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Original Research

Immune checkpoint therapy responders display early clonal expansion of tumor infiltrating lymphocytes

, , , , , , , , , , , , , , , , , , , , & ORCID Icon show all
Article: 2345859 | Received 02 Aug 2023, Accepted 17 Apr 2024, Published online: 26 Apr 2024

References

  • Hellmann MD, Paz-Ares L, Bernabe Caro R, Zurawski B, Kim S-W, Carcereny Costa E, Park K, Alexandru A, Lupinacci L, De La Mora Jimenez E. et al. Nivolumab plus Ipilimumab in Advanced Non–Small-Cell Lung Cancer. N Engl J Med. 2019;381(21):2020–14. doi:10.1056/NEJMoa1910231.
  • Larkin J, Chiarion-Sileni V, Gonzalez R, Grob J-J, Rutkowski P, Lao CD, Cowey CL, Schadendorf D, Wagstaff J, Dummer R. et al. Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2019;381(16):1535–1546. doi:10.1056/NEJMoa1910836.
  • Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WEE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E. et al. Nivolumab versus Docetaxel in advanced squamous-cell non–small-Cell lung cancer. N Engl J Med. 2015;373(2):123–135. doi:10.1056/NEJMoa1504627.
  • Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS. Mutational landscape determines sensitivity to PD-1 blockade in non–small cell lung cancer. Science. 2015;348(6230):124–128. doi:10.1126/science.aaa1348.
  • Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, Walsh LA, Postow MA, Wong P, Ho TS. et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014;371(23):2189–2199. doi:10.1056/NEJMoa1406498.
  • Lesterhuis WJ, Bosco A, Millward MJ, Small M, Nowak AK, Lake RA. Dynamic versus static biomarkers in cancer immune checkpoint blockade: unravelling complexity. Nat Rev Drug Discov. 2017;16(4):264–272. doi:10.1038/nrd.2016.233.
  • Sade-Feldman M, Yizhak K, Bjorgaard SL, Ray JP, de Boer CG, Jenkins RW, Lieb DJ, Chen JH, Frederick DT, Barzily-Rokni M. et al. Defining T cell states associated with response to checkpoint immunotherapy in melanoma. Cell. 2018;175(4):998–1013.e1020. doi:10.1016/j.cell.2018.10.038.
  • Han J, Duan J, Bai H, Wang Y, Wan R, Wang X, Chen S, Tian Y, Wang D, Fei K. et al. TCR repertoire diversity of peripheral PD-1+CD8+ T cells predicts clinical outcomes after immunotherapy in patients with non–small cell lung cancer. Cancer Immunol Res. 2020;8(1):146–154. doi:10.1158/2326-6066.CIR-19-0398.
  • Kidman J, Principe N, Watson M, Lassmann T, Holt RA, Nowak AK, Lesterhuis WJ, Lake RA, Chee J. Characteristics of TCR repertoire associated with successful immune checkpoint therapy responses. Front Immunol. 2020;11:11(2668. doi:10.3389/fimmu.2020.587014.
  • Freeman JD, Warren RL, Webb JR, Nelson BH, Holt RA. Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res. 2009;19(10):1817–1824. doi:10.1101/gr.092924.109.
  • Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJM, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V. et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515(7528):568–571. doi:10.1038/nature13954.
  • Riaz N, Havel JJ, Makarov V, Desrichard A, Urba WJ, Sims JS, Hodi FS, Martín-Algarra S, Mandal R, Sharfman WH. et al. Tumor and microenvironment evolution during immunotherapy with Nivolumab. Cell. 2017;171(4):934–949.e916. doi:10.1016/j.cell.2017.09.028.
  • Roh W, Chen P-L, Reuben A, Spencer CN, Prieto PA, Miller JP, Gopalakrishnan V, Wang F, Cooper ZA, Reddy SM. et al. Integrated molecular analysis of tumor biopsies on sequential CTLA-4 and PD-1 blockade reveals markers of response and resistance. Sci Transl Med. 2017;9(379):eaah3560. doi:10.1126/scitranslmed.aah3560.
  • Hopkins AC, Yarchoan M, Durham JN, Yusko EC, Rytlewski JA, Robins HS, Laheru DA, Le DT, Lutz ER, Jaffee EM. T cell receptor repertoire features associated with survival in immunotherapy-treated pancreatic ductal adenocarcinoma. JCI Insight. 2018;3(13). doi:10.1172/jci.insight.122092.
