A decade of checkpoint blockade immunotherapy in melanoma: understanding the molecular basis for immune sensitivity and resistance.

Humans Immune Checkpoint Inhibitors Immunotherapy Ipilimumab / therapeutic use Melanoma / drug therapy Tumor Microenvironment

Journal

Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354

Informations de publication

Date de publication:
05 2022
Historique:
received: 18 09 2021
accepted: 18 01 2022
pubmed: 5 3 2022
medline: 18 5 2022
entrez: 4 3 2022
Statut: ppublish

Résumé

Ten years since the immune checkpoint inhibitor ipilimumab was approved for advanced melanoma, it is time to reflect on the lessons learned regarding modulation of the immune system to treat cancer and on novel approaches to further extend the efficacy of current and emerging immunotherapies. Here, we review the studies that led to our current understanding of the melanoma immune microenvironment in humans and the mechanistic work supporting these observations. We discuss how this information is guiding more precise analyses of the mechanisms of action of immune checkpoint blockade and novel immunotherapeutic approaches. Lastly, we review emerging evidence supporting the negative impact of melanoma metabolic adaptation on anti-tumor immunity and discuss how to counteract such mechanisms for more successful use of immunotherapy.

Identifiants

DOI: 10.1038/s41590-022-01141-1 PMID: 35241833 PMC: PMC9106900
pubmed: 35241833
doi: 10.1038/s41590-022-01141-1
pii: 10.1038/s41590-022-01141-1
pmc: PMC9106900
mid: NIHMS1799423
doi:

Substances chimiques

Immune Checkpoint Inhibitors 0
Ipilimumab 0

Types de publication

Journal Article Review Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

660-670

Subventions

Organisme : NCI NIH HHS
ID : K08 CA230157
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA192937
Pays : United States

Informations de copyright

© 2022. Springer Nature America, Inc.

