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Published in: Current Nutrition Reports 1/2019

Open Access 01-03-2019 | Metastasis | Cancer (MF Leitzmann, Section Editor)

The Role of the Microbiome in Cancer Initiation and Progression: How Microbes and Cancer Cells Utilize Excess Energy and Promote One Another’s Growth

Authors: Corrie M. Whisner, C. Athena Aktipis

Published in: Current Nutrition Reports | Issue 1/2019

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Abstract

Purpose of Review

We use an ecological lens to understand how microbes and cancer cells coevolve inside the ecosystems of our bodies. We describe how microbe-cancer cell interactions contribute to cancer progression, including cooperation between microbes and cancer cells. We discuss the role of the immune system in preventing this apparent ‘collusion’ and describe how microbe-cancer cell interactions lead to opportunities and challenges in treating cancer.

Recent Findings

Microbiota influence many aspects of our health including our cancer risk. Since both microbes and cancer cells rely on incoming resources for their survival and replication, excess energy and nutrient input from the host can play a role in cancer initiation and progression.

Summary

Certain microbes enhance cancer cell fitness by promoting proliferation and protecting cancer cells from the immune system. How diet influences these interactions remains largely unknown but recent evidence suggests a role for nutrients across the cancer continuum.
Literature
1.
go back to reference Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30.PubMed Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30.PubMed
3.
go back to reference Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148(6):1258–70.PubMedPubMedCentral Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148(6):1258–70.PubMedPubMedCentral
4.
go back to reference Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533.PubMedPubMedCentral Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533.PubMedPubMedCentral
5.
go back to reference Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.PubMedPubMedCentral Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.PubMedPubMedCentral
6.
go back to reference Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. Role of the normal gut microbiota. World J Gastroenterol. 2015;21(29):8787–803.PubMedPubMedCentral Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. Role of the normal gut microbiota. World J Gastroenterol. 2015;21(29):8787–803.PubMedPubMedCentral
7.
go back to reference Meng C, Bai C, Brown TD, Hood LE, Tian Q. Human gut microbiota and gastrointestinal cancer. Genomics Proteomics Bioinformatics. 2018;16(1):33–49.PubMedPubMedCentral Meng C, Bai C, Brown TD, Hood LE, Tian Q. Human gut microbiota and gastrointestinal cancer. Genomics Proteomics Bioinformatics. 2018;16(1):33–49.PubMedPubMedCentral
8.
go back to reference Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol. 2015;31(1):69–75.PubMedPubMedCentral Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol. 2015;31(1):69–75.PubMedPubMedCentral
9.
go back to reference Ley RE, Knight R, Gordon JI. The human microbiome: eliminating the biomedical/environmental dichotomy in microbial ecology. Environ Microbiol. 2007;9(1):3–4.PubMed Ley RE, Knight R, Gordon JI. The human microbiome: eliminating the biomedical/environmental dichotomy in microbial ecology. Environ Microbiol. 2007;9(1):3–4.PubMed
10.
go back to reference Natividad JMM, Verdu EF. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol Res. 2013;69(1):42–51.PubMed Natividad JMM, Verdu EF. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol Res. 2013;69(1):42–51.PubMed
11.
go back to reference de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13(6):607–15.PubMed de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13(6):607–15.PubMed
13.
go back to reference Wasielewski H, Alcock J, Aktipis A. Resource conflict and cooperation between human host and gut microbiota: implications for nutrition and health. Ann N Y Acad Sci. 2016;1372(1):20–8.PubMed Wasielewski H, Alcock J, Aktipis A. Resource conflict and cooperation between human host and gut microbiota: implications for nutrition and health. Ann N Y Acad Sci. 2016;1372(1):20–8.PubMed
14.
go back to reference Polyak K, Haviv I, Campbell IG. Co-evolution of tumor cells and their microenvironment. Trends Genet. 2009;25(1):30–8.PubMed Polyak K, Haviv I, Campbell IG. Co-evolution of tumor cells and their microenvironment. Trends Genet. 2009;25(1):30–8.PubMed
15.
go back to reference Merlo LF, Pepper JW, Reid BJ, Maley CC. Cancer as an evolutionary and ecological process. Nat Rev Cancer. 2006;6(12):924–35.PubMed Merlo LF, Pepper JW, Reid BJ, Maley CC. Cancer as an evolutionary and ecological process. Nat Rev Cancer. 2006;6(12):924–35.PubMed
16.
go back to reference de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6(1):24–37.PubMed de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6(1):24–37.PubMed
18.
