Cancer stem cell-immune cell crosstalk in tumour progression.
Journal
Nature reviews. Cancer
ISSN: 1474-1768
Titre abrégé: Nat Rev Cancer
Pays: England
ID NLM: 101124168
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
accepted:
29
04
2021
pubmed:
10
6
2021
medline:
24
9
2021
entrez:
9
6
2021
Statut:
ppublish
Résumé
Cellular heterogeneity and an immunosuppressive tumour microenvironment are independent yet synergistic drivers of tumour progression and underlie therapeutic resistance. Recent studies have highlighted the complex interaction between these cell-intrinsic and cell-extrinsic mechanisms. The reciprocal communication between cancer stem cells (CSCs) and infiltrating immune cell populations in the tumour microenvironment is a paradigm for these interactions. In this Perspective, we discuss the signalling programmes that simultaneously induce CSCs and reprogramme the immune response to facilitate tumour immune evasion, metastasis and recurrence. We further highlight biological factors that can impact the nature of CSC-immune cell communication. Finally, we discuss targeting opportunities for simultaneous regulation of the CSC niche and immunosurveillance.
Identifiants
pubmed: 34103704
doi: 10.1038/s41568-021-00366-w
pii: 10.1038/s41568-021-00366-w
pmc: PMC8740903
mid: NIHMS1762149
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
526-536Subventions
Organisme : NINDS NIH HHS
ID : R01 NS117104
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS109742
Pays : United States
Organisme : NCI NIH HHS
ID : K99 CA248611
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA245705
Pays : United States
Organisme : NCI NIH HHS
ID : F32 CA243314
Pays : United States
Informations de copyright
© 2021. Springer Nature Limited.
Références
Batlle, E. & Clevers, H. Cancer stem cells revisited. Nat. Med. 23, 1124–1134 (2017).
pubmed: 28985214
doi: 10.1038/nm.4409
Saygin, C., Matei, D., Majeti, R., Reizes, O. & Lathia, J. D. Targeting cancer stemness in the clinic: from hype to hope. Cell Stem Cell 24, 25–40 (2019).
pubmed: 30595497
doi: 10.1016/j.stem.2018.11.017
Clara, J. A., Monge, C., Yang, Y. & Takebe, N. Targeting signalling pathways and the immune microenvironment of cancer stem cells - a clinical update. Nat. Rev. Clin. Oncol. 17, 204–232 (2020).
pubmed: 31792354
doi: 10.1038/s41571-019-0293-2
Galluzzi, L., Chan, T. A., Kroemer, G., Wolchok, J. D. & Lopez-Soto, A. The hallmarks of successful anticancer immunotherapy. Sci. Transl. Med. 10, eaat7807 (2018).
pubmed: 30232229
doi: 10.1126/scitranslmed.aat7807
Hinshaw, D. C. & Shevde, L. A. The tumor microenvironment innately modulates cancer progression. Cancer Res. 79, 4557–4566 (2019).
pubmed: 31350295
pmcid: 6744958
doi: 10.1158/0008-5472.CAN-18-3962
Miranda, A. et al. Cancer stemness, intratumoral heterogeneity, and immune response across cancers. Proc. Natl Acad. Sci. USA 116, 9020–9029 (2019).
pubmed: 30996127
pmcid: 6500180
doi: 10.1073/pnas.1818210116
Engblom, C., Pfirschke, C. & Pittet, M. J. The role of myeloid cells in cancer therapies. Nat. Rev. Cancer 16, 447–462 (2016).
pubmed: 27339708
doi: 10.1038/nrc.2016.54
Davies, L. C., Jenkins, S. J., Allen, J. E. & Taylor, P. R. Tissue-resident macrophages. Nat. Immunol. 14, 986–995 (2013).
pubmed: 24048120
pmcid: 4045180
doi: 10.1038/ni.2705
Mass, E. et al. Specification of tissue-resident macrophages during organogenesis. Science 353, aaf4238 (2016).
pubmed: 27492475
pmcid: 5066309
doi: 10.1126/science.aaf4238
Raggi, C. et al. Cholangiocarcinoma stem-like subset shapes tumor-initiating niche by educating associated macrophages. J. Hepatol. 66, 102–115 (2017).
pubmed: 27593106
doi: 10.1016/j.jhep.2016.08.012
Hide, T. et al. Oligodendrocyte progenitor cells and macrophages/microglia produce glioma stem cell niches at the tumor border. EBioMedicine 30, 94–104 (2018).
pubmed: 29559295
pmcid: 5952226
doi: 10.1016/j.ebiom.2018.02.024
Huang, Y. K. et al. Macrophage spatial heterogeneity in gastric cancer defined by multiplex immunohistochemistry. Nat. Commun. 10, 3928 (2019).
pubmed: 31477692
pmcid: 6718690
doi: 10.1038/s41467-019-11788-4
Bowman, R. L. et al. Macrophage ontogeny underlies differences in tumor-specific education in brain malignancies. Cell Rep. 17, 2445–2459 (2016).
pubmed: 27840052
pmcid: 5450644
doi: 10.1016/j.celrep.2016.10.052
Cassetta, L. et al. Human tumor-associated macrophage and monocyte transcriptional landscapes reveal cancer-specific reprogramming, biomarkers, and therapeutic targets. Cancer Cell 35, 588–602 e510 (2019).