Références

Jakob, J. A. et al. NRAS mutation status is an independent prognostic factor in metastatic melanoma. Cancer 118, 4014–4023 (2012).
pubmed: 22180178 doi: 10.1002/cncr.26724
Cohen, B. E., Manga, P., Lin, K. & Elbuluk, N. Vitiligo and melanoma-associated vitiligo: understanding their similarities and differences. Am. J. Clin. Dermatol. 21, 669–680 (2020).
pubmed: 32468356 doi: 10.1007/s40257-020-00524-0
Clark, W. H. Jr, From, L., Bernardino, E. A. & Mihm, M. C. The histogenesis and biologic behavior of primary human malignant melanomas of the skin. Cancer Res. 29, 705–727 (1969).
pubmed: 5773814
Clark, W. H. Jr. et al. Model predicting survival in stage I melanoma based on tumor progression. J. Natl Cancer Inst. 81, 1893–1904 (1989).
pubmed: 2593166 doi: 10.1093/jnci/81.24.1893
Clemente, C. G. et al. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 77, 1303–1310 (1996).
pubmed: 8608507 doi: 10.1002/(SICI)1097-0142(19960401)77:7<1303::AID-CNCR12>3.0.CO;2-5
Azimi, F. et al. Tumor-infiltrating lymphocyte grade is an independent predictor of sentinel lymph node status and survival in patients with cutaneous melanoma. J. Clin. Oncol. 30, 2678–2683 (2012).
pubmed: 22711850 doi: 10.1200/JCO.2011.37.8539
Thomas, N. E. et al. Tumor-infiltrating lymphocyte grade in primary melanomas is independently associated with melanoma-specific survival in the population-based genes, environment and melanoma study. J. Clin. Oncol. 31, 4252–4259 (2013).
pubmed: 24127443 pmcid: 3821014 doi: 10.1200/JCO.2013.51.3002
Leach, D. R., Krummel, M. F. & Allison, J. P. Enhancement of antitumor immunity by CTLA-4 blockade. Science 271, 1734–1736 (1996).
pubmed: 8596936 doi: 10.1126/science.271.5256.1734
Hodi, F. S. et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363, 711–723 (2010).
pubmed: 20525992 pmcid: 3549297 doi: 10.1056/NEJMoa1003466
Robert, C. et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N. Engl. J. Med. 364, 2517–2526 (2011).
pubmed: 21639810 doi: 10.1056/NEJMoa1104621
Pauken, K. E., Torchia, J. A., Chaudhri, A., Sharpe, A. H. & Freeman, G. J. Emerging concepts in PD-1 checkpoint biology. Semin. Immunol. 52, 101480 (2021).
Strome, S. E. et al. B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res. 63, 6501–6505 (2003).
pubmed: 14559843
Iwai, Y. et al. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl Acad. Sci. USA 99, 12293–12297 (2002).
pubmed: 12218188 pmcid: 129438 doi: 10.1073/pnas.192461099
Barber, D. L. et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682–687 (2006).
pubmed: 16382236 doi: 10.1038/nature04444
Robert, C. et al. Pembrolizumab versus ipilimumab in advanced melanoma. N. Engl. J. Med. 372, 2521–2532 (2015).
pubmed: 25891173 doi: 10.1056/NEJMoa1503093
Robert, C. et al. Pembrolizumab versus ipilimumab in advanced melanoma (KEYNOTE-006): post-hoc 5-year results from an open-label, multicentre, randomised, controlled, phase 3 study. Lancet Oncol. 20, 1239–1251 (2019).
pubmed: 31345627 doi: 10.1016/S1470-2045(19)30388-2
Ascierto, P. A. et al. Survival outcomes in patients with previously untreated BRAF wild-type advanced melanoma treated with nivolumab therapy: three-year follow-up of a randomized phase 3 trial. JAMA Oncol. 5, 187–194 (2019).
pubmed: 30422243 doi: 10.1001/jamaoncol.2018.4514
Robert, C. et al. Nivolumab in previously untreated melanoma without BRAF mutation. N. Engl. J. Med. 372, 320–330 (2015).
pubmed: 25399552 doi: 10.1056/NEJMoa1412082
Brahmer, J. R. et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol. 28, 3167–3175 (2010).
pubmed: 20516446 pmcid: 4834717 doi: 10.1200/JCO.2009.26.7609
Wolchok, J. D. et al. Long-term outcomes with nivolumab plus ipilimumab or nivolumab alone versus ipilimumab in patients with advanced melanoma. J. Clin. Oncol. 40, 127–137 (2021)
Zappasodi, R., Wolchok, J. D. & Merghoub, T. Strategies for predicting response to checkpoint inhibitors. Curr. Hematol. Malig. Rep. 13, 383–395 (2018).
pubmed: 30159703 pmcid: 6719799 doi: 10.1007/s11899-018-0471-9
Ruscetti, F. W., Morgan, D. A. & Gallo, R. C. Functional and morphologic characterization of human T cells continuously grown in vitro. J. Immunol. 119, 131–138 (1977).
pubmed: 141483
Kvistborg, P. et al. TIL therapy broadens the tumor-reactive CD8
pubmed: 22754759 pmcid: 3382882 doi: 10.4161/onci.18851
Andersen, R. S. et al. Dissection of T-cell antigen specificity in human melanoma. Cancer Res. 72, 1642–1650 (2012).
pubmed: 22311675 doi: 10.1158/0008-5472.CAN-11-2614
Tran, E., Robbins, P. F. & Rosenberg, S. A. ‘Final common pathway’ of human cancer immunotherapy: targeting random somatic mutations. Nat. Immunol. 18, 255–262 (2017).
pubmed: 28198830 pmcid: 6295671 doi: 10.1038/ni.3682
Alexandrov, L. B. et al. Signatures of mutational processes in human cancer. Nature 500, 415–421 (2013).
pubmed: 23945592 pmcid: 3776390 doi: 10.1038/nature12477
Van den Eynde, B. J. & van der Bruggen, P. T cell defined tumor antigens. Curr. Opin. Immunol. 9, 684–693 (1997).
pubmed: 9368778 doi: 10.1016/S0952-7915(97)80050-7
Lennerz, V. et al. The response of autologous T cells to a human melanoma is dominated by mutated neoantigens. Proc. Natl Acad. Sci. USA 102, 16013–16018 (2005).
pubmed: 16247014 pmcid: 1266037 doi: 10.1073/pnas.0500090102
Oliveira, G. et al. Phenotype, specificity and avidity of antitumour CD8
pubmed: 34290406 doi: 10.1038/s41586-021-03704-y
Ott, P. A. et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature 547, 217–221 (2017).
pubmed: 28678778 pmcid: 5577644 doi: 10.1038/nature22991
Sahin, U. et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature 547, 222–226 (2017).
pubmed: 28678784 doi: 10.1038/nature23003
Carreno, B. M. et al. Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 348, 803–808 (2015).
pubmed: 25837513 pmcid: 4549796 doi: 10.1126/science.aaa3828
Itzhaki, O. et al. Establishment and large-scale expansion of minimally cultured “young” tumor infiltrating lymphocytes for adoptive transfer therapy. J. Immunother. 34, 212–220 (2011).
pubmed: 21304398 doi: 10.1097/CJI.0b013e318209c94c
Radvanyi, L. G. et al. Specific lymphocyte subsets predict response to adoptive cell therapy using expanded autologous tumor-infiltrating lymphocytes in metastatic melanoma patients. Clin. Cancer Res. 18, 6758–6770 (2012).
pubmed: 23032743 pmcid: 3525747 doi: 10.1158/1078-0432.CCR-12-1177
Rosenberg, S. A. et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17, 4550–4557 (2011).
pubmed: 21498393 pmcid: 3131487 doi: 10.1158/1078-0432.CCR-11-0116
Goff, S. L. et al. Randomized, prospective evaluation comparing intensity of lymphodepletion before adoptive transfer of tumor-infiltrating lymphocytes for patients with metastatic melanoma. J. Clin. Oncol. 34, 2389–2397 (2016).
pubmed: 27217459 pmcid: 4981979 doi: 10.1200/JCO.2016.66.7220
Linnemann, C. et al. High-throughput epitope discovery reveals frequent recognition of neo-antigens by CD4+ T cells in human melanoma. Nat. Med. 21, 81–85 (2015).
pubmed: 25531942 doi: 10.1038/nm.3773
Lu, Y. C. et al. Mutated PPP1R3B is recognized by T cells used to treat a melanoma patient who experienced a durable complete tumor regression. J. Immunol. 190, 6034–6042 (2013).
pubmed: 23690473 doi: 10.4049/jimmunol.1202830
Prickett, T. D. et al. Durable complete response from metastatic melanoma after transfer of autologous T cells recognizing 10 mutated tumor antigens. Cancer Immunol. Res. 4, 669–678 (2016).
pubmed: 27312342 pmcid: 4970903 doi: 10.1158/2326-6066.CIR-15-0215
Robbins, P. F. et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat. Med. 19, 747–752 (2013).
pubmed: 23644516 pmcid: 3757932 doi: 10.1038/nm.3161
Tran, E. et al. Immunogenicity of somatic mutations in human gastrointestinal cancers. Science 350, 1387–1390 (2015).
pubmed: 26516200 pmcid: 7445892 doi: 10.1126/science.aad1253
Krishna, S. et al. Stem-like CD8 T cells mediate response of adoptive cell immunotherapy against human cancer. Science 370, 1328–1334 (2020).
pubmed: 33303615 pmcid: 8883579 doi: 10.1126/science.abb9847
Gilbert, A. E. et al. Monitoring the systemic human memory B cell compartment of melanoma patients for anti-tumor IgG antibodies. PLoS ONE 6, e19330 (2011).
pubmed: 21559411 pmcid: 3084832 doi: 10.1371/journal.pone.0019330
Pfreundschuh, M. The genealogy of SEREX. Cancer Immun. 12, 7 (2012).
pubmed: 22896752 pmcid: 3380345
Sahin, U. et al. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc. Natl Acad. Sci. USA 92, 11810–11813 (1995).
pubmed: 8524854 pmcid: 40492 doi: 10.1073/pnas.92.25.11810
Vijayasaradhi, S., Bouchard, B. & Houghton, A. N. The melanoma antigen gp75 is the human homologue of the mouse b (brown) locus gene product. J. Exp. Med. 171, 1375–1380 (1990).
pubmed: 2324688 doi: 10.1084/jem.171.4.1375
Wang, R. F., Robbins, P. F., Kawakami, Y., Kang, X. Q. & Rosenberg, S. A. Identification of a gene encoding a melanoma tumor antigen recognized by HLA-A31-restricted tumor-infiltrating lymphocytes. J. Exp. Med. 181, 799–804 (1995).
pubmed: 7836932 doi: 10.1084/jem.181.2.799
Livingston, P. O. et al. Improved survival in stage III melanoma patients with GM2 antibodies: a randomized trial of adjuvant vaccination with GM2 ganglioside. J. Clin. Oncol. 12, 1036–1044 (1994).
pubmed: 8164027 doi: 10.1200/JCO.1994.12.5.1036
Cipponi, A. et al. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res. 72, 3997–4007 (2012).
pubmed: 22850419 doi: 10.1158/0008-5472.CAN-12-1377
Ladanyi, A. et al. Prognostic impact of B-cell density in cutaneous melanoma. Cancer Immunol. Immunother. 60, 1729–1738 (2011).
pubmed: 21779876 doi: 10.1007/s00262-011-1071-x
