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Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota
Open accessAbstract
Gut microbes affect immunotherapy: The unleashing of antitumor T cell responses has ushered in a new era of cancer treatment. Although these therapies can cause dramatic tumor regressions in some patients, many patients inexplicably see no benefit. Mice have been used in two studies to investigate what might be happening. Specific members of the gut microbiota influence the efficacy of this type of immunotherapy (see the Perspective by Snyder et al. ). Vétizou et al. found that optimal responses to anticytotoxic T lymphocyte antigen blockade required specific Bacteroides spp. Similarly, Sivan et al. discovered that Bifidobacterium spp. enhanced the efficacy of antiprogrammed cell death ligand 1 therapy. Science , this issue, p. 1079 and p. 1084 ; see also p. 1031
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In the citing paper
“In mice receiving anti-CTLA-4 immunotherapy, antitumor immunity was dependent on the presence of specific Bacteroides species [7].”
From Relating the gut metagenome and metatranscriptome to immunotherapy responses in melanoma patients (2019) · cites this paper as [7]
In the citing paper
“Bacteroides fragilis enhanced the antitumor effect of CTLA-4 blockade by triggering DC maturation and stimulating IL-12-dependent Th1 cell immune responses [17].”
From Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies (2022) · cites this paper as [17]
In the citing paper
“Currently, several lines of evidence from preclinical to clinical research have gradually established that the gut microbiota can modulate antitumor immunity and affect the efficacy of cancer immunotherapies, especially immune checkpoint inhibitors (ICIs).”
From Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies (2022) · cites this paper as [17]
In the citing paper
“Mouse models have verified that Bifidobacteria, Bacteroides fragilis, and Burkholderia cepacia can ameliorate intestinal immunopathology in the context of anti-CTLA-4 therapy [17, 125, 126].”
From Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies (2022) · cites this paper as [17]
In the citing paper
“Supporting this contention, we and others reported that primary responses to anti-PD-1/ PD-L1 antibodies in patients with epithelial tumours and melanoma could, at least in part, be attributed to the taxonomic composition of the gut microbial ecosystem 18,20,25 .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“Similarly, antibiotics (ATB) prior to ICI initiation drastically reduced the clinical benefit in several cohorts of patients across various cancer types (melanoma, advanced NSCLC, renal cell carcinoma (RCC), and urothelial cancer) 18,[20][21][22] .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“A diverse microbiota and the presence of specific bacteria such as Akkermansia muciniphila, Ruminococcus or Bifidobacterium genera were associated with improved clinical response to ICI, correlating with increased systemic immune tonus 18,20,25 .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“These results support the possibility that Akk could promote the elicitation or recirculation of Th1 cells into the tumor microenvironment, as previously shown in mouse models 18,19 .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“Akk was also overrepresented in patients with progression free-survival (PFS) > 3 months, when analyzing a subgroup of 60 patients with NSCLC 18 .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“We previously reported the stool metagenomic profiling of 100 patients diagnosed with refractory NSCLC or RCC receiving second or third line anti-PD-1 antibodies, concluding that the prevalence of A. muciniphila (Akk) was increased in patients presenting partial response or stable disease, as compared with patients in progressive disease (61 versus 34% respectively, p=0.007) 18 .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“We used MCA-205 fibrosarcomas because it is normally -in SPF eubiotic mice-sensitive to anti-PD-1 Ab and has been used as a reference mouse model in our previous avatar experiments reported in 18 and 37 , both papers showing that results obtained with MCA-205 were recapitulated in orthotopic TC1 lung cancer or RENCA RENal CArcinoma models, respectively.”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“These results expand on previous observations that have been made in smaller cohorts of patients with NSCLC 18,41 and provide evidence that gut microbiome diversity and composition, specifically the relative abundance of Akk, offer relevant information to predict survival of patients with NSCLC amenable to ICI.”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“Here, we provide preclinical data suggesting that Akk could therapeutically bypass the resistance to anti-PD-1 blockade conferred by FMT bereft of endogenous Akk (Extended Figure 6 and 17,18 ).”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“Of note, the 60 patients with NSCLC already described in our previous report 18 were excluded from the principal analysis.”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [18]
In the citing paper
“For immune checkpoint inhibition (ICI) therapy, mounting evidence suggests that the gut microbiome can determine patient treatment outcomes.”
From Meta-analysis of the gut microbiota in predicting response to cancer immunotherapy in metastatic melanoma (2020) · cites this paper as [13]
In the citing paper
“Recently, several studies have demonstrated that members of the gut microbiota are able to enhance the anti-tumor efficacy of PD-1 and CTLA4 blockade therapy6,7.”
From Microbial short-chain fatty acids modulate CD8+ T cell responses and improve adoptive immunotherapy for cancer (2021) · cites this paper as [6]
In the citing paper
“Recently, the gut microbiota has emerged as a potent new factor associated with the efficacy of anti–CTLA4, anti–PD-1, and anti–PD-L1 treatment (8-14).”