20.
go back to reference Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille-Michaud A, et al. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One. 2013;8(2):e56964.PubMedPubMedCentral Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille-Michaud A, et al. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One. 2013;8(2):e56964.PubMedPubMedCentral
21.
go back to reference Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R. The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes. 2014;5(5):675–80.PubMedPubMedCentral Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R. The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes. 2014;5(5):675–80.PubMedPubMedCentral
22.
go back to reference Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A. 2014;111(51):18321–6.PubMedPubMedCentral Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A. 2014;111(51):18321–6.PubMedPubMedCentral
23.
go back to reference David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63.PubMed David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63.PubMed
24.
go back to reference Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332(6032):970–4.PubMedPubMedCentral Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332(6032):970–4.PubMedPubMedCentral
25.
go back to reference 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(6052):105–8.PubMedPubMedCentral 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(6052):105–8.PubMedPubMedCentral
26.
go back to reference De Filippo C, Cavalieri D, Di Paola M, 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(33):14691–6.PubMedPubMedCentral De Filippo C, Cavalieri D, Di Paola M, 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(33):14691–6.PubMedPubMedCentral
27.
go back to reference Newmark HL, Yang K, Kurihara N, Fan K, Augenlicht LH, Lipkin M. Western-style diet-induced colonic tumors and their modulation by calcium and vitamin D in C57Bl/6 mice: a preclinical model for human sporadic colon cancer. Carcinogenesis. 2009;30(1):88–92.PubMed Newmark HL, Yang K, Kurihara N, Fan K, Augenlicht LH, Lipkin M. Western-style diet-induced colonic tumors and their modulation by calcium and vitamin D in C57Bl/6 mice: a preclinical model for human sporadic colon cancer. Carcinogenesis. 2009;30(1):88–92.PubMed
28.
go back to reference Newmark HL, Yang K, Lipkin M, Kopelovich L, Liu Y, Fan K, et al. A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice. Carcinogenesis. 2001;22(11):1871–5.PubMed Newmark HL, Yang K, Lipkin M, Kopelovich L, Liu Y, Fan K, et al. A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice. Carcinogenesis. 2001;22(11):1871–5.PubMed
29.
go back to reference Longo VD, Fontana L. Calorie restriction and cancer prevention: metabolic and molecular mechanisms. Trends Pharmacol Sci. 2010;31(2):89–98.PubMedPubMedCentral Longo VD, Fontana L. Calorie restriction and cancer prevention: metabolic and molecular mechanisms. Trends Pharmacol Sci. 2010;31(2):89–98.PubMedPubMedCentral
30.
go back to reference Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31.PubMed Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31.PubMed
31.
go back to reference Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214.PubMed Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214.PubMed
32.
go back to reference Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010;18(1):190–5.PubMed Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010;18(1):190–5.PubMed
34.
go back to reference • Ott B, Skurk T, Hastreiter L, et al. Effect of caloric restriction on gut permeability, inflammation markers, and fecal microbiota in obese women. Sci Rep. 2017;7(1):11955 This paper expands knowledge of caloric restriction diets on gut microbial communities, gut barrier function, and weight loss in a cohort of obese women. Findings from this work may inform cancer research as similar inflammatory and gut barrier mechanisms have been implicated in cancer research. Interestingly, the authors did not find major consistent changes in microbial abundance in the intestines of women following very low-calorie diets; however, reductions in inflammatory markers CRP and lipopolysaccharide were observed. PubMedPubMedCentral • Ott B, Skurk T, Hastreiter L, et al. Effect of caloric restriction on gut permeability, inflammation markers, and fecal microbiota in obese women. Sci Rep. 2017;7(1):11955 This paper expands knowledge of caloric restriction diets on gut microbial communities, gut barrier function, and weight loss in a cohort of obese women. Findings from this work may inform cancer research as similar inflammatory and gut barrier mechanisms have been implicated in cancer research. Interestingly, the authors did not find major consistent changes in microbial abundance in the intestines of women following very low-calorie diets; however, reductions in inflammatory markers CRP and lipopolysaccharide were observed. PubMedPubMedCentral
35.