pubmed: 30930117
pmcid: 6472943
doi: 10.1016/j.ccell.2019.02.009
Hashimoto, D. et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792–804 (2013).
pubmed: 23601688
doi: 10.1016/j.immuni.2013.04.004
Ginhoux, F. & Guilliams, M. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44, 439–449 (2016).
pubmed: 26982352
doi: 10.1016/j.immuni.2016.02.024
Laviron, M. & Boissonnas, A. Ontogeny of tumor-associated macrophages. Front. Immunol. 10, 1799 (2019).
pubmed: 31417566
pmcid: 6684758
doi: 10.3389/fimmu.2019.01799
Qian, B. Z. et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475, 222–225 (2011).
pubmed: 21654748
pmcid: 3208506
doi: 10.1038/nature10138
Tao, W. et al. Dual role of WISP1 in maintaining glioma stem cells and tumor-supportive macrophages in glioblastoma. Nat. Commun. 11, 3015 (2020).
pubmed: 32541784
pmcid: 7295765
doi: 10.1038/s41467-020-16827-z
Zhou, W. et al. Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat. Cell Biol. 17, 170–182 (2015).
pubmed: 25580734
pmcid: 4312504
doi: 10.1038/ncb3090
Guo, X. et al. Single tumor-initiating cells evade immune clearance by recruiting type II macrophages. Genes Dev. 31, 247–259 (2017).
pubmed: 28223311
pmcid: 5358722
doi: 10.1101/gad.294348.116
Wu, A. et al. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol. 12, 1113–1125 (2010).
pubmed: 20667896
pmcid: 3098021
doi: 10.1093/neuonc/noq082
Yi, L. et al. Glioma-initiating cells: a predominant role in microglia/macrophages tropism to glioma. J. Neuroimmunol. 232, 75–82 (2011).
pubmed: 21056915
doi: 10.1016/j.jneuroim.2010.10.011
Guo, X., Pan, Y. & Gutmann, D. H. Genetic and genomic alterations differentially dictate low-grade glioma growth through cancer stem cell-specific chemokine recruitment of T cells and microglia. Neuro Oncol. 21, 1250–1262 (2019).
pubmed: 31111915
pmcid: 6784288
doi: 10.1093/neuonc/noz080
Jinushi, M. et al. Tumor-associated macrophages regulate tumorigenicity and anticancer drug responses of cancer stem/initiating cells. Proc. Natl Acad. Sci. USA 108, 12425–12430 (2011).
pubmed: 21746895
pmcid: 3145680
doi: 10.1073/pnas.1106645108
Fan, Q. M. et al. Tumor-associated macrophages promote cancer stem cell-like properties via transforming growth factor-beta1-induced epithelial-mesenchymal transition in hepatocellular carcinoma. Cancer Lett. 352, 160–168 (2014).
pubmed: 24892648
doi: 10.1016/j.canlet.2014.05.008
Lu, H. et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat. Cell Biol. 16, 1105–1117 (2014).
pubmed: 25266422
pmcid: 4296514
doi: 10.1038/ncb3041
Shi, Y. et al. Tumour-associated macrophages secrete pleiotrophin to promote PTPRZ1 signalling in glioblastoma stem cells for tumour growth. Nat. Commun. 8, 15080 (2017).
pubmed: 28569747
pmcid: 5461490
doi: 10.1038/ncomms15080
Wan, S. et al. Tumor-associated macrophages produce interleukin 6 and signal via STAT3 to promote expansion of human hepatocellular carcinoma stem cells. Gastroenterology 147, 1393–1404 (2014).
pubmed: 25181692
doi: 10.1053/j.gastro.2014.08.039
Zhang, B. et al. Macrophage-expressed CD51 promotes cancer stem cell properties via the TGF-beta1/smad2/3 axis in pancreatic cancer. Cancer Lett. 459, 204–215 (2019).
pubmed: 31199988
doi: 10.1016/j.canlet.2019.06.005
Su, W. et al. The Polycomb repressor complex 1 drives double-negative prostate cancer metastasis by coordinating stemness and immune suppression. Cancer Cell 36, 139–155 e110 (2019).
pubmed: 31327655
pmcid: 7210785
doi: 10.1016/j.ccell.2019.06.009
Cannarile, M. A. et al. Colony-stimulating factor 1 receptor (CSF1R) inhibitors in cancer therapy. J. Immunother. Cancer 5, 53 (2017).
pubmed: 28716061
pmcid: 5514481
doi: 10.1186/s40425-017-0257-y
Theocharides, A. P. et al. Disruption of SIRPalpha signaling in macrophages eliminates human acute myeloid leukemia stem cells in xenografts. J. Exp. Med. 209, 1883–1899 (2012).
pubmed: 22945919
pmcid: 3457732
doi: 10.1084/jem.20120502
Lee, T. K. et al. Blockade of CD47-mediated cathepsin S/protease-activated receptor 2 signaling provides a therapeutic target for hepatocellular carcinoma. Hepatology 60, 179–191 (2014).
