Investig Clin Urol.  2020 Feb;61(Suppl 1):S43-S50. 10.4111/icu.2020.61.S1.S43.

The human gastrointestinal microbiota and prostate cancer development and treatment

Affiliations
  • 1Dartmouth Medical School, Hanover, NH, USA. Sybil.T.Sha.MED@dartmouth.edu
  • 2University of Central Florida, Orlando, FL, USA.
  • 3University of East Anglia, Norwich, UK.
  • 4Central Florida Cancer Institute, Davenport, FL, USA.

Abstract

The human gastrointestinal microbiome contains commensal bacteria and other microbiota that have been gaining increasing attention in the context of cancer development and response to treatment. Microbiota play a role in the maintenance of host barrier surfaces that contribute to both local inflammation and other systemic metabolic functions. In the context of prostate cancer, the gastrointestinal microbiome may play a role through metabolism of estrogen, an increase of which has been linked to the induction of prostatic neoplasia. Specific microbiota such as Bacteroides, Streptococcus, Bacteroides massiliensis, Faecalibacterium prausnitzii, Eubacterium rectalie, and Mycoplasma genitalium have been associated with differing risks of prostate cancer development or extensiveness of prostate cancer disease. In this Review, we discuss gastrointestinal microbiota's effects on prostate cancer development, the ability of the microbiome to regulate chemotherapy for prostate cancer treatment, and the importance of using Next Generation Sequencing to further discern the microbiome's systemic influence on prostate cancer.

Keyword

Microbiota; Prostatic neoplasms

MeSH Terms

Bacteria
Bacteroides
Drug Therapy
Estrogens
Eubacterium
Gastrointestinal Microbiome*
Humans*
Inflammation
Metabolism
Microbiota
Mycoplasma genitalium
Prostate*
Prostatic Neoplasms*
Streptococcus
Estrogens

Cited by  1 articles

Celebrating the 60th anniversary of Investigative and Clinical Urology
Kwangsung Park
Investig Clin Urol. 2020;61(Suppl 1):S1-S2.    doi: 10.4111/icu.2020.61.S1.S1.