From Enterococcus peptidoglycan remodeling promotes checkpoint inhibitor cancer immunotherapy (2021) · cites this paper as [8]
In the citing paper
“These include TH1 immune responses directed at B. fragilis and A. muciniphila were associated with responses to the anti-CTLA4 antibody ipilimumab in patients with melanoma125 and to anti-PD-1 antibodies in patients with RCC or NSCLC, respectively42 (Table 1).”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [125]
In the citing paper
“These results confirm previous observations of biphasic effects for the Bacteroides genus dependent on the specific treatment agent(s) used9,40,41.”
From Longitudinal gut microbiome changes in immune checkpoint blockade-treated advanced melanoma (2024) · cites this paper as [41]
In the citing paper
“The intestinal microbiome has emerged as a tumor-extrinsic predictive biomarker to immune checkpoint blockade (ICB)1–6.”
From Intestinal microbiota signatures of clinical response and immune-related adverse events in melanoma patients treated with anti-PD-1 (2022) · cites this paper as [2]
In the citing paper
“In mouse models, certain gut commensals mediate efficacy of anticancer therapies, including chemotherapy, radiotherapy, and immunotherapies such as adoptive T cell transfer, intratumoral CpG-oligonucleotides, and ICIs.”
From Melanoma and microbiota: Current understanding and future directions (2024) · cites this paper as [5]
In the citing paper
“During CTLA-4 blockade in various cancers, Bacteroides fragilis triggers TLR2–4-dependent interleukin (IL)-12 release that is associated with anticancer effects.”
From Melanoma and microbiota: Current understanding and future directions (2024) · cites this paper as [5]
In the citing paper
“Second, exposures including medications, especially antibiotics and proton pump inhibitors, and diet that shape the microbiota are associated with ICI responses in patient cohorts and preclinical models.”
From Melanoma and microbiota: Current understanding and future directions (2024) · cites this paper as [5]
In the citing paper
“as the gut and tumour microbiota can affect the survival of patients with cancer and their responses to therapy8,14,40–42,50”
From Identification of bacteria-derived HLA-bound peptides in melanoma (2021) · cites this paper as [50]
In the citing paper
“The role of the gut microbiome in modulating tumor responses to immunotherapy in melanoma [5–7], non-small cell lung cancer, renal cell carcinoma, and urothelial carcinoma [6, 8] has received increased attention across a series of studies in recent years.”
From Gut microbiome affects the response to anti-PD-1 immunotherapy in patients with hepatocellular carcinoma (2019) · cites this paper as [6]
In the citing paper
“On the contrary, tumors in antibiotic-treated or germ-free mice did not respond to CTLA blockade (180).”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [180]
In the citing paper
“Moreover, in mice and patients, T cell responses specific for Bacteroides species, such as thetaiotaomicron or fragilis were associated with the efficacy of CTLA-4 blockade.”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [180]
In the citing paper
“Such as Bacteroides fragilis, Bacteroides thetaiotaomicron, Bifidobacterium, Akkermansia muciniphila and Faecalibacterium spp. have been shown to have favourable responses to cancer immunotherapy in both preclinical tumour models and patients with cancer.12–15”
In the citing paper
“Bacteroides spp. have a protective effect on gastrointestinal toxicity during CTLA-4 mAb treatment.13”
In the citing paper
“The genus Bacteroides enhance the antitumour effect and alleviate the gastrointestinal toxicity in melanoma patients treated with CTLA-4 blockade.13”
In the citing paper
“Anti-CTLA-4 treatment was found to be ineffective in mice reared under sterile conditions and to induce a shift in the gut flora of conventionally reared mice.”
From Anti-PD-1 and Anti-CTLA-4 Therapies in Cancer: Mechanisms of Action, Efficacy, and Limitations (2018) · cites this paper as [97]
In the citing paper
“Further experiments showed that the presence of certain bacterial strains, in particular Bacteroides fragilis, promoted Th1 polarization in the animals and was associated with an improved anti-tumor immune response (97).”
From Anti-PD-1 and Anti-CTLA-4 Therapies in Cancer: Mechanisms of Action, Efficacy, and Limitations (2018) · cites this paper as [97]
In the citing paper
“Anti-CTLA-4 treatment was found to be ineffective in mice reared under sterile conditions and to induce a shift in the gut flora of conventionally reared mice.”
From Anti-PD-1 and Anti-CTLA-4 Therapies in Cancer: Mechanisms of Action, Efficacy, and Limitations (2018) · cites this paper as [97]
In the citing paper
“In a similar study, administration of B. fragilis to sterile mice treated with anti-CTLA-4 resulted in reduced tumor growth, most likely by inducing a favorable shift toward Th1 responses (97).”
