Home LiteratureArticle Details
PMID: 28529325 Published · ppublish English Journal Article Review

Anticancer effects of the microbiome and its products.

Nature reviews. Microbiology ·Vol. 15 ·No. 8 ·2017-08-00 ·Pages 465-478

Zitvogel L, Daillère R, Roberti MP, Routy B, Kroemer G

Abstract

The human gut microbiome modulates many host processes, including metabolism, inflammation, and immune and cellular responses. It is becoming increasingly apparent that the microbiome can also influence the development of cancer. In preclinical models, the host response to cancer treatment has been improved by modulating the gut microbiome; this is known to have an altered composition in many diseases, including cancer. In addition, cancer treatment with microbial agents or their products has the potential to shrink tumours. However, the microbiome could also negatively influence cancer prognosis through the production of potentially oncogenic toxins and metabolites by bacteria. Thus, future antineoplastic treatments could combine the modulation of the microbiome and its products with immunotherapeutics and more conventional approaches that directly target malignant cells.

MeSH Terms
Bacteria/metabolism Gastrointestinal Microbiome Gastrointestinal Tract/microbiology,physiology Humans Neoplasms/microbiology,prevention & control,therapy
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Zitvogel Laurence
Institut de Cancérologie Gustave Roussy Cancer Campus (GRCC), 114 rue Edouard Vaillant, Villejuif 94805, France. | Institut National de la Santé Et de la Recherche Medicale (INSERM), U1015, GRCC, Villejuif 94805, France. | University of Paris-Saclay, Kremlin Bicêtre 94270, France. | Center of Clinical Investigations CIC1428, GRCC, Villejuif 94805, France.
Daillère Romain
Institut de Cancérologie Gustave Roussy Cancer Campus (GRCC), 114 rue Edouard Vaillant, Villejuif 94805, France. | Institut National de la Santé Et de la Recherche Medicale (INSERM), U1015, GRCC, Villejuif 94805, France. | University of Paris-Saclay, Kremlin Bicêtre 94270, France.
Roberti María Paula
Institut de Cancérologie Gustave Roussy Cancer Campus (GRCC), 114 rue Edouard Vaillant, Villejuif 94805, France. | Institut National de la Santé Et de la Recherche Medicale (INSERM), U1015, GRCC, Villejuif 94805, France. | University of Paris-Saclay, Kremlin Bicêtre 94270, France.
Routy Bertrand
Institut de Cancérologie Gustave Roussy Cancer Campus (GRCC), 114 rue Edouard Vaillant, Villejuif 94805, France. | Institut National de la Santé Et de la Recherche Medicale (INSERM), U1015, GRCC, Villejuif 94805, France. | University of Paris-Saclay, Kremlin Bicêtre 94270, France.
Kroemer Guido
Center of Clinical Investigations CIC1428, GRCC, Villejuif 94805, France. | Equipe 11 labelisée par la Ligue Nationale contre le Cancer, INSERM U1138, Centre de Recherche des Cordeliers, Paris 75006, France. | University of Paris Descartes, Sorbonne Paris Cité, Paris 75006, France. | University of Pierre et Marie Curie, Paris 75006, France. | Pôle de Biologie, Hôpital Européen Georges Pompidou, Paris 75015, France. | Metabolomics and Cell Biology Platforms, GRCC, Villejuif 94805, France. | Karolinska Institute, Department of Women's and Children's Health, Karolinska University Hospital, Stockholm 17176, Sweden.
References (158)
158 references, click to expand
  1. Manipulation of the gut microbiota using resistant starch is associated with protection against colitis-associated colorectal cancer in rats.
    Carcinogenesis. 2016 Apr;37(4):366-375 PMID: 26905582
  2. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.
    Nature. 2013 Dec 19;504(7480):446-50 PMID: 24226770
  3. Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity.
    Sci Rep. 2015 Nov 17;5:16865 PMID: 26574055
  4. The Intestinal Microbiome and Estrogen Receptor-Positive Female Breast Cancer.
    J Natl Cancer Inst. 2016 Apr 22;108(8): PMID: 27107051
  5. Acetyl-CoA synthetase 2 promotes acetate utilization and maintains cancer cell growth under metabolic stress.
    Cancer Cell. 2015 Jan 12;27(1):57-71 PMID: 25584894
  6. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota.