go back to reference • Fraumene C, Manghina V, Cadoni E, et al. Caloric restriction promotes rapid expansion and long-lasting increase of Lactobacillus in the rat fecal microbiota. Gut Microbes. 2018;9(2):104–14 This paper suggests that caloric restriction in rats, at a young age, may allow beneficial alterations to the gut microbiome to persist into adulthood. Specifically, caloric restriction significantly increased the abundance of potentially beneficial Lactobacillus . PubMed • Fraumene C, Manghina V, Cadoni E, et al. Caloric restriction promotes rapid expansion and long-lasting increase of Lactobacillus in the rat fecal microbiota. Gut Microbes. 2018;9(2):104–14 This paper suggests that caloric restriction in rats, at a young age, may allow beneficial alterations to the gut microbiome to persist into adulthood. Specifically, caloric restriction significantly increased the abundance of potentially beneficial Lactobacillus . PubMed
36.
go back to reference Tollefsbol TO. Dietary epigenetics in cancer and aging. Cancer Treat Res. 2014;159:257–67.PubMed Tollefsbol TO. Dietary epigenetics in cancer and aging. Cancer Treat Res. 2014;159:257–67.PubMed
37.
go back to reference O’Flanagan CH, Smith LA, McDonell SB, Hursting SD. When less may be more: calorie restriction and response to cancer therapy. BMC Med. 2017;15(1):106.PubMedPubMedCentral O’Flanagan CH, Smith LA, McDonell SB, Hursting SD. When less may be more: calorie restriction and response to cancer therapy. BMC Med. 2017;15(1):106.PubMedPubMedCentral
38.
go back to reference Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029–33.PubMedPubMedCentral Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029–33.PubMedPubMedCentral
39.
go back to reference Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol. 2004;70(10):5810–7.PubMedPubMedCentral Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol. 2004;70(10):5810–7.PubMedPubMedCentral
42.
go back to reference La Vecchia C, Franceschi S, Dolara P, Bidoli E, Barbone F. Refined-sugar intake and the risk of colorectal cancer in humans. Int J Cancer. 1993;55(3):386–9.PubMed La Vecchia C, Franceschi S, Dolara P, Bidoli E, Barbone F. Refined-sugar intake and the risk of colorectal cancer in humans. Int J Cancer. 1993;55(3):386–9.PubMed
43.
go back to reference Makarem N, Lin Y, Bandera EV, Jacques PF, Parekh N. Concordance with World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) guidelines for cancer prevention and obesity-related cancer risk in the Framingham Offspring cohort (1991-2008). Cancer Causes Control. 2015;26(2):277–86.PubMedPubMedCentral Makarem N, Lin Y, Bandera EV, Jacques PF, Parekh N. Concordance with World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) guidelines for cancer prevention and obesity-related cancer risk in the Framingham Offspring cohort (1991-2008). Cancer Causes Control. 2015;26(2):277–86.PubMedPubMedCentral
44.
go back to reference Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–9.PubMedPubMedCentral Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–9.PubMedPubMedCentral
45.
go back to reference Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilán CG, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185.PubMedPubMedCentral Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilán CG, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185.PubMedPubMedCentral
46.
go back to reference Augeron C, Laboisse CL. Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res. 1984;44(9):3961–9.PubMed Augeron C, Laboisse CL. Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res. 1984;44(9):3961–9.PubMed
47.
go back to reference Hague A, Manning AM, Hanlon KA, Huschtscha LI, Hart D, 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. 1993;55(3):498–505.PubMed Hague A, Manning AM, Hanlon KA, Huschtscha LI, Hart D, 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. 1993;55(3):498–505.PubMed
48.
