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Published in: European Journal of Clinical Microbiology & Infectious Diseases 12/2018

01-12-2018 | Review

Roles of intestinal microbiota in response to cancer immunotherapy

Authors: Jing Cong, Xiaochun Zhang

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 12/2018

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Abstract

Cancer immunotherapy has been significantly effective on multiple cancers; however, there are still a distinct number of non-responding patients and various immune-related adverse events in responding patients. It is known that heterogeneity of intestinal microbiota may lead to different outcomes of therapy. Previous studies have reported that intestinal microbiota is probably attributed to influence the efficacy of cancer immunotherapy. Some intestinal bacteria could synergize with immune checkpoint blockade agents and optimize the immune response against multiple cancers. Therefore, understanding the roles of intestinal microbiota could help to improve the clinical efficacy of cancer immunotherapy. In this review, we first introduced the close relationships between intestinal microbiota and intestinal immune system. Then, we described the emerging evidences that intestinal microbiota responses to cancer immunotherapy. Finally, we briefly reviewed the technical development on intestinal microbiota research.
Literature
1.
go back to reference Restifo NP, Dudley ME, Rosenberg SA (2012) Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 12(4):269CrossRef Restifo NP, Dudley ME, Rosenberg SA (2012) Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 12(4):269CrossRef
2.
go back to reference Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WEE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E (2015) Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 373(17):123–135CrossRef Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WEE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E (2015) Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 373(17):123–135CrossRef
3.
go back to reference Shalapour S, Lin XJ, Bastian IN, Brain J, Burt AD, Aksenov AA, Vrbanac AF, Li W, Perkins A, Matsutani T (2017) Erratum: inflammation-induced IgA+ cells dismantle anti-liver cancer immunity. Nature 551(7680):340–345CrossRef Shalapour S, Lin XJ, Bastian IN, Brain J, Burt AD, Aksenov AA, Vrbanac AF, Li W, Perkins A, Matsutani T (2017) Erratum: inflammation-induced IgA+ cells dismantle anti-liver cancer immunity. Nature 551(7680):340–345CrossRef
4.
go back to reference Ribas A, Kefford R, Marshall MA, Punt CJ, Haanen JB, Marmol M, Garbe C, Gogas H, Schachter J, Linette G (2013) Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol 31(5):616–622CrossRef Ribas A, Kefford R, Marshall MA, Punt CJ, Haanen JB, Marmol M, Garbe C, Gogas H, Schachter J, Linette G (2013) Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol 31(5):616–622CrossRef
5.
go back to reference Kwon ED, Drake CG, Scher HI, Fizazi K, Bossi A, Aj VDE, Krainer M, Houede N, Santos R, Mahammedi H (2014) Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. Lancet Oncol 15(10):700–712CrossRef Kwon ED, Drake CG, Scher HI, Fizazi K, Bossi A, Aj VDE, Krainer M, Houede N, Santos R, Mahammedi H (2014) Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. Lancet Oncol 15(10):700–712CrossRef
6.
go back to reference Lynch TJ, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, Sebastian M, Neal J, Lu H, Cuillerot JM (2012) Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol 30(17):2046–2054CrossRef Lynch TJ, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, Sebastian M, Neal J, Lu H, Cuillerot JM (2012) Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol 30(17):2046–2054CrossRef
7.
go back to reference Aglietta M, Barone C, Sawyer MB, Moore MJ, Jr MW, Bagalà C, Colombi F, Cagnazzo C, Gioeni L, Wang E (2014) A phase I dose escalation trial of tremelimumab (CP-675,206) in combination with gemcitabine in chemotherapy-naive patients with metastatic pancreatic cancer. Ann Oncol 25(9):1750CrossRef Aglietta M, Barone C, Sawyer MB, Moore MJ, Jr MW, Bagalà C, Colombi F, Cagnazzo C, Gioeni L, Wang E (2014) A phase I dose escalation trial of tremelimumab (CP-675,206) in combination with gemcitabine in chemotherapy-naive patients with metastatic pancreatic cancer. Ann Oncol 25(9):1750CrossRef
8.
go back to reference Hodi FS, O’Day SJ, Mcdermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC (2016) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711–723CrossRef Hodi FS, O’Day SJ, Mcdermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC (2016) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711–723CrossRef
9.
go back to reference Zou W (2005) Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5(4):263–274CrossRef Zou W (2005) Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5(4):263–274CrossRef
10.
go back to reference Larkin J, Chiarionsileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P (2015) Combined nivolumab and ipilimumab or monotherapy in previously untreated melanoma. N Engl J Med 373(1):23CrossRef Larkin J, Chiarionsileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P (2015) Combined nivolumab and ipilimumab or monotherapy in previously untreated melanoma. N Engl J Med 373(1):23CrossRef
11.
go back to reference Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, Mcneil C, Lotem M (2015) Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med 372(26):2521–2532CrossRef Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, Mcneil C, Lotem M (2015) Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med 372(26):2521–2532CrossRef
12.
go back to reference Postow MA, Callahan MK, Wolchok JD (2015) Immune checkpoint blockade in cancer therapy. J Clin Oncol 33(17):1974–1982CrossRef Postow MA, Callahan MK, Wolchok JD (2015) Immune checkpoint blockade in cancer therapy. J Clin Oncol 33(17):1974–1982CrossRef
13.
go back to reference Weber JS, Kähler KC, Hauschild A (2012) Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol 30(21):2691–2697CrossRef Weber JS, Kähler KC, Hauschild A (2012) Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol 30(21):2691–2697CrossRef
14.
go back to reference Peled JU, Devlin SM, Staffas A, Lumish M, Khanin R, Littmann ER, Ling L, Kosuri S, Maloy M, Slingerland JB (2017) Intestinal microbiota and relapse after hematopoietic-cell transplantation. J Clin Oncol 35(15):JCO2016703348CrossRef Peled JU, Devlin SM, Staffas A, Lumish M, Khanin R, Littmann ER, Ling L, Kosuri S, Maloy M, Slingerland JB (2017) Intestinal microbiota and relapse after hematopoietic-cell transplantation. J Clin Oncol 35(15):JCO2016703348CrossRef
15.
go back to reference Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S (2013) Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342(6161):967–970CrossRef Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S (2013) Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342(6161):967–970CrossRef
16.
go back to reference Sivan A, Corrales L, Hubert N, Williams JB, Aquinomichaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML (2015) Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350(6264):1084–1089CrossRef Sivan A, Corrales L, Hubert N, Williams JB, Aquinomichaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML (2015) Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350(6264):1084–1089CrossRef
17.
go back to reference Brestoff JR, Artis D (2013) Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 14(7):676CrossRef Brestoff JR, Artis D (2013) Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 14(7):676CrossRef
18.
go back to reference Randall TD, Mebius RE (2014) The development and function of mucosal lymphoid tissues: a balancing act with micro-organisms. Mucosal Immunol 7(3):455CrossRef Randall TD, Mebius RE (2014) The development and function of mucosal lymphoid tissues: a balancing act with micro-organisms. Mucosal Immunol 7(3):455CrossRef
19.
go back to reference Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, Merad M (2014) Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343(6178):1249288CrossRef Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, Merad M (2014) Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343(6178):1249288CrossRef
20.
go back to reference Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267CrossRef Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267CrossRef
21.
go back to reference Goto Y, Ivanov II (2013) Intestinal epithelial cells as mediators of the commensal–host immune crosstalk. Immunol Cell Biol 91(3):204–214CrossRef Goto Y, Ivanov II (2013) Intestinal epithelial cells as mediators of the commensal–host immune crosstalk. Immunol Cell Biol 91(3):204–214CrossRef
22.
go back to reference Collins SM, Surette M, Bercik P (2012) The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10(11):735CrossRef Collins SM, Surette M, Bercik P (2012) The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10(11):735CrossRef
23.
go back to reference Lavelle EC, Murphy C, O’Neill LAJ, Creagh EM (2009) The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol 3(1):17CrossRef Lavelle EC, Murphy C, O’Neill LAJ, Creagh EM (2009) The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol 3(1):17CrossRef
24.
go back to reference Cani PD, Everard A, Duparc T (2013) Gut microbiota, enteroendocrine functions and metabolism. Curr Opin Pharmacol 13(6):935–940CrossRef Cani PD, Everard A, Duparc T (2013) Gut microbiota, enteroendocrine functions and metabolism. Curr Opin Pharmacol 13(6):935–940CrossRef
25.
go back to reference Kamada N, Seo SU, Chen GY, Núñez G (2013) Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 13(5):321–335CrossRef Kamada N, Seo SU, Chen GY, Núñez G (2013) Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 13(5):321–335CrossRef
26.