pubmed: 24523067
doi: 10.1002/hep.27070
Cioffi, M. et al. Inhibition of CD47 effectively targets pancreatic cancer stem cells via dual mechanisms. Clin. Cancer Res. 21, 2325–2337 (2015).
pubmed: 25717063
doi: 10.1158/1078-0432.CCR-14-1399
Liu, L. et al. Anti-CD47 antibody as a targeted therapeutic agent for human lung cancer and cancer stem cells. Front. Immunol. 8, 404 (2017).
pubmed: 28484448
pmcid: 5399041
doi: 10.3389/fimmu.2017.00404
Hutter, G. et al. Microglia are effector cells of CD47-SIRPalpha antiphagocytic axis disruption against glioblastoma. Proc. Natl Acad. Sci. USA 116, 997–1006 (2019).
pubmed: 30602457
pmcid: 6338872
doi: 10.1073/pnas.1721434116
Sikic, B. I. et al. First-in-human, first-in-class phase I trial of the anti-CD47 antibody Hu5F9-G4 in patients with advanced cancers. J. Clin. Oncol. 37, 946–953 (2019).
pubmed: 30811285
pmcid: 7186585
doi: 10.1200/JCO.18.02018
Kenkel, J. A. et al. An immunosuppressive dendritic cell subset accumulates at secondary sites and promotes metastasis in pancreatic cancer. Cancer Res. 77, 4158–4170 (2017).
pubmed: 28611041
pmcid: 5550516
doi: 10.1158/0008-5472.CAN-16-2212
Barilla, R. M. et al. Specialized dendritic cells induce tumor-promoting IL-10
pubmed: 30926808
pmcid: 6441038
doi: 10.1038/s41467-019-09416-2
Grange, C. et al. Role of HLA-G and extracellular vesicles in renal cancer stem cell-induced inhibition of dendritic cell differentiation. BMC Cancer 15, 1009 (2015).
pubmed: 26704308
pmcid: 4690241
doi: 10.1186/s12885-015-2025-z
Liang, S. et al. Modulation of dendritic cell differentiation by HLA-G and ILT4 requires the IL-6–STAT3 signaling pathway. Proc. Natl Acad. Sci. USA 105, 8357–8362 (2008).
pubmed: 18550825
pmcid: 2448841
doi: 10.1073/pnas.0803341105
Hsu, Y. L. et al. Interaction between tumor-associated dendritic cells and colon cancer cells contributes to tumor progression via CXCL1. Int. J. Mol. Sci. https://doi.org/10.3390/ijms19082427 (2018).
doi: 10.3390/ijms19082427
pubmed: 30585203
pmcid: 6337379
Wang, D., Sun, H., Wei, J., Cen, B. & DuBois, R. N. CXCL1 is critical for premetastatic niche formation and metastasis in colorectal cancer. Cancer Res. 77, 3655–3665 (2017).
pubmed: 28455419
pmcid: 5877403
doi: 10.1158/0008-5472.CAN-16-3199
Lee, C. G. et al. A rare fraction of drug-resistant follicular lymphoma cancer stem cells interacts with follicular dendritic cells to maintain tumourigenic potential. Br. J. Haematol. 158, 79–90 (2012).
pubmed: 22509798
pmcid: 3374069
doi: 10.1111/j.1365-2141.2012.09123.x
Pellegatta, S. et al. Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res. 66, 10247–10252 (2006).
pubmed: 17079441
doi: 10.1158/0008-5472.CAN-06-2048
Ning, N. et al. Cancer stem cell vaccination confers significant antitumor immunity. Cancer Res. 72, 1853–1864 (2012).
pubmed: 22473314
pmcid: 3320735
doi: 10.1158/0008-5472.CAN-11-1400
Lechner, M. G. et al. Immunogenicity of murine solid tumor models as a defining feature of in vivo behavior and response to immunotherapy. J. Immunother. 36, 477–489 (2013).
pubmed: 24145359
pmcid: 3910494
doi: 10.1097/01.cji.0000436722.46675.4a
Veglia, F., Sanseviero, E. & Gabrilovich, D. I. Myeloid-derived suppressor cells in the era of increasing myeloid cell diversity. Nat. Rev. Immunol. https://doi.org/10.1038/s41577-020-00490-y (2021).
doi: 10.1038/s41577-020-00490-y
pubmed: 33526920
pmcid: 7849958
Ouzounova, M. et al. Monocytic and granulocytic myeloid derived suppressor cells differentially regulate spatiotemporal tumour plasticity during metastatic cascade. Nat. Commun. 8, 14979 (2017).
pubmed: 28382931
pmcid: 5384228
doi: 10.1038/ncomms14979
Zhou, J., Nefedova, Y., Lei, A. & Gabrilovich, D. Neutrophils and PMN-MDSC: their biological role and interaction with stromal cells. Semin. Immunol. 35, 19–28 (2018).
pubmed: 29254756
doi: 10.1016/j.smim.2017.12.004
Cui, T. X. et al. Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing microRNA101 and suppressing the corepressor CtBP2. Immunity 39, 611–621 (2013).
pubmed: 24012420
doi: 10.1016/j.immuni.2013.08.025
Panni, R. Z. et al. Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer. Cancer Immunol. Immunother. 63, 513–528 (2014).