    Science. 2015 Nov 27;350(6264):1079-84 PMID: 26541610
  7. Human symbionts inject and neutralize antibacterial toxins to persist in the gut.
    Proc Natl Acad Sci U S A. 2016 Mar 29;113(13):3639-44 PMID: 26957597
  8. Structure and Inhibition of Microbiome β-Glucuronidases Essential to the Alleviation of Cancer Drug Toxicity.
    Chem Biol. 2015 Sep 17;22(9):1238-49 PMID: 26364932
  9. Safety and survival with GVAX pancreas prime and Listeria Monocytogenes-expressing mesothelin (CRS-207) boost vaccines for metastatic pancreatic cancer.
    J Clin Oncol. 2015 Apr 20;33(12):1325-33 PMID: 25584002
  10. Nontoxic potentiation of cancer chemotherapy by dietary oligofructose or inulin.
    Nutr Cancer. 2000;38(1):1-5 PMID: 11341034
  11. Phase I trial of systemic intravenous infusion of interleukin-13-Pseudomonas exotoxin in patients with metastatic adrenocortical carcinoma.
    Cancer Med. 2015 Jul;4(7):1060-8 PMID: 25767039
  12. The potential role of lung microbiota in lung cancer attributed to household coal burning exposures.
    Environ Mol Mutagen. 2014 Oct;55(8):643-51 PMID: 24895247
  13. The treatment of malignant tumors by bacterial toxins as developed by the late William B. Coley, M.D., reviewed in the light of modern research.
    Cancer Res. 1946 Apr;6:205-16 PMID: 21018724
  14. Does an apple a day keep the oncologist away?
    Ann Oncol. 2005 Nov;16(11):1841-4 PMID: 16091428
  15. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype.
    Gut. 2014 Dec;63(12):1932-42 PMID: 24658599
  16. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria.
    Cell Death Differ. 2002 Feb;9(2):179-88 PMID: 11840168
  17. Gut mucosal microbiome across stages of colorectal carcinogenesis.
    Nat Commun. 2015 Oct 30;6:8727 PMID: 26515465
  18. Induction of autophagy by spermidine promotes longevity.
    Nat Cell Biol. 2009 Nov;11(11):1305-14 PMID: 19801973
  19. Characterizing human lung tissue microbiota and its relationship to epidemiological and clinical features.
    Genome Biol. 2016 Jul 28;17 (1):163 PMID: 27468850
  20. TLR7 promotes tumor progression, chemotherapy resistance, and poor clinical outcomes in non-small cell lung cancer.
    Cancer Res. 2014 Sep 15;74(18):5008-18 PMID: 25074614
  21. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation.
    Nature. 2013 Dec 19;504(7480):451-5 PMID: 24226773
  22. Tissue Microbiome Profiling Identifies an Enrichment of Specific Enteric Bacteria in Opisthorchis viverrini Associated Cholangiocarcinoma.
    EBioMedicine. 2016 Jun;8:195-202 PMID: 27428430
  23. An intra-patient placebo-controlled phase I trial to evaluate the safety and tolerability of intradermal IMM-101 in melanoma.
    Ann Oncol. 2012 May;23(5):1314-9 PMID: 21930686
  24. Continuous intravenous administration of live genetically modified salmonella typhimurium in patients with metastatic melanoma.
    J Immunother. 2003 Mar-Apr;26(2):179-80 PMID: 12616110
  25. From Hype to Hope: The Gut Microbiota in Enteric Infectious Disease.
    Cell. 2015 Dec 3;163(6):1326-32 PMID: 26638069
  26. Probiotic Lactobacillus acidophilus and L. casei mix sensitize colorectal tumoral cells to 5-fluorouracil-induced apoptosis.
    Nutr Cancer. 2010;62(3):371-8 PMID: 20358475
  27. Prophylactic effect of a Lactobacillus casei preparation on the recurrence of superficial bladder cancer. BLP Study Group.
    Urol Int. 1992;49(3):125-9 PMID: 1466089
  28. Targeting the interleukin-11 receptor α in metastatic prostate cancer: A first-in-man study.
    Cancer. 2015 Jul 15;121(14):2411-21 PMID: 25832466
  29. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22.
    Immunity. 2013 Aug 22;39(2):372-85 PMID: 23973224
  30. Mental health: thinking from the gut.
    Nature. 2015 Feb 26;518(7540):S12-5 PMID: 25715275
  31. Bacillus Calmette-Guerin versus doxorubicin versus thiotepa: a randomized prospective study in 202 patients with superficial bladder cancer.
