardin SE, Martin A and Philpott DJ: The multifaceted role of the intestinal microbiota in colon cancer. Mol Cell 54: 309-320, 2014.
12. Schwabe RF and Jobin C: The microbiome and cancer. Nat Rev Cancer 13: 800-812, 2013.
13. Ernst M, Najdovska M, Grail D, Lundgren-May T, Buchert M, Tye H, Matthews VB, Armes J, Bhathal PS, Hughes NR, et al: STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice. J Clin Invest 118: 1727-1738, 2008.
14. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, et al: A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15: 1016-1022, 2009.
15. Winter SE, Lopez CA and Bäumler AJ: The dynamics of gut-associated microbial communities during inflammation. EMBO Rep 14: 319-327, 2013.
16. Kuper H, Adami HO and Trichopoulos D: Infections as a major preventable cause of human cancer. J Intern Med 248: 171-183, 2000.
17. Mantovani A, Garlanda C and Allavena P: Molecular pathways and targets in cancer-related inflammation. Ann Med 42: 161-170, 2010.
18. Lundberg JO, Weitzberg E, Cole JA and Benjamin N: Nitrate, bacteria and human health. Nat Rev Microbiol 2: 593-602, 2004.
19. -/- mice is independent of nitric oxide-induced DNA mutations. PLoS One 8: e65204, 2013.
20. Cooke MS, Evans MD, Dizdaroglu M and Lunec J: Oxidative DNA damage: Mechanisms, mutation, and disease. FASEB J 17: 1195-1214, 2003.
21. Evans MD, Dizdaroglu M and Cooke MS: Oxidative DNA damage and disease: Induction, repair and significance. Mutat Res 567: 1-61, 2004.
22. Christl SU, Scheppach W and Kasper H: Hydrogen metabolism in the large intestine - physiology and clinical implications. Z Gastroenterol 33: 408-413, 1995 (In German).
23. Deplancke B, Finster K, Graham WV, Collier CT, Thurmond JE and Gaskins HR: Gastrointestinal and microbial responses to sulfate-supplemented drinking water in mice. Exp Biol Med (Maywood) 228: 424-433, 2003.
24. Hughes R, Cross AJ, Pollock JR and Bingham S: Dose-dependent effect of dietary meat on endogenous colonic N-nitrosation. Carcinogenesis 22: 199-202, 2001.
25. Norat T and Riboli E: Meat consumption and colorectal cancer: A review of epidemiologic evidence. Nutr Rev 59: 37-47, 2001.
26. Hague A, Manning AM, Hanlon KA, Huschtscha LI, Hart D and Paraskeva C: Sodium butyrate induces apoptosis in human colonic tumour cell lines in a p53-independent pathway: Implications for the possible role of dietary fibre in the prevention of large-bowel cancer. Int J Cancer 55: 498-505, 1993.
27. Heerdt BG, Houston MA and Augenlicht LH: Potentiation by specific short-chain fatty acids of differentiation and apoptosis in human colonic carcinoma cell lines. Cancer Res 54: 3288-3293, 1994.
28. Nagashima K, Mochizuki J, Hisada T, Suzuki S and Shimomura K: Phylogenetic analysis of 16S ribosomal RNA gene sequences from human fecal microbiota and improved utility of terminal restriction fragment length polymorphism profiling. Biosci Microflora 25: 99-107, 2006.
29. Nagashima K, Hisada T, Sato M and Mochizuki J: Application of new primer-enzyme combinations to terminal restriction fragment length polymorphism profiling of bacterial populations in human feces. Appl Environ Microbiol 69: 1251-1262, 2003.
30. Takahashi S, Tomita J, Nishioka K, Hisada T and Nishijima M: Development of a prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing. PLoS One 9: e105592, 2014.
31. Muyzer G, de Waal EC and Uitterlinden AG: Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700, 1993.
32. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N and Knight R: Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108 (Suppl 1): 4516-4522, 2011.
33. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, Barnes R, Watson P, Allen-Vercoe E, Moore RA, et al: Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22: 299-306, 2012.
34. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, et al: Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 22: 292-298, 2012.
35. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL, et al: Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14: 207-215, 2013.
36. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G and Han YW: Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 14: 195-206, 2013.
37. Matthies A, Blaut M and Braune A: Isolation of a human intestinal bacterium capable of daidzein and genistein conversion. Appl Environ Microbiol 75: 1740-1744, 2009.
