Microparticles from tumors exposed to radiation promote immune evasion in part by PD-L1.

Szczegóły
Abstrakt

Tytuł:: Microparticles from tumors exposed to radiation promote immune evasion in part by PD-L1.
Autorzy:: Timaner M; Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion, Haifa, Israel.
Kotsofruk R; Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion, Haifa, Israel.
Raviv Z; Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion, Haifa, Israel.
Magidey K; Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion, Haifa, Israel.
Shechter D; Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion, Haifa, Israel.
Kan T; Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion, Haifa, Israel.
Nevelsky A; Oncology Institute, Radiation Oncology Unit, Rambam Health Care Campus, Haifa, Israel.
Daniel S; Oncology Institute, Radiation Oncology Unit, Rambam Health Care Campus, Haifa, Israel.
de Vries EGE; Department of Medical Oncology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
Zhang T; Division of Cancer Epidemiology & Genetics, Integrative Tumor Epidemiology Branch, National Cancer Institute, National Institute of Health, Bethesda, MD, USA.
Kaidar-Person O; Oncology Institute, Radiation Oncology Unit, Rambam Health Care Campus, Haifa, Israel.
Kerbel RS; Sunnybrook Health Sciences Centre, Toronto, ON, Canada.
Shaked Y; Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion, Haifa, Israel. .
Źródło:: Oncogene [Oncogene] 2020 Jan; Vol. 39 (1), pp. 187-203. Date of Electronic Publication: 2019 Aug 29.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Publication: <2002->: Basingstoke : Nature Publishing Group
Original Publication: Basingstoke, Hampshire, UK : Scientific & Medical Division, MacMillan Press, c1987-
MeSH Terms:: B7-H1 Antigen/*genetics
Breast Neoplasms/*radiotherapy
Cell-Derived Microparticles/*immunology
Immunomodulation/*immunology
Animals ; B7-H1 Antigen/immunology ; Breast Neoplasms/genetics ; Breast Neoplasms/immunology ; Cell Line, Tumor ; Cell-Derived Microparticles/genetics ; Cell-Derived Microparticles/radiation effects ; Female ; Heterografts ; Humans ; Immune Evasion/immunology ; Immune Evasion/radiation effects ; Immunomodulation/radiation effects ; Mice ; Programmed Cell Death 1 Receptor/genetics ; Programmed Cell Death 1 Receptor/immunology ; Signal Transduction/radiation effects ; T-Lymphocytes, Cytotoxic/immunology ; T-Lymphocytes, Cytotoxic/radiation effects
References:: Barcellos-Hoff MH. Integrative radiation carcinogenesis: interactions between cell and tissue responses to DNA damage. Semin Cancer Biol. 2005;15:138–48. (PMID: 1565245910.1016/j.semcancer.2004.08.010)
Stone HB, Peters LJ, Milas L. Effect of host immune capability on radiocurability and subsequent transplantability of a murine fibrosarcoma. J Natl Cancer Inst. 1979;63:1229–35. (PMID: 291749)
Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment - tumorigenesis and therapy. Nat Rev Cancer. 2005;5:867–75. (PMID: 1632776510.1038/nrc1735)
Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol. 2009;10:718–26. (PMID: 19573801278294310.1016/S1470-2045(09)70082-8)
Timaner M, Bril R, Kaidar-Person O, Rachman-Tzemah C, Alishekevitz D, Kotsofruk R, et al. Dequalinium blocks macrophage-induced metastasis following local radiation. Oncotarget. 2015;6:27537–54. (PMID: 26348470469500710.18632/oncotarget.4826)
De Palma M, Lewis CE. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell. 2013;23:277–86. (PMID: 2351834710.1016/j.ccr.2013.02.013)
