Tumor-derived exosomes modulate PD-L1 expression in monocytes

Science Immunology

Volumn 2, Issue 13, 2017, Pages

  Haderk, Franziska ^a   Schulz, Ralph ^a   Iskar, Murat ^a   Cid, Laura Llaó ^a   Worst, Thomas ^a   Willmund, Karolin V ^a   Schulz, Angela ^a   Warnken, Uwe ^a   Seiler, Jana ^a   Benner, Axel ^a   Nessling, Michelle ^a   Zenz, Thorsten ^b   Göbel, Maria ^c   Dürig, Jan ^c   Diederichs, Sven ^a,d   Paggetti, Jérôme ^e   Moussay, Etienne ^e   Stilgenbauer, Stephan ^f   Zapatka, Marc ^a   Lichter, Peter ^a   Seiffert, Martina ^a   more..

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^f UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85032353718     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aah5509     Document Type: Article

References (54)

1. D. Hanahan, R. A. Weinberg, Hallmarks of cancer: The next generation. Cell 144, 646–674 (2011).
2. A. Mantovani, F. Marchesi, A. Malesci, L. Laghi, P. Allavena, Tumour-associated macrophages as treatment targets in oncology. Nat. Rev. Clin. Oncol. 14, 399–416 (2017).
3. N. S. Nicholas, B. Apollonio, A. G. Ramsay, Tumor microenvironment (TME)-driven immune suppression in B cell malignancy. Biochim. Biophys. Acta 1863, 471–482 (2016).
4. A. Schulz, G. Toedt, T. Zenz, S. Stilgenbauer, P. Lichter, M. Seiffert, Inflammatory cytokines and signaling pathways are associated with survival of primary chronic lymphocytic leukemia cells in vitro: A dominant role of CCL2. Haematologica 96, 408–416 (2011).
5. lo myeloid-derived suppressor cells that inhibit T-cell responses and promote TRegs. Blood 124, 750–760 (2014).
6. R. Maffei, J. Bulgarelli, S. Fiorcari, L. Bertoncelli, S. Martinelli, C. Guarnotta, I. Castelli, S. Deaglio, G. Debbia, S. De Biasi, G. Bonacorsi, P. Zucchini, F. Narni, C. Tripodo, M. Luppi, A. Cossarizza, R. Marasca, The monocytic population in chronic lymphocytic leukemia shows altered composition and deregulation of genes involved in phagocytosis and inflammation. Haematologica 98, 1115–1123 (2013).
7. B. S. Hanna, F. McClanahan, H. Yazdanparast, N. Zaborsky, V. Kalter, P. M. Rößner, A. Benner, C. Dürr, A. Egle, J. G. Gribben, P. Lichter, M. Seiffert, Depletion of CLL-associated patrolling monocytes and macrophages controls disease development and repairs immune dysfunction in vivo. Leukemia 30, 570–579 (2016).
8. F. McClanahan, B. Hanna, S. Miller, A. J. Clear, P. Lichter, J. G. Gribben, M. Seiffert, PD-L1 checkpoint blockade prevents immune dysfunction and leukemia development in a mouse model of chronic lymphocytic leukemia. Blood 126, 203–211 (2015).
9. S. El-Andaloussi, Y. Lee, S. Lakhal-Littleton, J. Li, Y. Seow, C. Gardiner, L. Alvarez-Erviti, I. L. Sargent, M. J. A. Wood, Exosome-mediated delivery of siRNA in vitro and in vivo. Nat. Protoc. 7, 2112–2126 (2012).
10. P. D. Robbins, A. E. Morelli, Regulation of immune responses by extracellular vesicles. Nat. Rev. Immunol. 14, 195–208 (2014).
11. C. Théry, M. Ostrowski, E. Segura, Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581–593 (2009).
12. M. Colombo, G. Raposo, C. Théry, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30, 255–289 (2014).
13. G. Raposo, W. Stoorvogel, Extracellular vesicles: Exosomes, microvesicles, and friends. J. Cell Biol. 200, 373–383 (2013).
14. A. Zomer, C. Maynard, F. J. Verweij, A. Kamermans, R. Schäfer, E. Beerling, R. Michel Schiffelers, E. de Wit, J. Berenguer, S. I. J. Ellenbroek, T. Wurdinger, D. M. Pegtel, J. van Rheenen, In vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior. Cell 161, 1046–1057 (2015).
15. A. Montecalvo, A. T. Larregina, W. J. Shufesky, D. B. Stolz, M. L. G. Sullivan, J. M. Karlsson, C. J. Baty, G. A. Gibson, G. Erdos, Z. Wang, J. Milosevic, O. A. Tkacheva, S. J. Divito, R. Jordan, J. Lyons-Weiler, S. C. Watkins, A. E. Morelli, Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119, 756–766 (2012).
16. J. Skog, T. Würdinger, S. van Rijn, D. H. Meijer, L. Gainche, W. T. Curry Jr., B. S. Carter, A. M. Krichevsky, X. O. Breakefield, Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470–1476 (2008).