    J Urol. 1990 Mar;143(3):502-6 PMID: 2106041
  32. Estimation of the potential antitumor activity of microencapsulated Lactobacillus acidophilus yogurt formulation in the attenuation of tumorigenesis in Apc(Min/+) mice.
    Dig Dis Sci. 2009 Feb;54(2):264-73 PMID: 18633708
  33. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice.
    Proc Natl Acad Sci U S A. 2016 Mar 1;113(9):E1306-15 PMID: 26884164
  34. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology.
    Gut. 2016 Mar;65(3):426-36 PMID: 26100928
  35. Antitumor effects of the intravesical instillation of heat killed cells of the Lactobacillus casei strain Shirota on the murine orthotopic bladder tumor MBT-2.
    J Urol. 2001 Dec;166(6):2506-11 PMID: 11696819
  36. Limitations in doxorubicin production from Streptomyces peucetius.
    Microbiol Res. 2010 Jul 20;165(5):427-35 PMID: 20116225
  37. Acetate dependence of tumors.
    Cell. 2014 Dec 18;159(7):1591-602 PMID: 25525877
  38. Synbiotic intervention of Bifidobacterium lactis and resistant starch protects against colorectal cancer development in rats.
    Carcinogenesis. 2010 Feb;31(2):246-51 PMID: 19696163
  39. Orally delivered microencapsulated probiotic formulation favorably impacts polyp formation in APC (Min/+) model of intestinal carcinogenesis.
    Artif Cells Nanomed Biotechnol. 2016;44(1):1-11 PMID: 25060720
  40. Discordant humoral and cellular immune responses to Cytomegalovirus (CMV) in glioblastoma patients whose tumors are positive for CMV.
    Oncoimmunology. 2015 Feb 25;4(2):e982391 PMID: 25949880
  41. Fasting-Mimicking Diet Reduces HO-1 to Promote T Cell-Mediated Tumor Cytotoxicity.
    Cancer Cell. 2016 Jul 11;30(1):136-46 PMID: 27411588
  42. Anti-cancer activity of targeted pro-apoptotic peptides.
    Nat Med. 1999 Sep;5(9):1032-8 PMID: 10470080
  43. The long-term stability of the human gut microbiota.
    Science. 2013 Jul 5;341(6141):1237439 PMID: 23828941
  44. Mini-review: perspective of the microbiome in the pathogenesis of urothelial carcinoma.
    Am J Clin Exp Urol. 2014 Apr 15;2(1):57-61 PMID: 25126590
  45. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2013.
    Eur Urol. 2013 Oct;64(4):639-53 PMID: 23827737
  46. Normalizing Microbiota-Induced Retinoic Acid Deficiency Stimulates Protective CD8(+) T Cell-Mediated Immunity in Colorectal Cancer.
    Immunity. 2016 Sep 20;45(3):641-55 PMID: 27590114
  47. The microbiota in adaptive immune homeostasis and disease.
    Nature. 2016 Jul 06;535(7610):75-84 PMID: 27383982
  48. Butyrate production from high-fiber diet protects against lymphoma tumor.
    Leuk Lymphoma. 2016 Oct;57(10):2401-8 PMID: 26885564
  49. Lactobacillus casei BL23 regulates Treg and Th17 T-cell populations and reduces DMH-associated colorectal cancer.
    J Gastroenterol. 2016 Sep;51(9):862-73 PMID: 26749362
  50. Acidic extracellular pH shifts colorectal cancer cell death from apoptosis to necrosis upon exposure to propionate and acetate, major end-products of the human probiotic propionibacteria.
    Apoptosis. 2007 Mar;12 (3):573-91 PMID: 17195096
  51. Microbiome-wide association studies link dynamic microbial consortia to disease.
    Nature. 2016 Jul 06;535(7610):94-103 PMID: 27383984
  52. Host-microbial interactions in the metabolism of therapeutic and diet-derived xenobiotics.
    J Clin Invest. 2014 Oct;124(10):4173-81 PMID: 25105361
  53. The Colonic Crypt Protects Stem Cells from Microbiota-Derived Metabolites.
    Cell. 2016 Jun 16;165(7):1708-20 PMID: 27264604
  54. Fecal Microbiota Transplantation Induces Remission in Patients With Active Ulcerative Colitis in a Randomized Controlled Trial.