  • Hogan SA, Courtier A, Cheng PF, Jaberg-Bentele NF, Goldinger SM, Manuel M, Perez S, Plantier N, Mouret J-F, Nguyen-Kim TDL. et al. Peripheral blood TCR repertoire profiling May facilitate patient stratification for immunotherapy against Melanoma. Cancer Immunol Res. 2019;7(1):77–85. doi:10.1158/2326-6066.CIR-18-0136.
  • Forde PM, Chaft JE, Smith KN, Anagnostou V, Cottrell TR, Hellmann MD, Zahurak M, Yang SC, Jones DR, Broderick S. et al. Neoadjuvant PD-1 blockade in resectable lung cancer. N Engl J Med. 2018;378(21):1976–1986. doi:10.1056/NEJMoa1716078.
  • Glanville J, Huang H, Nau A, Hatton O, Wagar LE, Rubelt F, Ji X, Han A, Krams SM, Pettus C. et al. Identifying specificity groups in the T cell receptor repertoire. Nature. 2017;547(7661):94–98. doi:10.1038/nature22976.
  • Dash P, Fiore-Gartland AJ, Hertz T, Wang GC, Sharma S, Souquette A, Crawford JC, Clemens EB, Nguyen THO, Kedzierska K. et al. Quantifiable predictive features define epitope-specific T cell receptor repertoires. Nature. 2017;547(7661):89–93. doi:10.1038/nature22383.
  • Zemek RM, De Jong E, Chin WL, Schuster IS, Fear VS, Casey TH, Forbes C, Dart SJ, Leslie C, Zaitouny A. et al. Sensitization to immune checkpoint blockade through activation of a STAT1/NK axis in the tumor microenvironment. Sci Transl Med. 2019;11(501):eaav7816. doi:10.1126/scitranslmed.aav7816.
  • Zemek RM, Fear VS, Forbes C, De Jong E, Casey TH, Boon L, Lassmann T, Bosco A, Millward MJ, Nowak AK. et al. Bilateral murine tumor models for characterizing the response to immune checkpoint blockade. Nat Protoc. 2020;15(5):1628–1648. doi:10.1038/s41596-020-0299-3.
  • Marzo AL, Lake RA, Robinson BWS, Scott B. T-Cell receptor transgenic analysis of tumor-specific CD8 and CD4 responses in the eradication of solid tumors. Cancer Res. 1999;59:1071–1079.
  • Fear VS, Tilsed C, Chee J, Forbes CA, Casey T, Solin JN, Lansley SM, Lesterhuis WJ, Dick IM, Nowak AK. et al. Combination immune checkpoint blockade as an effective therapy for mesothelioma. OncoImmunology. 2018;7(10):e1494111. doi:10.1080/2162402X.2018.1494111.
  • Principe N, Kidman J, Goh S, Tilsed CM, Fisher SA, Fear VS, Forbes CA, Zemek RM, Chopra A, Watson M. et al. Tumor infiltrating effector memory antigen-specific CD8+ T cells predict response to immune checkpoint therapy. Front Immunol. 2020;11:11. doi:10.3389/fimmu.2020.584423.
  • Bolotin DA, Poslavsky S, Mitrophanov I, Shugay M, Mamedov IZ, Putintseva EV, Chudakov DM. MiXCR: software for comprehensive adaptive immunity profiling. Nat Methods. 2015;12(5):380–381. doi:10.1038/nmeth.3364.
  • Laydon DJ, Bangham CRM, Asquith B. Estimating T-cell repertoire diversity: limitations of classical estimators and a new approach. Phil Trans R Soc B. 2015;370(1675):20140291. doi:10.1098/rstb.2014.0291.
  • Sidhom JW, Oliveira G, Ross-MacDonald P, Wind-Rotolo M, Wu CJ, Pardoll DM, Baras AS. Deep learning reveals predictive sequence concepts within immune repertoires to immunotherapy. Sci Adv. 2022;8(37):eabq5089. doi:10.1126/sciadv.abq5089.
  • Sidhom J-W, Larman HB, Pardoll DM, Baras AS. DeepTCR is a deep learning framework for revealing sequence concepts within T-cell repertoires. Nat Commun. 2021;12(1). doi:10.1038/s41467-021-21879-w.
  • Walsh I, Fishman D, Garcia-Gasulla D, Titma T, Pollastri G, EMLF G, Harrow J, Psomopoulos FE, Tosatto SCE, Del Conte A. DOME: recommendations for supervised machine learning validation in biology. Nat Methods. 2021;18(10):1122–1127. doi:10.1038/s41592-021-01205-4.