17. H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J. J. Lee, J. O. Lötvall, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654–659 (2007).
18. X. Huang, T. Yuan, M. Tschannen, Z. Sun, H. Jacob, M. Du, M. Liang, R. L. Dittmar, Y. Liu, M. Liang, M. Kohli, S. N. Thibodeau, L. Boardman, L. Wang, Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics 14, 319 (2013).
19. E. N. M. Nolte-’t Hoen, H. P. J. Buermans, M. Waasdorp, W. Stoorvogel, M. H. M. Wauben, P. A. C.’t Hoen, Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res. 40, 9272–9285 (2012).
20. C. P. Christov, T. J. Gardiner, D. Szüts, T. Krude, Functional requirement of noncoding Y RNAs for human chromosomal DNA replication. Mol. Cell. Biol. 26, 6993–7004 (2006).
21. S. Sim, D. E. Weinberg, G. Fuchs, K. Choi, J. Chung, S. L. Wolin, The subcellular distribution of an RNA quality control protein, the Ro autoantigen, is regulated by noncoding Y RNA binding. Mol. Biol. Cell 20, 1555–1564 (2009).
22. M. P. Kowalski, T. Krude, Functional roles of non-coding Y RNAs. Int. J. Biochem. Cell Biol. 66, 20–29 (2015).
23. F. E. Nicolas, A. E. Hall, T. Csorba, C. Turnbull, T. Dalmay, Biogenesis of Y RNA-derived small RNAs is independent of the microRNA pathway. FEBS Lett. 586, 1226–1230 (2012).
24. Y.-Y. Yeh, H. G. Ozer, A. M. Lehman, K. Maddocks, L. Yu, A. J. Johnson, J. C. Byrd, Characterization of CLL exosomes reveals a distinct microRNA signature and enhanced secretion by activation of BCR signaling. Blood 125, 3297–3305 (2015).
25. A. K. Ghosh, C. R. Secreto, T. R. Knox, W. Ding, D. Mukhopadhyay, N. E. Kay, Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: Implications for disease progression. Blood 115, 1755–1764 (2010).
26. J. Paggetti, F. Haderk, M. Seiffert, B. Janji, U. Distler, W. Ammerlaan, Y. J. Kim, J. Adam, P. Lichter, E. Solary, G. Berchem, E. Moussay, Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 126, 1106–1117 (2015).
27. F. Haderk, B. Hanna, K. Richter, M. Schnölzer, T. Zenz, S. Stilgenbauer, P. Lichter, M. Seiffert, Extracellular vesicles in chronic lymphocytic leukemia. Leuk. Lymphoma 54, 1826–1830 (2013).
28. T. Aung, B. Chapuy, D. Vogel, D. Wenzel, M. Oppermann, M. Lahmann, T. Weinhage, K. Menck, T. Hupfeld, R. Koch, L. Trümper, G. G. Wulf, Exosomal evasion of humoral immunotherapy in aggressive B-cell lymphoma modulated by ATP-binding cassette transporter A3. Proc. Natl. Acad. Sci. U.S.A. 108, 15336–15341 (2011).
29. V. Balatti, Y. Pekarky, C. M. Croce, Role of microRNA in chronic lymphocytic leukemia onset and progression. J. Hematol. Oncol. 8, 12 (2015).
30. G. A. Calin, M. Ferracin, A. Cimmino, G. Di Leva, M. Shimizu, S. E. Wojcik, M. V. Iorio, R. Visone, N. I. Sever, M. Fabbri, R. Iuliano, T. Palumbo, F. Pichiorri, C. Roldo, R. Garzon, C. Sevignani, L. Rassenti, H. Alder, S. Volinia, C.G. Liu, T. J. Kipps, M. Negrini, C. M. Croce, A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353, 1793–1801 (2005).
31. J. M. Dhahbi, S. R. Spindler, H. Atamna, D. Boffelli, P. Mote, D. I. K. Martin, 5′-YRNA fragments derived by processing of transcripts from specific YRNA genes and pseudogenes are abundant in human serum and plasma. Physiol. Genomics 45, 990–998 (2013).
32. J. P. Tosar, F. Gámbaro, J. Sanguinetti, B. Bonilla, K. W. Witwer, A. Cayota, Assessment of small RNA sorting into different extracellular fractions revealed by high-throughput sequencing of breast cell lines. Nucleic Acids Res. 43, 5601–5616 (2015).
33. M. Köhn, N. Pazaitis, S. Hüttelmaier, Why YRNAs? About versatile RNAs and their functions. Biomolecules 3, 143–156 (2013).
34. C. P. Christov, E. Trivier, T. Krude, Noncoding human Y RNAs are overexpressed in tumours and required for cell proliferation. Br. J. Cancer 98, 981–988 (2008).
35. M. Fabbri, A. Paone, F. Calore, R. Galli, E. Gaudio, R. Santhanam, F. Lovat, P. Fadda, C. Mao, G. J. Nuovo, N. Zanesi, M. Crawford, G. H. Ozer, D. Wernicke, H. Alder, M. A. Caligiuri, P. Nana-Sinkam, D. Perrotti, C. M. Croce, microRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. U.S.A. 109, E2110–E2116 (2012).