    Gastroenterology. 2015 Jul;149(1):102-109.e6 PMID: 25857665
  55. Tumor regression with regional distribution of the targeted toxin TF-CRM107 in patients with malignant brain tumors.
    Nat Med. 1997 Dec;3(12):1362-8 PMID: 9396606
  56. Gut microbiome-derived metabolites modulate intestinal epithelial cell damage and mitigate graft-versus-host disease.
    Nat Immunol. 2016 May;17(5):505-13 PMID: 26998764
  57. Enterococcus hirae and Barnesiella intestinihominis Facilitate Cyclophosphamide-Induced Therapeutic Immunomodulatory Effects.
    Immunity. 2016 Oct 18;45(4):931-943 PMID: 27717798
  58. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome.
    Nature. 2016 Jun 08;534(7606):213-7 PMID: 27279214
  59. Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation.
    Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11276-81 PMID: 19549860
  60. High throughput sequencing reveals distinct microbial populations within the mucosal and luminal niches in healthy individuals.
    Gut Microbes. 2015;6(3):173-81 PMID: 25915459
  61. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  62. Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis.
    Nat Commun. 2016 Feb 02;7:10391 PMID: 26837003
  63. Microbial influences in inflammatory bowel diseases.
    Gastroenterology. 2008 Feb;134(2):577-94 PMID: 18242222
  64. Probiotic potential of lactic acid bacteria isolated from fermented dairy milks on antiproliferation of colon cancer cells.
    Biotechnol Lett. 2009 Apr;31(4):571-6 PMID: 19116692
  65. An inulin and doxorubicin conjugate for improving cancer therapy.
    J Drug Deliv Sci Technol. 2013;23(2):111-118 PMID: 24734120
  66. Longevity in mice is promoted by probiotic-induced suppression of colonic senescence dependent on upregulation of gut bacterial polyamine production.
    PLoS One. 2011;6(8):e23652 PMID: 21858192
  67. Reprogrammed and transmissible intestinal microbiota confer diminished susceptibility to induced colitis in TMF-/- mice.
    Proc Natl Acad Sci U S A. 2014 Apr 1;111(13):4964-9 PMID: 24639530
  68. Repertoire of human gut microbes.
    Microb Pathog. 2017 May;106:103-112 PMID: 27317857
  69. Small-molecule inhibitors prevent the genotoxic and protumoural effects induced by colibactin-producing bacteria.
    Gut. 2016 Feb;65(2):278-85 PMID: 25588406
  70. The hallmarks of aging.
    Cell. 2013 Jun 6;153(6):1194-217 PMID: 23746838
  71. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy.
    Science. 2015 Nov 27;350(6264):1084-9 PMID: 26541606
  72. Lactobacillus rhamnosus GG Activation of Dendritic Cells and Neutrophils Depends on the Dose and Time of Exposure.
    J Immunol Res. 2016;2016:7402760 PMID: 27525288
  73. Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands.
    Cancer Cell. 2004 Sep;6(3):275-84 PMID: 15380518
  74. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome.
    Nature. 2013 Jul 4;499(7456):97-101 PMID: 23803760
  75. Expression of chemokine/cytokine genes and immune cell recruitment following the instillation of Mycobacterium bovis, bacillus Calmette-Guérin or Lactobacillus rhamnosus strain GG in the healthy murine bladder.
    Immunology. 2008 Jul;124(3):419-27 PMID: 18217952
  76. Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens.
    Science. 2016 Apr 29;352(6285):535-8 PMID: 27126035
  77. AhR sensing of bacterial pigments regulates antibacterial defence.
    Nature. 2014 Aug 28;512(7515):387-92 PMID: 25119038
  78. Habitual intake of lactic acid bacteria and risk reduction of bladder cancer.
    Urol Int. 2002;68(4):273-80 PMID: 12053032
  79. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment.
    Science. 2013 Nov 22;342(6161):967-70 PMID: 24264989
  80. Fecal microbiota transplantation for patients with steroid-resistant acute graft-versus-host disease of the gut.
    Blood. 2016 Oct 20;128(16):2083-2088 PMID: 27461930
  81. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.
    Science. 2013 Aug 2;341(6145):569-73 PMID: 23828891
  82. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells.
    Cell. 2014 Jul 17;158(2):288-99 PMID: 25036629
  83. Inhibition of Growth and Metastasis of Breast Cancer in Mice by Milk Fermented With Lactobacillus casei CRL 431.
    J Immunother. 2015 Jun;38(5):185-96 PMID: 25962107
  84. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma.