pubmed: 24652403
pmcid: 3994288
doi: 10.1007/s00262-014-1527-x
Peng, D. et al. Myeloid-derived suppressor cells endow stem-like qualities to breast cancer cells through IL6/STAT3 and NO/NOTCH cross-talk signaling. Cancer Res. 76, 3156–3165 (2016).
pubmed: 27197152
pmcid: 4891237
doi: 10.1158/0008-5472.CAN-15-2528
Otvos, B. et al. Cancer stem cell-secreted macrophage migration inhibitory factor stimulates myeloid derived suppressor cell function and facilitates glioblastoma immune evasion. Stem Cell 34, 2026–2039 (2016).
doi: 10.1002/stem.2393
Alban, T. J. et al. Glioblastoma myeloid-derived suppressor cell subsets express differential macrophage migration inhibitory factor receptor profiles that can be targeted to reduce immune suppression. Front. Immunol. 11, 1191 (2020).
pubmed: 32625208
pmcid: 7315581
doi: 10.3389/fimmu.2020.01191
Wang, G. et al. Targeting YAP-dependent MDSC infiltration impairs tumor progression. Cancer Discov. 6, 80–95 (2016).
pubmed: 26701088
doi: 10.1158/2159-8290.CD-15-0224
Shidal, C., Singh, N. P., Nagarkatti, P. & Nagarkatti, M. MicroRNA-92 expression in CD133
pubmed: 31015227
pmcid: 6635067
Kuroda, H. et al. Prostaglandin E2 produced by myeloid-derived suppressive cells induces cancer stem cells in uterine cervical cancer. Oncotarget 9, 36317–36330 (2018).
pubmed: 30555631
pmcid: 6284736
doi: 10.18632/oncotarget.26347
Ai, L. et al. Myeloid-derived suppressor cells endow stem-like qualities to multiple myeloma cells by inducing piRNA-823 expression and DNMT3B activation. Mol. Cancer 18, 88 (2019).
pubmed: 30979371
pmcid: 6461814
doi: 10.1186/s12943-019-1011-5
Wang, Y. et al. Granulocytic myeloid-derived suppressor cells promote the stemness of colorectal cancer cells through exosomal S100A9. Adv. Sci. 6, 1901278 (2019).
doi: 10.1002/advs.201901278
Fridlender, Z. G. et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16, 183–194 (2009).
pubmed: 19732719
pmcid: 2754404
doi: 10.1016/j.ccr.2009.06.017
Zhou, S. L. et al. A positive feedback loop between cancer stem-like cells and tumor-associated neutrophils controls hepatocellular carcinoma progression. Hepatology 70, 1214–1230 (2019).
pubmed: 30933361
doi: 10.1002/hep.30630
Di Tomaso, T. et al. Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin. Cancer Res. 16, 800–813 (2010).
pubmed: 20103663
pmcid: 2842003
doi: 10.1158/1078-0432.CCR-09-2730
Volonte, A. et al. Cancer-initiating cells from colorectal cancer patients escape from T cell-mediated immunosurveillance in vitro through membrane-bound IL-4. J. Immunol. 192, 523–532 (2014).
pubmed: 24277698
doi: 10.4049/jimmunol.1301342
Morrison, B. J., Steel, J. C. & Morris, J. C. Reduction of MHC-I expression limits T-lymphocyte-mediated killing of cancer-initiating cells. BMC Cancer 18, 469 (2018).
pubmed: 29699516
pmcid: 5918869
doi: 10.1186/s12885-018-4389-3
Schatton, T. et al. Modulation of T-cell activation by malignant melanoma initiating cells. Cancer Res. 70, 697–708 (2010).
pubmed: 20068175
pmcid: 2883769
doi: 10.1158/0008-5472.CAN-09-1592
Paczulla, A. M. et al. Absence of NKG2D ligands defines leukaemia stem cells and mediates their immune evasion. Nature 572, 254–259 (2019).
pubmed: 31316209
pmcid: 6934414
doi: 10.1038/s41586-019-1410-1
Wu, A. et al. Expression of MHC I and NK ligands on human CD133+ glioma cells: possible targets of immunotherapy. J. Neurooncol. 83, 121–131 (2007).
pubmed: 17077937
doi: 10.1007/s11060-006-9265-3
Tallerico, R. et al. Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. J. Immunol. 190, 2381–2390 (2013).
pubmed: 23345327
doi: 10.4049/jimmunol.1201542
Beier, C. P. et al. The cancer stem cell subtype determines immune infiltration of glioblastoma. Stem Cell Dev. 21, 2753–2761 (2012).
doi: 10.1089/scd.2011.0660
Sharonov, G. V., Serebrovskaya, E. O., Yuzhakova, D. V., Britanova, O. V. & Chudakov, D. M. B cells, plasma cells and antibody repertoires in the tumour microenvironment. Nat. Rev. Immunol. 20, 294–307 (2020).
pubmed: 31988391
doi: 10.1038/s41577-019-0257-x
Bruchard, M. & Ghiringhelli, F. Deciphering the roles of innate lymphoid cells in cancer. Front. Immunol. 10, 656 (2019).
