Skip to main content
Erschienen in: European Journal of Clinical Microbiology & Infectious Diseases 12/2018

12.09.2018 | Review

Roles of intestinal microbiota in response to cancer immunotherapy

verfasst von: Jing Cong, Xiaochun Zhang

Erschienen in: European Journal of Clinical Microbiology & Infectious Diseases | Ausgabe 12/2018

Einloggen, um Zugang zu erhalten

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.
Literatur
1.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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
Metadaten
Titel
Roles of intestinal microbiota in response to cancer immunotherapy
verfasst von
Jing Cong
Xiaochun Zhang
Publikationsdatum
12.09.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Clinical Microbiology & Infectious Diseases / Ausgabe 12/2018
Print ISSN: 0934-9723
Elektronische ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-018-3374-8

Weitere Artikel der Ausgabe 12/2018

European Journal of Clinical Microbiology & Infectious Diseases 12/2018 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.