The microbiota of breast tissue and its association with breast cancer

Applied and Environmental Microbiology

Volumn 82, Issue 16, 2016, Pages 5039-5048

  Urbaniak, Camilla ^a,b   Gloor, Gregory B ^b   Brackstone, Muriel ^c   Scott, Leslie ^c   Tangney, Mark ^d   Reida, Gregor ^a,b  

^a LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c LONDON REGIONAL CANCER PROGRAM   (Canada)

^d UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; DISEASES; ESCHERICHIA COLI; LANTHANUM COMPOUNDS; RNA;

BREAST CANCER; BREAST TISSUES; DISEASE DEVELOPMENT; ENTEROBACTERIACEAE; ENVIRONMENTAL FACTORS; HEALTHY CONTROLS; RELATIVE ABUNDANCE; STAPHYLOCOCCUS EPIDERMIDIS;

TISSUE;

BACTERIUM; CANCER; CELLS AND CELL COMPONENTS; ENVIRONMENTAL FACTOR; GENETIC ANALYSIS; HEALTH RISK; MICROBIAL COMMUNITY; TUMOR; WOMENS HEALTH;

UNITED STATES;

ENTEROBACTERIACEAE; ESCHERICHIA COLI; STAPHYLOCOCCUS; STAPHYLOCOCCUS EPIDERMIDIS;

RNA 16S;

ADULT; AGED; BACTERIUM; BREAST; BREAST TUMOR; CLASSIFICATION; DNA SEQUENCE; FEMALE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; MIDDLE AGED; ONTARIO; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; BACTERIA; BREAST; BREAST NEOPLASMS; FEMALE; HUMANS; MICROBIOTA; MIDDLE AGED; ONTARIO; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; YOUNG ADULT;

EID: 84982133117     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01235-16     Document Type: Article

References (52)

