Exosome RNA Unshielding Couples Stromal Activation to Pattern Recognition Receptor Signaling in Cancer

Cell

Volumn 170, Issue 2, 2017, Pages 352-366.e13

  Nabet, Barzin Y ^a   Qiu, Yu ^a   Shabason, Jacob E ^a   Wu, Tony J ^a   Yoon, Taewon ^a   Kim, Brian C ^a   Benci, Joseph L ^a   DeMichele, Angela M ^a,b   Tchou, Julia ^a,b   Marcotrigiano, Joseph ^c   Minn, Andy J ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

breast cancer; exosomes; fibroblasts; pattern recognition receptors; radiation therapy; RIG I; RNA binding proteins; shielding; stromal activation; tumor microenvironment

Indexed keywords

DAMAGE ASSOCIATED MOLECULAR PATTERN; DNA DIRECTED RNA POLYMERASE III; MEMBRANE PROTEIN; MYC PROTEIN; NOTCH RECEPTOR; PATTERN RECOGNITION RECEPTOR; PROTEIN SRP14; PROTEIN SRP9; RETINOIC ACID INDUCIBLE PROTEIN I; RN7SL1 RNA; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; DDX58 PROTEIN, HUMAN; INTERFERON REGULATORY FACTOR; SIGNAL RECOGNITION PARTICLE; SRP14 PROTEIN, HUMAN; SRP9 PROTEIN, HUMAN; UNTRANSLATED RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CELL; CANCER GROWTH; CANCER RESISTANCE; CONTROLLED STUDY; EXOSOME; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA PROCESSING; RNA UNSHIELDING; SIGNAL TRANSDUCTION; STOICHIOMETRY; STROMA; STROMA ACTIVATION; BREAST TUMOR; GENETICS; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; STROMA CELL; TUMOR MICROENVIRONMENT; VIRUS INFECTION;

BREAST NEOPLASMS; DEAD BOX PROTEIN 58; EXOSOMES; HUMANS; INTERFERON REGULATORY FACTORS; MCF-7 CELLS; NEOPLASM METASTASIS; RECEPTORS, PATTERN RECOGNITION; RNA POLYMERASE III; RNA, UNTRANSLATED; SIGNAL RECOGNITION PARTICLE; STROMAL CELLS; TUMOR MICROENVIRONMENT; VIRUS DISEASES;

EID: 85023641492     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.06.031     Document Type: Article

References (38)