Sautes-Fridman, C., Petitprez, F., Calderaro, J. & Fridman, W. H. Tertiary lymphoid structures in the era of cancer immunotherapy. Nat. Rev. Cancer 19, 307–325 (2019).
pubmed: 31092904 doi: 10.1038/s41568-019-0144-6
Liu, W., Peng, Y. & Tobin, D. J. A new 12-gene diagnostic biomarker signature of melanoma revealed by integrated microarray analysis. PeerJ 1, e49 (2013).
pubmed: 23638386 pmcid: 3628745 doi: 10.7717/peerj.49
Mortarini, R. et al. Constitutive expression and costimulatory function of LIGHT/TNFSF14 on human melanoma cells and melanoma-derived microvesicles. Cancer Res. 65, 3428–3436 (2005).
pubmed: 15833878 doi: 10.1158/0008-5472.CAN-04-3239
Erdag, G. et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 72, 1070–1080 (2012).
pubmed: 22266112 pmcid: 3306813 doi: 10.1158/0008-5472.CAN-11-3218
Garg, K. et al. Tumor-associated B cells in cutaneous primary melanoma and improved clinical outcome. Hum. Pathol. 54, 157–164 (2016).
pubmed: 27107457 doi: 10.1016/j.humpath.2016.03.022
Martinez-Rodriguez, M., Thompson, A. K. & Monteagudo, C. A significant percentage of CD20-positive TILs correlates with poor prognosis in patients with primary cutaneous malignant melanoma. Histopathology 65, 726–728 (2014).
pubmed: 24750176 doi: 10.1111/his.12437
Eschweiler, S. et al. Intratumoral follicular regulatory T cells curtail anti-PD-1 treatment efficacy. Nat. Immunol. 22, 1052–1063 (2021).
pubmed: 34168370 pmcid: 8434898 doi: 10.1038/s41590-021-00958-6
Joshi, N. S. et al. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity 43, 579–590 (2015).
pubmed: 26341400 pmcid: 4826619 doi: 10.1016/j.immuni.2015.08.006
Zlotnik, A., Burkhardt, A. M. & Homey, B. Homeostatic chemokine receptors and organ-specific metastasis. Nat. Rev. Immunol. 11, 597–606 (2011).
pubmed: 21866172 doi: 10.1038/nri3049
Crawford, A. et al. Molecular and transcriptional basis of CD4
pubmed: 24530057 pmcid: 3990591 doi: 10.1016/j.immuni.2014.01.005
Zappasodi, R. et al. Non-conventional inhibitory CD4
pubmed: 29894689 pmcid: 6648657 doi: 10.1016/j.ccell.2018.05.009
Cabrita, R. et al. Tertiary lymphoid structures improve immunotherapy and survival in melanoma. Nature 577, 561–565 (2020).
pubmed: 31942071 doi: 10.1038/s41586-019-1914-8
Helmink, B. A. et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature 577, 549–555 (2020).
pubmed: 31942075 pmcid: 8762581 doi: 10.1038/s41586-019-1922-8
Petitprez, F. et al. B cells are associated with survival and immunotherapy response in sarcoma. Nature 577, 556–560 (2020).
pubmed: 31942077 doi: 10.1038/s41586-019-1906-8
Spranger, S. et al. Up-regulation of PD-L1, IDO, and T
pubmed: 23986400 pmcid: 4136707 doi: 10.1126/scitranslmed.3006504
Taube, J. M. et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci. Transl. Med. 4, 127ra137 (2012).
doi: 10.1126/scitranslmed.3003689
Zippelius, A. et al. Effector function of human tumor-specific CD8 T cells in melanoma lesions: a state of local functional tolerance. Cancer Res. 64, 2865–2873 (2004).
pubmed: 15087405 doi: 10.1158/0008-5472.CAN-03-3066
Ahmadzadeh, M. et al. FOXP3 expression accurately defines the population of intratumoral regulatory T cells that selectively accumulate in metastatic melanoma lesions. Blood 112, 4953–4960 (2008).
pubmed: 18820132 pmcid: 2954707 doi: 10.1182/blood-2008-06-163048
Viguier, M. et al. Foxp3 expressing CD4
pubmed: 15240741 doi: 10.4049/jimmunol.173.2.1444
Mukherji, B. et al. Clonal analysis of cytotoxic and regulatory T cell responses against human melanoma. J. Exp. Med. 169, 1961–1976 (1989).
pubmed: 2471770 doi: 10.1084/jem.169.6.1961
Wang, H. Y., Peng, G., Guo, Z., Shevach, E. M. & Wang, R. F. Recognition of a new ARTC1 peptide ligand uniquely expressed in tumor cells by antigen-specific CD4
pubmed: 15728473 doi: 10.4049/jimmunol.174.5.2661
Oliveira, G. et al. 655 Landscape of helper and regulatory CD4
doi: 10.1136/jitc-2021-SITC2021.655
Enninga, E. A., Nevala, W. K., Holtan, S. G., Leontovich, A. A. & Markovic, S. N. Galectin-9 modulates immunity by promoting Th2/M2 differentiation and impacts survival in patients with metastatic melanoma. Melanoma Res. 26, 429–441 (2016).
pubmed: 27455380 pmcid: 5929986 doi: 10.1097/CMR.0000000000000281
Lauerova, L. et al. Malignant melanoma associates with T
pubmed: 12098001
Nevala, W. K. et al. Evidence of systemic T
pubmed: 19240164 pmcid: 2757059 doi: 10.1158/1078-0432.CCR-08-1980
Klarquist, J. S. & Janssen, E. M. Melanoma-infiltrating dendritic cells: limitations and opportunities of mouse models. Oncoimmunology 1, 1584–1593 (2012).
pubmed: 23264904 pmcid: 3525613 doi: 10.4161/onci.22660
Marzagalli, M., Ebelt, N. D. & Manuel, E. R. Unraveling the crosstalk between melanoma and immune cells in the tumor microenvironment. Semin Cancer Biol. 59, 236–250 (2019).
pubmed: 31404607 doi: 10.1016/j.semcancer.2019.08.002
Pieniazek, M., Matkowski, R. & Donizy, P. Macrophages in skin melanoma-the key element in melanomagenesis. Oncol. Lett. 15, 5399–5404 (2018).
pubmed: 29552183 pmcid: 5840697
Tucci, M. et al. Immune system evasion as hallmark of melanoma progression: the role of dendritic cells. Front Oncol. 9, 1148 (2019).
pubmed: 31750245 pmcid: 6848379 doi: 10.3389/fonc.2019.01148
Spranger, S., Bao, R. & Gajewski, T. F. Melanoma-intrinsic beta-catenin signalling prevents anti-tumour immunity. Nature 523, 231–235 (2015).
pubmed: 25970248 doi: 10.1038/nature14404
Spranger, S., Dai, D., Horton, B. & Gajewski, T. F. Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy. Cancer Cell 31, 711–723 e714 (2017).
pubmed: 28486109 pmcid: 5650691 doi: 10.1016/j.ccell.2017.04.003
Böttcher, J. P. et al. NK cells stimulate recruitment of cDC1 into the tumor microenvironment promoting cancer immune control. Cell 172, 1022–1037 (2018).
pubmed: 29429633 pmcid: 5847168 doi: 10.1016/j.cell.2018.01.004
Sun, X., Zhang, N., Yin, C., Zhu, B. & Li, X. Ultraviolet radiation and melanomagenesis: from mechanism to immunotherapy. Front Oncol. 10, 951 (2020).
pubmed: 32714859 pmcid: 7343965 doi: 10.3389/fonc.2020.00951
Schwarz, A. et al. Langerhans cells are required for UVR-induced immunosuppression. J. Invest. Dermatol. 130, 1419–1427 (2010).
pubmed: 20090769 doi: 10.1038/jid.2009.429
Wang, L., Jameson, S. C. & Hogquist, K. A. Epidermal Langerhans cells are not required for UV-induced immunosuppression. J. Immunol. 183, 5548–5553 (2009).
pubmed: 19843938 doi: 10.4049/jimmunol.0900235
Nirschl, C. J. et al. IFNγ-dependent tissue-immune homeostasis is co-opted in the tumor microenvironment. Cell 170, 127–141.e115 (2017).
pubmed: 28666115 pmcid: 5569303 doi: 10.1016/j.cell.2017.06.016
Khalil, D. N. et al. In situ vaccination with defined factors overcomes T cell exhaustion in distant tumors. J. Clin. Invest. 129, 3435–3447 (2019).
pubmed: 31329159 pmcid: 6668692 doi: 10.1172/JCI128562
Esensten, J. H., Helou, Y. A., Chopra, G., Weiss, A. & Bluestone, J. A. CD28 costimulation: from mechanism to therapy. Immunity 44, 973–988 (2016).
pubmed: 27192564 pmcid: 4932896 doi: 10.1016/j.immuni.2016.04.020
Blackburn, S. D. et al. Coregulation of CD8
pubmed: 19043418 doi: 10.1038/ni.1679
Huang, A. C. et al. A single dose of neoadjuvant PD-1 blockade predicts clinical outcomes in resectable melanoma. Nat. Med. 25, 454–461 (2019).
pubmed: 30804515 pmcid: 6699626 doi: 10.1038/s41591-019-0357-y
Huang, A. C. et al. T-cell invigoration to tumour burden ratio associated with anti-PD-1 response. Nature 545, 60–65 (2017).
pubmed: 28397821 pmcid: 5554367 doi: 10.1038/nature22079
Kamphorst, A. O. et al. Proliferation of PD-1
pubmed: 28446615 pmcid: 5441721 doi: 10.1073/pnas.1705327114
Curiel, T. J. et al. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat. Med. 9, 562–567 (2003).
pubmed: 12704383 doi: 10.1038/nm863
Zappasodi, R., Merghoub, T. & Wolchok, J. D. Emerging concepts for immune checkpoint blockade-based combination therapies. Cancer Cell 33, 581–598 (2018).
pubmed: 29634946 pmcid: 5896787 doi: 10.1016/j.ccell.2018.03.005
Long, G. V. et al. Standard-dose pembrolizumab plus alternate-dose ipilimumab in advanced melanoma: KEYNOTE-029 cohort 1C, a phase 2 randomized study of two dosing schedules. Clin. Cancer Res. https://doi.org/10.1158/1078-0432.Ccr-21-0793 (2021).
Maruhashi, T., Sugiura, D., Okazaki, I. M. & Okazaki, T. LAG-3: from molecular functions to clinical applications. J. Immunother. Cancer 8, e001014 (2020).
Tawbi, H. A. et al. Relatlimab and nivolumab versus nivolumab in untreated advanced melanoma. N. Engl. J. Med. 386, 24–34 (2022).
pubmed: 34986285 doi: 10.1056/NEJMoa2109970
Shen, R. et al. LAG-3 expression on peripheral blood cells identifies patients with poorer outcomes after immune checkpoint blockade. Sci. Transl. Med. 13, eabf5107 (2021).
pubmed: 34433638 doi: 10.1126/scitranslmed.abf5107
Andrews, L. P. et al. Resistance to PD1 blockade in the absence of metalloprotease-mediated LAG3 shedding. Sci. Immunol. 5, eabc2728 (2020).
Eggermont, A. M. et al. Prolonged survival in stage III melanoma with ipilimumab adjuvant therapy. N. Engl. J. Med. 375, 1845–1855 (2016).
pubmed: 27717298 pmcid: 5648545 doi: 10.1056/NEJMoa1611299
Eggermont, A. M. M. et al. Adjuvant ipilimumab versus placebo after complete resection of stage III melanoma: long-term follow-up results of the European Organisation for Research and Treatment of Cancer 18071 double-blind phase 3 randomised trial. Eur. J. Cancer 119, 1–10 (2019).
pubmed: 31400634 doi: 10.1016/j.ejca.2019.07.001
Curti, B. D. & Faries, M. B. Recent advances in the treatment of melanoma. N. Engl. J. Med. 384, 2229–2240 (2021).
pubmed: 34107182 doi: 10.1056/NEJMra2034861
Eggermont, A. M. M. et al. Adjuvant pembrolizumab versus placebo in resected stage III melanoma (EORTC 1325-MG/KEYNOTE-054): distant metastasis-free survival results from a double-blind, randomised, controlled, phase 3 trial. Lancet Oncol. 22, 643–654 (2021).
pubmed: 33857412 doi: 10.1016/S1470-2045(21)00065-6
Luke, J. J. Pembrolizumab versus placebo after complete resection of high-risk stage II melanoma: efficacy and safety results from the KEYNOTE-716 double-blind phase III trial. Ann. Oncol. 32, S1283–S1346 (2021).
doi: 10.1016/j.annonc.2021.08.2116
Amaria, R. N. et al. Neoadjuvant systemic therapy in melanoma: recommendations of the International Neoadjuvant Melanoma Consortium. Lancet Oncol. 20, e378–e389 (2019).
pubmed: 31267972 doi: 10.1016/S1470-2045(19)30332-8
Tarhini, A. A. et al. Immune monitoring of the circulation and the tumor microenvironment in patients with regionally advanced melanoma receiving neoadjuvant ipilimumab. PLoS ONE 9, e87705 (2014).
pubmed: 24498358 pmcid: 3912016 doi: 10.1371/journal.pone.0087705
Amaria, R. N. et al. Neoadjuvant and adjuvant nivolumab (nivo) with anti-LAG3 antibody relatlimab (rela) for patients (pts) with resectable clinical stage III melanoma. J. Clin. Oncol. 39, 9502–9502 (2021).
doi: 10.1200/JCO.2021.39.15_suppl.9502
Menzies, A. M. et al. Pathological response and survival with neoadjuvant therapy in melanoma: a pooled analysis from the International Neoadjuvant Melanoma Consortium (INMC). Nat. Med. 27, 301–309 (2021).
pubmed: 33558722 doi: 10.1038/s41591-020-01188-3
Rawson, R. V. et al. Pathological response and tumour bed histopathological features correlate with survival following neoadjuvant immunotherapy in stage III melanoma. Ann. Oncol. 32, 766–777 (2021).
pubmed: 33744385 doi: 10.1016/j.annonc.2021.03.006
Rozeman, E. A. et al. Survival and biomarker analyses from the OpACIN-neo and OpACIN neoadjuvant immunotherapy trials in stage III melanoma. Nat. Med. 27, 256–263 (2021).
pubmed: 33558721 doi: 10.1038/s41591-020-01211-7
Blank, C. U. et al. First safety and efficacy results of PRADO: a phase II study of personalized response-driven surgery and adjuvant therapy after neoadjuvant ipilimumab (IPI) and nivolumab (NIVO) in resectable stage III melanoma. J. Clin. Oncol. 38, 10002–10002 (2020).
doi: 10.1200/JCO.2020.38.15_suppl.10002
Moschos, S. J. et al. Neoadjuvant treatment of regional stage IIIB melanoma with high-dose interferon alfa-2b induces objective tumor regression in association with modulation of tumor infiltrating host cellular immune responses. J. Clin. Oncol. 24, 3164–3171 (2006).
pubmed: 16809739 doi: 10.1200/JCO.2005.05.2498
Carthon, B. C. et al. Preoperative CTLA-4 blockade: tolerability and immune monitoring in the setting of a presurgical clinical trial. Clin. Cancer Res. 16, 2861–2871 (2010).
pubmed: 20460488 pmcid: 2919850 doi: 10.1158/1078-0432.CCR-10-0569
Ng Tang, D. et al. Increased frequency of ICOS
pubmed: 24777852 doi: 10.1158/2326-6066.CIR-13-0020
Wei, S. C., Duffy, C. R. & Allison, J. P. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Disco. 8, 1069–1086 (2018).
doi: 10.1158/2159-8290.CD-18-0367
Arce Vargas, F. et al. Fc effector function contributes to the activity of human anti-CTLA-4 antibodies. Cancer Cell 33, 649–663 (2018).
pubmed: 29576375 pmcid: 5904288 doi: 10.1016/j.ccell.2018.02.010
Romano, E. et al. Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc. Natl Acad. Sci. USA 112, 6140–6145 (2015).
pubmed: 25918390 pmcid: 4434760 doi: 10.1073/pnas.1417320112
Sharma, A. et al. Anti-CTLA-4 immunotherapy does not deplete FOXP3
pubmed: 30054281 doi: 10.1158/1078-0432.CCR-18-0762
Kavanagh, B. et al. CTLA4 blockade expands FoxP3
pubmed: 18523152 pmcid: 2515138 doi: 10.1182/blood-2007-11-125435
Selby, M. J. et al. Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells. Cancer Immunol. Res. 1, 32–42 (2013).
pubmed: 24777248 doi: 10.1158/2326-6066.CIR-13-0013
Wing, J. B., Ise, W., Kurosaki, T. & Sakaguchi, S. Regulatory T cells control antigen-specific expansion of T
pubmed: 25526312 doi: 10.1016/j.immuni.2014.12.006
Zappasodi, R. et al. CTLA-4 blockade drives loss of T
pubmed: 33588426 pmcid: 8057670 doi: 10.1038/s41586-021-03326-4
Korman, A. J. et al. Abstract SY09-01: next-generation anti-CTLA-4 antibodies. Cancer Res. 77, SY09-01 (2017).
doi: 10.1158/1538-7445.AM2017-SY09-01
Hashimoto, M. et al. CD8 T cell exhaustion in chronic infection and cancer: opportunities for interventions. Annu Rev. Med 69, 301–318 (2018).
pubmed: 29414259 doi: 10.1146/annurev-med-012017-043208
Valpione, S. et al. Immune-awakening revealed by peripheral T cell dynamics after one cycle of immunotherapy. Nat. Cancer 1, 210–221 (2020).
pubmed: 32110781 pmcid: 7046489 doi: 10.1038/s43018-019-0022-x
Kamada, T. et al. PD-1
pubmed: 31028147 pmcid: 6525547 doi: 10.1073/pnas.1822001116