36. U. Klein, M. Lia, M. Crespo, R. Siegel, Q. Shen, T. Mo, A. Ambesi-Impiombato, A. Califano, A. Migliazza, G. Bhagat, R. Dalla-Favera, The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17, 28–40 (2010).
37. F. Heil, H. Hemmi, H. Hochrein, F. Ampenberger, C. Kirschning, S. Akira, G. Lipford, H. Wagner, S. Bauer, Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 303, 1526–1529 (2004).
38. S. T. Sarvestani, B. R. G. Williams, M. P. Gantier, Human Toll-like receptor 8 can be cool too: Implications for foreign RNA sensing. J. Interferon Cytokine Res. 32, 350–361 (2012).
39. M. C. Boelens, T. J. Wu, B. Y. Nabet, B. Xu, Y. Qiu, T. Yoon, D. J. Azzam, C. T.-S. Victor, B. Z. Wiemann, H. Ishwaran, P. J. ter Brugge, J. Jonkers, J. Slingerland, A. J. Minn, Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell 159, 499–513 (2014).
40. A. Kužnik, M. Benčina, U. Švajger, M. Jeras, B. Rozman, R. Jerala, Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J. Immunol. 186, 4794–4804 (2011).
41. D. Koppers-Lalic, M. Hackenberg, I. V. Bijnsdorp, M. A. J. van Eijndhoven, P. Sadek, D. Sie, N. Zini, J. M. Middeldorp, B. Ylstra, R. X. de Menezes, T. Würdinger, G. A. Meijer, D. M. Pegtel, Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 8, 1649–1658 (2014).
42. B. W. M. van Balkom, A. S. Eisele, D. M. Pegtel, S. Bervoets, M. C. Verhaar, Quantitative and qualitative analysis of small RNAs in human endothelial cells and exosomes provides insights into localized RNA processing, degradation and sorting. J. Extracell. Vesicles 4, 26760 (2015).
43. L. Vojtech, S. Woo, S. Hughes, C. Levy, L. Ballweber, R. P. Sauteraud, J. Strobl, K. Westerberg, R. Gottardo, M. Tewari, F. Hladik, Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 42, 7290–7304 (2014).
44. A. Forsbach, J. G. Nemorin, C. Montino, C. Müller, U. Samulowitz, A. P. Vicari, M. Jurk, G. K. Mutwiri, A. M. Krieg, G. B. Lipford, J. Vollmer, Identification of RNA sequence motifs stimulating sequence-specific TLR8-dependent immune responses. J. Immunol. 180, 3729–3738 (2008).
45. A. G. Arimbasseri, K. Rijal, R. J. Maraia, Transcription termination by the eukaryotic RNA polymerase III. Biochim. Biophys. Acta 1829, 318–330 (2013).
46. M. Tkach, C. Théry, Communication by extracellular vesicles: Where we are and where we need to go. Cell 164, 1226–1232 (2016).
47. P. D. Robbins, A. Dorronsoro, C. N. Booker, Regulation of chronic inflammatory and immune processes by extracellular vesicles. J. Clin. Investig. 126, 1173–1180 (2016).
48. L. Lagneaux, A. Delforge, M. Dejeneffe, M. Massy, M. Bernier, D. Bron, Hydroxychloroquine-induced apoptosis of chronic lymphocytic leukemia involves activation of caspase-3 and modulation of Bcl-2/bax/ratio. Leuk. Lymphoma 43, 1087–1095 (2002).
49. S.-S. Chen, M. Kaufman, A. Caramanica, R. N. Damle, P. Garofalo, P. Ly, D. Janson, S. L. Allen, J. Kolitz, L. Quill, K. R. Rai, N. Chiorazzi, Efficacy and safety of hydroxychloroquine sulphate in chronic lymphocytic leukemia: Clinical trial experience in untreated patients. Blood 116, 1392–1392 (2010).
50. C. J. Blume, A. Hotz-Wagenblatt, J. Hüllein, L. Sellner, A. Jethwa, T. Stolz, M. Slabicki, K. Lee, A. Sharathchandra, A. Benner, S. Dietrich, C. C. Oakes, P. Dreger, D. te Raa, A. P. Kater, A. Jauch, O. Merkel, M. Oren, T. Hielscher, T. Zenz, p53-dependent non-coding RNA networks in chronic lymphocytic leukemia. Leukemia 29, 2015–2023 (2015).
51. Y. Liao, G. K. Smyth, W. Shi, featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
52. M. I. Love, W. Huber, S. Anders, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
53. H. Hemmi, T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, S. Akira, Small anti-viral compounds activate immune cells via the TLR7 MyD88–dependent signaling pathway. Nat. Immunol. 3, 196–200 (2002).
54. Q. Sun, L. Sun, H.-H. Liu, X. Chen, R. B. Seth, J. Forman, Z. J. Chen, The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24, 633–642 (2006).