1,211
Views
3
CrossRef citations to date
0
Altmetric
Original research

Bone marrow expands the repertoire of functional T cells targeting tumor-associated antigens in patients with resectable non-small-cell lung cancer

ORCID Icon, , , , , , , , , , , , & show all
Article: e1671762 | Received 21 Jun 2019, Accepted 19 Sep 2019, Published online: 23 Oct 2019

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):1–12. doi:10.3322/caac.21387.
  • Ettinger DS, Akerley W, Borghaei H, Chang AC, Cheney RT, Chirieac LR, D’Amico TA, Demmy TL, Govindan R, Grannis FW, et al. Non-small cell lung cancer, version 2.2013. J Natl Compr Canc Netw. 2013;11(6):645–653. doi:10.6004/jnccn.2013.0084.
  • Asamura H, Goya T, Koshiishi Y, Sohara Y, Eguchi K, Mori M, Nakanishi Y, Tsuchiya R, Shimokata K, Inoue H, et al. A Japanese lung cancer registry study: prognosis of 13,010 resected lung cancers. J Thorac Oncol. 2008;3(1):46–52. doi:10.1097/JTO.0b013e31815e8577.
  • Yamauchi Y, Muley T, Safi S, Rieken S, Bischoff H, Kappes J, Warth A, Herth FJ, Dienemann H, Hoffmann H. The dynamic pattern of recurrence in curatively resected non-small cell lung cancer patients: experiences at a single institution. Lung Cancer. 2015;90(2):224–229. doi:10.1016/j.lungcan.2015.09.010.
  • Goss GD, O’Callaghan C, Lorimer I, Tsao MS, Masters GA, Jett J, Edelman MJ, Lilenbaum R, Choy H, Khuri F, et al. Gefitinib versus placebo in completely resected non-small-cell lung cancer: results of the NCIC CTG BR19 study. J Clin Oncol. 2013;31(27):3320–3326. doi:10.1200/JCO.2013.51.1816.
  • Lievense LA, Sterman DH, Cornelissen R, Aerts JG. Checkpoint blockade in lung cancer and mesothelioma. Am J Respir Crit Care Med. 2017;196(3):274–282. doi:10.1164/rccm.201608-1755CI.
  • Vachani A, Sequist LV, Spira A. AJRCCM: 100-year anniversary. The shifting landscape for lung cancer: past, present, and future. Am J Respir Crit Care Med. 2017;195(9):1150–1160. doi:10.1164/rccm.201702-0433CI.
  • Safi S, Yamauchi Y, Rathinasamy A, Stamova S, Eichhorn M, Warth A, Rauch G, Dienemann H, Hoffmann H, Beckhove P. Functional T cells targeting tumor-associated antigens are predictive for recurrence-free survival of patients with radically operated non-small cell lung cancer. Oncoimmunology. 2017;6(11):e1360458. doi:10.1080/2162402X.2017.1360458.
  • Ganusov VV, De Boer RJ. Do most lymphocytes in humans really reside in the gut? Trends Immunol. 2007;28(12):514–518. doi:10.1016/j.it.2007.08.009.
  • Mazo IB, Honczarenko M, Leung H, Cavanagh LL, Bonasio R, Weninger W, Engelke K, Xia L, McEver RP, Koni PA, et al. Bone marrow is a major reservoir and site of recruitment for central memory CD8+ T cells. Immunity. 2005;22(2):259–270. doi:10.1016/j.immuni.2005.01.008.
  • Feuerer M, Beckhove P, Garbi N, Mahnke Y, Limmer A, Hommel M, Hammerling GJ, Kyewski B, Hamann A, Umansky V, et al. Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat Med. 2003;9(9):1151–1157. doi:10.1038/nm914.
  • Beckhove P, Feuerer M, Dolenc M, Schuetz F, Choi C, Sommerfeldt N, Schwendemann J, Ehlert K, Altevogt P, Bastert G, et al. Specifically activated memory T cell subsets from cancer patients recognize and reject xenotransplanted autologous tumors. J Clin Invest. 2004;114(1):67–76. doi:10.1172/JCI20278.
  • Domschke C, Ge Y, Bernhardt I, Schott S, Keim S, Juenger S, Bucur M, Mayer L, Blumenstein M, Rom J, et al. Long-term survival after adoptive bone marrow T cell therapy of advanced metastasized breast cancer: follow-up analysis of a clinical pilot trial. Cancer Immunol Immunother. 2013;62(6):1053–1060. doi:10.1007/s00262-013-1414-x.
  • Schmitz-Winnenthal FH, Volk C, Z’Graggen K, Galindo L, Nummer D, Ziouta Y, Bucur M, Weitz J, Schirrmacher V, Buchler MW, et al. High frequencies of functional tumor-reactive T cells in bone marrow and blood of pancreatic cancer patients. Cancer Res. 2005;65(21):10079–10087. doi:10.1158/0008-5472.can-05-1098.
