Single-cell profiling defines the prognostic benefit of CD39
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
22 09 2021
22 09 2021
Historique:
received:
09
08
2020
accepted:
12
08
2021
entrez:
23
9
2021
pubmed:
24
9
2021
medline:
15
12
2021
Statut:
epublish
Résumé
Luminal-like breast cancer (BC) constitutes the majority of BC subtypes, but, differently from highly aggressive triple negative BC, is poorly infiltrated by the immune system. The quality of the immune infiltrate in luminal-like BCs has been poorly studied, thereby limiting further investigation of immunotherapeutic strategies. By using high-dimensional single-cell technologies, we identify heterogeneous behavior within the tissue-resident memory CD8+ T (Trm) cells infiltrating luminal-like tumors. A subset of CD127- CD39
Identifiants
pubmed: 34552178
doi: 10.1038/s42003-021-02595-z
pii: 10.1038/s42003-021-02595-z
pmc: PMC8458450
doi:
Substances chimiques
Apyrase
EC 3.6.1.5
ENTPD1 protein, human
EC 3.6.1.5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1117Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2021. The Author(s).
Références
Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011).
pubmed: 21376230
doi: 10.1016/j.cell.2011.02.013
Sorlie, T. et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl Acad. Sci. USA 100, 8418–8423 (2003).
pubmed: 12829800
pmcid: 166244
doi: 10.1073/pnas.0932692100
Xu, J. et al. Elevated tumor mutation burden and immunogenic activity in patients with hormone receptor-negative or human epidermal growth factor receptor 2-positive breast cancer. Oncol. Lett. 18, 449–455 (2019).
pubmed: 31289516
pmcid: 6540262
Denkert, C. et al. Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy. Lancet Oncol. 19, 40–50 (2018).
pubmed: 29233559
doi: 10.1016/S1470-2045(17)30904-X
Loi, S. et al. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann. Oncol. 25, 1544–1550 (2014).
pubmed: 24608200
doi: 10.1093/annonc/mdu112
Loi, S. et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02–98. J. Clin. Oncol. 31, 860–867 (2013).
pubmed: 23341518
doi: 10.1200/JCO.2011.41.0902
Adams, S. et al. Prognostic value of tumor-infiltrating lymphocytes in triple-negative breast cancers from two phase III randomized adjuvant breast cancer trials: ECOG 2197 and ECOG 1199. J. Clin. Oncol. 32, 2959–2966 (2014).
pubmed: 25071121
pmcid: 4162494
doi: 10.1200/JCO.2013.55.0491
Dieci, M. V. et al. Prognostic value of tumor-infiltrating lymphocytes on residual disease after primary chemotherapy for triple-negative breast cancer: a retrospective multicenter study. Ann. Oncol. 25, 611–618 (2014).
pubmed: 24401929
pmcid: 3933248
doi: 10.1093/annonc/mdt556
Goel, S. et al. CDK4/6 inhibition triggers anti-tumour immunity. Nature 548, 471–475 (2017).
pubmed: 28813415
pmcid: 5570667
doi: 10.1038/nature23465
Wagner, J. et al. A single-cell atlas of the tumor and immune ecosystem of human breast cancer. Cell 177, 1330–1345 e1318 (2019).
pubmed: 30982598
pmcid: 6526772
doi: 10.1016/j.cell.2019.03.005
Azizi, E. et al. Single-cell map of diverse immune phenotypes in the breast tumor microenvironment. Cell 174, 1293–1308 e1236 (2018).
pubmed: 29961579
pmcid: 6348010
doi: 10.1016/j.cell.2018.05.060
Savas, P. et al. Single-cell profiling of breast cancer T cells reveals a tissue-resident memory subset associated with improved prognosis. Nat. Med. 24, 986–993 (2018).
pubmed: 29942092
doi: 10.1038/s41591-018-0078-7
Egelston, C. A. et al. Human breast tumor-infiltrating CD8(+) T cells retain polyfunctionality despite PD-1 expression. Nat. Commun. 9, 4297 (2018).
pubmed: 30327458
pmcid: 6191461
doi: 10.1038/s41467-018-06653-9
Kumar, B. V. et al. Human tissue-resident memory T cells are defined by core transcriptional and functional signatures in lymphoid and mucosal sites. Cell Rep. 20, 2921–2934 (2017).
pubmed: 28930685
pmcid: 5646692
doi: 10.1016/j.celrep.2017.08.078
Duhen, T. et al. Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors. Nat. Commun. 9, 2724 (2018).
pubmed: 30006565
pmcid: 6045647
doi: 10.1038/s41467-018-05072-0
Simoni, Y. et al. Bystander CD8(+) T cells are abundant and phenotypically distinct in human tumour infiltrates. Nature 557, 575–579 (2018).
pubmed: 29769722
doi: 10.1038/s41586-018-0130-2
Ganesan, A. P. et al. Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer. Nat. Immunol. 18, 940–950 (2017).
pubmed: 28628092
pmcid: 6036910
doi: 10.1038/ni.3775
Djenidi, F. et al. CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J. Immunol. 194, 3475–3486 (2015).
pubmed: 25725111
doi: 10.4049/jimmunol.1402711
Brummelman, J. et al. High-dimensional single cell analysis identifies stem-like cytotoxic CD8(+) T cells infiltrating human tumors. J. Exp. Med. 215, 2520–2535 (2018).
pubmed: 30154266
pmcid: 6170179
doi: 10.1084/jem.20180684
Chevrier, S. et al. An immune atlas of clear cell renal cell carcinoma. Cell 169, 736–749 e718 (2017).