Kumagai, S. et al. The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies. Nat. Immunol. 21, 1346–1358 (2020).
pubmed: 32868929 doi: 10.1038/s41590-020-0769-3
Sage, P. T., Paterson, A. M., Lovitch, S. B. & Sharpe, A. H. The coinhibitory receptor CTLA-4 controls B cell responses by modulating T follicular helper, T follicular regulatory, and T regulatory cells. Immunity 41, 1026–1039 (2014).
pubmed: 25526313 pmcid: 4309019 doi: 10.1016/j.immuni.2014.12.005
van der Leun, A. M., Thommen, D. S. & Schumacher, T. N. CD8
pubmed: 32024970 pmcid: 7115982 doi: 10.1038/s41568-019-0235-4
Li, H. et al. Dysfunctional CD8 T cells form a proliferative, dynamically regulated compartment within human melanoma. Cell 176, 775–789 (2019).
pubmed: 30595452 doi: 10.1016/j.cell.2018.11.043
Falck Miniotis, M. et al. MEK1/2 inhibition decreases lactate in BRAF-driven human cancer cells. Cancer Res. 73, 4039 (2013).
pubmed: 23639941 doi: 10.1158/0008-5472.CAN-12-1969
Hall, A. et al. Dysfunctional oxidative phosphorylation makes malignant melanoma cells addicted to glycolysis driven by the
pubmed: 23603840 pmcid: 3720606 doi: 10.18632/oncotarget.965
Haq, R. et al. Oncogenic BRAF regulates oxidative metabolism via PGC1α and MITF. Cancer Cell 23, 302–315 (2013).
pubmed: 23477830 pmcid: 3635826 doi: 10.1016/j.ccr.2013.02.003
Cascone, T. et al. Increased tumor glycolysis characterizes immune resistance to adoptive T cell therapy. Cell Metab. 27, 977–987 e974 (2018).
pubmed: 29628419 pmcid: 5932208 doi: 10.1016/j.cmet.2018.02.024
Peng, W. et al. Loss of PTEN promotes resistance to T cell-mediated immunotherapy. Cancer Discov. 6, 202–216 (2016).
pubmed: 26645196 doi: 10.1158/2159-8290.CD-15-0283
Brand, A. et al. LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK cells. Cell Metab. 24, 657–671 (2016).
pubmed: 27641098 doi: 10.1016/j.cmet.2016.08.011
Hugo, W. et al. Genomic and transcriptomic features of response to anti-PD-1 therapy in metastatic melanoma. Cell 165, 35–44 (2016).
pubmed: 26997480 pmcid: 4808437 doi: 10.1016/j.cell.2016.02.065
Fischer, G. M. et al. Molecular profiling reveals unique immune and metabolic features of melanoma brain metastases. Cancer Discov. 9, 628–645 (2019).
pubmed: 30787016 pmcid: 6497554 doi: 10.1158/2159-8290.CD-18-1489
Jaiswal, A. R. et al. Melanoma evolves complete immunotherapy resistance through the acquisition of a hypermetabolic phenotype. Cancer Immunol. Res. 8, 1365–1380 (2020).
pubmed: 32917656 pmcid: 7642111 doi: 10.1158/2326-6066.CIR-19-0005
Najjar, Y. G. et al. Tumor cell oxidative metabolism as a barrier to PD-1 blockade immunotherapy in melanoma. JCI Insight 4, e124989 (2019).
Kim, S. H. et al. Phenformin inhibits myeloid-derived suppressor cells and enhances the anti-tumor activity of PD-1 blockade in melanoma. J. Invest. Dermatol. 137, 1740–1748 (2017).
pubmed: 28433543 doi: 10.1016/j.jid.2017.03.033
Afzal, M. Z., Mercado, R. R. & Shirai, K. Efficacy of metformin in combination with immune checkpoint inhibitors (anti-PD-1/anti-CTLA-4) in metastatic malignant melanoma. J. Immunother. Cancer 6, 64 (2018).
pubmed: 29966520 pmcid: 6027578 doi: 10.1186/s40425-018-0375-1
Scharping, N. E. et al. Mitochondrial stress induced by continuous stimulation under hypoxia rapidly drives T cell exhaustion. Nat. Immunol. 22, 205–215 (2021).
pubmed: 33398183 pmcid: 7971090 doi: 10.1038/s41590-020-00834-9
Watson, M. J. et al. Metabolic support of tumour-infiltrating regulatory T cells by lactic acid. Nature 591, 645–651 (2021).
pubmed: 33589820 pmcid: 7990682 doi: 10.1038/s41586-020-03045-2
Wang, H. et al. CD36-mediated metabolic adaptation supports regulatory T cell survival and function in tumors. Nat. Immunol. 21, 298–308 (2020).
pubmed: 32066953 pmcid: 7043937 doi: 10.1038/s41590-019-0589-5
Brahmer, J. R. et al. Society for Immunotherapy of Cancer (SITC) clinical practice guideline on immune checkpoint inhibitor-related adverse events. J. Immunother. Cancer 9, e002435 (2021).
pubmed: 34172516 pmcid: 8237720 doi: 10.1136/jitc-2021-002435
Leko, V. & Rosenberg, S. A. Identifying and targeting human tumor antigens for T cell-based immunotherapy of solid tumors. Cancer Cell 38, 454–472 (2020).
pubmed: 32822573 pmcid: 7737225 doi: 10.1016/j.ccell.2020.07.013
Coulie, P. G., Van den Eynde, B. J., van der Bruggen, P. & Boon, T. Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat. Rev. Cancer 14, 135–146 (2014).
pubmed: 24457417 doi: 10.1038/nrc3670
Vogelstein, B. et al. Cancer genome landscapes. Science 339, 1546–1558 (2013).
pubmed: 23539594 pmcid: 3749880 doi: 10.1126/science.1235122
Turajlic, S. et al. Insertion-and-deletion-derived tumour-specific neoantigens and the immunogenic phenotype: a pan-cancer analysis. Lancet Oncol. 18, 1009–1021 (2017).
pubmed: 28694034 doi: 10.1016/S1470-2045(17)30516-8