go back to reference Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A, et al. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota- and butyrate-dependent manner. Cancer Discov. 2014;4(12):1387–97.PubMedPubMedCentral Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A, et al. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota- and butyrate-dependent manner. Cancer Discov. 2014;4(12):1387–97.PubMedPubMedCentral
49.
go back to reference Belcheva A, Irrazabal T, Robertson SJ, Streutker C, Maughan H, Rubino S, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014;158(2):288–99.PubMed Belcheva A, Irrazabal T, Robertson SJ, Streutker C, Maughan H, Rubino S, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014;158(2):288–99.PubMed
50.
go back to reference Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, et al. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature. 2016;534(7606):213–7.PubMedPubMedCentral Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, et al. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature. 2016;534(7606):213–7.PubMedPubMedCentral
51.
go back to reference Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, Fouhy F, et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut. 2010;59(12):1635–42.PubMed Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, Fouhy F, et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut. 2010;59(12):1635–42.PubMed
52.
go back to reference Romagnolo DF, Selmin OI. Flavonoids and cancer prevention: a review of the evidence. J Nutr Gerontol Geriatr. 2012;31(3):206–38.PubMed Romagnolo DF, Selmin OI. Flavonoids and cancer prevention: a review of the evidence. J Nutr Gerontol Geriatr. 2012;31(3):206–38.PubMed
54.
go back to reference Watson GW, Beaver LM, Williams DE, Dashwood RH, Ho E. Phytochemicals from cruciferous vegetables, epigenetics, and prostate cancer prevention. AAPS J. 2013;15(4):951–61. Watson GW, Beaver LM, Williams DE, Dashwood RH, Ho E. Phytochemicals from cruciferous vegetables, epigenetics, and prostate cancer prevention. AAPS J. 2013;15(4):951–61.
55.
go back to reference Abdull Razis AF, Noor NM. Cruciferous vegetables: dietary phytochemicals for cancer prevention. Asian Pac J Cancer Prev. 2013;14(3):1565–70.PubMed Abdull Razis AF, Noor NM. Cruciferous vegetables: dietary phytochemicals for cancer prevention. Asian Pac J Cancer Prev. 2013;14(3):1565–70.PubMed
56.
go back to reference Li F, Hullar MAJ, 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(9):1685–91.PubMedPubMedCentral Li F, Hullar MAJ, 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(9):1685–91.PubMedPubMedCentral
57.
go back to reference Salonen A, Lahti L, Salojärvi J, Holtrop G, Korpela K, Duncan SH, et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014;8(11):2218–30.PubMedPubMedCentral Salonen A, Lahti L, Salojärvi J, Holtrop G, Korpela K, Duncan SH, et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014;8(11):2218–30.PubMedPubMedCentral
58.
go back to reference • Desai MS, Seekatz AM, Koropatkin NM, et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 2016;167(5):1339–1353.e21 This paper supports the importance of dietary fiber in maintaining the intestinal mucus barrier, as low-fiber diets promoted the abundance of mucus-degrading microbes. In the absence of dietary fiber, gut microbes were driven to rely on mucus glycoproteins rather than non-digested complex carbohydrates which reduced intestinal barrier function, thereby increasing inflammation and susceptibility to pathogens. Most interesting was the finding that prebiotic supplementation, while correcting the microbiome transcriptome, was unable to correct the erosion of intestinal mucus. PubMedPubMedCentral • Desai MS, Seekatz AM, Koropatkin NM, et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 2016;167(5):1339–1353.e21 This paper supports the importance of dietary fiber in maintaining the intestinal mucus barrier, as low-fiber diets promoted the abundance of mucus-degrading microbes. In the absence of dietary fiber, gut microbes were driven to rely on mucus glycoproteins rather than non-digested complex carbohydrates which reduced intestinal barrier function, thereby increasing inflammation and susceptibility to pathogens. Most interesting was the finding that prebiotic supplementation, while correcting the microbiome transcriptome, was unable to correct the erosion of intestinal mucus. PubMedPubMedCentral
60.