From Anti-PD-1 and Anti-CTLA-4 Therapies in Cancer: Mechanisms of Action, Efficacy, and Limitations (2018) · cites this paper as [97]
In the citing paper
“Analysis of fecal samples revealed that the enrichment of specific gut commensals, such as Bifidobacterium [32] and Ruminococcaceae [33], had a significant positive correlation with CD8+T cell infiltration in the tumor bed or tumor-draining lymph node.”
From Gut microbiota-mediated immunomodulation in tumor (2021) · cites this paper as [32]
In the citing paper
“Both Bacteroides fragilis [31] and Bifidobacterium [32] were reported to promote the activation and maturation of DCs.”
From Gut microbiota-mediated immunomodulation in tumor (2021) · cites this paper as [32]
In the citing paper
“Further analysis identified Bifidobacterium as a positive regulator of therapeutic response [32].”
From Gut microbiota-mediated immunomodulation in tumor (2021) · cites this paper as [32]
In the citing paper
“mice with different commensal microbes exhibited difference in melanoma growth rate and response to PD-L1 blockade, which could be eliminated by cohousing and fecal FMT [32].”
From Gut microbiota-mediated immunomodulation in tumor (2021) · cites this paper as [32]
In the citing paper
“B. fragilis and some Akkermansia species drive IL-12-dependent T H 1 responses in the context of CTLA4 or PD-1 blockade 22,48”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [48]
In the citing paper
“adjuvant signals mediated by microbial-associated molecular patterns acting on pattern recognition receptors expressed on host immune cells 30,48,49”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [48]
In the citing paper
“Adjuvant signals produced by the microbiota include lipopolysaccharide (LPS) and specific surface proteins (such as Amuc_1100 present on the surface of A. muciniphila62 ) that act on Toll-like receptors such as TLR4 and TLR2, respectively, thus increasing the immune tonus.”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [48]
In the citing paper
“In oncology, converging findings demonstrate the negative impact of ATBinduced dysbiosis in mice.”
In the citing paper
“It is noteworthy that ATB-based conditionning of tumor bearing mice blunts the efficacy of PD-1 or PD-1 þ CTLA-4 blockade in otherwise 'normal' animals, suggesting a causal link between ATB and primary resistance to ICI and immunogenic chemotherapy [9,10,30,31].”
In the citing paper
“The microbiome has been described to majorly impact tumor immunity and response to ICI10–17”
From Dietary tryptophan metabolite released by intratumoral Lactobacillus reuteri facilitates immune checkpoint inhibitor treatment (2023) · cites this paper as [11]
In the citing paper
“Other groups have also demonstrated differential bacterial signatures in the gut microbiome of patients who develop ICI-associated colitis14–16”
From Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis (2018) · cites this paper as [15]
In the citing paper
“Upon CTLA-4 blockade, intraepithelial lymphocytes damage ileal epithelial cells, stimulating the accumulation of Bacteroides fragilis and Burkholderiales spp., activating IL-12-producing dendritic cells ( D C s )a n dTh e l p e r1( T H 1) immune responses (13).”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“16S ribosomal RNA (rRNA)-based sequencing of gene amplicons and shotgun DNA sequencing of patient stool samples have identified subsets of bacteria more abundant in responding versus nonresponding patients.”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“Soon after, it was observed that several anticancer treatment modalities showed reduced therapeutic effects in germ-free mice as well as in mice treated with broad-spectrum antibiotics (11)(12)(13)(14), or in mice lacking specific immunepotentiating bacterial species originating from different vendors (15).”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“Given these considerations, it is perhaps even more striking that bacteria generally associated with health (such as Clostridiales, Ruminococcacae, Faecalibacterium spp., Akkermansia muciniphila, B. fragilis,a n dBifidobacteria) (13, 14, 18-20) or immunogenicity (Enterococci, Collinsella, and Alistipes)( 11, 13, 14, 20) were found to be abundant in responding patients.”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“However, the microbial stimulation of anticancer memory T H 1/Tc1 cell responses only partially rely on TLR2/TLR4 in the context of treatments with cyclophosphamide (16)o rC T L A -4b l o c k a d e ( 13).”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“In terms of effects on pattern recognition receptors, DCs exposed to microbes (such as B. fragilis or A. muciniphila) associated with anticancer properties induce systemic IL-12-dependent T H 1/Tc1 immune responses beneficial against tumors treated with antibody to CTLA-4 (13)orPD-1/PD-L1(14).”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“This effect depended on distinct Bacteroides species in melanoma treated with ipilimumab (13) and at least partly on Faecalibacterium (19)inmelanomaandonVerrucomicrobiacae [more specifically, A. muciniphila (14)] in lung cancer patients treated with the PD-1 inhibitors pembrolizumab or nivolumab.”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“Accordingly, B. fragilis and Burkholderia cepacia administered via gavage to mice reduced the severity of colitis induced by mAb to CTLA-4 (13,22).”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“Notably, fecal microbial transplantation (FMT) o ff e c e sf r o mp a t i e n t s( w h os h o w e dc l i n i c a lr esponse to immune checkpoint blockade) transferred a”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [13]
In the citing paper
“Of note, antibiotics (except vancomycin),4”
From Custom scoring based on ecological topology of gut microbiota associated with cancer immunotherapy outcome (2024) · cites this paper as [12]
In the citing paper
“multiple studies demonstrated the negative impact of antibiotics in the context of treatment with ICB, likely due to their detrimental impact on gut microbial diversity”
From Hallmarks of response, resistance, and toxicity to immune checkpoint blockade (2021) · cites this paper as Vetizou et al., 2015
In the citing paper
“Other bacteria like Enterococcus hirae (Viaud et al., 2013), Bacteroides fragilis (Vétizou et al., 2015), and Eubacterium sp. AM28-29 (Thomas et al., 2023) have been linked to improved responses in preclinical and clinical settings, often through mechanisms such as dendritic cell maturation and cytokine production (including IL-12).”