1. Abbas, A.R., Baldwin, D., Ma, Y., Ouyang, W., Gurney, A., Martin, F., Fong, S., van Lookeren Campagne, M., Godowski, P., Williams, P.M., et al. Immune response in silico (IRIS): immune-specific genes identified from a compendium of microarray expression data. Genes Immun. 6 (2005), 319–331.
2. Akopian, D., Shen, K., Zhang, X., Shan, S.O., Signal recognition particle: an essential protein-targeting machine. Annu. Rev. Biochem. 82 (2013), 693–721.
3. Becher, B., Schlitzer, A., Chen, J., Mair, F., Sumatoh, H.R., Teng, K.W.W., Low, D., Ruedl, C., Riccardi-Castagnoli, P., Poidinger, M., et al. High-dimensional analysis of the murine myeloid cell system. Nat. Immunol. 15 (2014), 1181–1189.
4. Becker, A., Thakur, B.K., Weiss, J.M., Kim, H.S., Peinado, H., Lyden, D., Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell 30 (2016), 836–848.
5. Bernard, J.J., Cowing-Zitron, C., Nakatsuji, T., Muehleisen, B., Muto, J., Borkowski, A.W., Martinez, L., Greidinger, E.L., Yu, B.D., Gallo, R.L., Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat. Med. 18 (2012), 1286–1290.
6. Boelens, M.C., Wu, T.J., Nabet, B.Y., Xu, B., Qiu, Y., Yoon, T., Azzam, D.J., Twyman-Saint Victor, C., Wiemann, B.Z., Ishwaran, H., et al. Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell 159 (2014), 499–513.
7. Bridgeman, A., Maelfait, J., Davenne, T., Partridge, T., Peng, Y., Mayer, A., Dong, T., Kaever, V., Borrow, P., Rehwinkel, J., Viruses transfer the antiviral second messenger cGAMP between cells. Science 349 (2015), 1228–1232.
8. Chen, Q., Boire, A., Jin, X., Valiente, M., Er, E.E., Lopez-Soto, A., Jacob, L.S., Patwa, R., Shah, H., Xu, K., et al. Carcinoma-astrocyte gap junctions promote brain metastasis by cGAMP transfer. Nature 533 (2016), 493–498.
9. Chiappinelli, K.B., Strissel, P.L., Desrichard, A., Li, H., Henke, C., Akman, B., Hein, A., Rote, N.S., Cope, L.M., Snyder, A., et al. Inhibiting DNA methylation causes an interferon response in cancer via dsRNA including endogenous retroviruses. Cell 162 (2015), 974–986.
10. Devarkar, S.C., Wang, C., Miller, M.T., Ramanathan, A., Jiang, F., Khan, A.G., Patel, S.S., Marcotrigiano, J., Structural basis for m7G recognition and 2′-O-methyl discrimination in capped RNAs by the innate immune receptor RIG-I. Proc. Natl. Acad. Sci. USA 113 (2016), 596–601.
11. Eckard, S.C., Rice, G.I., Fabre, A., Badens, C., Gray, E.E., Hartley, J.L., Crow, Y.J., Stetson, D.B., The SKIV2L RNA exosome limits activation of the RIG-I-like receptors. Nat. Immunol. 15 (2014), 839–845.
12. Finak, G., Bertos, N., Pepin, F., Sadekova, S., Souleimanova, M., Zhao, H., Chen, H., Omeroglu, G., Meterissian, S., Omeroglu, A., et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 14 (2008), 518–527.
13. Gentili, M., Kowal, J., Tkach, M., Satoh, T., Lahaye, X., Conrad, C., Boyron, M., Lombard, B., Durand, S., Kroemer, G., et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 349 (2015), 1232–1236.
14. Gomez-Roman, N., Grandori, C., Eisenman, R.N., White, R.J., Direct activation of RNA polymerase III transcription by c-Myc. Nature 421 (2003), 290–294.
15. Hornung, V., Ellegast, J., Kim, S., Brzózka, K., Jung, A., Kato, H., Poeck, H., Akira, S., Conzelmann, K.-K., Schlee, M., et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314 (2006), 994–997.
16. Hung, T., Pratt, G.A., Sundararaman, B., Townsend, M.J., Chaivorapol, C., Bhangale, T., Graham, R.R., Ortmann, W., Criswell, L.A., Yeo, G.W., Behrens, T.W., The Ro60 autoantigen binds endogenous retroelements and regulates inflammatory gene expression. Science 350 (2015), 455–459.
17. Kalluri, R., The biology and function of fibroblasts in cancer. Nat. Rev. Cancer 16 (2016), 582–598.
18. Kang, Y., Siegel, P.M., Shu, W., Drobnjak, M., Kakonen, S.M., Cordón-Cardo, C., Guise, T.A., Massague, J., A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3 (2003), 537–549.
19. Liu, X., Holstege, H., van der Gulden, H., Treur-Mulder, M., Zevenhoven, J., Velds, A., Kerkhoven, R.M., van Vliet, M.H., Wessels, L.F., Peterse, J.L., et al. Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basal-like breast cancer. Proc. Natl. Acad. Sci. USA 104 (2007), 12111–12116.