Russell JS, Brown JM. The irradiated tumor microenvironment: role of tumor-associated macrophages in vascular recovery. Front Physiol. 2013;4:157. (PMID: 23882218371333110.3389/fphys.2013.00157)
Ahn GO, Brown JM. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell. 2008;13:193–205. (PMID: 18328424296744110.1016/j.ccr.2007.11.032)
Barker HE, Paget JT, Khan AA, Harrington KJ. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat Rev Cancer. 2015;15:409–25. (PMID: 26105538489638910.1038/nrc3958)
Shaked Y. Balancing efficacy of and host immune responses to cancer therapy: the yin and yang effects. Nat Rev Clin Oncol. 2016;13:611–26. (PMID: 2711849310.1038/nrclinonc.2016.57)
Wargo JA, Reuben A, Cooper ZA, Oh KS, Sullivan RJ. Immune effects of chemotherapy, radiation, and targeted therapy and opportunities for combination with immunotherapy. Semin Oncol. 2015;42:601–16. (PMID: 26320064495594010.1053/j.seminoncol.2015.05.007)
Ehlers G, Fridman M. Abscopal effect of radiation in papillary adenocarcinoma. Br J Radio. 1973;46:220–2. (PMID: 10.1259/0007-1285-46-543-220)
Wersall PJ, Blomgren H, Pisa P, Lax I, Kalkner KM, Svedman C. Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma. Acta Oncol. 2006;45:493–7. (PMID: 1676019010.1080/02841860600604611)
Rose B, Mitra D, Hong TS, Jee KW, Niemierko A, Drapek LN, et al. Irradiation of anatomically defined pelvic subsites and acute hematologic toxicity in anal cancer patients undergoing chemoradiation. Pr Radiat Oncol. 2017;7:e291–7. (PMID: 10.1016/j.prro.2017.03.008)
Mell LK, Sirak I, Wei L, Tarnawski R, Mahantshetty U, Yashar CM, et al. Bone marrow-sparing intensity modulated radiation therapy with concurrent cisplatin for stage IB-IVA cervical cancer: an international multicenter phase II clinical trial (INTERTECC-2). Int J Radiat Oncol Biol Phys. 2017;97:536–45. (PMID: 2812630310.1016/j.ijrobp.2016.11.027)
Sharabi AB, Lim M, DeWeese TL, Drake CG. Radiation and checkpoint blockade immunotherapy: radiosensitisation and potential mechanisms of synergy. Lancet Oncol. 2015;16:e498–509. (PMID: 2643382310.1016/S1470-2045(15)00007-8)
Reynders K, De Ruysscher D. Radiotherapy and immunotherapy: improving cancer treatment through synergy. Prog tumor Res. 2015;42:67–78. (PMID: 2638384810.1159/000437185)
Kang J, Demaria S, Formenti S. Current clinical trials testing the combination of immunotherapy with radiotherapy. J Immunother Cancer. 2016;4:51. (PMID: 27660705502896410.1186/s40425-016-0156-7)
Fremder E, Munster M, Aharon A, Miller V, Gingis-Velitski S, Voloshin T, et al. Tumor-derived microparticles induce bone marrow-derived cell mobilization and tumor homing: a process regulated by osteopontin. Int J cancer J Int du cancer. 2014;135:270–81. (PMID: 10.1002/ijc.28678)
Voloshin T, Fremder E, Shaked Y. Small but mighty: microparticles as mediators of tumor progression. Cancer Micro. 2014;7:11–21. (PMID: 10.1007/s12307-014-0144-8)
Al-Nedawi K, Meehan B, Rak J. Microvesicles: messengers and mediators of tumor progression. Cell Cycle. 2009;8:2014–8. (PMID: 1953589610.4161/cc.8.13.8988)
Rak J. Microparticles in cancer. Semin Thromb Hemost. 2010;36:888–906. (PMID: 2104939010.1055/s-0030-1267043)
Lee TH, D’Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J. Microvesicles as mediators of intercellular communication in cancer–the emerging science of cellular ‘debris’. Semin Immunopathol. 2011;33:455–67. (PMID: 2131841310.1007/s00281-011-0250-3)
Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. NatMed. 2012;18:883–91.