Reference

1. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. The application of ecological theory toward an understanding of the human microbiome. Science. 2012; 336:1255–1262.
Article
2. Roy S, Trinchieri G. Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer. 2017; 17:271–285.
Article
3. O'Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006; 7:688–693.
4. 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.
Article
5. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005; 308:1635–1638.
Article
6. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006; 312:1355–1359.
Article
7. Goodman B, Gardner H. The microbiome and cancer. J Pathol. 2018; 244:667–676.
Article
8. Tulstrup MV, Christensen EG, Carvalho V, Linninge C, Ahrné S, Højberg O, et al. Antibiotic treatment affects intestinal permeability and gut microbial composition in Wistar rats dependent on antibiotic class. PLoS One. 2015; 10:e0144854.
Article
9. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010; 107:11971–11975.
Article
10. Haller D. The gut microbiome in health and disease. Basel: Springer International Publishing;2018.
11. Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol. 2007; 19:59–69.
Article
12. Elkrief A, El Raichani L, Richard C, Messaoudene M, Belkaid W, Malo J, et al. Antibiotics are associated with decreased progression-free survival of advanced melanoma patients treated with immune checkpoint inhibitors. Oncoimmunology. 2019; 8:e1568812.
Article
13. Cimadamore A, Santoni M, Massari F, Gasparrini S, Cheng L, Lopez-Beltran A, et al. Microbiome and cancers, with focus on genitourinary tumors. Front Oncol. 2019; 9:178.
Article
14. Paulos CM, Wrzesinski C, Kaiser A, Hinrichs CS, Chieppa M, Cassard L, et al. Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. J Clin Invest. 2007; 117:2197–2204.
Article
15. Olsson J, Drott JB, Laurantzon L, Laurantzon O, Bergh A, Elgh F. Chronic prostatic infection and inflammation by Propionibacterium acnes in a rat prostate infection model. PLoS One. 2012; 7:e51434.
Article
16. Buti L, Spooner E, Van der Veen AG, Rappuoli R, Covacci A, Ploegh HL. Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc Natl Acad Sci U S A. 2011; 108:9238–9243.
Article
17. Lara-Tejero M, Galán JE. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science. 2000; 290:354–357.
Article
18. Vivarelli S, Salemi R, Candido S, Falzone L, Santagati M, Stefani S, et al. Gut microbiota and cancer: from pathogenesis to therapy. Cancers (Basel). 2019; 11:E38.
Article
19. Hatakeyama M. Structure and function of helicobacter pylori CagA, the first-identified bacterial protein involved in human cancer. Proc Jpn Acad Ser B Phys Biol Sci. 2017; 93:196–219.
20. Lenoir M, Del Carmen S, Cortes-Perez NG, Lozano-Ojalvo D, Muñoz-Provencio D, Chain F, et al. Lactobacillus casei BL23 regulates Treg and Th17 T-cell populations and reduces DMH-associated colorectal cancer. J Gastroenterol. 2016; 51:862–873.
21. Porter CM, Shrestha E, Peiffer LB, Sfanos KS. The microbiome in prostate inflammation and prostate cancer. Prostate Cancer Prostatic Dis. 2018; 21:345–354.
Article
22. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019; 69:7–34.
Article
23. The Global Cancer Observatory. Cancer fact sheets. Lyon: World Health Organization;2019.
24. Wilson KM, Giovannucci EL, Mucci LA. Lifestyle and dietary factors in the prevention of lethal prostate cancer. Asian J Androl. 2012; 14:365–374.
Article
25. Amirian ES, Petrosino JF, Ajami NJ, Liu Y, Mims MP, Scheurer ME. Potential role of gastrointestinal microbiota composition in prostate cancer risk. Infect Agent Cancer. 2013; 8:42.
Article
26. Lampe JW. Dairy products and cancer. J Am Coll Nutr. 2011; 30(5 Suppl 1):464S–470S.
Article
27. Punnen S, Hardin J, Cheng I, Klein EA, Witte JS. Impact of meat consumption, preparation, and mutagens on aggressive prostate cancer. PLoS One. 2011; 6:e27711.
Article
28. Sonn GA, Aronson W, Litwin MS. Impact of diet on prostate cancer: a review. Prostate Cancer Prostatic Dis. 2005; 8:304–310.
Article
29. Musso G, Gambino R, Cassader M. Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes. Annu Rev Med. 2011; 62:361–380.
Article
30. Masood MI, Qadir MI, Shirazi JH, Khan IU. Beneficial effects of lactic acid bacteria on human beings. Crit Rev Microbiol. 2011; 37:91–98.
Article
31. Russell SL, Finlay BB. The impact of gut microbes in allergic diseases. Curr Opin Gastroenterol. 2012; 28:563–569.
Article
32. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan TJ, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012; 338:120–123.
Article
33. Graessler J, Qin Y, Zhong H, Zhang J, Licinio J, Wong ML, et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics J. 2013; 13:514–522.
Article
34. Hunter PA, Dawson S, French GL, Goossens H, Hawkey PM, Kuijper EJ, et al. Antimicrobial-resistant pathogens in animals and man: prescribing, practices and policies. J Antimicrob Chemother. 2010; 65 Suppl 1:i3–i17.
Article
35. Boursi B, Mamtani R, Haynes K, Yang YX. Recurrent antibiotic exposure may promote cancer formation--Another step in understanding the role of the human microbiota? Eur J Cancer. 2015; 51:2655–2664.
36. Plottel CS, Blaser MJ. Microbiome and malignancy. Cell Host Microbe. 2011; 10:324–335.
Article
37. Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME. Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev. 2004; 13:1558–1568.
38. Dennis LK, Lynch CF, Torner JC. Epidemiologic association between prostatitis and prostate cancer. Urology. 2002; 60:78–83.
Article
39. Daniels NA, Ewing SK, Zmuda JM, Wilt TJ, Bauer DC. Osteoporotic Fractures in Men (MrOS) Research Group. Correlates and prevalence of prostatitis in a large community-based cohort of older men. Urology. 2005; 66:964–970.