pubmed: 31024531
pmcid: 6462996
doi: 10.3389/fimmu.2019.00656
Lindemans, C. A. et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528, 560–564 (2015).
pubmed: 26649819
pmcid: 4720437
doi: 10.1038/nature16460
You, Y. et al. Ovarian cancer stem cells promote tumour immune privilege and invasion via CCL5 and regulatory T cells. Clin. Exp. Immunol. 191, 60–73 (2018).
pubmed: 28868628
doi: 10.1111/cei.13044
Xu, Y. et al. Sox2 communicates with Tregs through CCL1 to promote the stemness property of breast cancer cells. Stem Cell 35, 2351–2365 (2017).
doi: 10.1002/stem.2720
Chang, A. L. et al. CCL2 produced by the glioma microenvironment is essential for the recruitment of regulatory T cells and myeloid-derived suppressor cells. Cancer Res. 76, 5671–5682 (2016).
pubmed: 27530322
pmcid: 5050119
doi: 10.1158/0008-5472.CAN-16-0144
Ban, Y. et al. Targeting autocrine CCL5-CCR5 axis reprograms immunosuppressive myeloid cells and reinvigorates antitumor immunity. Cancer Res. 77, 2857–2868 (2017).
pubmed: 28416485
pmcid: 5484057
doi: 10.1158/0008-5472.CAN-16-2913
Eruslanov, E. et al. Expansion of CCR8
pubmed: 23363815
pmcid: 3618575
doi: 10.1158/1078-0432.CCR-12-2091
Curiel, T. J. et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10, 942–949 (2004).
pubmed: 15322536
doi: 10.1038/nm1093
Wainwright, D. A. et al. IDO expression in brain tumors increases the recruitment of regulatory T cells and negatively impacts survival. Clin. Cancer Res. 18, 6110–6121 (2012).
pubmed: 22932670
pmcid: 3500434
doi: 10.1158/1078-0432.CCR-12-2130
Nakano, M. et al. Dedifferentiation process driven by TGF-beta signaling enhances stem cell properties in human colorectal cancer. Oncogene 38, 780–793 (2019).
pubmed: 30181548
doi: 10.1038/s41388-018-0480-0
Ozawa, Y. et al. Indoleamine 2,3-dioxygenase 1 is highly expressed in glioma stem cells. Biochem. Biophys. Res. Commun. 524, 723–729 (2020).
pubmed: 32035622
doi: 10.1016/j.bbrc.2020.01.148
Stapelberg, M. et al. Indoleamine-2,3-dioxygenase elevated in tumor-initiating cells is suppressed by mitocans. Free Radic. Biol. Med. 67, 41–50 (2014).
pubmed: 24145120
doi: 10.1016/j.freeradbiomed.2013.10.003
Sharma, M. D. et al. Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 113, 6102–6111 (2009).
pubmed: 19366986
pmcid: 2699232
doi: 10.1182/blood-2008-12-195354
Gagliani, N. et al. Th17 cells transdifferentiate into regulatory T cells during resolution of inflammation. Nature 523, 221–225 (2015).
pubmed: 25924064
pmcid: 4498984
doi: 10.1038/nature14452
Martin, F., Apetoh, L. & Ghiringhelli, F. Controversies on the role of Th17 in cancer: a TGF-beta-dependent immunosuppressive activity? Trends Mol. Med. 18, 742–749 (2012).
pubmed: 23083809
doi: 10.1016/j.molmed.2012.09.007
Yang, S. et al. Foxp3+IL-17+ T cells promote development of cancer-initiating cells in colorectal cancer. J. Leukoc. Biol. 89, 85–91 (2011).
pubmed: 20952660
doi: 10.1189/jlb.0910506
Zhang, Y. et al. Immune cell production of interleukin 17 induces stem cell features of pancreatic intraepithelial neoplasia cells. Gastroenterology 155, 210–223 e213 (2018).
pubmed: 29604293
doi: 10.1053/j.gastro.2018.03.041
Wang, R. et al. Th17 cell-derived IL-17A promoted tumor progression via STAT3/NF-kappaB/Notch1 signaling in non-small cell lung cancer. Oncoimmunology 7, e1461303 (2018).
pubmed: 30377557
pmcid: 6205058
doi: 10.1080/2162402X.2018.1461303
He, W. et al. IL22RA1/STAT3 signaling promotes stemness and tumorigenicity in pancreatic cancer. Cancer Res. 78, 3293–3305 (2018).
pubmed: 29572224
doi: 10.1158/0008-5472.CAN-17-3131
Jiang, R. et al. IL-22 is related to development of human colon cancer by activation of STAT3. BMC Cancer 13, 59 (2013).
pubmed: 23379788
pmcid: 3607898
doi: 10.1186/1471-2407-13-59
Miao, Y. et al. Adaptive immune resistance emerges from tumor-initiating stem cells. Cell 177, 1172–1186 e1114 (2019).
pubmed: 31031009
pmcid: 6525024
doi: 10.1016/j.cell.2019.03.025
Wu, Y. et al. Increased PD-L1 expression in breast and colon cancer stem cells. Clin. Exp. Pharmacol. Physiol. 44, 602–604 (2017).