go back to reference Round JL, Mazmanian SK (2009) The gut microbiome shapes intestinal immune responses during health and disease. Nat Rev Immunol 9(5):313–323CrossRef Round JL, Mazmanian SK (2009) The gut microbiome shapes intestinal immune responses during health and disease. Nat Rev Immunol 9(5):313–323CrossRef
27.
go back to reference Maynard CL, Elson CO, Hatton RD, Weaver CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489(7415):231–241CrossRef Maynard CL, Elson CO, Hatton RD, Weaver CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489(7415):231–241CrossRef
28.
go back to reference Masahata K, Umemoto E, Kayama H, Kotani M, Nakamura S, Kurakawa T, Kikuta J, Gotoh K, Motooka D, Sato S (2014) Generation of colonic IgA-secreting cells in the caecal patch. Nat Commun 5(4):3704CrossRef Masahata K, Umemoto E, Kayama H, Kotani M, Nakamura S, Kurakawa T, Kikuta J, Gotoh K, Motooka D, Sato S (2014) Generation of colonic IgA-secreting cells in the caecal patch. Nat Commun 5(4):3704CrossRef
29.
go back to reference Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500(7461):232CrossRef Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500(7461):232CrossRef
30.
go back to reference Cording S, Fleissner D, Heimesaat MM, Bereswill S, Loddenkemper C, Uematsu S, Akira S, Hamann A, Huehn J (2013) Commensal microbiota drive proliferation of conventional and Foxp3(+) regulatory CD4(+) T cells in mesenteric lymph nodes and Peyer’s patches. Eur J Microbiol Immunol 3(1):1CrossRef Cording S, Fleissner D, Heimesaat MM, Bereswill S, Loddenkemper C, Uematsu S, Akira S, Hamann A, Huehn J (2013) Commensal microbiota drive proliferation of conventional and Foxp3(+) regulatory CD4(+) T cells in mesenteric lymph nodes and Peyer’s patches. Eur J Microbiol Immunol 3(1):1CrossRef
31.
go back to reference Obata Y, Furusawa Y, Endo TA, Sharif J, Takahashi D, Atarashi K, Nakayama M, Onawa S, Fujimura Y, Takahashi M (2014) The epigenetic regulator Uhrf1 facilitates the proliferation and maturation of colonic regulatory T cells. Nat Immunol 15(6):571CrossRef Obata Y, Furusawa Y, Endo TA, Sharif J, Takahashi D, Atarashi K, Nakayama M, Onawa S, Fujimura Y, Takahashi M (2014) The epigenetic regulator Uhrf1 facilitates the proliferation and maturation of colonic regulatory T cells. Nat Immunol 15(6):571CrossRef
32.
go back to reference Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohloolyy M, Glickman JN, Garrett WS (2013) The microbial metabolites, short chain fatty acids, regulate colonic Treg cell homeostasis. Science 341(6145):569–573CrossRef Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohloolyy M, Glickman JN, Garrett WS (2013) The microbial metabolites, short chain fatty acids, regulate colonic Treg cell homeostasis. Science 341(6145):569–573CrossRef
33.
go back to reference Uetake C, Takahashi D, Topping DL, Miyauchi E, Nakato G, Koseki H, Ohno H, Clarke JM, Kikuchi J, Kato K (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446CrossRef Uetake C, Takahashi D, Topping DL, Miyauchi E, Nakato G, Koseki H, Ohno H, Clarke JM, Kikuchi J, Kato K (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446CrossRef
34.
go back to reference Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350(6264):1079CrossRef Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350(6264):1079CrossRef
35.
go back to reference Chaput N, Lepage P, Coutzac C, Soularue E, Le RK, Monot C, Boselli L, Routier E, Cassard L, Collins M (2017) Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol 28(6):1368CrossRef Chaput N, Lepage P, Coutzac C, Soularue E, Le RK, Monot C, Boselli L, Routier E, Cassard L, Collins M (2017) Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol 28(6):1368CrossRef
36.
go back to reference Frankel AE, Coughlin LA, Kim J, Froehlich TW, Yang X, Frenkel EP, Koh AY (2017) Metagenomic shotgun sequencing and unbiased metabolomic profiling identify specific human gut microbiota and metabolites associated with immune checkpoint therapy efficacy in melanoma patients. Neoplasia 19(10):848CrossRef Frankel AE, Coughlin LA, Kim J, Froehlich TW, Yang X, Frenkel EP, Koh AY (2017) Metagenomic shotgun sequencing and unbiased metabolomic profiling identify specific human gut microbiota and metabolites associated with immune checkpoint therapy efficacy in melanoma patients. Neoplasia 19(10):848CrossRef
37.
go back to reference Routy B, Le CE, Derosa L, Cpm D, Alou MT, Daillè R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP (2018) Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359(6371):91CrossRef Routy B, Le CE, Derosa L, Cpm D, Alou MT, Daillè R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP (2018) Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359(6371):91CrossRef
38.
go back to reference Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ, Gajewski TF (2018) The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359(6371):104CrossRef Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ, Gajewski TF (2018) The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359(6371):104CrossRef