From Microbiota-centered interventions to boost immune checkpoint blockade therapies (2025) · cites this paper as Vétizou et al., 2015
In the citing paper
“More recently, its role in boosting ICB response was first demonstrated in mice when the gut microbiome’s influence on ICB success was suddenly recognized (Routy et al., 2018b, 2023; Vétizou et al., 2015).”
From Microbiota-centered interventions to boost immune checkpoint blockade therapies (2025) · cites this paper as Vétizou et al., 2015
In the citing paper
“For example, mouse studies have shown that B. fragilis can restore anti-CTLA-4 efficacy after antibiotic treatment or in germ-free mice (Vétizou et al., 2015).”
From Microbiota-centered interventions to boost immune checkpoint blockade therapies (2025) · cites this paper as Vétizou et al., 2015
In the citing paper
“Immune responses to other anticancer treatments, including CTLA-4 blockade194 and cyclophosphamide,195 were also associated with distinct gut microbiome configurations.”
From Interaction between microbiota and immunity in health and disease (2020) · cites this paper as [194]
In the citing paper
“Important initial insights came from murine models (Sivan et al., 2015, Vetizou et al., 2015), and many of these findings have now been validated in several patient cohorts treated with immunotherapy, specifically immune checkpoint blockade.”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Vetizou et al., 2015
In the citing paper
“oral feeding with Bacteroides fragilis in combination with either Bacteroides thetaiotaomicron or Burkholderia cepacia augmented the action of anti-CTLA-4 therapy by eliciting a Th1 response in the lymph nodes and facilitating the maturation of intra-tumoral dendritic cells”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Vetizou et al., 2015
In the citing paper
“FMT from patients having dominant Bacteroides species in their gut resulted in improved tumor control compared to FMT from patients with distinct Bacteroides or Prevotella species”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Vetizou et al., 2015
In the citing paper
“The efficacy of anti-CTLA-4 therapy was markedly reduced in GF mice and SPF mice with broad-spectrum antibiotics.”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Vetizou et al., 2015
In the citing paper
“Pre- clinical models have demonstrated an improvement in toxicity scores in anti-CTLA-4-treated mice with oral gavage of Bacteroides fragilis and Burkholderia cepacia”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Vetizou et al., 2015
In the citing paper
“demonstrating that the composition of the gut microbiota could influence the response to immune checkpoint inhibitors targeting the cytotoxic T lymphocyte antigen-4 (CTLA-4) and the programmed death receptor-1 (PD-1)”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Vetizou et al., 2015
In the citing paper
“notable changes in the abundance of gut microbiota in mice were seen following anti- CTLA-4 therapy, with a relative increase in Bacteroidales and Burkholderiales, and a decrease in Clostridiales”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Vetizou et al., 2015
In the citing paper
“In addition, fecal transplants from patients who benefitted clinically from anti-CTLA-4 therapy favored the growth of B. fragilis, linking this species with improved response.”
From Immune Checkpoint Inhibitors for the Treatment of Cancer: Clinical Impact and Mechanisms of Response and Resistance (2021) · cites this paper as [99]
In the citing paper
“For example, in preclinical models, the therapeutic response to anti-CTLA-4 therapy was found to be dependent on Bacteroides species, as germfree mice or antibiotic-treated mice did not respond to anti-CTLA-4, but response was rescued through gavage of Bacteroides fragilis (99).”
From Immune Checkpoint Inhibitors for the Treatment of Cancer: Clinical Impact and Mechanisms of Response and Resistance (2021) · cites this paper as [99]
In the citing paper
“For example, mice transplanted with liquefied and filtered stool from patients with bacteroides‐rich microbiota population respond better to CTLA4 inhibitor treatment [431].”