  • Sommerfeldt N, Schutz F, Sohn C, Forster J, Schirrmacher V, Beckhove P. The shaping of a polyvalent and highly individual T-cell repertoire in the bone marrow of breast cancer patients. Cancer Research. 2006;66(16):8258–8265. doi:10.1158/0008-5472.can-05-4201.
  • Schirrmacher V. Cancer-reactive memory T cells from bone marrow: spontaneous induction and therapeutic potential (Review). Int J Oncol. 2015;47(6):2005–2016. doi:10.3892/ijo.2015.3197.
  • Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, Almeida JR, Gostick E, Yu Z, Carpenito C, et al. A human memory T cell subset with stem cell-like properties. Nat Med. 2011;17(10):1290–1297. doi:10.1038/nm.2446.
  • Mueller SN, Gebhardt T, Carbone FR, Heath WR. Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol. 2013:31137–31161. doi:10.1146/annurev-immunol-032712-095954.
  • Schwendemann J, Choi C, Schirrmacher V, Beckhove P. Dynamic differentiation of activated human peripheral blood CD8+ and CD4+ effector memory T cells. J Immunol. 2005;175(3):1433–1439. doi:10.4049/jimmunol.175.3.1433.
  • Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, Hoff ST, Andersen P, Reed SG, Morris SL, et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med. 2007;13(7):843–850. doi:10.1038/nm1592.
  • Reissfelder C, Stamova S, Gossmann C, Braun M, Bonertz A, Walliczek U, Grimm M, Rahbari NN, Koch M, Saadati M, et al. Tumor-specific cytotoxic T lymphocyte activity determines colorectal cancer patient prognosis. J Clin Invest. 2015;125(2):739–751. doi:10.1172/JCI74894.
  • Farber DL, Yudanin NA, Restifo NP. Human memory T cells: generation, compartmentalization and homeostasis. Nat Rev Immunol. 2014;14(1):24–35. doi:10.1038/nri3567.
  • Chen DS, Mellman I. Elements of cancer immunity and the cancer-immune set point. Nature. 2017;541(7637):321–330. doi:10.1038/nature21349.
  • Muller-Berghaus J, Ehlert K, Ugurel S, Umansky V, Bucur M, Schirrmacher V, Beckhove P, Schadendorf D. Melanoma-reactive T cells in the bone marrow of melanoma patients: association with disease stage and disease duration. Cancer Research. 2006;66(12):5997–6001. doi:10.1158/0008-5472.CAN-04-0484.
  • Koch M, Beckhove P, Winkel J, Autenrieth D, Wagner P, Nummer D, Specht S, Antolovic D, Galindo L, Schmitz-Winnenthal FH, et al. Tumor infiltrating T lymphocytes in colorectal cancer: tumor-selective activation and cytotoxic activity in situ. Annals of Surgery. 2006;244(6):986–992. doi:10.1097/01.sla.0000247058.43243.7b.
  • Krishnadas DK, Shusterman S, Bai F, Diller L, Sullivan JE, Cheerva AC, George RE, Lucas KG. A phase I trial combining decitabine/dendritic cell vaccine targeting MAGE-A1, MAGE-A3 and NY-ESO-1 for children with relapsed or therapy-refractory neuroblastoma and sarcoma. Cancer Immunol Immunother. 2015;64(10):1251–1260. doi:10.1007/s00262-015-1731-3.
  • Li D, Bentley C, Anderson A, Wiblin S, Cleary KLS, Koustoulidou S, Hassanali T, Yates J, Greig J, Nordkamp MO, et al. Development of a T-cell receptor mimic antibody against wild-type p53 for cancer immunotherapy. Cancer Res. 2017;77(10):2699–2711. doi:10.1158/0008-5472.CAN-16-3247.
  • Ahmed N, Brawley VS, Hegde M, Robertson C, Ghazi A, Gerken C, Liu E, Dakhova O, Ashoori A, Corder A, et al. Human epidermal growth factor receptor 2 (HER2) -specific chimeric antigen receptor-modified T cells for the immunotherapy of HER2-positive sarcoma. J Clin Oncol. 2015;33(15):1688–1696. doi:10.1200/JCO.2014.58.0225.
  • Casey NP, Fujiwara H, Ochi T, Yasukawa M. Novel immunotherapy for adult T-cell leukemia/lymphoma: targeting aurora kinase A. Oncoimmunology. 2016;5(11):e1239006. doi:10.1080/2162402X.2016.1239006.
  • Zou L, Barnett B, Safah H, Larussa VF, Evdemon-Hogan M, Mottram P, Wei S, David O, Curiel TJ, Zou W. Bone marrow is a reservoir for CD4+CD25+ regulatory T cells that traffic through CXCL12/CXCR4 signals. Cancer Res. 2004;64(22):8451–8455. doi:10.1158/0008-5472.CAN-04-1987.
  • Rathinasamy A, Domschke C, Ge Y, Bohm HH, Dettling S, Jansen D, Lasitschka F, Umansky L, Graler MH, Hartmann J, et al. Tumor specific regulatory T cells in the bone marrow of breast cancer patients selectively upregulate the emigration receptor S1P1. Cancer Immunol Immunother. 2017;66(5):593–603. doi:10.1007/s00262-017-1964-4.
  • Schmidt HH, Ge Y, Hartmann FJ, Conrad H, Klug F, Nittel S, Bernhard H, Domschke C, Schuetz F, Sohn C, et al. HLA Class II tetramers reveal tissue-specific regulatory T cells that suppress T-cell responses in breast carcinoma patients. Oncoimmunology. 2013;2(6):e24962. doi:10.4161/onci.24962.
  • Nagarsheth N, Wicha MS, Zou W. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nat Rev Immunol. 2017;17(9):559–572. doi:10.1038/nri.2017.49.
  • Pritz T, Landgraf-Rauf K, Herndler-Brandstetter D, Rauf R, Lair J, Gassner R, Weinberger B, Krismer M, Grubeck-Loebenstein B. Bone marrow T cells from the femur are similar to iliac crest derived cells in old age and represent a useful tool for studying the aged immune system. Immun Ageing. 2013;10(1):17. doi:10.1186/1742-4933-10-17.
  • Di Rosa F. Two Niches in the Bone Marrow: a hypothesis on life-long T cell memory. Trends Immunol. 2016;37(8):503–512. doi:10.1016/j.it.2016.05.004.
  • Choi C, Witzens M, Bucur M, Feuerer M, Sommerfeldt N, Trojan A, Ho A, Schirrmacher V, Goldschmidt H, Beckhove P. Enrichment of functional CD8 memory T cells specific for MUC1 in bone marrow of patients with multiple myeloma. Blood. 2005;105(5):2132–2134. doi:10.1182/blood-2004-01-0366.
  • Okhrimenko A, Grun JR, Westendorf K, Fang Z, Reinke S, von Roth P, Wassilew G, Kuhl AA, Kudernatsch R, Demski S, et al. Human memory T cells from the bone marrow are resting and maintain long-lasting systemic memory. Proc Natl Acad Sci U S A. 2014;111(25):9229–9234. doi:10.1073/pnas.1318731111.
  • Im SJ, Hashimoto M, Gerner MY, Lee J, Kissick HT, Burger MC, Shan Q, Hale JS, Lee J, Nasti TH, et al. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature. 2016;537(7620):417–421. doi:10.1038/nature19330.
  • Schulze T, Kemmner W, Weitz J, Wernecke KD, Schirrmacher V, Schlag PM. Efficiency of adjuvant active specific immunization with Newcastle disease virus modified tumor cells in colorectal cancer patients following resection of liver metastases: results of a prospective randomized trial. Cancer Immunol Immunother. 2009;58(1):61–69. doi:10.1007/s00262-008-0526-1.
  • Schirrmacher V, Fournier P, Schlag P. Autologous tumor cell vaccines for post-operative active-specific immunotherapy of colorectal carcinoma: long-term patient survival and mechanism of function. Expert Rev Vaccines. 2014;13(1):117–130. doi:10.1586/14760584.2014.854169.
  • Sharma P, Hu-Lieskovan S, Wargo JA, Primary RA. Adaptive, and acquired resistance to cancer immunotherapy. Cell. 2017;168(4):707–723. doi:10.1016/j.cell.2017.01.017.
  • Feuerer M, Beckhove P, Bai L, Solomayer EF, Bastert G, Diel IJ, Pedain C, Oberniedermayr M, Schirrmacher V, Umansky V. Therapy of human tumors in NOD/SCID mice with patient-derived reactivated memory T cells from bone marrow. Nat Med. 2001;7:452–458.
  • Dienemann H, Hoffmann H, Koebe HG. Technique and rationale of lymph node dissection in bronchial carcinoma. Chirurg. 1998;69(4):412–417. doi:10.1007/s001040050431.
  • Lardinois D, De Leyn P, Van Schil P, Porta RR, Waller D, Passlick B, Zielinski M, Lerut T, Weder W. ESTS guidelines for intraoperative lymph node staging in non-small cell lung cancer. Eur J Cardiothorac Surg. 2006;30(5):787–792. doi:10.1016/j.ejcts.2006.08.008.
  • Reissfelder C, Timke C, Schmitz-Winnenthal H, Rahbari NN, Koch M, Klug F, Roeder F, Edler L, Debus J, Buchler MW, et al. A randomized controlled trial to investigate the influence of low dose radiotherapy on immune stimulatory effects in liver metastases of colorectal cancer. BMC Cancer. 2011;11419. doi:10.1186/1471-2407-11-419.
  • Bland JM, Altman DG. Analysis of continuous data from small samples. BMJ. 2009:338a3166. doi:10.1136/bmj.a3166.
  • Karulin AY, Caspell R, Dittrich M, Lehmann PV. Normal distribution of CD8+ T-cell-derived ELISPOT counts within replicates justifies the reliance on parametric statistics for identifying positive responses. Cells. 2015;4(1):96–111. doi:10.3390/cells4010096.