Auteurs

Alexander C Huang (AC)

Division of Hematology/Oncology, Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. alexander.huang@pennmedicine.upenn.edu.
Department of Cancer Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. alexander.huang@pennmedicine.upenn.edu.
Abramson Cancer Center, University of Pennsylvania, Philadelphia, PA, USA. alexander.huang@pennmedicine.upenn.edu.
Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. alexander.huang@pennmedicine.upenn.edu.
Parker Institute for Cancer Immunotherapy, San Francisco, CA, USA. alexander.huang@pennmedicine.upenn.edu.
ORCID: 0000-0002-0099-0492

Roberta Zappasodi (R)

Parker Institute for Cancer Immunotherapy, San Francisco, CA, USA. roz4002@med.cornell.edu.
Division of Hematology & Medical Oncology, Department of Medicine, Weill Cornell Medicine, New York, NY, USA. roz4002@med.cornell.edu.
Immunology and Microbial Pathogenesis Program, Weill Cornell Graduate School of Medical Sciences, New York, NY, USA. roz4002@med.cornell.edu.
Human Oncology & Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA. roz4002@med.cornell.edu.
ORCID: 0000-0002-7031-6671

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › A decade of checkpoint blockade immunotherapy...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Utilisations thérapeutiques › Antinéoplasiques › Antinéoplasiques immunologiques › Inhibiteurs de points de contrôle immunitaires › A decade of checkpoint blockade immunotherapy...
questionsmedicales.fr › Thérapeutique › Biothérapie › Immunothérapie › A decade of checkpoint blockade immunotherapy...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Globulines › Sérum-globulines › Immunoglobulines › Anticorps › Anticorps monoclonaux › Anticorps monoclonaux humanisés › Ipilimumab › A decade of checkpoint blockade immunotherapy...
questionsmedicales.fr › Tumeurs › Tumeurs par type histologique › Naevus et mélanomes › Mélanome › A decade of checkpoint blockade immunotherapy...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Microenvironnement cellulaire › Microenvironnement tumoral › A decade of checkpoint blockade immunotherapy...