39.
go back to reference Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC (2018) Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359(6371):97CrossRef Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC (2018) Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359(6371):97CrossRef
40.
go back to reference Pardoll D (2015) Cancer and the immune system: basic concepts and targets for intervention. Semin Oncol 42(4):523–538CrossRef Pardoll D (2015) Cancer and the immune system: basic concepts and targets for intervention. Semin Oncol 42(4):523–538CrossRef
41.
go back to reference Beck KE, Blansfield JA, Tran KQ, Feldman AL, Hughes MS, Royal RE, Kammula US, Topalian SL, Sherry RM, Kleiner D (2006) Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 24(15):2283–2289CrossRef Beck KE, Blansfield JA, Tran KQ, Feldman AL, Hughes MS, Royal RE, Kammula US, Topalian SL, Sherry RM, Kleiner D (2006) Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 24(15):2283–2289CrossRef
42.
go back to reference Mao K, Baptista AP, Tamoutounour S, Zhuang L, Bouladoux N, Martins AJ, Huang Y, Gerner MY, Belkaid Y, Germain RN (2018) Innate and adaptive lymphocytes sequentially shape the gut microbiota and lipid metabolism. Nature 554 (7691)CrossRef Mao K, Baptista AP, Tamoutounour S, Zhuang L, Bouladoux N, Martins AJ, Huang Y, Gerner MY, Belkaid Y, Germain RN (2018) Innate and adaptive lymphocytes sequentially shape the gut microbiota and lipid metabolism. Nature 554 (7691)CrossRef
43.
go back to reference Dubin K, Callahan MK, Ren B, Khanin R, Viale A, Ling L, No D, Gobourne A, Littmann E, Huttenhower C (2016) Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun 7:10391CrossRef Dubin K, Callahan MK, Ren B, Khanin R, Viale A, Ling L, No D, Gobourne A, Littmann E, Huttenhower C (2016) Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun 7:10391CrossRef
44.
go back to reference Lucke K, Miehlke S, Jacobs E, Schuppler M (2006) Prevalence of Bacteroides and Prevotella spp. in ulcerative colitis. J Med Microbiol 55(5):617–624CrossRef Lucke K, Miehlke S, Jacobs E, Schuppler M (2006) Prevalence of Bacteroides and Prevotella spp. in ulcerative colitis. J Med Microbiol 55(5):617–624CrossRef
45.
go back to reference Nguyen TLA, Vieira-Silva S, Liston A, Raes J (2015) How informative is the mouse for human gut microbiota research? Dis Model Mech 8(1):1–16CrossRef Nguyen TLA, Vieira-Silva S, Liston A, Raes J (2015) How informative is the mouse for human gut microbiota research? Dis Model Mech 8(1):1–16CrossRef
46.
go back to reference Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102(31):11070–11075CrossRef Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102(31):11070–11075CrossRef
47.
go back to reference Graf D, Cagno RD, Fåk F, Flint HJ, Nyman M, Saarela M, Watzl B (2015) Contribution of diet to the composition of the human gut microbiota. Biochem J 26(1):477–480 Graf D, Cagno RD, Fåk F, Flint HJ, Nyman M, Saarela M, Watzl B (2015) Contribution of diet to the composition of the human gut microbiota. Biochem J 26(1):477–480
48.
go back to reference Conlon M, Bird A (2015) The impact of diet and lifestyle on gut microbiota and human health. Nutrients 7(1):17–44CrossRef Conlon M, Bird A (2015) The impact of diet and lifestyle on gut microbiota and human health. Nutrients 7(1):17–44CrossRef
49.
go back to reference Lamendella R, Verberkmoes N, Jansson JK (2012) ‘Omics’ of the mammalian gut – new insights into function. Curr Opin Biotechnol 23(3):491–500CrossRef Lamendella R, Verberkmoes N, Jansson JK (2012) ‘Omics’ of the mammalian gut – new insights into function. Curr Opin Biotechnol 23(3):491–500CrossRef
50.
go back to reference Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Järnerot G, Tysk C, Jansson JK, Engstrand L (2011) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139(6):1844–1854.e1CrossRef Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Järnerot G, Tysk C, Jansson JK, Engstrand L (2011) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139(6):1844–1854.e1CrossRef
51.
go back to reference Zoetendal EG, Raes J, Bogert BVD, Arumugam M, Booijink CC, Troost FJ, Bork P, Wels M, Vos WMD, Kleerebezem M (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6(7):1415–1426CrossRef Zoetendal EG, Raes J, Bogert BVD, Arumugam M, Booijink CC, Troost FJ, Bork P, Wels M, Vos WMD, Kleerebezem M (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6(7):1415–1426CrossRef
52.
go back to reference Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230CrossRef Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230CrossRef
Metadata
Title
Roles of intestinal microbiota in response to cancer immunotherapy
Authors
Jing Cong
Xiaochun Zhang
Publication date
01-12-2018
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 12/2018
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-018-3374-8

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