pubmed: 28107571
doi: 10.1111/1440-1681.12732
Hsu, J. M. et al. STT3-dependent PD-L1 accumulation on cancer stem cells promotes immune evasion. Nat. Commun. 9, 1908 (2018).
pubmed: 29765039
pmcid: 5954021
doi: 10.1038/s41467-018-04313-6
Zhi, Y. et al. B7H1 expression and epithelial-to-mesenchymal transition phenotypes on colorectal cancer stem-like cells. PLoS ONE 10, e0135528 (2015).
pubmed: 26284927
pmcid: 4540313
doi: 10.1371/journal.pone.0135528
Lee, Y. et al. CD44+ cells in head and neck squamous cell carcinoma suppress T-cell-mediated immunity by selective constitutive and inducible expression of PD-L1. Clin. Cancer Res. 22, 3571–3581 (2016).
pubmed: 26864211
pmcid: 5623594
doi: 10.1158/1078-0432.CCR-15-2665
Yao, Y. et al. B7-H4(B7x)-mediated cross-talk between glioma-initiating cells and macrophages via the IL6/JAK/STAT3 pathway lead to poor prognosis in glioma patients. Clin. Cancer Res. 22, 2778–2790 (2016).
pubmed: 27001312
pmcid: 4891287
doi: 10.1158/1078-0432.CCR-15-0858
Wei, J. et al. Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal transducers and activators of transcription 3 pathway. Mol. Cancer Ther. 9, 67–78 (2010).
pubmed: 20053772
pmcid: 2939737
doi: 10.1158/1535-7163.MCT-09-0734
Domenis, R. et al. Systemic T cells immunosuppression of glioma stem cell-derived exosomes is mediated by monocytic myeloid-derived suppressor cells. PLoS ONE 12, e0169932 (2017).
pubmed: 28107450
pmcid: 5249124
doi: 10.1371/journal.pone.0169932
Gabrusiewicz, K. et al. Glioblastoma stem cell-derived exosomes induce M2 macrophages and PD-L1 expression on human monocytes. Oncoimmunology 7, e1412909 (2018).
pubmed: 29632728
pmcid: 5889290
doi: 10.1080/2162402X.2017.1412909
Mirzaei, R. et al. Brain tumor-initiating cells export tenascin-C associated with exosomes to suppress T cell activity. Oncoimmunology 7, e1478647 (2018).
pubmed: 30288344
pmcid: 6169571
doi: 10.1080/2162402X.2018.1478647
Jachetti, E. et al. Tenascin-C protects cancer stem-like cells from immune surveillance by arresting T-cell activation. Cancer Res. 75, 2095–2108 (2015).
pubmed: 25808872
doi: 10.1158/0008-5472.CAN-14-2346
Stein, R. G. et al. Cognate nonlytic interactions between CD8
pubmed: 30692216
doi: 10.1158/0008-5472.CAN-18-0387
Wang, D. et al. CRISPR screening of CAR T cells and cancer stem cells reveals critical dependencies for cell-based therapies. Cancer Discov. https://doi.org/10.1158/2159-8290.CD-20-1243 (2020).
doi: 10.1158/2159-8290.CD-20-1243
pubmed: 33328215
pmcid: 8591992
Clocchiatti, A., Cora, E., Zhang, Y. & Dotto, G. P. Sexual dimorphism in cancer. Nat. Rev. Cancer 16, 330–339 (2016).
pubmed: 27079803
doi: 10.1038/nrc.2016.30
Klein, S. L. & Flanagan, K. L. Sex differences in immune responses. Nat. Rev. Immunol. 16, 626–638 (2016).
pubmed: 27546235
doi: 10.1038/nri.2016.90
Sun, T. et al. Sexually dimorphic RB inactivation underlies mesenchymal glioblastoma prevalence in males. J. Clin. Invest. 124, 4123–4133 (2014).
pubmed: 25083989
pmcid: 4151215
doi: 10.1172/JCI71048
Bayik, D. et al. Myeloid-derived suppressor cell subsets drive glioblastoma growth in a sex-specific manner. Cancer Discov. 10, 1210–1225 (2020).
pubmed: 32300059
pmcid: 7415660
doi: 10.1158/2159-8290.CD-19-1355
Fillmore, C. M. et al. Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc. Natl Acad. Sci. USA 107, 21737–21742 (2010).
pubmed: 21098263
pmcid: 3003123
doi: 10.1073/pnas.1007863107
Sun, Y. et al. Estrogen promotes stemness and invasiveness of ER-positive breast cancer cells through Gli1 activation. Mol. Cancer 13, 137 (2014).
pubmed: 24889938
pmcid: 4057898
doi: 10.1186/1476-4598-13-137
Svoronos, N. et al. Tumor cell-independent estrogen signaling drives disease progression through mobilization of myeloid-derived suppressor cells. Cancer Discov. 7, 72–85 (2017).
pubmed: 27694385
doi: 10.1158/2159-8290.CD-16-0502
Generali, D. et al. Immunomodulation of FOXP3+ regulatory T cells by the aromatase inhibitor letrozole in breast cancer patients. Clin. Cancer Res. 15, 1046–1051 (2009).