  • Denisenko E, Guo BB, Jones M, Hou R, De Kock L, Lassmann T, Poppe D, Clément O, Simmons RK, Lister R. et al. Systematic assessment of tissue dissociation and storage biases in single-cell and single-nucleus RNA-seq workflows. Genome Biol. 2020;21(1). doi:10.1186/s13059-020-02048-6.
  • Xie Z, Bailey A, Kuleshov MV, Clarke DJB, Evangelista JE, Jenkins SL, Lachmann A, Wojciechowicz ML, Kropiwnicki E, Jagodnik KM. et al. Gene set knowledge discovery with Enrichr. Curr Protoc. 2021;1(3):e90. doi:10.1002/cpz1.90.
  • Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP. GSEA-P: a desktop application for gene set enrichment analysis. Bioinformatics. 2007;23(23):3251–3253. doi:10.1093/bioinformatics/btm369.
  • Kurtulus S, Madi A, Escobar G, Klapholz M, Nyman J, Christian E, Pawlak M, Dionne D, Xia J, Rozenblatt-Rosen O. et al. Checkpoint blockade immunotherapy induces dynamic changes in PD-1−CD8+ tumor-infiltrating T cells. Immunity. 2019;50(1):181–194.e186. doi:10.1016/j.immuni.2018.11.014.
  • Miller BC, Sen DR, Al Abosy R, Bi K, Virkud YV, Lafleur MW, Yates KB, Lako A, Felt K, Naik GS. et al. Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade. Nat Immunol. 2019;20(3):326–336. doi:10.1038/s41590-019-0312-6.
  • Kaech SM, Hemby S, Kersh E, Ahmed R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell. 2002;111(6):837–851. doi:10.1016/S0092-8674(02)01139-X.
  • Fairfax BP, Taylor CA, Watson RA, Nassiri I, Danielli S, Fang H, Mahé EA, Cooper R, Woodcock V, Traill Z. et al. Peripheral CD8+ T cell characteristics associated with durable responses to immune checkpoint blockade in patients with metastatic melanoma. Nat Med. 2020;26(2):193–199. doi:10.1038/s41591-019-0734-6.
  • Watson RA, Tong O, Cooper R, Taylor CA, Sharma PK, de Los Aires AV, Mahé EA, Ruffieux H, Nassiri I, Middleton MR. et al. Immune checkpoint blockade sensitivity and progression-free survival associates with baseline CD8(+) T cell clone size and cytotoxicity. Sci Immunol. 2021;6(64):eabj8825. doi:10.1126/sciimmunol.abj8825.
  • Valpione S, Galvani E, Tweedy J, Mundra PA, Banyard A, Middlehurst P, Barry J, Mills S, Salih Z, Weightman J. et al. Immune awakening revealed by peripheral T cell dynamics after one cycle of immunotherapy. Nat Cancer. 2020;1(2):210–221. doi:10.1038/s43018-019-0022-x.
  • Morgan DJ, Liblau R, Scott B, Fleck S, McDevitt HO, Sarvetnick N, Lo D, Sherman LA. CD8(+) T cell-mediated spontaneous diabetes in neonatal mice. J Immunol. 1996;157(3):978–983. doi:10.4049/jimmunol.157.3.978.
  • Zemek RM, Chin WL, Fear VS, Wylie B, Casey TH, Forbes C, Tilsed CM, Boon L, Guo BB, Bosco A. et al. Temporally restricted activation of IFNbeta signaling underlies response to immune checkpoint therapy in mice. Nat Commun. 2022;13(1):4895. doi:10.1038/s41467-022-32567-8.
  • Huuhtanen J, Chen L, Jokinen E, Kasanen H, Lonnberg T, Kreutzman A, Peltola K, Hernberg M, Wang C, Yee C. et al. Evolution and modulation of antigen-specific T cell responses in melanoma patients. Nat Commun. 2022;13(1):5988. doi:10.1038/s41467-022-33720-z.
  • Tan Z, Chiu MS, Yan CW, Man K, Chen Z. Eliminating mesothelioma by AAV-vectored, PD1-based vaccination in the tumor microenvironment. Mol Ther Oncolytics. 2021;20:373–386. doi:10.1016/j.omto.2021.01.010.
  • Rudqvist N-P, Pilones KA, Lhuillier C, Wennerberg E, Sidhom J-W, Emerson RO, Robins HS, Schneck J, Formenti SC, Demaria S. Radiotherapy and CTLA-4 blockade shape the TCR repertoire of tumor-infiltrating T cells. Cancer Immunol Res. 2018;6(2):139–150. doi:10.1158/2326-6066.CIR-17-0134.
