Enterolignan-producing phenotypes are associated with increased gut microbial diversity and altered composition in premenopausal women in the United States

Cancer Epidemiology Biomarkers and Prevention

Volumn 24, Issue 3, 2015, Pages 546-554

  Hullar, Meredith A J ^a   Lancaster, Samuel M ^a,b   Li, Fei ^b   Tseng, Elizabeth ^b   Beer, Karlyn ^b   Atkinson, Charlotte ^c   Wähälä, Kristiina ^d   Copeland, Wade K ^a   Randolph, Timothy W ^a   Newton, Katherine M ^e   Lampe, Johanna W ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d UNIVERSITY OF HELSINKI   (Finland)

^e GROUP HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENTERODIOL; ENTEROLACTONE; ENTEROLIGNAN; LIGNAN; RNA 16S; UNCLASSIFIED DRUG; 2,3-BIS(3'-HYDROXYBENZYL)BUTANE-1,4-DIOL; 2,3-BIS(3'-HYDROXYBENZYL)BUTYROLACTONE; GAMMA BUTYROLACTONE;

ADULT; ARTICLE; BREAST CANCER; CANCER PREVENTION; CANCER RISK; COLON CANCER; DIETARY INTAKE; FECES ANALYSIS; FEMALE; GENE SEQUENCE; HUMAN; INTESTINE FLORA; MAJOR CLINICAL STUDY; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; MIDDLE AGED; MULTIVARIATE ANALYSIS; NONHUMAN; OBSERVATIONAL STUDY; PLANT; PREMENOPAUSE; PRIORITY JOURNAL; STREPTOBACILLUS; UNITED STATES; UNIVARIATE ANALYSIS; URINARY EXCRETION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; GASTROINTESTINAL TRACT; MEDICAL RECORD; METABOLISM; MICROBIOLOGY; MICROFLORA; PHENOTYPE;

4-BUTYROLACTONE; ADULT; DIET RECORDS; FEMALE; GASTROINTESTINAL TRACT; HUMANS; LIGNANS; MICROBIOTA; MIDDLE AGED; PHENOTYPE; PREMENOPAUSE; UNITED STATES;

EID: 84927759887     PISSN: 10559965     EISSN: None     Source Type: Journal    
DOI: 10.1158/1055-9965.EPI-14-0262     Document Type: Article

References (95)