    J Clin Oncol. 2002 Jan 1;20(1):142-52 PMID: 11773163
  85. Global cancer statistics, 2012.
    CA Cancer J Clin. 2015 Mar;65(2):87-108 PMID: 25651787
  86. Relationship between the in vitro response of dendritic cells to Lactobacillus and prevention of tumorigenesis in the mouse.
    J Gastroenterol. 2008;43(9):661-9 PMID: 18807127
  87. Microbiota modulate tumoral immune surveillance in lung through a γδT17 immune cell-dependent mechanism.
    Cancer Res. 2014 Aug 1;74(15):4030-41 PMID: 24947042
  88. Immunogenic cell death in cancer therapy.
    Annu Rev Immunol. 2013;31:51-72 PMID: 23157435
  89. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme.
    Science. 2010 Nov 5;330(6005):831-5 PMID: 21051639
  90. Beneficial bacteria inhibit cachexia.
    Oncotarget. 2016 Mar 15;7(11):11803-16 PMID: 26933816
  91. Chemokine receptor patterns in lymphocytes mirror metastatic spreading in melanoma.
    J Clin Invest. 2016 Mar 1;126(3):921-37 PMID: 26854930
  92. Cervical Microbiota Associated with Higher Grade Cervical Intraepithelial Neoplasia in Women Infected with High-Risk Human Papillomaviruses.
    Cancer Prev Res (Phila). 2016 May;9(5):357-66 PMID: 26935422
  93. Cardioprotection and lifespan extension by the natural polyamine spermidine.
    Nat Med. 2016 Dec;22(12 ):1428-1438 PMID: 27841876
  94. Differential induction of apoptosis in human colonic carcinoma cells (Caco-2) by Atopobium, and commensal, probiotic and enteropathogenic bacteria: mediation by the mitochondrial pathway.
    Int J Food Microbiol. 2010 Feb 28;137(2-3):190-203 PMID: 20036023
  95. Randomised, open-label, phase II study of gemcitabine with and without IMM-101 for advanced pancreatic cancer.
    Br J Cancer. 2016 Sep 27;115(7):789-96 PMID: 27599039
  96. Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum.
    J Vet Sci. 2004 Mar;5(1):41-8 PMID: 15028884
  97. Gut Microbiota Orchestrates Energy Homeostasis during Cold.
    Cell. 2015 Dec 3;163(6):1360-74 PMID: 26638070
  98. Anti-tumour immune effect of oral administration of Lactobacillus plantarum to CT26 tumour-bearing mice.
    J Biosci. 2015 Jun;40(2):269-79 PMID: 25963256
  99. Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid.
    Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10462-7 PMID: 22689992
  100. The probiotic approach: an alternative treatment option in urology.
    Eur Urol. 2005 Mar;47(3):288-96 PMID: 15716188
  101. Mediterranean diet and faecal microbiota: a transversal study.
    Food Funct. 2016 May 18;7(5):2347-56 PMID: 27137178
  102. Caloric Restriction Mimetics Enhance Anticancer Immunosurveillance.
    Cancer Cell. 2016 Jul 11;30(1):147-60 PMID: 27411589
  103. [Influence of Lactobacillus casei on rat bladder carcinogenesis].
    Nihon Hinyokika Gakkai Zasshi. 1994 Apr;85(4):655-63 PMID: 8189664
  104. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces.
    Appl Environ Microbiol. 2002 Jul;68(7):3401-7 PMID: 12089021
  105. A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model.
    Mol Syst Biol. 2007;3:112 PMID: 17515922
  106. Association of seropositivity to Helicobacter species and biliary tract cancer in the ATBC study.
    Hepatology. 2014 Dec;60(6):1963-71 PMID: 24797247
  107. Probiotic-derived ferrichrome inhibits colon cancer progression via JNK-mediated apoptosis.
    Nat Commun. 2016 Aug 10;7:12365 PMID: 27507542
  108. Expression of functional toll like receptor 4 in estrogen receptor/progesterone receptor-negative breast cancer.
    Breast Cancer Res. 2015 Sep 22;17:130 PMID: 26392082
  109. Microbial-derived butyrate: an oncometabolite or tumor-suppressive metabolite?
    Cell Host Microbe. 2014 Aug 13;16(2):143-5 PMID: 25121740
  110. Effects of oral administration of Lactobacillus casei on antitumor responses induced by tumor resection in mice.
    Int J Immunopharmacol. 1994 Jan;16(1):29-36 PMID: 8150553
  111. Trial Watch: Experimental Toll-like receptor agonists for cancer therapy.
    Oncoimmunology. 2012 Aug 1;1(5):699-716 PMID: 22934262
  112. Hexokinase Is an Innate Immune Receptor for the Detection of Bacterial Peptidoglycan.
    Cell. 2016 Jul 28;166(3):624-36 PMID: 27374331
  113. Regulatory T-cell Response to Enterotoxigenic Bacteroides fragilis Colonization Triggers IL17-Dependent Colon Carcinogenesis.