go back to reference Rowland IR, Wiseman H, Sanders TA, Adlercreutz H, Bowey EA. Interindividual variation in metabolism of soy isoflavones and lignans: influence of habitual diet on equol production by the gut microflora. Nutr Cancer. 2000;36(1):27–32.PubMed Rowland IR, Wiseman H, Sanders TA, Adlercreutz H, Bowey EA. Interindividual variation in metabolism of soy isoflavones and lignans: influence of habitual diet on equol production by the gut microflora. Nutr Cancer. 2000;36(1):27–32.PubMed
61.
go back to reference Nyangale EP, Mottram DS, Gibson GR. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J Proteome Res. 2012;11(12):5573–85.PubMed Nyangale EP, Mottram DS, Gibson GR. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J Proteome Res. 2012;11(12):5573–85.PubMed
62.
go back to reference Joyce SA, Gahan CGM. Disease-associated changes in bile acid profiles and links to altered gut microbiota. Dig Dis. 2017;35(3):169–77.PubMed Joyce SA, Gahan CGM. Disease-associated changes in bile acid profiles and links to altered gut microbiota. Dig Dis. 2017;35(3):169–77.PubMed
63.
go back to reference Bernstein C, Holubec H, Bhattacharyya AK, Nguyen H, Payne CM, Zaitlin B, et al. Carcinogenicity of deoxycholate, a secondary bile acid. Arch Toxicol. 2011;85(8):863–71.PubMedPubMedCentral Bernstein C, Holubec H, Bhattacharyya AK, Nguyen H, Payne CM, Zaitlin B, et al. Carcinogenicity of deoxycholate, a secondary bile acid. Arch Toxicol. 2011;85(8):863–71.PubMedPubMedCentral
64.
go back to reference Bernstein C, Payne CM, Bernstein H. Bile acids: promoters or carcinogens in colon cancer. J Carcinogene Mutagene. 2011;2:101e. Bernstein C, Payne CM, Bernstein H. Bile acids: promoters or carcinogens in colon cancer. J Carcinogene Mutagene. 2011;2:101e.
65.
go back to reference Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr. 2011;93(5):1062–72.PubMed Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr. 2011;93(5):1062–72.PubMed
66.
go back to reference O’Keefe SJD, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015;6:6342.PubMed O’Keefe SJD, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015;6:6342.PubMed
67.
go back to reference O’Keefe SJ, Kidd M, Espitalier-Noel G, Owira P. Rarity of colon cancer in Africans is associated with low animal product consumption, not fiber. Am J Gastroenterol. 1999;94(5):1373–80.PubMed O’Keefe SJ, Kidd M, Espitalier-Noel G, Owira P. Rarity of colon cancer in Africans is associated with low animal product consumption, not fiber. Am J Gastroenterol. 1999;94(5):1373–80.PubMed
68.
go back to reference Fletcher JA, Doebeli M. A simple and general explanation for the evolution of altruism. Proc R Soc B Biol Sci. 2009;276(1654):13–9. Fletcher JA, Doebeli M. A simple and general explanation for the evolution of altruism. Proc R Soc B Biol Sci. 2009;276(1654):13–9.
69.
go back to reference Noe R, Hammerstein P. Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol. 1994;35(1):1–11 %@ 0340–5443. Noe R, Hammerstein P. Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol. 1994;35(1):1–11 %@ 0340–5443.
70.
go back to reference Aktipis CA. Know when to walk away: contingent movement and the evolution of cooperation. J Theor Biol. 2004;231(2):249–60.PubMed Aktipis CA. Know when to walk away: contingent movement and the evolution of cooperation. J Theor Biol. 2004;231(2):249–60.PubMed
71.
go back to reference Aktipis A, Cronk L, Alcock J, et al. Understanding cooperation through fitness interdependence. Nat Hum Behav. 2018;2:429–431. Aktipis A, Cronk L, Alcock J, et al. Understanding cooperation through fitness interdependence. Nat Hum Behav. 2018;2:429–431.