From Tumor microenvironment signaling and therapeutics in cancer progression (2023) · cites this paper as [431]
In the citing paper
“In GF or ATB-treated mice, activation of effector CD4+ T cells and TILs elicited by CTLA-4 blockade was considerably dampened.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“A combination of ATBs (ampicillin, colistin, and streptomycin) or imipenem alone destroyed the function of CTLA-4 inhibitors against the tumor.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“Moreover, recolonization of ATB-treated or GF mice with commensal bacteria, such as Bacteroides and Burkholderia genres, could restore the CTLA-4 blockade-mediated anticancer responses.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“In other words, management of gut microbiome elicits modification of TME and turns on a switch for the development of resistance to immune therapy, which enables tumor cells to escape immune surveillance.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“Interestingly, it was discovered that CTLA-4 blocking therapy could reverse the gut bacteria repertoire, causing a decrease in beneficial bacteria and an increase in bacteria that blunt the response to ipilimumab.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“In fact, dietary supplements with Bacteroides fragilis induced Th1 immune responses in the tumor-draining lymph nodes prompted the maturation of DCs in the TME and facilitated the restoration of the clinical response to CTLA-4 blockade.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“In this study, CTLA-4 blocking therapy was found to be effective against sarcoma, melanoma, and colon cancer in SPF mice but not in GF mice.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“These preliminary results showed that gut microbiota might be indispensable for the antitumor efficacy of anti-CTLA-4 treatment.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“Therefore, the production of cytokines may be one of the mechanisms used by the gut microbiome to alter resistance to therapy.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“The gut bacteria that significantly prolong PFS show a preserved cytokine response to PD-1-target treatment, whereas antibiotics have been demonstrated to decrease the level of cytokines in TME (67).”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“orally feeding B. fragilis induced Th1 immune response in the tumor-draining lymph nodes and catalyzed the maturation of DCs in the TME, facilitating the restoration of the clinical response to CTLA-4 blockade (67).”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [67]
In the citing paper
“Vetizou et al. demonstrated that the efficacy of anti-CTLA4 antibodies in reducing sarcoma tumor growth in mice is significantly increased when the gut microbiome is enriched in Bacteroides fragilis and Burkholderia cepacia [175].”
From Gut Microbiota and Cancer: From Pathogenesis to Therapy (2019) · cites this paper as [175]
In the citing paper
“In animals, oral gavage of Bacterioides fragilis and Burkholderia cepacia demonstrated an amelioration of such immunotherapy-associated toxic side effects [175].”
From Gut Microbiota and Cancer: From Pathogenesis to Therapy (2019) · cites this paper as [175]
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Items 1,001–1,041 of 1,041
Peric, Z., Botti, S., Stringer, J., Krawczyk, J., van der Werf, S., van Biezen, A., Aljurf, M., Murray, J., Liptrott, S., Greenfield, D. M., et al. (2018) · Bone Marrow Transplantation · doi:10.1038/s41409-018-0137-1 · Cited by 54
Li, Y., Ye, Z., Zhu, J., Fang, S., Meng, L., & Zhou, C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.844335 · Cited by 45
Kim, C. G., Koh, J.-Y., Shin, S.-J., Shin, J.-H., Hong, M., Chung, H. C., Rha, S. Y., Kim, H. S., Lee, C.-K., Lee, J. H., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.101251 · Cited by 45
The metabolic dialogue between intratumoural microbes and cancer: implications for immunotherapy
Situ, Y., Zhang, P., Zhang, C., Jiang, A., Zhang, N., Zhu, L., Mou, W., Liu, Z., Wong, H. Z. H., Zhang, J., et al. (2025) · eBioMedicine · doi:10.1016/j.ebiom.2025.105708 · Cited by 45
Age effects of distinct immune checkpoint blockade treatments in a mouse melanoma model
Padrón, Á., Hurez, V., Gupta, H. B., Clark, C. A., Pandeswara, S. L., Yuan, B., Svatek, R. S., Turk, M. J., Drerup, J. M., Li, R., et al. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2017.12.025 · Cited by 44
The intestinal microbiome influences checkpoint blockade
Sears, C. L., & Pardoll, D. M. (2018) · Nature Medicine · doi:10.1038/nm.4511 · Cited by 43
Facts and Hopes for Gut Microbiota Interventions in Cancer Immunotherapy
Davar, D., & Zarour, H. M. (2022) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-21-1129 · Cited by 40
“In addition, B. intestinalis (phylum Bacteroidetes) was linked to colitis in patients treated with anti–PD-1 and anti–CTLA-4 combination therapy (110).”
BackgroundResultInfluentialJenkins, S. V., Robeson, M. S., Griffin, R. J., Quick, C. M., Siegel, E. R., Cannon, M. J., Vang, K. B., & Dings, R. P. M. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-4108 · Cited by 41
“cytotoxic T-lymphocyte-associated protein 4 (CTLA-4; CD152) and programmed cell death protein-1 (PD-1) blockage only reduced tumor growth in mice harboring Bacteroides and Bifidobacterium species respectively (33, 34).”