1. World Cancer Research Fund. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington, DC: American Institute for Cancer Research; 2007.
2. Buck K, Zaineddin AK, Vrieling A, Heinz J, Linseisen J, Flesch-Janys D, et al. Estimated enterolignans, lignan-rich foods, and fibre in relation to survival after postmenopausal breast cancer. Br J Cancer 2011;105:1151-7.
3. Buck K, Zaineddin AK, Vrieling A, Linseisen J, Chang-Claude J. Metaanalyses of lignans and enterolignans in relation to breast cancer risk. Am J Clin Nutr 2010;92:141-53.
4. Guglielmini P, Rubagotti A, Boccardo F. Serum enterolactone levels and mortality outcome in women with early breast cancer: a retrospective cohort study. Breast Cancer Res Treat 2012;132:661-8.
5. McCann SE, Hootman KC, Weaver AM, Thompson LU, Morrison C, Hwang H, et al. Dietary intakes of total and specific lignans are associated with clinical breast tumor characteristics. J Nutr 2012;142:91-8.
6. Toure A, Xueming X. Flaxseed lignans: source, biosynthesis, metabolism, antioxidant activity, bio-active components, and health benefits. Compr Rev Food Sci Food Saf 2010;9:261-9.
7. Velentzis LS, Cantwell MM, Cardwell C, Keshtgar MR, Leathem AJ, Woodside JV. Lignans and breast cancer risk in pre- and postmenopausal women: meta-analyses of observational studies. Br J Cancer 2009;100:1492-8.
8. Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey A, Harper P. Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr 2006;136:3046-53.
9. Kuijsten A, Arts IC, Hollman PC, van't Veer P, Kampman E. Plasma enterolignans are associated with lower colorectal adenoma risk. Cancer Epidemiol Biomarkers Prev 2006;15:1132-6.
10. Webb AL, McCullough ML. Dietary lignans: potential role in cancer prevention. Nutr Cancer 2005;51:117-31.
11. Frankenfeld CL. Relationship of obesity and high urinary enterolignan concentrations in 6806 children and adults: analysis of National Health and Nutrition Examination Survey data. Eur J Clin Nutr 2013;67:887-9.
12. Clavel T, Henderson G, Engst W, Dore J, Blaut M. Phylogeny of human intestinal bacteria that activate the dietary lignan secoisolariciresinol diglucoside. FEMS Microbiol Ecol 2006;55:471-8.
13. Kuijsten A, Arts IC, Vree TB, Hollman PC. Pharmacokinetics of enterolignans in healthy men and women consuming a single dose of secoisolariciresinol diglucoside. J Nutr 2005;135:795-801.
14. Heinonen S, Nurmi T, Liukkonen K, Poutanen K, Wahala K, Deyama T, et al. In vitro metabolism of plant lignans: new precursors of mammalian lignans enterolactone and enterodiol. J Agric Food Chem 2001;49:3178-86.
15. Jin JS, Zhao YF, Nakamura N, Akao T, Kakiuchi N, Min BS, et al. Enantioselective dehydroxylation of enterodiol and enterolactone precursors by human intestinal bacteria. Biol Pharm Bull 2007;30:2113-9.
16. Clavel T, Lippman R, Gavini F, Dore J, Blaut M. Clostridium saccharogumia sp. nov. and Lactonifactor longoviformis gen. nov., sp. nov. two novel human faecal bacteria involved in the conversion of the dietary phytoestrogen secoisolariciresinol diglucoside. Syst Appl Microbiol 2007;30:16-26.
17. Jin JS, Hattori M. Human intestinal bacterium, Strain END-2, is responsible for demethylation as well as lactonization during plant lignan metabolism. Biol Pharm Bull 2010;33:1443-7.
18. Atkinson C, Newton KM, Bowles EJ, Yong M, Lampe JW. Demographic, anthropometric, and lifestyle factors and dietary intakes in relation to daidzein-metabolizing phenotypes among premenopausal women in the United States. Am J Clin Nutr 2008;87:679-87.
19. Lampe JW, Martini MC, Kurzer MS, Adlercreutz H, Slavin JL. Urinary lignan and isoflavonoid excretion in premenopausal women consuming flaxseed powder. Am J Clin Nutr 1994;60:122-8.
20. Li F, Hullar MA, Schwarz Y, Lampe JW. Human gut bacterial communities are altered by addition of cruciferous vegetables to a controlled fruit- and vegetable-free diet. J Nutr 2009;139:1685-91.
21. Atkinson C, Lampe JW, Scholes D, Chen C, Wahala K, Schwartz SM. Lignan and isoflavone excretion in relation to uterine fibroids: a case-control study of young to middle-aged women in the United States. Am J Clin Nutr 2006;84:587-93.
22. Li F, Hullar MA, Lampe JW. Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J Microbiol Methods 2007;68:303-11.
23. Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA. Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) formicrobiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis 2008;5:459-72.
24. Callaway TR, Dowd SE, Wolcott RD, Sun Y, McReynolds JL, Edrington TS, et al. Evaluation of the bacterial diversity in cecal contents of laying hens fed various molting diets by using bacterial tag-encoded FLX amplicon pyrosequencing. Poult Sci 2009;88:298-302.
25. Wickham ME, Lupp C, Vazquez A, Mascarenhas M, Coburn B, Coombes BK, et al. Citrobacterium rodentium virulence in mice associates with bacterial load and the type III effector NleE. Microbes Infect 2007;9:400-7.
26. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterol 2010;139:1844-54.
27. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007;73:5261-7.
28. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537-41.
29. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ. Removing noise from pyrosequenced amplicons. BMC Bioinformatics 2011;12:38-56.
30. Schloss PD. Secondary structure improves OTU assignments of 16S rRNA gene sequences. ISME J 2013;7:457-60.
31. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007;35:7188-96.
32. Huse SM, Welch DM, Morrison HG, Sogin ML. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 2010;12:1889-98.
33. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27: 2194-200.
34. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 2011;21:494-504.
35. Kim M, Morrison M, Yu Z. Evaluation of different partial 16S rRNA gene sequence regions for phylogenetic analysis of microbiomes. J Microbiol Methods 2011;84:81-7.
36. Magurran A. Measuring biological diversity. Oxford, UK: Blackwell; 2004.
37. Yue JC, Clayton MK. A similarity measure based on species proportions. Commun Stat-Theor M 2005;34:2123-31.
38. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005;71:8228-35.
39. Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 2007; 73:1576-85.
40. Sheneman L, Evans J, Foster JA. Clearcut: a fast implementation of relaxed neighbor joining. Bioinformatics 2006;22:2823-4.
41. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A 2011;108 Suppl 1:4586-91.
42. Kuczynski J, Lauber CL, Walters WA, Parfrey LW, Clemente JC, Gevers D, et al. Experimental and analytical tools for studying the human microbiome. Nat Rev Genet 2012;13:47-58.
43. Navas-Molina JA, Peralta-Sanchez JM, Gonzalez A, McMurdie PJ, Vazquez-Baeza Y, Xu ZJ, et al. Advancing our understanding of the human micro-biome using QIIME. Methods Enzymol 2013;531:371-444.
44. Endres DM, Schindelin JE. A new metric for probability distributions. IEEE Trans Info Theory 2003;49:1858-60.
45. Kruskal JB. Nonmetric multidimensional scaling: a numerical method. Psycometrika 1964;29:115-29.
46. McCune B, Grace JB. Analysis of ecological communities. First edition. Glendenen Beach, OR: MjM Software; 2002.
47. Calinski T, Harabasz J. A dendrite method for cluster analysis. Comm Stat 1974;3:1-27.
48. Brumback BA, Ruppert D, Wand MP. Variable selection and function estimation in additive nonparametric regression using a data-based prior-comment. J Am Stat Assoc 1999;94:794-7.
49. Dixon P. VEGAN, a package of R functions for community ecology. J Vegetation Sci 2003;14:927-30.
50. Letunic I, Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 2011;39: W475-8.
51. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature 2011;473: 174-80.
52. Carlier JP, K'Ouas G, Han XY. Moryella indoligenes gen. nov., sp. nov., an anaerobic bacterium isolated from clinical specimens. Int J Syst Evol Microbiol 2007;57:725-9.
53. Chen S, Dong X. Acetanaerobacterium elongatum gen. nov., sp. nov., from paper mill waste water. Int J Syst Evol Microbiol 2004;54: 2257-62.
54. Falsen E, Collins MD, Welinder-Olsson C, Song Y, Finegold SM, Lawson PA. Fastidiosipila sanguinis gen. nov., sp. nov., a new Gram-positive, coccus-shaped organism from human blood. Int J Syst Evol Microbiol 2005;55:853-8.
55. Larcia LH, Estacio RC, Dalmacio LM. Bacterial diversity in Philippine fermented mustard (Burongmustasa)asrevealedby16SrRNA gene analysis. Beneficial Microbes 2011;2:263-71.
56. Elliott SP. Rat bite fever and Streptobacillus moniliformis. Clin Microbiol Rev 2007;20:13-22.
57. Eichholzer M, Richard A, Nicastro HL, Platz EA, Linseisen J, Rohrmann S. Urinary lignans and inflammatory markers in the US National Health and Nutrition Examination Survey (NHANES) 1999-2004 and 2005-2008. Cancer Causes Control 2014;25:395-403.
58. Sun Q, Wedick NM, Pan A, Townsend MK, Cassidy A, Franke AA, et al. Gut microbiota metabolites of dietary lignans and risk of type 2 diabetes: a prospective investigation in two cohorts of U.S. women. Diabetes Care 2014;37:1287-95.
59. Goodman MT, Shvetsov YB, Wilkens LR, Franke AA, Le Marchand L, Kakazu KK, et al. Urinary phytoestrogen excretion and postmenopausal breast cancer risk: the multiethnic cohort study. Cancer Prev Res 2009;2:887-94.
60. Clavel T, Henderson G, Alpert CA, Philippe C, Rigottier-Gois L, Dore J, et al. Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Appl Environ Microbiol 2005;71:6077-85.
61. Clavel T, Dore J, Blaut M. Bioavailability of lignans in human subjects. Nutr Res Rev 2006;19:187-96.
62. Lampe JW, Atkinson C, Hullar MA. Assessing exposure to lignans and their metabolites in humans. J AOAC Int 2006;89:1174-81.
63. Eeckhaut E, Struijs K, Possemiers S, Vincken JP, Keukeleire DD, Verstraete W. Metabolism of the lignan macromolecule into enterolignans in the gastrointestinal lumen as determined in the simulator of the human intestinal microbial ecosystem. J Agric Food Chem 2008; 56:4806-12.
64. Wang L, Meselhy MR, LI Y, Qin G, Hattori M. Human intestinal bacteria capable of transforming secoisolariciresinol diglucoside to mammalian lignans, enterodiol and enterolactone. Chem Pharmol Bull 2000; 48:1606-10.
