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Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling
Open accessAbstract
Lymphodepletion with total body irradiation (TBI) increases the efficacy of adoptively transferred tumor-specific CD8(+) T cells by depleting inhibitory lymphocytes and increasing homeostatic cytokine levels. We found that TBI augmented the function of adoptively transferred CD8(+) T cells in mice genetically deficient in all lymphocytes, indicating the existence of another TBI mechanism of action. Additional investigation revealed commensal gut microflora in the mesenteric lymph nodes and elevated LPS levels in the sera of irradiated mice. These findings correlated with increased dendritic cell activation and heightened levels of systemic inflammatory cytokines. Reduction of host microflora using antibiotics, neutralization of serum LPS using polymyxin B, or removal of LPS signaling components using mice genetically deficient in CD14 and TLR4 reduced the beneficial effects of TBI on tumor regression. Conversely, administration of microbial ligand-containing serum or ultrapure LPS from irradiated animals to nonirradiated antibody-lymphodepleted mice enhanced CD8(+) T cell activation and improved tumor regression. Administration of ultrapure LPS to irradiated animals further enhanced the number and function of the adoptively transferred cells, leading to long-term cure of mice with large B16F10 tumors and enhanced autoimmune vitiligo. Thus, disruption of the homeostatic balance between the host and microbes can enhance cell-based tumor immunotherapy.
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“A number of studies have shown that the gut microbiome may influence anti-tumor immune responses via innate and adaptive immunity (11, 12)”
From Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients (2018) · cites this paper as [11]
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 [2]
In the citing paper
“total-body irradiation, which enhanced the efficacy of tumor-specific T cell transfer through translocation of a bacterial product, the toll-like receptor 4L (TLR4L) lipopolysaccharide, from the intestinal lumen to secondary lymphoid organs (10).”
From The microbiome in cancer immunotherapy: Diagnostic tools and therapeutic strategies (2018) · cites this paper as [10]
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“administration of antibiotics significantly abrogated anti-tumor activity in a murine model of adoptive cell therapy for melanoma”
From The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy (2018) · cites this paper as Paulos et al., 2007
In the citing paper
“For example, the widely studied bacterial lipopolysaccharide (LPS), a major component of the outer membrane in gram-negative bacteria, activates the host’s cell surface receptor toll-like receptor 4 (TLR4), belonging to the family of pattern recognition receptors (PRRs), thus activating immune T cell-mediated response against cancer cells [40].”
From Gut Microbiota and Cancer: From Pathogenesis to Therapy (2019) · cites this paper as [40]
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Baecklund, T. M., Morrison, J., Donaldson, M. E., Hueffer, K., & Kyle, C. J. (2021) · PLoS ONE · doi:10.1371/journal.pone.0249176 · Cited by 2
The role of microbiota and immune system crosstalk in cancer development and therapy
Behrouzi, A., Katebi, A., Riazi‐Rad, F., Mazaheri, H., & Ajdary, S. (2022) · Acta Microbiologica et Immunologica Hungarica · doi:10.1556/030.2022.01650 · Cited by 2
“Knockout of LPS signaling components (including CD14 or TLR4), antibiotic sterilization of the gut, or inhibition of LPS by polymyxin B reduced the destruction of tumors by the adoptively transferred cells [41].”
BackgroundImmunogenic Cell Death in Cancer
Humeau, J., Naour, J. L., Kroemer, G., & Pol, J. G. (2023) · Interdisciplinary cancer research · doi:10.1007/16833_2022_121 · Cited by 2
Ketogenic Diet Therapy for Glioma: Combined Effects
Qin, H., Zhang, F., & Gao, S. (2023) · Current Cancer Therapy Reviews · doi:10.2174/1573394719666230717160843 · Cited by 2
Wang, S., Yuan, Z., Gao, X., Wu, J., Ren, Y., Yu, X., Li, J., & Wei, W. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1414196 · Cited by 2
“Emerging research has demonstrated that gut microbiota may enhance the radiosensitivity (Crawford and Gordon, 2005; Paulos et al., 2007; Cui et al., 2016).”