72.
go back to reference Nougayrède J-P, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313(5788):848–51.PubMed Nougayrède J-P, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313(5788):848–51.PubMed
73.
go back to reference Bhatt AP, Redinbo MR, Bultman SJ. The role of the microbiome in cancer development and therapy. CA Cancer J Clin. 2017;67(4):326–44.PubMedPubMedCentral Bhatt AP, Redinbo MR, Bultman SJ. The role of the microbiome in cancer development and therapy. CA Cancer J Clin. 2017;67(4):326–44.PubMedPubMedCentral
74.
go back to reference Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci U S A. 2011;108(37):15354–9.PubMedPubMedCentral Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci U S A. 2011;108(37):15354–9.PubMedPubMedCentral
75.
go back to reference Watanabe T, Tada M, Nagai H, Sasaki S, Nakao M. Helicobacter pylori infection induces gastric cancer in mongolian gerbils. Gastroenterology. 1998;115(3):642–8.PubMed Watanabe T, Tada M, Nagai H, Sasaki S, Nakao M. Helicobacter pylori infection induces gastric cancer in mongolian gerbils. Gastroenterology. 1998;115(3):642–8.PubMed
76.
go back to reference Helicobacter and Cancer Collaborative Group. Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut. 2001;49(3):347–53. Helicobacter and Cancer Collaborative Group. Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut. 2001;49(3):347–53.
78.
go back to reference •• Suarez G, Romero-Gallo J, Sierra JC, et al. Genetic manipulation of helicobacter pylori virulence function by host carcinogenic phenotypes. Cancer Res. 2017;77(9):2401–12 This in vivo work in a rodent model of human gastric cancer highlights that H. pylori pathogenesis and influence on gastric cancer is related to host phenotype. This work further suggests the integrated role of gut microbes in cancer progression via host-integration of microbial virulence factors. PubMedPubMedCentral •• Suarez G, Romero-Gallo J, Sierra JC, et al. Genetic manipulation of helicobacter pylori virulence function by host carcinogenic phenotypes. Cancer Res. 2017;77(9):2401–12 This in vivo work in a rodent model of human gastric cancer highlights that H. pylori pathogenesis and influence on gastric cancer is related to host phenotype. This work further suggests the integrated role of gut microbes in cancer progression via host-integration of microbial virulence factors. PubMedPubMedCentral
79.
go back to reference Amieva M, Peek RM Jr. Pathobiology of Helicobacter pylori-induced gastric cancer. Gastroenterology. 2016;150(1):64–78.PubMed Amieva M, Peek RM Jr. Pathobiology of Helicobacter pylori-induced gastric cancer. Gastroenterology. 2016;150(1):64–78.PubMed
80.
go back to reference Cougnoux A, Dalmasso G, Martinez R, Buc E, Delmas J, Gibold L, et al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut. 2014;63(12):1932–42.PubMed Cougnoux A, Dalmasso G, Martinez R, Buc E, Delmas J, Gibold L, et al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut. 2014;63(12):1932–42.PubMed
81.
go back to reference Hussell T, Isaacson PG, Crabtree JE, Spencer J. Helicobacter pylori-specific tumour-infiltrating T cells provide contact dependent help for the growth of malignant B cells in low-grade gastric lymphoma of mucosa-associated lymphoid tissue. J Pathol. 1996;178(2):122–7.PubMed Hussell T, Isaacson PG, Crabtree JE, Spencer J. Helicobacter pylori-specific tumour-infiltrating T cells provide contact dependent help for the growth of malignant B cells in low-grade gastric lymphoma of mucosa-associated lymphoid tissue. J Pathol. 1996;178(2):122–7.PubMed
82.
go back to reference Lecuit M, Abachin E, Martin A, Poyart C, Pochart P, Suarez F, et al. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med. 2004;350(3):239–48.PubMed Lecuit M, Abachin E, Martin A, Poyart C, Pochart P, Suarez F, et al. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med. 2004;350(3):239–48.PubMed
83.
go back to reference Ferreri AJM, Govi S, Pasini E, Mappa S, Bertoni F, Zaja F, et al. Chlamydophila psittaci eradication with doxycycline as first-line targeted therapy for ocular adnexae lymphoma: final results of an international phase II trial. J Clin Oncol. 2012;30(24):2988–94.PubMed Ferreri AJM, Govi S, Pasini E, Mappa S, Bertoni F, Zaja F, et al. Chlamydophila psittaci eradication with doxycycline as first-line targeted therapy for ocular adnexae lymphoma: final results of an international phase II trial. J Clin Oncol. 2012;30(24):2988–94.PubMed
84.
