Tumor Exosomal RNAs Promote Lung Pre-metastatic Niche Formation by Activating Alveolar Epithelial TLR3 to Recruit Neutrophils

Cancer Cell

Volumn 30, Issue 2, 2016, Pages 243-256

  Liu, Yanfang ^a   Gu, Yan ^a   Han, Yanmei ^a   Zhang, Qian ^a   Jiang, Zhengping ^a   Zhang, Xiang ^a   Huang, Bo ^b   Xu, Xiaoqing ^b   Zheng, Jianming ^c   Cao, Xuetao ^a,b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

alveolar epithelial cell; exosomal RNA; metastasis; pre metastatic niche; TLR3

Indexed keywords

CHEMOKINE; RNA; SMALL NUCLEAR RNA; TOLL LIKE RECEPTOR 3; TUMOR EXOSOMAL RNA; UNCLASSIFIED DRUG; TLR3 PROTEIN, HUMAN; TLR3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ALVEOLUS EPITHELIUM CELL; LUNG METASTASIS; LUNG PRE METASTASIS; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; DEFICIENCY; EPITHELIUM CELL; EXOSOME; EXPERIMENTAL MELANOMA; GENETICS; LEWIS CARCINOMA; LUNG TUMOR; METABOLISM; METASTASIS; NUCLEOTIDE SEQUENCE; PATHOLOGY; SECONDARY; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; CARCINOMA, LEWIS LUNG; EPITHELIAL CELLS; EXOSOMES; HUMANS; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASM METASTASIS; NEUTROPHIL INFILTRATION; RNA, NEOPLASM; RNA, SMALL NUCLEAR; TOLL-LIKE RECEPTOR 3;

EID: 84989843940     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2016.06.021     Document Type: Article

References (60)