BackgroundDissecting the causal links between gut microbiome, immune traits and polyp using genetic evidence
Zhou, C., Ye, X., Liu, Z., Liu, T., Li, S., Yang, J., Wei, J., Yu, P., Jia, R., & Zhao, W. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1431990 · Cited by 2
The microbiome and lung cancer: microbial effects on host immune responses and treatment outcomes
Bailey, A., Leuther, K. K., & Robinson, L. A. (2025) · Frontiers in Microbiomes · doi:10.3389/frmbi.2025.1606551 · Cited by 3
Wang, F., & Yang, Y. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.09.078 · Cited by 2
RetractedStubborn Tregs limit T-cell therapy
Klebanoff, C. A., & Gattinoni, L. (2012) · Blood · doi:10.1182/blood-2012-08-445239 · Cited by 2
Self-citationCAR T Cells: Precision Cancer Immunotherapy
Meiliana, A., Dewi, N. M., & Wijaya, A. (2018) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v10i3.635 · Cited by 3
Guth, A., & DOW, S. W. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-2362-5.00013-x · Cited by 3
Combinatorial Strategies for T Lymphocyte-Based Cancer Immunotherapy
Hargadon, K. M., & Wall, J. B. (2022) · Springer eBooks · doi:10.1007/978-3-030-80962-1_211-1 · Cited by 2
The Synergy Between Ionizing Radiation and Immunotherapy in the Treatment of Prostate Cancer
Sathianathen, N. J., Krishna, S. R., Konety, B. R., & Griffith, T. S. (2017) · Immunotherapy · doi:10.2217/imt-2017-0051 · Cited by 2
Antibiotic Treatment and Immune Checkpoint Inhibitor Therapy in Patients With Cancer—Reply
Pinato, D. J., Newsom-Davis, T. E., & Bower, M. (2020) · JAMA Oncology · doi:10.1001/jamaoncol.2019.6868 · Cited by 2
Johnson, C. B., Salem, M. L., Mehrotra, S., Cole, D. J., & Rubinstein, M. P. (2013) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0001432.pub3 · Cited by 2
Kwon, S. K., Kim, N., & Park, Y. J. (2021) · International Journal of Thyroidology · doi:10.11106/ijt.2021.14.2.117 · Cited by 1
Hayabuchi, H., Tokifuji, Y., Takahashi, H., Amagai, M., Yoshimura, A., & Chikuma, S. (2024) · International Immunology · doi:10.1093/intimm/dxae018 · Cited by 1
“TBI causes bacterial translocation, activating innate immune cells that prime strong expansion and activation of cytotoxic T cells in a cancer setting (53).”
BackgroundZhang, T., Cui, K., Liu, X., Han, Y., Li, L., Xie, J., Dong, X., Bao, Y., Ren, S., Lei, Z., et al. (2025) · Cancer Pathogenesis and Therapy · doi:10.1016/j.cpt.2024.12.003 · Cited by 1
“17,18 Camrelizumab is a highly selective, high-af fi nity, humanized monoclonal anti-programmed cell death 1 (PD-1) antibody, that has shown therapeutic ef fi cacy against various malignancies.”
The multipotential effect of microbiome in lung cancer development and progression
Karimi, N., Anda, A. B. D., Yang, R., Aksan, E., Grimaldo, M. T., & Moghaddam, S. J. (2025) · International review of cytology · doi:10.1016/bs.ircmb.2024.12.011 · Cited by 1
Arjmand, B., Badamchizadeh, S., Mehran, P., Sarvari, M., Alavi-Moghadam, S., Arjmand, R., Rezaei–Tavirani, M., Janbabaei, G., Vaezi, M., & Larijani, B. A. (2025) · Stem Cell Reviews and Reports · doi:10.1007/s12015-025-10958-w · Cited by 1
Combinatorial Strategies for T Lymphocyte-Based Cancer Immunotherapy
Hargadon, K. M., & Wall, J. B. (2025) · Springer eBooks · doi:10.1007/978-3-032-00767-4_211 · Cited by 1
Adverse Effects of CAR T-Cell Therapy and Management: Cytokine Release Syndrome and Neurotoxicity
Kushwaha, M., Kumar, V., Khodlan, P., Verma, S., Teotia, A., Singh, R., Singh, A. K., Kumar, U., & Kumar, A. (2026) · Springer eBooks · doi:10.1007/978-981-95-3628-3_6 · Cited by 1
Chowdhary, R., Goyal, M. K., Arora, K., Sehgal, T., Dawer, P., Anirudh, Berinstein, J. A., Bishu, S., & Matt-Amaral, L. B. (2026) · JGH Open · doi:10.1002/jgh3.70409 · Cited by 1
“It is thought that a healthy microbiota “primes” the systemic immune system, for example by increasing the pool of effector CD8 + T cells or modulating myeloid cells in a way that enhances anti-tumor immunity in the lung microenvironment [33, 74, 75].”
Targeting the intratumoral microbiota to overcome cancer immunotherapy resistance
Tang, B., Jiang, T., Lin, Y. N., Zhang, W., Fan, H., Yang, M., Li, B., Liu, Y., Li, C., Xl, J., et al. (2026) · Interdisciplinary medicine · doi:10.1002/inmd.70155 · Cited by 1
Li, X., Zuo-Quan, X., & Geng, M. (2026) · Acta Pharmacologica Sinica · doi:10.1038/s41401-026-01882-x · Cited by 1
“For example, cipro fl oxacin treatment has been reported to reduce ACT-mediated tumor control, whereas total body irradiation (TBI) preconditioning can promote microbial translocation and enhance adoptively transferred T cell expansion in a manner dependent on LPS – TLR4 signaling [123].”
Paulos, C. M., Nelson, M. H., & Yu, X. (2014) · Springer eBooks · doi:10.1007/978-1-4899-8056-4_2 · Cited by 1
Self-citationSalem, M. L., Hammad, S. M., El-Shanshory, M. R., Attia, M. A., & Zidan, A. A. (2014) · InTech eBooks · doi:10.5772/58575 · Cited by 2
“Recent studies, including ours have demonstrated the adjuvant effects of TLRLs to ACT in lympho‐ depleted hosts [112-114].”
ResultOrigins of cancer: tackling provocative questions
Solitro, A. R., & Schaaf, N. A. V. (2017) · Genes & Cancer · doi:10.18632/genesandcancer.150 · Cited by 1
“Paulos finds that treatment with the antibiotic Ciprofloxacin diminishes the benefit of lymphodepletion, suggesting that bacteria are partially responsible [14].”
Background
Metadata
- Authors
- Paulos, C. M., Wrzesinski, C., Kaiser, Hinrichs, C. S., Chieppa, M., Cassard, L., Palmer, D. C., Boni, A., Muranski, P., Yu, Z., Gattinoni, L., Antony, P. A., Rosenberg, S. A., & Restifo, N. P.
- Affiliations
- National Institutes of Health (US)
- National Cancer Institute (US)
- Johns Hopkins University (US)
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2007-08-01
- Volume
- 117
- Issue
- 8
- Pages
- 2197-2204
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC1924500
- OpenAlex
- W2153512326
- Cited by
- 586
- References
- 63
- Citations by year
- 2026: 20 · 2025: 43 · 2024: 40 · 2023: 42 · 2022: 42 · 2021: 51 · 2020: 49 · 2019: 36 · 2018: 26 · 2017: 32 · 2016: 23 · 2015: 29 · 2014: 27 · 2013: 20 · 2012: 23
- FWCI
- 8.55
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- AIRUS (submittedVersion)
- Funders
- National Institutes of Health (Z99 CA999999)
- National Cancer Institute (Z01BC010763)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- microbial translocation, total body irradiation, lymphocyte depletion, adoptive T cell therapy, CD8+ T cells, TLR4 signaling, lipopolysaccharide, commensal gut microbiota, dendritic cell activation, inflammatory cytokines, cancer immunotherapy, B16F10 melanoma, vitiligo, CD14
- MeSH terms
- Animals, Anti-Bacterial Agents, Autoimmune Diseases, Intestines, Lipopolysaccharides, Lymphocyte Depletion, Lymphocyte Activation, Neoplasm Transplantation, Neoplasms, Experimental, Polymyxin B, Vitiligo, Whole-Body Irradiation, Signal Transduction, Autoimmunity, Cytokines, CD8-Positive T-Lymphocytes, Lipopolysaccharide Receptors, Bacterial Translocation, Adoptive Transfer, Cell Line, Tumor, Toll-Like Receptor 4, Mice
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