pubmed: 19188178
doi: 10.1158/1078-0432.CCR-08-1507
Sarmiento-Castro, A. et al. Increased expression of interleukin-1 receptor characterizes anti-estrogen-resistant ALDH
doi: 10.1016/j.stemcr.2020.06.020
White, M. C. et al. Age and cancer risk: a potentially modifiable relationship. Am. J. Prev. Med. 46, S7–15 (2014).
pubmed: 24512933
pmcid: 4544764
doi: 10.1016/j.amepre.2013.10.029
Ge, Y. et al. Stem cell lineage infidelity drives wound repair and cancer. Cell 169, 636–650 e614 (2017).
pubmed: 28434617
pmcid: 5510746
doi: 10.1016/j.cell.2017.03.042
Kalamakis, G. et al. Quiescence modulates stem cell maintenance and regenerative capacity in the aging brain. Cell 176, 1407–1419 e1414 (2019).
pubmed: 30827680
doi: 10.1016/j.cell.2019.01.040
Agudo, J. et al. Quiescent tissue stem cells evade immune surveillance. Immunity 48, 271–285 e275 (2018).
pubmed: 29466757
pmcid: 5824652
doi: 10.1016/j.immuni.2018.02.001
Bocci, F. et al. Toward understanding cancer stem cell heterogeneity in the tumor microenvironment. Proc. Natl Acad. Sci. USA 116, 148–157 (2019).
pubmed: 30587589
doi: 10.1073/pnas.1815345116
Kaler, P., Godasi, B. N., Augenlicht, L. & Klampfer, L. The NF-kappaB/AKT-dependent induction of Wnt signaling in colon cancer cells by macrophages and IL-1beta. Cancer Microenviron. 2, 69–80 (2009).
pubmed: 19779850
pmcid: 2787930
doi: 10.1007/s12307-009-0030-y
Pang, W. W. et al. Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc. Natl Acad. Sci. USA 108, 20012–20017 (2011).
pubmed: 22123971
pmcid: 3250139
doi: 10.1073/pnas.1116110108
Marquez, E. J. et al. Sexual-dimorphism in human immune system aging. Nat. Commun. 11, 751 (2020).
pubmed: 32029736
pmcid: 7005316
doi: 10.1038/s41467-020-14396-9
Li, Y., Wang, L., Pappan, L., Galliher-Beckley, A. & Shi, J. IL-1beta promotes stemness and invasiveness of colon cancer cells through Zeb1 activation. Mol. Cancer 11, 87 (2012).
pubmed: 23174018
pmcid: 3532073
doi: 10.1186/1476-4598-11-87
Nomura, A. et al. NFkappaB-mediated invasiveness in CD133
pubmed: 28970361
doi: 10.1158/1541-7786.MCR-17-0221
Lauby-Secretan, B. et al. Body fatness and cancer–viewpoint of the IARC Working Group. N. Engl. J. Med. 375, 794–798 (2016).
pubmed: 27557308
pmcid: 6754861
doi: 10.1056/NEJMsr1606602
Duan, Y. et al. Inflammatory links between high fat diets and diseases. Front. Immunol. 9, 2649 (2018).
pubmed: 30483273
pmcid: 6243058
doi: 10.3389/fimmu.2018.02649
Naik, S. et al. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature 550, 475–480 (2017).
pubmed: 29045388
pmcid: 5808576
doi: 10.1038/nature24271
Li, X. F. et al. Chronic inflammation-elicited liver progenitor cell conversion to liver cancer stem cell with clinical significance. Hepatology 66, 1934–1951 (2017).
pubmed: 28714104
doi: 10.1002/hep.29372
Beyaz, S. et al. High-fat diet enhances stemness and tumorigenicity of intestinal progenitors. Nature 531, 53–58 (2016).
pubmed: 26935695
pmcid: 4846772
doi: 10.1038/nature17173
Yoshimoto, S. et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499, 97–101 (2013).
pubmed: 23803760
doi: 10.1038/nature12347
David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).
pubmed: 24336217
doi: 10.1038/nature12820
Luo, Y. et al. Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche. Cell Metab. 22, 886–894 (2015).
pubmed: 26387866
doi: 10.1016/j.cmet.2015.08.020
Mitroulis, I. et al. Modulation of myelopoiesis progenitors is an integral component of trained immunity. Cell 172, 147–161 e112 (2018).
pubmed: 29328910
pmcid: 5766828
doi: 10.1016/j.cell.2017.11.034
Kaiko, G. E. et al. The colonic crypt protects stem cells from microbiota-derived metabolites. Cell 165, 1708–1720 (2016).
pubmed: 27264604
pmcid: 5026192
doi: 10.1016/j.cell.2016.05.018
Mager, L. F. et al. Microbiome-derived inosine modulates response to checkpoint inhibitor immunotherapy. Science 369, 1481–1489 (2020).
pubmed: 32792462
doi: 10.1126/science.abc3421
Gopalakrishnan, V. et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359, 97–103 (2018).
pubmed: 29097493
doi: 10.1126/science.aan4236
Matson, V. et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359, 104–108 (2018).
pubmed: 29302014
pmcid: 6707353
doi: 10.1126/science.aao3290
Routy, B. et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359, 91–97 (2018).