Article
40. Bostwick DG, Burke HB, Djakiew D, Euling S, Ho SM, Landolph J, et al. Human prostate cancer risk factors. Cancer. 2004; 101(10 Suppl):2371–2490.
Article
41. Cheng I, Witte JS, Jacobsen SJ, Haque R, Quinn VP, Quesenberry CP, et al. Prostatitis, sexually transmitted diseases, and prostate cancer: the California men's health study. PLoS One. 2010; 5:e8736.
Article
42. Roberts RO, Bergstralh EJ, Bass SE, Lieber MM, Jacobsen SJ. Prostatitis as a risk factor for prostate cancer. Epidemiology. 2004; 15:93–99.
Article
43. Poutahidis T, Cappelle K, Levkovich T, Lee CW, Doulberis M, Ge Z, et al. Pathogenic intestinal bacteria enhance prostate cancer development via systemic activation of immune cells in mice. PLoS One. 2013; 8:e73933.
Article
44. Liss MA, White JR, Goros M, Gelfond J, Leach R, Johnson-Pais T, et al. Metabolic biosynthesis pathways identified from fecal microbiome associated with prostate cancer. Eur Urol. 2018; 74:575–582.
Article
45. Nakai Y, Nonomura N. Inflammation and prostate carcinogenesis. Int J Urol. 2013; 20:150–160.
Article
46. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Grönberg H, Drake CG, et al. Inflammation in prostate carcinogenesis. Nat Rev Cancer. 2007; 7:256–269.
Article
47. De Marzo AM, Marchi VL, Epstein JI, Nelson WG. Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol. 1999; 155:1985–1992.
48. Redman MG, Ward EJ, Phillips RS. The efficacy and safety of probiotics in people with cancer: a systematic review. Ann Oncol. 2014; 25:1919–1929.
Article
49. Ridlon JM, Ikegawa S, Alves JM, Zhou B, Kobayashi A, Iida T, et al. Clostridium scindens: a human gut microbe with a high potential to convert glucocorticoids into androgens. J Lipid Res. 2013; 54:2437–2449.
Article
50. Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrède JP. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A. 2010; 107:11537–11542.
Article
51. Elkahwaji JE, Hauke RJ, Brawner CM. Chronic bacterial inflammation induces prostatic intraepithelial neoplasia in mouse prostate. Br J Cancer. 2009; 101:1740–1748.
Article
52. Figueiredo JC, Grau MV, Haile RW, Sandler RS, Summers RW, Bresalier RS, et al. Folic acid and risk of prostate cancer: results from a randomized clinical trial. J Natl Cancer Inst. 2009; 101:432–435.
Article
53. Alanee S, El-Zawahry A, Dynda D, Dabaja A, McVary K, Karr M, et al. A prospective study to examine the association of the urinary and fecal microbiota with prostate cancer diagnosis after transrectal biopsy of the prostate using 16sRNA gene analysis. Prostate. 2019; 79:81–87.
Article
54. Golombos DM, Ayangbesan A, O'Malley P, Lewicki P, Barlow L, Barbieri CE, et al. The role of gut microbiome in the pathogenesis of prostate cancer: a prospective, pilot study. Urology. 2018; 111:122–128.
Article
55. Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013; 16:255–261.
Article
56. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008; 105:16731–16736.
Article
57. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009; 15:1183–1189.
Article
58. Cockburn DW, Orlovsky NI, Foley MH, Kwiatkowski KJ, Bahr CM, Maynard M, et al. Molecular details of a starch utilization pathway in the human gut symbiont Eubacterium rectale. Mol Microbiol. 2015; 95:209–230.
59. Miyake M, Ohnishi K, Hori S, Nakano A, Nakano R, Yano H, et al. Mycoplasma genitalium infection and chronic inflammation in human prostate cancer: detection using prostatectomy and needle biopsy specimens. Cells. 2019; 8:E212.
Article
60. Sfanos KS, Markowski MC, Peiffer LB, Ernst SE, White JR, Pienta KJ, et al. Compositional differences in gastrointestinal microbiota in prostate cancer patients treated with androgen axis-targeted therapies. Prostate Cancer Prostatic Dis. 2018; 21:539–548.
Article
61. Mosca A, Leclerc M, Hugot JP. Gut microbiota diversity and human diseases: should we reintroduce key predators in our ecosystem. Front Microbiol. 2016; 7:455.
Article
62. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillère R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013; 342:971–976.
Article
63. Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013; 342:967–970.
Article
64. Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015; 350:1079–1084.
Article
65. Alexander JL, Wilson ID, Teare J, Marchesi JR, Nicholson JK, Kinross JM. Gut microbiota modulation of chemotherapy efficacy and toxicity. Nat Rev Gastroenterol Hepatol. 2017; 14:356–365.
Article
66. Montassier E, Gastinne T, Vangay P, Al-Ghalith GA, Bruley des Varannes S, Massart S, et al. Chemotherapy-driven dysbiosis in the intestinal microbiome. Aliment Pharmacol Ther. 2015; 42:515–528.
Article
67. Vande Voorde J, Vervaeke P, Liekens S, Balzarini J. Mycoplasma hyorhinis-encoded cytidine deaminase efficiently inactivates cytosine-based anticancer drugs. FEBS Open Bio. 2015; 5:634–639.
Article
68. Meldrum C, Doyle MA, Tothill RW. Next-generation sequencing for cancer diagnostics: a practical perspective. Clin Biochem Rev. 2011; 32:177–195.
69. Kamps R, Brandão RD, Bosch BJ, Paulussen AD, Xanthoulea S, Blok MJ, et al. Next-generation sequencing in oncology: genetic diagnosis, risk prediction and cancer classification. Int J Mol Sci. 2017; 18:E308.
Article
70. Mouraviev V, McDonald M. An implementation of next generation sequencing for prevention and diagnosis of urinary tract infection in urology. Can J Urol. 2018; 25:9349–9356.
71. Hamada T, Nowak JA, Milner DA Jr, Song M, Ogino S. Integration of microbiology, molecular pathology, and epidemiology: a new paradigm to explore the pathogenesis of microbiomedriven neoplasms. J Pathol. 2019; 247:615–628.
Article
Full Text Links
  • ICU
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr