Obesity induces PD-1 on macrophages to suppress anti-tumour immunity.

Journal

Nature

ISSN: 1476-4687

Titre abrégé: Nature

Pays: England

ID NLM: 0410462

Informations de publication

Date de publication:
12 Jun 2024

Historique:

received: 04 11 2022

accepted: 07 05 2024

medline: 13 6 2024

pubmed: 13 6 2024

entrez: 12 6 2024

Statut: aheadofprint

Résumé

Obesity is a leading risk factor for progression and metastasis of many cancers

Identifiants

DOI: 10.1038/s41586-024-07529-3 PMID: 38867043

pubmed: 38867043

doi: 10.1038/s41586-024-07529-3

pii: 10.1038/s41586-024-07529-3

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Informations de copyright

Références

Islami, F., Goding Sauer, A., Gapstur, S. M. & Jemal, A. Proportion of cancer cases attributable to excess body weight by US state, 2011–2015. JAMA Oncol. 5, 384–392 (2019).

pubmed: 30589925 doi: 10.1001/jamaoncol.2018.5639

Sung, H. et al. Global patterns in excess body weight and the associated cancer burden. CA Cancer J. Clin. 69, 88–112 (2019).

pubmed: 30548482 doi: 10.3322/caac.21499

Choi, Y. et al. Body mass index and survival in patients with renal cell carcinoma: a clinical-based cohort and meta-analysis. Int. J. Cancer 132, 625–634 (2013).

pubmed: 22610826 doi: 10.1002/ijc.27639

Hakimi, A. A. et al. An epidemiologic and genomic investigation into the obesity paradox in renal cell carcinoma. J. Natl Cancer Inst. 105, 1862–1870 (2013).

pubmed: 24285872 pmcid: 3866155 doi: 10.1093/jnci/djt310

Schlesinger, S. et al. Postdiagnosis body mass index and risk of mortality in colorectal cancer survivors: a prospective study and meta-analysis. Cancer Causes Control 25, 1407–1418 (2014).

pubmed: 25037235 doi: 10.1007/s10552-014-0435-x

Wang, Z. et al. Paradoxical effects of obesity on T cell function during tumor progression and PD-1 checkpoint blockade. Nat. Med. 25, 141–151 (2019).

pubmed: 30420753 doi: 10.1038/s41591-018-0221-5

Cortellini, A. et al. A multicenter study of body mass index in cancer patients treated with anti-PD-1/PD-L1 immune checkpoint inhibitors: when overweight becomes favorable. J. Immunother. Cancer 7, 57 (2019).

pubmed: 30813970 pmcid: 6391761 doi: 10.1186/s40425-019-0527-y

Assumpcao, J. A. F., Pasquarelli-do-Nascimento, G., Duarte, M. S. V., Bonamino, M. H. & Magalhaes, K. G. The ambiguous role of obesity in oncology by promoting cancer but boosting antitumor immunotherapy. J. Biomed. Sci. 29, 12 (2022).

pubmed: 35164764 pmcid: 8842976 doi: 10.1186/s12929-022-00796-0

Gordon, S. R. et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature 545, 495–499 (2017).

pubmed: 28514441 pmcid: 5931375 doi: 10.1038/nature22396

Huang, X. et al. PD-1 expression by macrophages plays a pathologic role in altering microbial clearance and the innate inflammatory response to sepsis. Proc. Natl Acad. Sci. USA 106, 6303–6308 (2009).

pubmed: 19332785 pmcid: 2669369 doi: 10.1073/pnas.0809422106

Strauss, L. et al. Targeted deletion of PD-1 in myeloid cells induces antitumor immunity. Sci. Immunol. 5, eaay1863 (2020).

pubmed: 31901074 pmcid: 7183328 doi: 10.1126/sciimmunol.aay1863

Yao, A. et al. Programmed death 1 deficiency induces the polarization of macrophages/microglia to the M1 phenotype after spinal cord injury in mice. Neurotherapeutics 11, 636–650 (2014).

pubmed: 24853068 pmcid: 4121443 doi: 10.1007/s13311-013-0254-x

Avgerinos, K. I., Spyrou, N., Mantzoros, C. S. & Dalamaga, M. Obesity and cancer risk: emerging biological mechanisms and perspectives. Metab. Clin. Exp. 92, 121–135 (2019).

pubmed: 30445141 doi: 10.1016/j.metabol.2018.11.001

Calle, E. E., Rodriguez, C., Walker-Thurmond, K. & Thun, M. J. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 348, 1625–1638 (2003).

Dai, Z., Xu, Y. C. & Niu, L. Obesity and colorectal cancer risk: a meta-analysis of cohort studies. World J. Gastroenterol. 13, 4199–4206 (2007).

pubmed: 17696248 pmcid: 4250618 doi: 10.3748/wjg.v13.i31.4199

Murphy, W. J. & Longo, D. L. The surprisingly positive association between obesity and cancer immunotherapy efficacy. JAMA 321, 1247–1248 (2019).

pubmed: 30882850 doi: 10.1001/jama.2019.0463

Donnelly, D. et al. The complex relationship between body mass index and response to immune checkpoint inhibition in metastatic melanoma patients. J. Immunother. Cancer 7, 222 (2019).

pubmed: 31426863 pmcid: 6700794 doi: 10.1186/s40425-019-0699-5

Naik, G. S. et al. Complex inter-relationship of body mass index, gender and serum creatinine on survival: exploring the obesity paradox in melanoma patients treated with checkpoint inhibition. J. Immunother. Cancer 7, 89 (2019).

pubmed: 30922394 pmcid: 6440018 doi: 10.1186/s40425-019-0512-5

Sanchez, A. et al. Transcriptomic signatures related to the obesity paradox in patients with clear cell renal cell carcinoma: a cohort study. Lancet Oncol. 21, 283–293 (2020).

pubmed: 31870811 doi: 10.1016/S1470-2045(19)30797-1

Woodall, M. J., Neumann, S., Campbell, K., Pattison, S. T. & Young, S. L. The effects of obesity on anti-cancer immunity and cancer immunotherapy. Cancers 12, 1230 (2020).

pubmed: 32422865 pmcid: 7281442 doi: 10.3390/cancers12051230

Boi, S. K. et al. Obesity diminishes response to PD-1-based immunotherapies in renal cancer. J Immunother. Cancer 8, e000725 (2020).

pubmed: 33427691 pmcid: 7757487 doi: 10.1136/jitc-2020-000725

Lennon, H., Sperrin, M., Badrick, E. & Renehan, A. G. The obesity paradox in cancer: a review. Curr. Oncol. Rep. 18, 56 (2016).

pubmed: 27475805 pmcid: 4967417 doi: 10.1007/s11912-016-0539-4

Le, C. T. et al. PD-1 blockade reverses obesity-mediated T cell priming impairment. Front. Immunol. 11, 590568 (2020).

pubmed: 33193426 pmcid: 7658608 doi: 10.3389/fimmu.2020.590568

Ringel, A. E. et al. Obesity shapes metabolism in the tumor microenvironment to suppress anti-tumor immunity. Cell 183, 1848–1866 (2020).

pubmed: 33301708 pmcid: 8064125 doi: 10.1016/j.cell.2020.11.009

Chakarov, S., Bleriot, C. & Ginhoux, F. Role of adipose tissue macrophages in obesity-related disorders. J. Exp. Med. 219, e20211948 (2022).

pubmed: 35543703 pmcid: 9098652 doi: 10.1084/jem.20211948

Hamada, K. et al. Obesity strongly promotes growth of mouse MC38 colon cancer in an orthotopic-syngeneic C57BL/6 mouse model. In Vivo 36, 1643–1646 (2022).

pubmed: 35738603 pmcid: 9301442 doi: 10.21873/invivo.12875

Wagner, A. et al. Metabolic modeling of single Th17 cells reveals regulators of autoimmunity. Cell 184, 4168–4185 (2021).

pubmed: 34216539 pmcid: 8621950 doi: 10.1016/j.cell.2021.05.045

Christofides, A. et al. SHP-2 and PD-1-SHP-2 signaling regulate myeloid cell differentiation and antitumor responses. Nat. Immunol. 24, 55–68 (2023).

pubmed: 36581713 doi: 10.1038/s41590-022-01385-x

Bally, A. P. et al. NF-kappaB regulates PD-1 expression in macrophages. J. Immunol. 194, 4545–4554 (2015).

pubmed: 25810391 doi: 10.4049/jimmunol.1402550

Obradovic, A. et al. Single-cell protein activity analysis identifies recurrence-associated renal tumor macrophages. Cell 184, 2988–3005 (2021).

pubmed: 34019793 pmcid: 8479759 doi: 10.1016/j.cell.2021.04.038

Pelka, K. et al. Spatially organized multicellular immune hubs in human colorectal cancer. Cell 184, 4734–4752 (2021).

pubmed: 34450029 pmcid: 8772395 doi: 10.1016/j.cell.2021.08.003

Katzenelenbogen, Y. et al. Coupled scRNA-seq and intracellular protein activity reveal an immunosuppressive role of TREM2 in cancer. Cell 182, 872–885 (2020).

pubmed: 32783915 doi: 10.1016/j.cell.2020.06.032

Wolf, E. M., Fingleton, B. & Hasty, A. H. The therapeutic potential of TREM2 in cancer. Front. Oncol. 12, 984193 (2022).

pubmed: 36119485 pmcid: 9479103 doi: 10.3389/fonc.2022.984193

Li, W. et al. Correlation between PD-1/PD-L1 expression and polarization in tumor-associated macrophages: a key player in tumor immunotherapy. Cytokine Growth Factor Rev. 67, 49–57 (2022).

pubmed: 35871139 doi: 10.1016/j.cytogfr.2022.07.004

Schmidt, F. M. et al. Inflammatory cytokines in general and central obesity and modulating effects of physical activity. PLoS ONE 10, e0121971 (2015).

pubmed: 25781614 pmcid: 4363366 doi: 10.1371/journal.pone.0121971

Kumar, R. et al. Association of leptin with obesity and insulin resistance. Cureus 12, e12178 (2020).

pubmed: 33489589 pmcid: 7815269

Zhao, L. et al. A panel of free fatty acid ratios to predict the development of metabolic abnormalities in healthy obese individuals. Sci. Rep. 6, 28418 (2016).

pubmed: 27344992 pmcid: 4921829 doi: 10.1038/srep28418

Kono, Y. et al. Increased PD-1-positive macrophages in the tissue of gastric cancer are closely associated with poor prognosis in gastric cancer patients. BMC Cancer 20, 175 (2020).

pubmed: 32131763 pmcid: 7057626 doi: 10.1186/s12885-020-6629-6

Freemerman, A. J. et al. Myeloid Slc2a1-deficient murine model revealed macrophage activation and metabolic phenotype are fueled by GLUT1. J. Immunol. 202, 1265–1286 (2019).

pubmed: 30659108 pmcid: 6360258 doi: 10.4049/jimmunol.1800002

Wang, W. et al. Diabetic hyperglycemia promotes primary tumor progression through glycation-induced tumor extracellular matrix stiffening. Sci. Adv. 8, eabo1673 (2022).

pubmed: 36399580 pmcid: 9674287 doi: 10.1126/sciadv.abo1673

Dudzinski, S. O. et al. Leptin augments antitumor immunity in obesity by repolarizing tumor-associated macrophages. J. Immunol. 207, 3122–3130 (2021).

pubmed: 34772698 doi: 10.4049/jimmunol.2001152

Reinfeld, B. I. et al. Cell-programmed nutrient partitioning in the tumour microenvironment. Nature 593, 282–288 (2021).

pubmed: 33828302 pmcid: 8122068 doi: 10.1038/s41586-021-03442-1

Sorrelle, N. et al. Improved multiplex immunohistochemistry for immune microenvironment evaluation of mouse formalin-fixed, paraffin-embedded tissues. J. Immunol. 202, 292–299 (2019).

pubmed: 30510069 doi: 10.4049/jimmunol.1800878

Zhang, L. et al. Single-cell analyses inform mechanisms of myeloid-targeted therapies in colon cancer. Cell 181, 442–459 (2020).

pubmed: 32302573 doi: 10.1016/j.cell.2020.03.048

Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587 (2021).

pubmed: 34062119 pmcid: 8238499 doi: 10.1016/j.cell.2021.04.048

Finak, G. et al. MAST: a flexible statistical framework for assessing transcriptional changes and characterizing heterogeneity in single-cell RNA sequencing data. Genome Biol. 16, 278 (2015).

pubmed: 26653891 pmcid: 4676162 doi: 10.1186/s13059-015-0844-5