BackgroundNon-Melanoma Skin Cancer: news from microbiota research
Squarzanti, D. F., Zavattaro, E., Pizzimenti, S., Amoruso, A., Savoia, P., & Azzimonti, B. (2020) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2020.1794792 · Cited by 40
Cross-reactivity between microbial and tumor antigens
Zitvogel, L., & Kroemer, G. (2022) · Current Opinion in Immunology · doi:10.1016/j.coi.2022.102171 · Cited by 40
Self-citationNetwork approach in liquidomics landscape
Santini, D., Botticelli, A., Galvano, A., Iuliani, M., Incorvaia, L., Gristina, V., Taffon, C., Foderaro, S., Paccagnella, E., Simonetti, S., et al. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02743-9 · Cited by 37
“Increasing evidence supports the role of the gut microbiota in the responsiveness and toxicities to immune-checkpoint inhibitors suggesting the utility of stool DNA beyond the detection of tumour DNA [251, 370–374].”
BackgroundComputational methods and challenges in analyzing intratumoral microbiome data
Wang, Q., Liu, Z., Ma, A., Li, Z., Liu, B., & Ma, Q. (2023) · Trends in Microbiology · doi:10.1016/j.tim.2023.01.011 · Cited by 37
Colorectal Cancer Immunotherapy: State of the Art and Future Directions
Cornista, A. M., Giolito, M. V., Baker, K., Hazime, H., Dufait, I., Datta, J., Khumukcham, S. S., De Ridder, M., Roper, J., Abreu, M. T., et al. (2023) · Gastro Hep Advances · doi:10.1016/j.gastha.2023.09.007 · Cited by 39
Castello, A., Rossi, S., Toschi, L., & Lopci, E. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10061251 · Cited by 36
Epigenetic mechanisms of tumor resistance to immunotherapy
Arenas-Ramirez, N., Sahin, D., & Boyman, O. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2908-7 · Cited by 36
Shen, Y.-C., Lee, P.-C., Kuo, Y.-L., Wu, W.-K., Chen, C.-C., Lei, C.-H., Yeh, C.-P., Hsu, C., Hsu, C.-H., Lin, Z.-Z., et al. (2021) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s315696 · Cited by 36
Guillot, N., Roméo, B., Manesh, S. S., Milano, G., Brest, P., Zitvogel, L., Hofman, P., & Mograbi, B. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.08.004 · Cited by 36
Self-citationSepich‐Poore, G. D., Guccione, C., Laplane, L., Pradeu, T., Curtius, K., & Knight, R. (2022) · BioEssays · doi:10.1002/bies.202100252 · Cited by 33
Contribution of Aging, Obesity, and Microbiota on Tumor Immunotherapy Efficacy and Toxicity
Baiden-Amissah, R. E. M., & Tuyaerts, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20143586 · Cited by 30
“Second, fecal microbiota transplantation (FMT) from cancer patients who responded to ICB into germ-free or antibiotic-treated mice ameliorated the antitumor effects of ICB, whereas FMT from non-responding patients failed to do so [66,68].”
BackgroundPietrzak, B., Tomela, K., Olejnik-Schmidt, A., Galus, Ł., Mackiewicz, J., Kaczmarek, M., Mackiewicz, A., & Schmidt, M. (2022) · Cancers · doi:10.3390/cancers14215369 · Cited by 36
The role of gut microbiota in immune checkpoint inhibitor therapy
Yi, M., Qin, S., Chu, Q., & Wu, K. (2018) · HepatoBiliary Surgery and Nutrition · doi:10.21037/hbsn.2018.11.12 · Cited by 32
Jamal, R., Messaoudene, M., de Figuieredo, M., & Routy, B. (2023) · Seminars in Immunology · doi:10.1016/j.smim.2023.101754 · Cited by 31
Self-citationBugs as drugs: The role of microbiome in cancer focusing on immunotherapeutics
Araujo, D. V., Watson, G. A., Oliva, M., Heirali, A., Coburn, B., Spreafico, A., & Siu, L. L. (2021) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2020.102125 · Cited by 29
Microbiome meets immunotherapy: unlocking the hidden predictors of immune checkpoint inhibitors
Huang, L., Li, Y., Zhang, C., Jiang, A., Zhu, L., Mou, W., Li, K., Zhang, J., Cui, C., Cui, X., et al. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00819-2 · Cited by 28
“Preclinical studies have shown that speci fi c gut microbiota, such as Bacteroides fragilis and Bi fi dobacterium , enhance CD8 + T cell in fi ltration and effectorfunctions,improvingmelanomaresponsestoICIs 21,22 .”
The Microbiota: A New Variable Impacting Cancer Treatment Outcomes
Fessler, J. L., & Gajewski, T. F. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-0864 · Cited by 24
“In parallel studies, CTLA-4 blockade was found to rely on the gut microbiota, and antitumor effects were reported to be dependent upon distinct Bacteroides species (4).”