  • Stringhini M, Probst P, Neri D. Immunotherapy of CT26 murine tumors is characterized by an oligoclonal response of tissue‐resident memory T cells against the AH1 rejection antigen. Eur J Immunol. 2020;50(10):1591–1597. doi:10.1002/eji.201948433.
  • Hosoi A, Takeda K, Nagaoka K, Iino T, Matsushita H, Ueha S, Aoki S, Matsushima K, Kubo M, Morikawa T. et al. Increased diversity with reduced “diversity evenness” of tumor infiltrating T-cells for the successful cancer immunotherapy. Sci Rep. 2018;8(1). doi:10.1038/s41598-018-19548-y.
  • Zhigalova EA, Izosimova AI, Yuzhakova DV, Volchkova LN, Shagina IA, Turchaninova MA, Serebrovskaya EO, Zagaynova EV, Chudakov DM, Sharonov GV. RNA-Seq-based TCR profiling reveals persistently increased intratumoral clonality in responders to anti-PD-1 therapy. Front Oncol. 2020;10(385). doi:10.3389/fonc.2020.00385.
  • Yusko E, Vignali M, Wilson RK, Mardis ER, Hodi FS, Horak C, Chang H, Woods DM, Robins H, Weber J. Association of tumor microenvironment T-cell repertoire and mutational load with clinical outcome after sequential checkpoint blockade in melanoma. Cancer Immunol Res. 2019;7(3):458–465. doi:10.1158/2326-6066.CIR-18-0226.
  • Valpione S, Mundra PA, Galvani E, Campana LG, Lorigan P, De Rosa F, Gupta A, Weightman J, Mills S, Dhomen N. et al. The T cell receptor repertoire of tumor infiltrating T cells is predictive and prognostic for cancer survival. Nat Commun. 2021;12(1). doi:10.1038/s41467-021-24343-x.
  • Amaria RN, Reddy SM, Tawbi HA, Davies MA, Ross MI, Glitza IC, Cormier JN, Lewis C, Hwu W-J, Hanna E. et al. Neoadjuvant immune checkpoint blockade in high-risk resectable melanoma. Nat Med. 2018;24(11):1649–1654. doi:10.1038/s41591-018-0197-1.
  • Johnson DB, Frampton GM, Rioth MJ, Yusko E, Xu Y, Guo X, Ennis RC, Fabrizio D, Chalmers ZR, Greenbowe J. et al. Targeted next generation sequencing identifies markers of response to PD-1 blockade. Cancer Immunol Res. 2016;4(11):959–967. doi:10.1158/2326-6066.CIR-16-0143.
  • Tsunoda M, Aoki H, Shimizu H, Shichino S, Matsushima K, Ueha S. Proportional tumor infiltration of T cells via circulation duplicates the T cell receptor repertoire in a bilateral tumor mouse model. Front Immunol. 2021;12:744381. doi:10.3389/fimmu.2021.744381.
  • Chen IX, Newcomer K, Pauken KE, Juneja VR, Naxerova K, Wu MW, Pinter M, Sen DR, Singer M, Sharpe AH. et al. A bilateral tumor model identifies transcriptional programs associated with patient response to immune checkpoint blockade. Proc Natl Acad Sci USA. 2020;117(38):23684–23694. doi:10.1073/pnas.2002806117.
  • Ma S, Chee J, Fear VS, Forbes CA, Boon L, Dick IM, Robinson BWS, Creaney J. Pre-treatment tumor neo-antigen responses in draining lymph nodes are infrequent but predict checkpoint blockade therapy outcome. OncoImmunology. 2020;9(1):1684714. doi:10.1080/2162402X.2019.1684714.
  • Siddiqui I, Schaeuble K, Chennupati V, Fuertes Marraco SA, Calderon-Copete S, Pais Ferreira D, Carmona SJ, Scarpellino L, Gfeller D, Pradervand S. et al. Intratumoral Tcf1+PD-1+CD8+ T cells with stem-like properties promote tumor control in response to vaccination and checkpoint blockade immunotherapy. Immunity. 2019;50(1):195–211.e110. doi:10.1016/j.immuni.2018.12.021.
  • Lee S, Zhao L, Little LD, Westin SN, Jazarei AA, Fleming ND, Zhang J, Futreal PA, Sood AK. Sood AK: distinct T cell receptor repertoire diversity of clinically defined high-grade serous ovarian cancer treatment subgroups. iScience. 2021;24(2):102053. doi:10.1016/j.isci.2021.102053.