pubmed: 28475899
pmcid: 5422211
doi: 10.1016/j.cell.2017.04.016
Wang, Z. Q. et al. CD103 and intratumoral immune response in breast cancer. Clin. Cancer Res. 22, 6290–6297 (2016).
pubmed: 27267849
doi: 10.1158/1078-0432.CCR-16-0732
van Montfoort, N. et al. NKG2A blockade potentiates CD8 T cell immunity induced by cancer vaccines. Cell 175, 1744–1755 e1715 (2018).
pubmed: 30503208
pmcid: 6354585
doi: 10.1016/j.cell.2018.10.028
Clarke, J. et al. Single-cell transcriptomic analysis of tissue-resident memory T cells in human lung cancer. J. Exp. Med. 216, 2128–2149 (2019).
pubmed: 31227543
pmcid: 6719422
doi: 10.1084/jem.20190249
Gautam, S. et al. The transcription factor c-Myb regulates CD8(+) T cell stemness and antitumor immunity. Nat. Immunol. 20, 337–349 (2019).
pubmed: 30778251
pmcid: 6489499
doi: 10.1038/s41590-018-0311-z
Doedens, A. L. et al. Molecular programming of tumor-infiltrating CD8+ T cells and IL15 resistance. Cancer Immunol. Res. 4, 799–811 (2016).
pubmed: 27485135
pmcid: 5010943
doi: 10.1158/2326-6066.CIR-15-0178
Kuwahara, M. et al. The transcription factor Sox4 is a downstream target of signaling by the cytokine TGF-beta and suppresses T(H)2 differentiation. Nat. Immunol. 13, 778–786 (2012).
pubmed: 22751141
pmcid: 3477402
doi: 10.1038/ni.2362
Kecha, O. et al. Involvement of insulin-like growth factors in early T cell development: a study using fetal thymic organ cultures. Endocrinology 141, 1209–1217 (2000).
pubmed: 10698198
doi: 10.1210/endo.141.3.7360
Zhang, L. & Romero, P. Metabolic control of CD8(+) T cell fate decisions and antitumor immunity. Trends Mol. Med. 24, 30–48 (2018).
pubmed: 29246759
doi: 10.1016/j.molmed.2017.11.005
Banerjee, A. et al. Lack of p53 augments antitumor functions in cytolytic T cells. Cancer Res. 76, 5229–5240 (2016).
pubmed: 27466285
pmcid: 5026612
doi: 10.1158/0008-5472.CAN-15-1798
Pearce, E. L. et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460, 103–107 (2009).
pubmed: 19494812
pmcid: 2803086
doi: 10.1038/nature08097
Muller, D. N., Wilck, N., Haase, S., Kleinewietfeld, M. & Linker, R. A. Sodium in the microenvironment regulates immune responses and tissue homeostasis. Nat. Rev. Immunol. 19, 243–254 (2019).
pubmed: 30644452
doi: 10.1038/s41577-018-0113-4
Eil, R. et al. Ionic immune suppression within the tumour microenvironment limits T cell effector function. Nature 537, 539–543 (2016).
pubmed: 27626381
pmcid: 5204372
doi: 10.1038/nature19364
Sim, J. H. et al. Differentially expressed potassium channels are associated with function of human effector memory CD8(+) T cells. Front. Immunol. 8, 859 (2017).
pubmed: 28791017
pmcid: 5522836
doi: 10.3389/fimmu.2017.00859
Curtis, C. et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486, 346–352 (2012).
pubmed: 22522925
pmcid: 3440846
doi: 10.1038/nature10983
Alvisi, G. et al. IRF4 instructs effector Treg differentiation and immune suppression in human cancer. J. Clin. Investig. 130, 3137–3150 (2020).
pubmed: 32125291
pmcid: 7260038
doi: 10.1172/JCI130426
Pan, H. et al. 20-year risks of breast-cancer recurrence after stopping endocrine therapy at 5 years. N. Engl. J. Med. 377, 1836–1846 (2017).
pubmed: 29117498
pmcid: 5734609
doi: 10.1056/NEJMoa1701830
Galletti, G. et al. Two subsets of stem-like CD8(+) memory T cell progenitors with distinct fate commitments in humans. Nat. Immunol. 21, 1552–1562 (2020).
pubmed: 33046887
pmcid: 7610790
doi: 10.1038/s41590-020-0791-5
Tallon de Lara, P. et al. CD39(+)PD-1(+)CD8(+) T cells mediate metastatic dormancy in breast cancer. Nat. Commun. 12, 769 (2021).
pubmed: 33536445
pmcid: 7859213
doi: 10.1038/s41467-021-21045-2
Brummelman, J. et al. Development, application and computational analysis of high-dimensional fluorescent antibody panels for single-cell flow cytometry. Nat. Protoc. 14, 1946–1969 (2019).
pubmed: 31160786
doi: 10.1038/s41596-019-0166-2
Lugli, E., Zanon, V., Mavilio, D. & Roberto, A. FACS analysis of memory T lymphocytes. Methods Mol. Biol. 1514, 31–47 (2017).
pubmed: 27787790
doi: 10.1007/978-1-4939-6548-9_3
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F. & Regev, A. Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33, 495–502 (2015).
pubmed: 25867923
pmcid: 4430369
doi: 10.1038/nbt.3192
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308
doi: 10.1093/bioinformatics/btp616
Cerami, E. et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2, 401–404 (2012).
pubmed: 22588877
doi: 10.1158/2159-8290.CD-12-0095