Keklikoglou I, Cianciaruso C, Guc E, Squadrito ML, Spring LM, Tazzyman S, et al. Chemotherapy elicits pro-metastatic extracellular vesicles in breast cancer models. Nat Cell Biol. 2019;21:190–202. (PMID: 3059853110.1038/s41556-018-0256-3)
Ricklefs FL, Alayo Q, Krenzlin H, Mahmoud AB, Speranza MC, Nakashima H, et al. Immune evasion mediated by PD-L1 on glioblastoma-derived extracellular vesicles. Sci Adv. 2018;4:eaar2766. (PMID: 29532035584203810.1126/sciadv.aar2766)
Chen G, Huang AC, Zhang W, Zhang G, Wu M, Xu W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 2018;560:382–6. (PMID: 30089911609574010.1038/s41586-018-0392-8)
Ma R, Ji T, Chen D, Dong W, Zhang H, Yin X, et al. Tumor cell-derived microparticles polarize M2 tumor-associated macrophages for tumor progression. Oncoimmunology. 2016;5:e1118599. (PMID: 27141404483932410.1080/2162402X.2015.1118599)
Tang K, Zhang Y, Zhang H, Xu P, Liu J, Ma J, et al. Delivery of chemotherapeutic drugs in tumour cell-derived microparticles. Nat Commun. 2012;3:1282. (PMID: 2325041210.1038/ncomms2282)
Mege D, Panicot-Dubois L, Dubois C. Tumor-derived microparticles to monitor colorectal cancer evolution. Methods Mol Biol. 2018;1765:271–7. (PMID: 2958931410.1007/978-1-4939-7765-9_17)
Zhao L, Bi Y, Kou J, Shi J, Piao D. Phosphatidylserine exposing-platelets and microparticles promote procoagulant activity in colon cancer patients. J Exp Clin Cancer Res. 2016;35:54. (PMID: 27015840480754310.1186/s13046-016-0328-9)
Jaiswal R, Luk F, Dalla PV, Grau GE, Bebawy M. Breast cancer-derived microparticles display tissue selectivity in the transfer of resistance proteins to cells. PloS ONE. 2013;8:e61515. (PMID: 23593486362515410.1371/journal.pone.0061515)
Issman L, Brenner B, Talmon Y, Aharon A. Cryogenic transmission electron microscopy nanostructural study of shed microparticles. PloS ONE. 2013;8:e83680. (PMID: 24386253387332510.1371/journal.pone.0083680)
Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA. 2001;98:5116–21. (PMID: 1130949910.1073/pnas.09106249833173)
Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–64. (PMID: 22437870485602310.1038/nrc3239)
Sharma P, Allison JP. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell. 2015;161:205–14. (PMID: 25860605590567410.1016/j.cell.2015.03.030)
Makinde AY, Eke I, Aryankalayil MJ, Ahmed MM, Coleman CN. Exploiting gene expression kinetics in conventional radiotherapy, hyperfractionation, and hypofractionation for targeted therapy. Semin Radiat Oncol. 2016;26:254–60. (PMID: 27619247502306610.1016/j.semradonc.2016.07.001)
Palayoor ST, John-Aryankalayil M, Makinde AY, Falduto MT, Magnuson SR, Coleman CN. Differential expression of stress and immune response pathway transcripts and miRNAs in normal human endothelial cells subjected to fractionated or single-dose radiation. Mol Cancer Res. 2014;12:1002–15. (PMID: 24784841410105310.1158/1541-7786.MCR-13-0623)
Hutchinson L. Radiotherapy: repopulating tumor cells–dying for caspase 3. Nat Rev Clin Oncol. 2011;8:508. (PMID: 2178897210.1038/nrclinonc.2011.112)
Matsumura S, Wang B, Kawashima N, Braunstein S, Badura M, Cameron TO, et al. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol. 2008;181:3099–107. (PMID: 1871398010.4049/jimmunol.181.5.3099)
Meng Y, Mauceri HJ, Khodarev NN, Darga TE, Pitroda SP, Beckett MA, et al. Ad.Egr-TNF and local ionizing radiation suppress metastases by interferon-beta-dependent activation of antigen-specific CD8+ T cells. Mol Ther : J Am Soc Gene Ther. 2010;18:912–20. (PMID: 10.1038/mt.2010.18)
Koller KM, Mackley HB, Liu J, Wagner H, Talamo G, Schell TD, et al. Improved survival and complete response rates in patients with advanced melanoma treated with concurrent ipilimumab and radiotherapy versus ipilimumab alone. Cancer Biol Ther. 2017;18:36–42. (PMID: 2790582410.1080/15384047.2016.1264543)
Dovedi SJ, Adlard AL, Lipowska-Bhalla G, McKenna C, Jones S, Cheadle EJ, et al. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res. 2014;74:5458–68. (PMID: 2527403210.1158/0008-5472.CAN-14-1258)