20. Liu, Y., Gu, Y., Han, Y., Zhang, Q., Jiang, Z., Zhang, X., Huang, B., Xu, X., Zheng, J., Cao, X., Tumor exosomal RNAs promote lung pre-metastatic niche formation by activating alveolar epithelial TLR3 to recruit neutrophils. Cancer Cell 30 (2016), 243–256.
21. Mercado-López, X., Cotter, C.R., Kim, W.K., Sun, Y., Muñoz, L., Tapia, K., López, C.B., Highly immunostimulatory RNA derived from a Sendai virus defective viral genome. Vaccine 31 (2013), 5713–5721.
22. Minn, A.J., Gupta, G.P., Siegel, P.M., Bos, P.D., Shu, W., Giri, D.D., Viale, A., Olshen, A.B., Gerald, W.L., Massagué, J., Genes that mediate breast cancer metastasis to lung. Nature 436 (2005), 518–524.
23. Moroishi, T., Hayashi, T., Pan, W.W., Fujita, Y., Holt, M.V., Qin, J., Carson, D.A., Guan, K.L., The Hippo pathway kinases LATS1/2 suppress cancer immunity. Cell 167 (2016), 1525–1539.e17.
24. Oler, A.J., Alla, R.K., Roberts, D.N., Wong, A., Hollenhorst, P.C., Chandler, K.J., Cassiday, P.A., Nelson, C.A., Hagedorn, C.H., Graves, B.J., Cairns, B.R., Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat. Struct. Mol. Biol. 17 (2010), 620–628.
25. Ranoa, D.R.E., Parekh, A.D., Pitroda, S.P., Huang, X., Darga, T., Wong, A.C., Huang, L., Andrade, J., Staley, J.P., Satoh, T., et al. Cancer therapies activate RIG-I-like receptor pathway through endogenous non-coding RNAs. Oncotarget 7 (2016), 26496–26515.
26. Roulois, D., Loo Yau, H., Singhania, R., Wang, Y., Danesh, A., Shen, S.Y., Han, H., Liang, G., Jones, P.A., Pugh, T.J., et al. DNA-demethylating agents target colorectal cancer cells by inducing viral mimicry by endogenous transcripts. Cell 162 (2015), 961–973.
27. Saito, T., Owen, D.M., Jiang, F., Marcotrigiano, J., Gale, M. Jr., Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454 (2008), 523–527.
28. Schlee, M., Hartmann, G., Discriminating self from non-self in nucleic acid sensing. Nat. Rev. Immunol. 16 (2016), 566–580.
29. Schuberth-Wagner, C., Ludwig, J., Bruder, A.K., Herzner, A.-M., Zillinger, T., Goldeck, M., Schmidt, T., Schmid-Burgk, J.L., Kerber, R., Wolter, S., et al. A conserved histidine in the RNA sensor RIG-I controls immune tolerance to N1-2’O-methylated self RNA. Immunity 43 (2015), 41–51.
30. Sistigu, A., Yamazaki, T., Vacchelli, E., Chaba, K., Enot, D.P., Adam, J., Vitale, I., Goubar, A., Baracco, E.E., Remédios, C., et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat. Med. 20 (2014), 1301–1309.
31. Tchou, J., Kossenkov, A.V., Chang, L., Satija, C., Herlyn, M., Showe, L.C., Puré, E., Human breast cancer associated fibroblasts exhibit subtype specific gene expression profiles. BMC Med. Genomics, 5, 2012, 39.
32. Telesnitsky, A., Wolin, S.L., The host RNAs in retroviral particles. Viruses 8 (2016), 1–15.
33. Théry, C., Amigorena, S., Raposo, G., Clayton, A., Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol., Chapter 3, 2006, Unit 3.22.
34. Wang, Y., Ludwig, J., Schuberth, C., Goldeck, M., Schlee, M., Li, H., Juranek, S., Sheng, G., Micura, R., Tuschl, T., et al. Structural and functional insights into 5′-ppp RNA pattern recognition by the innate immune receptor RIG-I. Nat. Struct. Mol. Biol. 17 (2010), 781–787.
35. Weichselbaum, R.R., Ishwaran, H., Yoon, T., Nuyten, D.S., Baker, S.W., Khodarev, N., Su, A.W., Shaikh, A.Y., Roach, P., Kreike, B., et al. An interferon-related gene signature for DNA damage resistance is a predictive marker for chemotherapy and radiation for breast cancer. Proc. Natl. Acad. Sci. USA 105 (2008), 18490–18495.
36. Weng, A.P., Millholland, J.M., Yashiro-Ohtani, Y., Arcangeli, M.L., Lau, A., Wai, C., Del Bianco, C., Rodriguez, C.G., Sai, H., Tobias, J., et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 20 (2006), 2096–2109.
37. White, R.J., Transcription by RNA polymerase III: more complex than we thought. Nat. Rev. Genet. 12 (2011), 459–463.
38. Wu, L., Pan, J., Thoroddsen, V., Wysong, D.R., Blackman, R.K., Bulawa, C.E., Gould, A.E., Ocain, T.D., Dick, L.R., Errada, P., et al. Novel small-molecule inhibitors of RNA polymerase III. Eukaryot. Cell 2 (2003), 256–264.