1. Darveau RP. 2010. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8:481-490. http://dx.doi.org/10.1038 /nrmicro2337.
2. Ximénez-Fyvie LA, Haffajee AD, Socransky SS. 2000. Comparison of the microbiota of supra-and subgingival plaque in health and periodontitis. J Clin Periodontol 27:648-657. http://dx.doi.org/10.1034/j.1600-051x .2000.027009648.x.
3. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. 2007. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104:13780-13785. http://dx.doi.org/10.1073/pnas.0706625104.
4. Gao Z, Tseng C, Strober BE, Pei Z, Blaser MJ. 2008. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS One 3:e2719. http://dx.doi.org/10.1371/journal.pone.0002719.
5. Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, Davies J, Ervine A, Poulter L, Pachter L, Moffatt MF, Cookson WOC. 2010. Disordered microbial communities in asthmatic airways. PLoS One 5:e8578. http://dx.doi.org/10.1371/journal.pone.0008578.
6. Larsen N, Vogensen FK, van den Berg FWJ, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M. 2010. Gut microbiota in human adults with type 2 diabetes differs from nondiabetic adults. PLoS One 5:e9085. http://dx.doi.org/10.1371/journal.pone .0009085.
7. Hummelen R, Fernandes AD, Macklaim JM, Dickson RJ, Changalucha J, Gloor GB, Reid G. 2010. Deep sequencing of the vaginal microbiota of women with HIV. PLoS One 5:e12078. http://dx.doi.org/10.1371/journal .pone.0012078.
8. Mira-Pascual L, Cabrera-Rubio R, Ocon S, Costales P, Parra A, Suarez A, Moris F, Rodrigo L, Mira A, Collado MC. 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. http://dx.doi.org/10.1007/s00535-014-0963-x.
9. Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH. 2007. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 131:33-45. http://dx.doi.org/10.1016/j.cell.2007.08.017.
10. Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, Schloss PD. 2013. The gut microbiome modulates colon tumorigenesis. mBio 4:e00692-13. http://dx.doi.org/10.1128/mBio.00692-13.
11. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. 2009. A core gut microbiome in obese and lean twins. Nature 457:480-484. http://dx.doi.org/10.1038 /nature07540.
12. Le GM, Gomez SL, Clarke CA, Glaser SL, West DW. 2002. Cancer incidence patterns among Vietnamese in the United States and Ha Noi, Vietnam. Int J Cancer 102:412-417. http://dx.doi.org/10.1002/ijc.10725.
13. Shimizu H, Ross RK, Bernstein L, Yatani R, Henderson BE, Mack TM. 1991. Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County. Br J Cancer 63:963-966. http://dx.doi .org/10.1038/bjc.1991.210.
14. Urbaniak C, Cummins J, Brackstone M, Macklaim JM, Gloor GB, Baban CK, Scott L, O'Hanlon DM, Burton JP, Francis KP, Tangney M, Reid G. 2014. Microbiota of human breast tissue. Appl Environ Microbiol 80:3007-3014. http://dx.doi.org/10.1128/AEM.00242-14.
15. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460 -2461. http://dx.doi.org/10.1093 /bioinformatics/btq461.
16. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188-7196. http://dx.doi.org/10.1093/nar/gkm864.
17. Lozupone C, Knight R. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228-8235. http://dx.doi.org/10.1128/AEM.71.12.8228-8235.2005.
18. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
19. Price MN, Dehal PS, Arkin AP. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641-1650. http://dx.doi.org/10.1093/molbev/msp077.
20. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. http://dx.doi.org/10.1186/1471-2105-5-113.
21. Fernandes AD, Reid JN, Macklaim JM, McMurrough TA, Edgell DR, Gloor GB. 2014. Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome 2:15. http://dx.doi.org/10.1186/2049-2618-2-15.
22. Aitchison J. 1986. The statistical analysis of compositional data. Chapman and Hall, London, England.
23. Zhao N, Chen J, Carroll IM, Ringel-Kulka T, Epstein MP, Zhou H, Zhou JJ, Ringel Y, Li H, Wu MC. 2015. Testing in microbiome-profiling studies with Mirkat, the microbiome regression-based kernel association test. Am J Hum Genet 96:797-807. http://dx.doi.org/10.1016/j.ajhg.2015 .04.003.
24. Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, Collman RG, Bushman FD, Li H. 2012. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28:2106 -2113. http://dx.doi.org/10.1093 /bioinformatics/bts342.
25. Lehouritis P, Cummins J, Stanton M, Murphy CT, McCarthy FO, Reid G, Urbaniak C, Byrne WL, Tangney M. 2015. Local bacteria affect the efficacy of chemotherapeutic drugs. Sci Rep 5:14554. http://dx.doi.org/10 .1038/srep14554.
26. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan T-J, Campbell BJ, Abujamel T, Dogan B, Rogers AB, Rhodes JM, Stintzi A, Simpson KW, Hansen JJ, Keku TO, Fodor AA, Jobin C. 2012. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338:120-123. http://dx.doi.org/10.1126/science.1224820.
27. Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille-Michaud A, Pezet D, Bonnet R. 2013. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One 8:e56964. http://dx.doi.org/10.1371/journal.pone.0056964.
28. Nougayrède J-P, 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 313:848-851. http://dx.doi.org/10.1126/science.1127059.
29. Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrède J-P. 2010. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A 107: 11537-11542. http://dx.doi.org/10.1073/pnas.1001261107.
30. Weir TL, Manter DK, Sheflin AM, Barnett BA, Heuberger AL, Ryan EP. 2013. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One 8:e70803. http://dx.doi.org /10.1371/journal.pone.0070803.
31. Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, Jia W, Cai S, Zhao L. 2012. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 6:320-329. http://dx.doi.org/10 .1038/ismej.2011.109.
32. Mager DL, Haffajee AD, Devlin PM, Norris CM, Posner MR, Goodson JM. 2005. The salivary microbiota as a diagnostic indicator of oral cancer: a descriptive, nonrandomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med 3:27. http://dx.doi.org/10.1186/1479-5876-3-27.
33. Schwabe RF, Jobin C. 2013. The microbiome and cancer. Nat Rev Cancer 13:800-812. http://dx.doi.org/10.1038/nrc3610.
34. Ahn J, Chen CY, Hayes RB. 2012. Oral microbiome and oral and gastrointestinal cancer risk. Cancer Causes Control 23:399-404. http://dx .doi.org/10.1007/s10552-011-9892-7.
35. Lees-Miller S. 2003. Repair of DNA double-strand breaks by nonhomologous end joining. Biochimie 85:1161-1173. http://dx.doi.org/10.1016/j .biochi.2003.10.011.
36. Khanna KK, Jackson SP. 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 27:247-254. http://dx.doi .org/10.1038/85798.
37. Toller IM, Neelsen KJ, Steger M, Hartung ML, Hottiger MO, Stucki M, Kalali B, Gerhard M, Sartori AA, Lopes M, Müller A. 2011. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci U S A 108:14944-14949. http://dx.doi.org/10.1073/pnas.1100959108.
38. Negrini S, Gorgoulis VG, Halazonetis TD. 2010. Genomic instability: an evolving hallmark of cancer. Nat Rev Mol Cell Biol 11:220-228. http://dx .doi.org/10.1038/nrm2858.
39. Ojanotko-Harri A, Nikkari T, Harri MP, Paunio KU. 1990. Metabolism of progesterone and testosterone by Bacillus cereus strain Socransky 67 and Streptococcus mutans strain Ingbritt. Oral Microbiol Immunol 5:237-239.http://dx.doi.org/10.1111/j.1399-302X.1990.tb00653.x.
40. Wiebe JP, Muzia D, Hu J, Szwajcer D, Hill SA, Seachrist JL. 2000. The 4-pregnene and 5-alpha-pregnane progesterone metabolites formed in nontumorous and tumorous breast tissue have opposite effects on breast cell proliferation and adhesion. Cancer Res 60:936-943.
41. Wiebe JP. 2006. Progesterone metabolites in breast cancer. Endocr Relat Cancer 13:717-738. http://dx.doi.org/10.1677/erc.1.01010.
42. van't Veer P, Dekker JM, Lamers JW, Kok FJ, Schouten EG, Brants HA, Sturmans F, Hermus RJ. 1989. Consumption of fermented milk products and breast cancer: a case-control study in the Netherlands. Cancer Res 49:4020-4023.
43. Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K. 2000. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356:1795-1799. http://dx.doi.org/10.1016/S0140-6736(00)03231-1.
44. Strayer DR, Carter WA, Mayberry SD, Pequignot E, Brodsky I. 1984. Low natural cytotoxicity of peripheral blood mononuclear cells in individuals with high familial incidences of cancer. Cancer Res 44:370-374.
45. Kosaka A, Yan H, Ohashi S, Gotoh Y, Sato A, Tsutsui H, Kaisho T, Toda T, Tsuji NM. 2012. Lactococcus lactis subsp. cremoris FC triggers IFN-γ production from NK and T cells via IL-12 and IL-18. Int Immunopharmacol 14:729-733. http://dx.doi.org/10.1016/j.intimp.2012.10.007.
46. Carrega P, Bonaccorsi I, Di Carlo E, Morandi B, Paul P, Rizzello V, Cipollone G, Navarra G, Mingari MC, Moretta L, Ferlazzo G. 2014. CD56 (bright) perforin (low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J Immunol 192:3805-3815. http://dx .doi.org/10.4049/jimmunol.1301889.
47. Koller VJ, Marian B, Stidl R, Nersesyan A, Winter H, Simić T, Sontag G, Knasmüller S. 2008. Impact of lactic acid bacteria on oxidative DNA damage in human derived colon cells. Food Chem Toxicol 46:1221-1229.http://dx.doi.org/10.1016/j.fct.2007.09.005.
48. de Moreno de LeBlanc A, Matar C, Thériault C, Perdigón G. 2005. Effects of milk fermented by Lactobacillus helveticus R389 on immune cells associated to mammary glands in normal and a breast cancer model. Immunobiology 210:349-358. http://dx.doi.org/10.1016/j.imbio.2005.05.024.
49. Shiou S-R, Yu Y, Guo Y, He S-M, Mziray-Andrew CH, Hoenig J, Sun J, Petrof EO, Claud EC. 2013. Synergistic protection of combined probiotic conditioned media against neonatal necrotizing enterocolitis-like intestinal injury. PLoS One 8:e65108. http://dx.doi.org/10.1371/journal .pone.0065108.
50. Hosseini E, Grootaert C, Verstraete W, Van de Wiele T. 2011. Propionate as a health-promoting microbial metabolite in the human gut. Nutr Rev 69:245-258. http://dx.doi.org/10.1111/j.1753-4887.2011.00388.x.
51. Louis P, Hold GL, Flint HJ. 2014. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12:661-672. http://dx.doi .org/10.1038/nrmicro3344.
52. Aldunate M, Srbinovski D, Hearps AC, Latham CF, Ramsland PA, Gugasyan R, Cone RA, Tachedjian G. 2015. Antimicrobial and immune modulatory effects of lactic acid and short-chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis. Front Physiol 6:164.