BackgroundMessaoudene, M., Ferreira, S., Saint-Lu, N., Ponce, M., Truntzer, C., Boidot, R., Le Bescop, C., Loppinet, T., Corbel, T., Féger, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-52373-8 · Cited by 24
“…the key role of the microbiota in ICI wasgathered from antibiotic (ATB)-treated mice, where altering the microbiota by ATB inhibited responses to programmed cell death protein 1 (PD-1) blockers used alone or in combination with a cytotoxic T-lymphocyte associated protein 4 (CTLA-4) inhibitor 9,19 .”
Self-citationGut microbiota dysbiosis induced by brain tumors modulates the efficacy of immunotherapy
Kim, H. C., Kim, H.-J., La, J., Park, W. H., Park, S. H., Kang, B. H., Kim, Y., & Lee, H. K. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115825 · Cited by 23
Gut Microbiota–Related Biomarkers in Immuno-Oncology
Silva, C. A. C., Fidelle, M., Almonte, A. A., Derosa, L., & Zitvogel, L. (2025) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-061124-102218 · Cited by 22
Self-citationImpact of the ONCOBIOME network in cancer microbiome research
Zitvogel, L., Derosa, L., Routy, B., Loibl, S., Heinzerling, L., de Vries, I. J. M., Engstrand, L., ONCOBIOME Network, Silva, C. A. C., Barbieri, D., et al. (2025) · Nature Medicine · doi:10.1038/s41591-025-03608-8 · Cited by 23
“…as adjuvant signals mediated by microbial-associated molecular patterns acting on pattern recognition receptors expressed on host immune cells 30,48,49 ; molecular mimicry between microbial and tumor-associated antigens, resulting in cross-reactive T cell responses 55 ; the migration of immune…”
InfluentialSelf-citationHow does the gut microbiome influence immune checkpoint blockade therapy?
Almonte, A. A., Rangarajan, H., Yip, D., & Fahrer, A. M. (2021) · Immunology & Cell Biology · doi:10.1111/imcb.12423 · Cited by 21
“In mouse models, shortening of intestinal villi and perturbations in the gut lining have been observed following anti-CTLA-4 treatment.(34,35) This damage is reminiscent of injury caused by cyclophosphamide treatments, which were shown to allow bacteria to translocate out of the gut into secondary lymphoid organs.”
BackgroundMethodResultInfluentialThe role of host molecules in communication with the resident and pathogenic microbiota: A review
White, J. R., Dauros-Singorenko, P., Hong, J., Vanholsbeeck, F., Phillips, A., & Swift, S. (2020) · Medicine in Microecology · doi:10.1016/j.medmic.2020.100005 · Cited by 21
Najmi, M., Tran, T., Witt, R. G., & Nelson, K. C. (2022) · Dermatology and Therapy · doi:10.1007/s13555-022-00810-1 · Cited by 21
“The tumors continued to progress in the antibiotic-treated mice, but in the control mice with intact gut flora, the tumors were stable [12].”
BackgroundInfluentialMicrobiota-centered interventions to boost immune checkpoint blockade therapies
Almonte, A. A., Thomas, S., & Zitvogel, L. (2025) · Journal of Experimental Medicine · doi:10.1084/jem.20250378 · Cited by 19
Self-citationOey, O., Liu, Y.-Y., Sunjaya, A. F., Simadibrata, D. M., Khattak, M. A., & Gray, E. (2022) · World Journal of Clinical Oncology · doi:10.5306/wjco.v13.i11.929 · Cited by 15
From mucosal infection to successful cancer immunotherapy
Goubet, A.-G., Rouanne, M., Derosa, L., Kroemer, G., & Zitvogel, L. (2023) · Nature Reviews Urology · doi:10.1038/s41585-023-00784-5 · Cited by 11
“Moreover, humoral or cellular immune responses directed against a specific panel of commensals residing in the digestive tract are associated with clinical outcome to cancer therapies across different countries and continents 109,114–117 .”