38. Setchell KD and Clerici C: Equol: History, chemistry, and formation. J Nutr 140: 1355S-1362S, 2010.
39. Watanabe S, Yamaguchi M, Sobue T, Takahashi T, Miura T, Arai Y, Mazur W, Wähälä K and Adlercreutz H: Pharmacokinetics of soybean isoflavones in plasma, urine and feces of men after ingestion of 60 g baked soybean powder (kinako). J Nutr 128: 1710-1715, 1998.
40. Setchell KD and Cole SJ: Method of defining equol-producer status and its frequency among vegetarians. J Nutr 136: 2188-2193, 2006.
41. Setchell KD, Zhao X, Shoaf SE and Ragland K: The pharmacokinetics of S-(-)equol administered as SE5-OH tablets to healthy postmenopausal women. J Nutr 139: 2037-2043, 2009.
42. Song KB, Atkinson C, Frankenfeld CL, Jokela T, Wähälä K, Thomas WK and Lampe JW: Prevalence of daidzein-metabolizing phenotypes differs between Caucasian and Korean American women and girls. J Nutr 136: 1347-1351, 2006.
43. Setchell KD: Phytoestrogens: The biochemistry, physiology, and implications for human health of soy isoflavones. Am J Clin Nutr 68 (Suppl 6): 1333S-1346S, 1998.
44. Cai Y, Guo K, Chen C, Wang P, Zhang B, Zhou Q, Mei F and Su Y: Soya isoflavone consumption in relation to carotid intima-media thickness in Chinese equol excretors aged 40-65 years. Br J Nutr 108: 1698-1704, 2012.
45. Lund TD, Munson DJ, Haldy ME, Setchell KD, Lephart ED and Handa RJ: Equol is a novel anti-androgen that inhibits prostate growth and hormone feedback. Biol Reprod 70: 1188-1195, 2004.
46. Brown NM, Belles CA, Lindley SL, Zimmer-Nechemias L, Witte DP, Kim MO and Setchell KD: Mammary gland differentiation by ea rly life exposure to enantiomers of the soy isoflavone metabolite equol. Food Chem Toxicol 48: 3042-3050, 2010.
47. Uematsu H, Sato N, Hossain MZ, Ikeda T and Hoshino E: Degradation of arginine and other amino acids by butyrate-producing asaccharolytic anaerobic Gram-positive rods in periodontal pockets. Arch Oral Biol 48: 423-429, 2003.
48. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C and Flint HJ: Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66: 1654-1661, 2000.
49. Wong JM, de Souza R, Kendall CW, Emam A and Jenkins DJ: Colonic health: Fermentation and short chain fatty acids. J Clin Gastroenterol 40: 235-243, 2006.
50. Dronamraju SS, Coxhead JM, Kelly SB and Mathers JC: Differential antineoplastic effects of butyrate in cells with and without a functioning DNA mismatch repair. Nutr Cancer 62: 105-115, 2010.
51. Ooi CC, Good NM, Williams DB, Lewanowitsch T, Cosgrove LJ, Lockett TJ and Head RJ: Efficacy of butyrate analogues in HT-29 cancer cells. Clin Exp Pharmacol Physiol 37: 482-489, 2010.
52. Roy MJ, Dionne S, Marx G, Qureshi I, Sarma D, Levy E and Seidman EG: In vitro studies on the inhibition of colon cancer by butyrate and carnitine. Nutrition 25: 1193-1201, 2009.
53. Freier TA, Beitz DC, Li L and Hartman PA: Characterization of Eubacterium coprostanoligenes sp. nov., a cholesterol-reducing anaerobe. Int J Syst Bacteriol 44: 137-142, 1994.
54. Stadler J, Stern HS, Yeung KS, McGuire V, Furrer R, Marcon N and Bruce WR: Effect of high fat consumption on cell proliferation activity of colorectal mucosa and on soluble faecal bile acids. Gut 29: 1326-1331, 1988.
55. Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, Gaskins HR and O'Keefe SJ: Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr 98: 111-120, 2013.
56. Mantovani A, Allavena P, Sica A and Balkwill F: Cancer-related inflammation. Nature 454: 436-444, 2008.
57. Toprak NU, Yagci A, Gulluoglu BM, Akin ML, Demirkalem P, Celenk T and Soyletir G: A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin microbiol Infect 12: 782-786, 2006.