go back to reference Wu S, Rhee K-J, Albesiano E, Rabizadeh S, Wu X, Yen HR, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15(9):1016–22.PubMedPubMedCentral Wu S, Rhee K-J, Albesiano E, Rabizadeh S, Wu X, Yen HR, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15(9):1016–22.PubMedPubMedCentral
85.
go back to reference Goodman B, Gardner H. The microbiome and cancer. J Pathol. 2018;244(5):667–76.PubMed Goodman B, Gardner H. The microbiome and cancer. J Pathol. 2018;244(5):667–76.PubMed
87.
go back to reference Flemming H-C, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8(9):623–33.PubMed Flemming H-C, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8(9):623–33.PubMed
88.
go back to reference Williams VM, Filippova M, Soto U, Duerksen-Hughes PJ. HPV-DNA integration and carcinogenesis: putative roles for inflammation and oxidative stress. Future Virol. 2011;6(1):45–57.PubMedPubMedCentral Williams VM, Filippova M, Soto U, Duerksen-Hughes PJ. HPV-DNA integration and carcinogenesis: putative roles for inflammation and oxidative stress. Future Virol. 2011;6(1):45–57.PubMedPubMedCentral
89.
go back to reference Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14(2):195–206.PubMedPubMedCentral Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14(2):195–206.PubMedPubMedCentral
90.
go back to reference Gaines S, Williamson AJ, Hyman N, Kandel J. How the microbiome is shaping our understanding of cancer biology and its treatment. Semin Colon Rectal Surg. 2018;29(1):12–6. Gaines S, Williamson AJ, Hyman N, Kandel J. How the microbiome is shaping our understanding of cancer biology and its treatment. Semin Colon Rectal Surg. 2018;29(1):12–6.
91.
go back to reference •• Wynendaele E, Verbeke F, D’Hondt M, et al. Crosstalk between the microbiome and cancer cells by quorum sensing peptides. Peptides. 2015;64:40–8 This paper is one of the first to expand current knowledge on how gut microbes interact with human cells to influence health and disease. The authors report on several quorum sensing peptides produced by specific microbial species that initiate cancer cell invasion in the colon and further promote angiogenisis and metastasis of cancer tissue. PubMed •• Wynendaele E, Verbeke F, D’Hondt M, et al. Crosstalk between the microbiome and cancer cells by quorum sensing peptides. Peptides. 2015;64:40–8 This paper is one of the first to expand current knowledge on how gut microbes interact with human cells to influence health and disease. The authors report on several quorum sensing peptides produced by specific microbial species that initiate cancer cell invasion in the colon and further promote angiogenisis and metastasis of cancer tissue. PubMed
92.
go back to reference Tahara T, Hirata I, Nakano N, Tahara S, Horiguchi N, Kawamura T, et al. Potential link between Fusobacterium enrichment and DNA methylation accumulation in the inflammatory colonic mucosa in ulcerative colitis. Oncotarget. 2017;8(37):61917–26.PubMedPubMedCentral Tahara T, Hirata I, Nakano N, Tahara S, Horiguchi N, Kawamura T, et al. Potential link between Fusobacterium enrichment and DNA methylation accumulation in the inflammatory colonic mucosa in ulcerative colitis. Oncotarget. 2017;8(37):61917–26.PubMedPubMedCentral
93.
go back to reference Ito M, Kanno S, Nosho K, Sukawa Y, Mitsuhashi K, Kurihara H, et al. Association of Fusobacterium nucleatum with clinical and molecular features in colorectal serrated pathway. Int J Cancer. 2015;137(6):1258–68.PubMed Ito M, Kanno S, Nosho K, Sukawa Y, Mitsuhashi K, Kurihara H, et al. Association of Fusobacterium nucleatum with clinical and molecular features in colorectal serrated pathway. Int J Cancer. 2015;137(6):1258–68.PubMed
94.