    Cancer Discov. 2015 Oct;5(10):1098-109 PMID: 26201900
  114. Safety, tolerability, and tumor response of IL4-Pseudomonas exotoxin (NBI-3001) in patients with recurrent malignant glioma.
    J Neurooncol. 2003 Aug-Sep;64(1-2):125-37 PMID: 12952293
  115. Prognostic impact of vitamin B6 metabolism in lung cancer.
    Cell Rep. 2012 Aug 30;2(2):257-69 PMID: 22854025
  116. Acetate is a bioenergetic substrate for human glioblastoma and brain metastases.
    Cell. 2014 Dec 18;159(7):1603-14 PMID: 25525878
  117. Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism.
    Cell. 2013 Mar 28;153(1):228-39 PMID: 23540700
  118. Antibiotic use predicts an increased risk of cancer.
    Int J Cancer. 2008 Nov 1;123(9):2152-5 PMID: 18704945
  119. The anticancer effect of probiotic Bacillus polyfermenticus on human colon cancer cells is mediated through ErbB2 and ErbB3 inhibition.
    Int J Cancer. 2010 Aug 15;127(4):780-90 PMID: 19876926
  120. Cell-bound exopolysaccharide from probiotic bacteria induces autophagic cell death of tumour cells.
    Lett Appl Microbiol. 2010 Aug;51(2):123-30 PMID: 20536712
  121. Direct Activation of STING in the Tumor Microenvironment Leads to Potent and Systemic Tumor Regression and Immunity.
    Cell Rep. 2015 May 19;11(7):1018-30 PMID: 25959818
  122. Policy: How to regulate faecal transplants.
    Nature. 2014 Feb 20;506(7488):290-1 PMID: 24558658
  123. Engineering Bacillus subtilis for the conversion of the antimetabolite 4-hydroxy-l-threonine to pyridoxine.
    Metab Eng. 2015 May;29:196-207 PMID: 25777134
  124. Compositional data analysis of the microbiome: fundamentals, tools, and challenges.
    Ann Epidemiol. 2016 May;26(5):330-5 PMID: 27255738
  125. Effect of hydrogen peroxide of bacterial origin on apoptosis and necrosis of gut mucosa epithelial cells as a possible pathomechanism of inflammatory bowel disease and cancer.
    J Physiol Pharmacol. 2009 Dec;60 Suppl 6:55-60 PMID: 20224152
  126. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study.
    Gut. 2016 Oct 14;:null PMID: 27742762
  127. 16S rRNA amplicon sequencing identifies microbiota associated with oral cancer, human papilloma virus infection and surgical treatment.
    Oncotarget. 2016 Aug 9;7(32):51320-51334 PMID: 27259999
  128. Genetic and Metabolic Signals during Acute Enteric Bacterial Infection Alter the Microbiota and Drive Progression to Chronic Inflammatory Disease.
    Cell Host Microbe. 2016 Jan 13;19(1):21-31 PMID: 26764594
  129. The three Es of cancer immunoediting.
    Annu Rev Immunol. 2004;22:329-60 PMID: 15032581
  130. Synchronized cycles of bacterial lysis for in vivo delivery.
    Nature. 2016 Aug 4;536(7614):81-5 PMID: 27437587
  131. Antitumor activity of Lactobacillus casei in mice.
    Gan. 1981 Aug;72(4):517-23 PMID: 6796451
  132. Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes.
    Front Genet. 2015 Apr 20;6:148 PMID: 25941533
  133. Immune mechanisms in bacillus Calmette-Guerin immunotherapy for superficial bladder cancer.
    J Urol. 2003 Sep;170(3):964-9 PMID: 12913751
  134. Tumor immunity produced by the intradermal inoculation of living tumor cells and living Mycobacterium bovis (strain BCG).
    Science. 1970 Dec 11;170(3963):1217-8 PMID: 4920656
  135. Sporadic colorectal cancer: microbial contributors to disease prevention, development and therapy.
    Br J Cancer. 2016 Jul 26;115(3):273-80 PMID: 27380134
  136. Changes in abundance of oral microbiota associated with oral cancer.
    PLoS One. 2014 Jun 02;9(6):e98741 PMID: 24887397
  137. Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women.
    Lancet. 2009 Jul 25;374(9686):301-14 PMID: 19586656
  138. Intestinal Crosstalk between Bile Acids and Microbiota and Its Impact on Host Metabolism.
    Cell Metab. 2016 Jul 12;24(1):41-50 PMID: 27320064
  139. Antibiotic-Induced Changes in the Intestinal Microbiota and Disease.
    Trends Mol Med. 2016 Jun;22(6):458-78 PMID: 27178527
  140. Targeting Cancer Metabolism: Dietary and Pharmacologic Interventions.
    Cancer Discov. 2016 Dec;6(12 ):1315-1333 PMID: 27872127
  141. Gastrointestinal microbial populations can distinguish pediatric and adolescent Acute Lymphoblastic Leukemia (ALL) at the time of disease diagnosis.
    BMC Genomics. 2016 Aug 15;17(1):635 PMID: 27527070
  142. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2.
    J Exp Med. 2006 Dec 25;203(13):2853-63 PMID: 17178920
  143. Microbiome and Anticancer Immunosurveillance.
    Cell. 2016 Apr 7;165(2):276-87 PMID: 27058662
  144. Lactobacillus species is more cytotoxic to human bladder cancer cells than Mycobacterium Bovis (bacillus Calmette-Guerin).
    J Urol. 2002 Nov;168(5):2236-9 PMID: 12394766
  145. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide.
    Science. 2013 Nov 22;342(6161):971-6 PMID: 24264990
  146. Characterization of the microbiome of nipple aspirate fluid of breast cancer survivors.
    Sci Rep. 2016 Jun 21;6:28061 PMID: 27324944
  147. Role of the microbiome in non-gastrointestinal cancers.
    World J Clin Oncol. 2016 Apr 10;7(2):200-13 PMID: 27081642
  148. Immune-dependent antineoplastic effects of cisplatin plus pyridoxine in non-small-cell lung cancer.
    Oncogene. 2015 Jun 4;34(23):3053-62 PMID: 25065595
  149. The Microbiome of Aseptically Collected Human Breast Tissue in Benign and Malignant Disease.
    Sci Rep. 2016 Aug 03;6:30751 PMID: 27485780
  150. The yin yang of bacterial polysaccharides: lessons learned from B. fragilis PSA.
    Immunol Rev. 2012 Jan;245(1):13-26 PMID: 22168411
  151. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients.
    Cancer Gene Ther. 2003 Oct;10(10):737-44 PMID: 14502226
  152. Enhancement of natural killer cytotoxicity delayed murine carcinogenesis by a probiotic microorganism.
    Carcinogenesis. 2001 Apr;22(4):599-605 PMID: 11285195
  153. Pore-forming toxins: ancient, but never really out of fashion.
    Nat Rev Microbiol. 2016 Feb;14(2):77-92 PMID: 26639780
  154. Non-absorbable apple procyanidins prevent obesity associated with gut microbial and metabolomic changes.
    Sci Rep. 2016 Aug 10;6:31208 PMID: 27506289
  155. Production of butyrate from lysine and the Amadori product fructoselysine by a human gut commensal.
    Nat Commun. 2015 Dec 01;6:10062 PMID: 26620920
  156. Intratumoral injection of Clostridium novyi-NT spores induces antitumor responses.
    Sci Transl Med. 2014 Aug 13;6(249):249ra111 PMID: 25122639
  157. Aldara activates TLR7-independent immune defence.
    Nat Commun. 2013;4:1560 PMID: 23463003
  158. Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling.
    J Clin Invest. 2007 Aug;117(8):2197-204 PMID: 17657310
Article Info
Journal
Nature reviews. Microbiology
Abbr.
Nat Rev Microbiol
ISSN
1740-1534
DOI
10.1038/nrmicro.2017.44
Published
2017-08-00
Epub
2017-00-22
Pages
465-478
Language
English
Region
England
NLM ID
101190261
Subset
IM
External Links
PubMed source DOI: 10.1038/nrmicro.2017.44 View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2