pubmed: 29097494
doi: 10.1126/science.aan3706
Riquelme, E. et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell 178, 795–806 e712 (2019).
pubmed: 31398337
pmcid: 7288240
doi: 10.1016/j.cell.2019.07.008
Lathia, J. D., Mack, S. C., Mulkearns-Hubert, E. E., Valentim, C. L. & Rich, J. N. Cancer stem cells in glioblastoma. Genes Dev. 29, 1203–1217 (2015).
pubmed: 26109046
pmcid: 4495393
doi: 10.1101/gad.261982.115
Yamashina, T. et al. Cancer stem-like cells derived from chemoresistant tumors have a unique capacity to prime tumorigenic myeloid cells. Cancer Res. 74, 2698–2709 (2014).
pubmed: 24638980
doi: 10.1158/0008-5472.CAN-13-2169
Sharma, S. V. et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69–80 (2010).
pubmed: 20371346
pmcid: 2851638
doi: 10.1016/j.cell.2010.02.027
Mitchem, J. B. et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res. 73, 1128–1141 (2013).
pubmed: 23221383
doi: 10.1158/0008-5472.CAN-12-2731
Raghavan, S., Mehta, P., Xie, Y., Lei, Y. L. & Mehta, G. Ovarian cancer stem cells and macrophages reciprocally interact through the WNT pathway to promote pro-tumoral and malignant phenotypes in 3D engineered microenvironments. J. Immunother. Cancer 7, 190 (2019).
pubmed: 31324218
pmcid: 6642605
doi: 10.1186/s40425-019-0666-1
Zou, S. et al. Targeting STAT3 in cancer immunotherapy. Mol. Cancer 19, 145 (2020).
pubmed: 32972405
pmcid: 7513516
doi: 10.1186/s12943-020-01258-7
Ciardiello, D., Elez, E., Tabernero, J. & Seoane, J. Clinical development of therapies targeting TGFbeta: current knowledge and future perspectives. Ann. Oncol. 31, 1336–1349 (2020).
pubmed: 32710930
doi: 10.1016/j.annonc.2020.07.009
Laplane, L. & Solary, E. Towards a classification of stem cells. eLife https://doi.org/10.7554/eLife.46563 (2019).
doi: 10.7554/eLife.46563
pubmed: 30864951
pmcid: 6415933
Naik, S., Larsen, S. B., Cowley, C. J. & Fuchs, E. Two to Tango: dialog between immunity and stem cells in health and disease. Cell 175, 908–920 (2018).
pubmed: 30388451
pmcid: 6294328
doi: 10.1016/j.cell.2018.08.071
Sehgal, A. et al. The role of CSF1R-dependent macrophages in control of the intestinal stem-cell niche. Nat. Commun. 9, 1272 (2018).
pubmed: 29593242
pmcid: 5871851
doi: 10.1038/s41467-018-03638-6
Chow, A. et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J. Exp. Med. 208, 261–271 (2011).
pubmed: 21282381
pmcid: 3039855
doi: 10.1084/jem.20101688
Gyorki, D. E., Asselin-Labat, M. L., van Rooijen, N., Lindeman, G. J. & Visvader, J. E. Resident macrophages influence stem cell activity in the mammary gland. Breast Cancer Res. 11, R62 (2009).
pubmed: 19706193
pmcid: 2750124
doi: 10.1186/bcr2353
Van Nguyen, A. & Pollard, J. W. Colony stimulating factor-1 is required to recruit macrophages into the mammary gland to facilitate mammary ductal outgrowth. Dev. Biol. 247, 11–25 (2002).
pubmed: 12074549
doi: 10.1006/dbio.2002.0669
Chakrabarti, R. et al. Notch ligand Dll1 mediates cross-talk between mammary stem cells and the macrophageal niche. Science https://doi.org/10.1126/science.aan4153 (2018).
doi: 10.1126/science.aan4153
pubmed: 29773667
pmcid: 7881440
Chen, C. C. et al. Organ-level quorum sensing directs regeneration in hair stem cell populations. Cell 161, 277–290 (2015).
pubmed: 25860610
pmcid: 4393531
doi: 10.1016/j.cell.2015.02.016
Fujisaki, J. et al. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 474, 216–219 (2011).
pubmed: 21654805
pmcid: 3725645
doi: 10.1038/nature10160
Ali, N. et al. Regulatory T cells in skin facilitate epithelial stem cell differentiation. Cell 169, 1119–1129 e1111 (2017).
pubmed: 28552347
pmcid: 5504703
doi: 10.1016/j.cell.2017.05.002
Hirata, Y. et al. CD150
pubmed: 29456159
pmcid: 6534147
doi: 10.1016/j.stem.2018.01.017
Biton, M. et al. T helper cell cytokines modulate intestinal stem cell renewal and differentiation. Cell 175, 1307–1320 e1322 (2018).
pubmed: 30392957
pmcid: 6239889
doi: 10.1016/j.cell.2018.10.008
Bellomo, C., Caja, L. & Moustakas, A. Transforming growth factor beta as regulator of cancer stemness and metastasis. Br. J. Cancer 115, 761–769 (2016).
pubmed: 27537386
pmcid: 5046208
doi: 10.1038/bjc.2016.255