go back to reference Demehri FR, Frykman PK, Cheng Z, Ruan C, Wester T, Nordenskjöld A, et al. Altered fecal short chain fatty acid composition in children with a history of Hirschsprung-associated enterocolitis. J Pediatr Surg. 2016;51(1):81–6.PubMed Demehri FR, Frykman PK, Cheng Z, Ruan C, Wester T, Nordenskjöld A, et al. Altered fecal short chain fatty acid composition in children with a history of Hirschsprung-associated enterocolitis. J Pediatr Surg. 2016;51(1):81–6.PubMed
95.
go back to reference Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446–50.PubMed Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446–50.PubMed
96.
go back to reference Liang L, Ai L, Qian J, Fang J-Y, Xu J. Long noncoding RNA expression profiles in gut tissues constitute molecular signatures that reflect the types of microbes. Sci Rep. 2015;5:11763.PubMedPubMedCentral Liang L, Ai L, Qian J, Fang J-Y, Xu J. Long noncoding RNA expression profiles in gut tissues constitute molecular signatures that reflect the types of microbes. Sci Rep. 2015;5:11763.PubMedPubMedCentral
97.
go back to reference Maudet C, Mano M, Sunkavalli U, Sharan M, Giacca M, Förstner KU, et al. Functional high-throughput screening identifies the miR-15 microRNA family as cellular restriction factors for Salmonella infection. Nat Commun. 2014;5:4718.PubMed Maudet C, Mano M, Sunkavalli U, Sharan M, Giacca M, Förstner KU, et al. Functional high-throughput screening identifies the miR-15 microRNA family as cellular restriction factors for Salmonella infection. Nat Commun. 2014;5:4718.PubMed
98.
go back to reference •• Yu T, Guo F, Yu Y, et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell. 2017;170(3):548–563.e16 This reference provides clinical, mechanistic, and functional data to support the ability of pathogen Fusobacterium nucleatum to mediate resistance to chemotherapy in recurrent colon cancer patients. F. nucleatum appears to facilitate this response by interacting with human cell gene expression at the tumor site, specifically through integrated Toll-like receptor, microRNA, and autophagy signaling which ultimately inhibit apoptosis. PubMedPubMedCentral •• Yu T, Guo F, Yu Y, et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell. 2017;170(3):548–563.e16 This reference provides clinical, mechanistic, and functional data to support the ability of pathogen Fusobacterium nucleatum to mediate resistance to chemotherapy in recurrent colon cancer patients. F. nucleatum appears to facilitate this response by interacting with human cell gene expression at the tumor site, specifically through integrated Toll-like receptor, microRNA, and autophagy signaling which ultimately inhibit apoptosis. PubMedPubMedCentral
99.
go back to reference 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(6161):967–70.PubMedPubMedCentral 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(6161):967–70.PubMedPubMedCentral
100.
go back to reference Cesaro S, Chinello P, Rossi L, Zanesco L. Saccharomyces cerevisiae fungemia in a neutropenic patient treated with Saccharomyces boulardii. Support Care Cancer. 2000;8(6):504–5.PubMed Cesaro S, Chinello P, Rossi L, Zanesco L. Saccharomyces cerevisiae fungemia in a neutropenic patient treated with Saccharomyces boulardii. Support Care Cancer. 2000;8(6):504–5.PubMed
101.
go back to reference Scott AJ, Merrifield CA, Younes JA, Pekelharing EP. Pre-, pro- and synbiotics in cancer prevention and treatment—a review of basic and clinical research. Ecancermedicalscience. 2018;12:869.PubMedPubMedCentral Scott AJ, Merrifield CA, Younes JA, Pekelharing EP. Pre-, pro- and synbiotics in cancer prevention and treatment—a review of basic and clinical research. Ecancermedicalscience. 2018;12:869.PubMedPubMedCentral
Metadata
Title
The Role of the Microbiome in Cancer Initiation and Progression: How Microbes and Cancer Cells Utilize Excess Energy and Promote One Another’s Growth
Authors
Corrie M. Whisner
C. Athena Aktipis
Publication date
01-03-2019
Publisher
Springer US
Published in
Current Nutrition Reports / Issue 1/2019
Electronic ISSN: 2161-3311
DOI
https://doi.org/10.1007/s13668-019-0257-2

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