BackgroundSelf-citationAntibiotics impair immunotherapy for urothelial cancer
Derosa, L., & Zitvogel, L. (2020) · Nature Reviews Urology · doi:10.1038/s41585-020-0373-1 · Cited by 9
Self-citationHarnessing Microbiota to Improve Immunotherapy for Gastrointestinal Cancers
Goc, J., & Sonnenberg, G. F. (2022) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-22-0164 · Cited by 8
Snyder, A. M., Abbott, J., Jensen, M. K., & Secrest, A. M. (2021) · World Journal of Dermatology · doi:10.5314/wjd.v9.i1.1 · Cited by 8
A precision medicine approach to pharmacological adjuncts to extinction: A call to broaden research
King, G., Baker, K. D., Bisby, M. A., Chan, D., Cowan, C. S. M., Stylianakis, A. A., Zimmermann, K. S., & Richardson, R. (2019) · Psychopharmacology · doi:10.1007/s00213-018-4999-0 · Cited by 6
El Alam, M. B., Sims, T. T., Kouzy, R., Biegert, G. W. G., Abi Jaoude, J., Karpinets, T. V., Yoshida-Court, K., Wu, X., Delgado Medrano, A. Y., Mezzari, M. P., et al. (2020) · doi:10.1101/2020.04.10.036426 · Cited by 41
Inhibiting tumor cell-intrinsic UBA6 by inosine augments tumor immunogenicity
He, B., Zhang, L., Jiang, L., Yu, L., Li, Q., Tian, X., He, J.-Q., Zeng, L., Yang, Y., Wang, C., et al. (2021) · doi:10.21203/rs.3.rs-620390/v1 · Cited by 82
Metadata
- Authors
- Vétizou, M., Pitt, J. M., Daillère, R., Lepage, P., Waldschmitt, N., Flament, C., Rusakiewicz, S., Routy, B., Roberti, M. P., Duong, C. P. M., Poirier-Colame, V., Roux, A., Becharef, S., Formenti, S., Golden, E., Cording, S., Eberl, G., Schlitzer, A., Ginhoux, F., Mani, S., Yamazaki, T., Jacquelot, N., Enot, D. P., Bérard, M., Nigou, J., Opolon, P., Eggermont, A., Woerther, P.-L., Chachaty, E., Chaput, N., Robert, C., Mateus, C., Kroemer, G., Raoult, D., Boneca, I. G., Carbonnel, F., Chamaillard, M., & Zitvogel, L.
- Affiliations
- Université Paris-Sud (FR)
- Microbiologie de l’alimentation au service de la santé (FR)
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Institut de Cancérologie Gustave Roussy Cancer Campus (GRCC), 114 rue Edouard Vaillant, 94805 Villejuif, France.
- New York University (US)
- Institut Pasteur (FR)
- Microenvironment and Immunity Unit, Institut Pasteur, Paris, France.
- Agency for Science, Technology and Research (SG)
- Albert Einstein College of Medicine (US)
- Institut Gustave Roussy (FR)
- Animalerie Centrale, Institut Pasteur, Paris, France.
- Service de microbiologie, GRCC, Villejuif, France.
- Université de la Méditerranée Aix-Marseille II (FR)
- Corresponding author
- Boneca, Ivo Gomperts
- Carbonnel, Franck
- Chamaillard, Mathias
- Zitvogel, Laurence
- ORCID
- Vétizou, Marie
- Daillère, Romain
- Lepage, Patricia
- Flament, Caroline
- Rusakiewicz, Sylvie
- Routy, Bertrand
- Duong, Connie P. M.
- Roux, Antoine
- Becharef, Sonia
- Formenti, Silvia
- Cording, Sascha
- Schlitzer, Andreas
- Ginhoux, Florent
- Mani, Sridhar
- Yamazaki, Takahiro
- Jacquelot, Nicolas
- Nigou, Jérôme
- Opolon, Paule
- Eggermont, Alexander
- Woerther, Paul-Louis
- Chaput, Nathalie
- Robert, Caroline
- Kroemer, Guido
- Raoult, Didier
- Boneca, Ivo Gomperts
- Carbonnel, Franck
- Chamaillard, Mathias
- Zitvogel, Laurence
- Venue
- Science
- Published
- 2015-11-27
- Volume
- 350
- Issue
- 6264
- Pages
- 1079-1084
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC4721659
- OpenAlex
- W2165456770
- Cited by
- 3,488
- References
- 35
- Citations by year
- 2026: 239 · 2025: 332 · 2024: 340 · 2023: 406 · 2022: 416 · 2021: 398 · 2020: 386 · 2019: 303 · 2018: 280 · 2017: 223 · 2016: 147 · 2015: 13
- FWCI
- 96.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, other-oa)
- LillOA (Université de Lille (University Of Lille)) (submittedVersion, other-oa)
- Funders
- European Commission
- Agence Nationale de la Recherche (ANR-10-LABX-0015, ANR-10-IBHU-0001)
- Fondation pour la Recherche Médicale
- Ligue Contre le Cancer
- Fondation de France
- Institut National Du Cancer
- Institut Gustave-Roussy
- Swiss Bridge Foundation
- National Cancer Institute (R01CA161879)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- CTLA-4 blockade, cancer immunotherapy, gut microbiota, Bacteroides fragilis, Bacteroides thetaiotaomicron, Bacteroidales, melanoma, germ-free mice, fecal microbiota transplantation, adoptive T cell therapy, T cell response, antibiotic therapy
- MeSH terms
- Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Ipilimumab, Adult, Aged, Aged, 80 and over, Animals, Anti-Bacterial Agents, Antibodies, Monoclonal, Bacteroides, Female, Germ-Free Life, Humans, Immunologic Memory, Immunotherapy, Intestines, Male, Melanoma, Mice, Inbred C57BL, Middle Aged, Skin Neoplasms, T-Lymphocytes, Mice, CTLA-4 Antigen, Dysbiosis
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