Deng L, Liang H, Burnette B, Beckett M, Darga T, Weichselbaum RR, et al. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest. 2014;124:687–95. (PMID: 24382348390460110.1172/JCI67313)
Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer. 2017;17:302–17. (PMID: 2830390510.1038/nrc.2017.6)
Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol. 2015;33:1974–82. (PMID: 25605845498057310.1200/JCO.2014.59.4358)
Wolford CC, McConoughey SJ, Jalgaonkar SP, Leon M, Merchant AS, Dominick JL, et al. Transcription factor ATF3 links host adaptive response to breast cancer metastasis. J Clin Invest. 2013;123:2893–906. (PMID: 23921126369654810.1172/JCI64410)
Fu YX, Watson G, Jimenez JJ, Wang Y, Lopez DM. Expansion of immunoregulatory macrophages by granulocyte-macrophage colony-stimulating factor derived from a murine mammary tumor. Cancer Res. 1990;50:227–34. (PMID: 2136804)
Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8:2281–308. (PMID: 24157548396986010.1038/nprot.2013.143)
Tyanova S, Cox J. Perseus: a bioinformatics platform for integrative analysis of proteomics data in cancer research. Methods Mol Biol. 2018;1711:133–48. (PMID: 2934488810.1007/978-1-4939-7493-1_7)
Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, Mann M. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteom:MCP. 2014;13:2513–26. (PMID: 10.1074/mcp.M113.031591)
Timaner M, Beyar-Katz O, Shaked Y. Analysis of the stromal cellular components of the solid tumor microenvironment using flow cytometry. Curr Protoc Cell Biol. 2016;70:19 8 1–8 2. (PMID: 10.1002/0471143030.cb1918s70)
Genovesi EV, Pettey CL, Collins JJ. Use of adoptive transfer and Winn assay procedures in the further analysis of antiviral acquired immunity in mice protected against friend leukemia virus-induced disease by passive serum therapy. Cancer Res. 1984;44:1489–98. (PMID: 6608407)
Winn HJ. Immune mechanisms in homotransplantation. II. Quantitative assay of the immunologic activity of lymphoid cells stimulated by tumor homografts. J Immunol. 1961;86:228–39. (PMID: 13785862)
Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol methods. 1995;184:39–51. (PMID: 762286810.1016/0022-1759(95)00072-I)
Grant Information:: 260633 International ERC_ European Research Council; 771112 International ERC_ European Research Council
Substance Nomenclature:: 0 (B7-H1 Antigen)
0 (CD274 protein, human)
0 (PDCD1 protein, human)
0 (Programmed Cell Death 1 Receptor)
Entry Date(s):: Date Created: 20190831 Date Completed: 20200420 Latest Revision: 20220421
Update Code:: 20240104
PubMed Central ID:: PMC6937213
DOI:: 10.1038/s41388-019-0971-7
PMID:: 31467431
: Czasopismo naukowe

Radiotherapy induces immune-related responses in cancer patients by various mechanisms. Here, we investigate the immunomodulatory role of tumor-derived microparticles (TMPs)-extracellular vesicles shed from tumor cells-following radiotherapy. We demonstrate that breast carcinoma cells exposed to radiation shed TMPs containing elevated levels of immune-modulating proteins, one of which is programmed death-ligand 1 (PD-L1). These TMPs inhibit cytotoxic T lymphocyte (CTL) activity both in vitro and in vivo, and thus promote tumor growth. Evidently, adoptive transfer of CTLs pre-cultured with TMPs from irradiated breast carcinoma cells increases tumor growth rates in mice recipients in comparison with control mice receiving CTLs pre-cultured with TMPs from untreated tumor cells. In addition, blocking the PD-1-PD-L1 axis, either genetically or pharmacologically, partially alleviates TMP-mediated inhibition of CTL activity, suggesting that the immunomodulatory effects of TMPs in response to radiotherapy is mediated, in part, by PD-L1. Overall, our findings provide mechanistic insights into the tumor immune surveillance state in response to radiotherapy and suggest a therapeutic synergy between radiotherapy and immune checkpoint inhibitors.

Informacja