65. Clavel T, Borrmann D, Braune A, Dore J, Blaut M. Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe 2006;12:140-7.
66. Jin J-S, Kakiuchi N, Hattori M. Enantioselective oxidation of enterodiol to enterolactone by human intestinal bacteria. Biol Pharm Bull 2007;30: 2204-6.
67. Jin JS, Hattori M. Further studies on a human intestinal Bacterium Ruminococcus sp END-1 for transformation of plant lignans to mammalian lignans. J Agric Food Chem 2009;57:7537-42.
68. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 2010;107:14691-6.
69. Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N, Le Chatelier E, et al. Dietary intervention impact on gut microbial gene richness. Nature 2013;500:585-8.
70. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, et al. Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008;197: 435-8.
71. Adlercreutz H, Fotsis T, Bannwart C, Wähälä K, Mäkelä T, Brunow G, et al. Determination of urinary lignans and phytoestrogen metabolites, potential antiestrogens and anticarcinogens, in urine of women on various habitual diets. J Steroid Biochem 1986;25:791-7.
72. Horner NK, Kristal AR, Prunty J, Skor HE, Potter JD, Lampe JW. Dietary determinants of plasma enterolactone. Cancer EpidemiolBiomarkers Prev 2002;11:121-6.
73. Lampe JW, Gustafson DR, Hutchins AM, Martini MC, Li S, Wähälä K, et al. Urinary isoflavonoid and lignan excretion on a Western diet: relation to soy, vegetable, and fruit intake. Cancer Epidemiol Biomarkers Prev 1999;8:699-707.
74. Lampe JW. Isoflavonoid and lignan phytoestrogens as dietary biomarkers. J Nutr 2003;133:956S-64S.
75. Aura A-M, Myllymäki O, Bailey M, Penalvo JL, Adlercreutz H, Poutanen K. Interrelationships between carbohydrate type, phenolic acids and initial pH on invitro conversion of enterolactone from rye lignans. In: Salovaara H, Gates F, Tenkanen M, editors. Dietary fibre: components and functions. Wageningen, The Netherlands: Wageningen Academic Publishers; 2007. p. 235-45.
76. Hullar MA, Lampe JW. The gut microbiome and obesity. Nestle Nutr Inst Workshop Ser 2012;73:67-79.
77. Frankenfeld CL, Lampe JW, Shannon J, Gao DL, Li W, Ray RM, et al. Fruit and vegetable intakes in relation to plasma nutrient concentrations in women in Shanghai, China. Public Health Nutr 2012;15:167-75.
78. Kilkkinen A, Valsta LM, Virtamo J, Stumpf K, Adlercreutz H, Pietinen P. Intake of lignans is associated with serum enterolactone concentration in Finnish men and women. J Nutr 2003;133:1830-3.
79. Roncaglia L, Amaretti A, Raimondi S, Leonardi A, Rossi M. Role of bifidobacteria in the activation of the lignan secoisolariciresinol diglucoside. Appl Microbiol Biotechnol 2011;92:159-68.
80. Yoder S, Lancaster S, Hullar MAJ, Lampe JW. Gut microbial metabolism of plant lignans: influence on human health. In: Del Rio D, Tuohy K, editors. Diet-microbe interactions in the gut: Oxford, UK: Elsevier; 2014.
81. Lee GH, Kumar S, Lee JH, Chang DH, Kim DS, Choi SH, et al. Genome sequence of Oscillibacter ruminantium strain GH1, isolated from rumen of Korean native cattle. J Bacteriol 2012;194:6362.
82. Lee GH, Rhee MS, Chang DH, Lee J, Kim S, Yoon MH, et al. Oscillibacter ruminantium sp. nov., isolated from the rumen of Korean native cattle. Int J Syst Evol Microbiol 2013;63:1942-6.
83. Turnbaugh PJ, Gordon JI. The core gut microbiome, energy balance and obesity. J Physiol 2009;587:4153-8.
84. O'Keefe SJ. Nutrition and colonic health: the critical role of the microbiota. Curr Opin Gastroenterol 2008;24:51-8.
85. Wu GD, Bewtra M, Hoffmann C, Chen YY, Keilbaugh SA, Bittinger K, et al. Controlled feeding experiments demonstrate the impact of diet on the composition of the human gut microbiome. Gastroenterology 2011;140: S47-S.
86. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334:105-8.
87. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59-65.
88. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature 2009;457: 480-4.
89. Claesson MJ, O'Toole PW. Evaluating the latest high-throughput molecular techniques for the exploration of microbial gut communities. Gut Microbes 2010;1:277-8.
90. Koren O, Spor A, Felin J, Fak F, Stombaugh J, Tremaroli V, et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A 2011;108 Suppl 1:4592-8.
91. Huse SM, Ye Y, Zhou Y, Fodor AA. A core human microbiome as viewed through 16S rRNA sequence clusters. PLoS ONE 2012;7:e34242.
92. Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature 2012;486:207-14.
93. Rajilic-Stojanovic M, Heilig HG, Tims S, Zoetendal EG, de Vos WM. Longterm monitoring of the human intestinal microbiota composition. Environ Microbiol 2012;15:1146-59.
94. Adlercreutz H, Honjo H, Higashi A, Fotsis T, Hämäläinen E, Hasegawa T, et al. Urinary excretion of lignans and isoflavonoid phytoestrogens in Japanese men and women consuming a traditional Japanese diet. Am J Clin Nutr 1991;54:1093-100.
95. Milder IEJ. Lignan intake in the Netherlands and its relation with mortality. Helsinki, Finland: Wageningen Universiteit; 2007.