1. Akira, S., Takeda, K., Toll-like receptor signalling. Nat. Rev. Immunol. 4 (2004), 499–511.
2. Alexopoulou, L., Holt, A.C., Medzhitov, R., Flavell, R.A., Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001), 732–738.
3. Babiceanu, M.C., Howard, B.A., Rumore, A.C., Kita, H., Lawrence, C.B., Analysis of global gene expression changes in human bronchial epithelial cells exposed to spores of the allergenic fungus, Alternaria alternata. Front Microbiol., 4, 2013, 196.
4. Bald, T., Quast, T., Landsberg, J., Rogava, M., Glodde, N., Lopez-Ramos, D., Kohlmeyer, J., Riesenberg, S., van den Boorn-Konijnenberg, D., Homig-Holzel, C., et al. Ultraviolet-radiation-induced inflammation promotes angiotropism and metastasis in melanoma. Nature 507 (2014), 109–113.
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. Brody, J.S., Steiling, K., Interaction of cigarette exposure and airway epithelial cell gene expression. Annu. Rev. Physiol. 73 (2011), 437–456.
8. Cao, X., Self-regulation and cross-regulation of pattern-recognition receptor signalling in health and disease. Nat. Rev. Immunol. 16 (2016), 35–50.
9. Cavassani, K.A., Ishii, M., Wen, H., Schaller, M.A., Lincoln, P.M., Lukacs, N.W., Hogaboam, C.M., Kunkel, S.L., TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J. Exp. Med. 205 (2008), 2609–2621.
10. Chen, T., Guo, J., Yang, M., Zhu, X., Cao, X., Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J. Immunol. 186 (2011), 2219–2228.
11. Cherfils-Vicini, J., Platonova, S., Gillard, M., Laurans, L., Validire, P., Caliandro, R., Magdeleinat, P., Mami-Chouaib, F., Dieu-Nosjean, M.C., Fridman, W.H., et al. Triggering of TLR7 and TLR8 expressed by human lung cancer cells induces cell survival and chemoresistance. J. Clin. Invest. 120 (2010), 1285–1297.
12. Chin, A.I., Miyahira, A.K., Covarrubias, A., Teague, J., Guo, B., Dempsey, P.W., Cheng, G., Toll-like receptor 3-mediated suppression of TRAMP prostate cancer shows the critical role of type I interferons in tumor immune surveillance. Cancer Res. 70 (2010), 2595–2603.
13. Chow, A., Zhou, W., Liu, L., Fong, M.Y., Champer, J., Van Haute, D., Chin, A.R., Ren, X., Gugiu, B.G., Meng, Z., et al. Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-kappaB. Sci. Rep., 4, 2014, 5750.
14. Coffelt, S.B., Kersten, K., Doornebal, C.W., Weiden, J., Vrijland, K., Hau, C.S., Verstegen, N.J., Ciampricotti, M., Hawinkels, L.J., Jonkers, J., et al. IL-17-producing gammadelta T cells and neutrophils conspire to promote breast cancer metastasis. Nature 522 (2015), 345–348.
15. Cools-Lartigue, J., Spicer, J., McDonald, B., Gowing, S., Chow, S., Giannias, B., Bourdeau, F., Kubes, P., Ferri, L., Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J. Clin. Invest. 123 (2013), 3446–3458.
16. Couzin, J., Cell biology: the ins and outs of exosomes. Science 308 (2005), 1862–1863.
17. Dapito, D.H., Mencin, A., Gwak, G.Y., Pradere, J.P., Jang, M.K., Mederacke, I., Caviglia, J.M., Khiabanian, H., Adeyemi, A., Bataller, R., et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 21 (2012), 504–516.
18. DuPage, M., Dooley, A.L., Jacks, T., Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat. Protoc. 4 (2009), 1064–1072.
19. Erler, J.T., Bennewith, K.L., Cox, T.R., Lang, G., Bird, D., Koong, A., Le, Q.T., Giaccia, A.J., Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15 (2009), 35–44.
20. Fabbri, M., Paone, A., Calore, F., Galli, R., Gaudio, E., Santhanam, R., Lovat, F., Fadda, P., Mao, C., Nuovo, G.J., et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA 109 (2012), E2110–E2116.
21. Forte, G., Rega, A., Morello, S., Luciano, A., Arra, C., Pinto, A., Sorrentino, R., Polyinosinic-polycytidylic acid limits tumor outgrowth in a mouse model of metastatic lung cancer. J. Immunol. 188 (2012), 5357–5364.
22. Fridlender, Z.G., Sun, J., Kim, S., Kapoor, V., Cheng, G., Ling, L., Worthen, G.S., Albelda, S.M., Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16 (2009), 183–194.
23. Granot, Z., Henke, E., Comen, E.A., King, T.A., Norton, L., Benezra, R., Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 20 (2011), 300–314.
24. Guillerey, C., Chow, M.T., Miles, K., Olver, S., Sceneay, J., Takeda, K., Moller, A., Smyth, M.J., Toll-like receptor 3 regulates NK cell responses to cytokines and controls experimental metastasis. Oncoimmunology, 4, 2015, e1027468.
25. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
26. Handke, W., Oelschlegel, R., Franke, R., Kruger, D.H., Rang, A., Hantaan virus triggers TLR3-dependent innate immune responses. J. Immunol. 182 (2009), 2849–2858.
27. Harris, P., Sridhar, S., Peng, R., Phillips, J.E., Cohn, R.G., Burns, L., Woods, J., Ramanujam, M., Loubeau, M., Tyagi, G., et al. Double-stranded RNA induces molecular and inflammatory signatures that are directly relevant to COPD. Mucosal Immunol. 6 (2013), 474–484.
28. Hartl, D., Latzin, P., Hordijk, P., Marcos, V., Rudolph, C., Woischnik, M., Krauss-Etschmann, S., Koller, B., Reinhardt, D., Roscher, A.A., et al. Cleavage of CXCR1 on neutrophils disables bacterial killing in cystic fibrosis lung disease. Nat. Med. 13 (2007), 1423–1430.
29. Hasan, U.A., Caux, C., Perrot, I., Doffin, A.C., Menetrier-Caux, C., Trinchieri, G., Tommasino, M., Vlach, J., Cell proliferation and survival induced by Toll-like receptors is antagonized by type I IFNs. Proc. Natl. Acad. Sci. USA 104 (2007), 8047–8052.
30. He, W., Liu, Q., Wang, L., Chen, W., Li, N., Cao, X., TLR4 signaling promotes immune escape of human lung cancer cells by inducing immunosuppressive cytokines and apoptosis resistance. Mol. Immunol. 44 (2007), 2850–2859.
31. Hiratsuka, S., Watanabe, A., Aburatani, H., Maru, Y., Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 8 (2006), 1369–1375.
32. Hoshino, A., Costa-Silva, B., Shen, T.L., Rodrigues, G., Hashimoto, A., Tesic Mark, M., Molina, H., Kohsaka, S., Di Giannatale, A., Ceder, S., et al. Tumour exosome integrins determine organotropic metastasis. Nature 527 (2015), 329–335.
33. Hood, J.L., San, R.S., Wickline, S.A., Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 71 (2011), 3792–3801.
34. Juncadella, I.J., Kadl, A., Sharma, A.K., Shim, Y.M., Hochreiter-Hufford, A., Borish, L., Ravichandran, K.S., Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature 493 (2013), 547–551.
35. Kaplan, R.N., Riba, R.D., Zacharoulis, S., Bramley, A.H., Vincent, L., Costa, C., MacDonald, D.D., Jin, D.K., Shido, K., Kerns, S.A., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438 (2005), 820–827.
36. Khanna, C., Hunter, K., Modeling metastasis in vivo. Carcinogenesis 26 (2005), 513–523.
37. Kim, S., Takahashi, H., Lin, W.W., Descargues, P., Grivennikov, S., Kim, Y., Luo, J.L., Karin, M., Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457 (2009), 102–106.
38. Korfhagen, T.R., Kitzmiller, J., Chen, G., Sridharan, A., Haitchi, H.M., Hegde, R.S., Divanovic, S., Karp, C.L., Whitsett, J.A., SAM-pointed domain ETS factor mediates epithelial cell-intrinsic innate immune signaling during airway mucous metaplasia. Proc. Natl. Acad. Sci. USA 109 (2012), 16630–16635.
39. Kowanetz, M., Wu, X., Lee, J., Tan, M., Hagenbeek, T., Qu, X., Yu, L., Ross, J., Korsisaari, N., Cao, T., et al. Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes. Proc. Natl. Acad. Sci. USA 107 (2010), 21248–21255.
40. Liu, Y., Cao, X., Immunosuppressive cells in tumor immune escape and metastasis. J. Mol. Med. 94 (2016), 509–522.
41. Liu, L., Botos, I., Wang, Y., Leonard, J.N., Shiloach, J., Segal, D.M., Davies, D.R., Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320 (2008), 379–381.
42. Liu, Y., Gu, Y., Cao, X., The exosomes in tumor immunity. Oncoimmunology, 4, 2015, e1027472.
43. Melo, S.A., Sugimoto, H., O'Connell, J.T., Kato, N., Villanueva, A., Vidal, A., Qiu, L., Vitkin, E., Perelman, L.T., Melo, C.A., et al. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell 26 (2014), 707–721.
44. Milara, J., Morell, A., Ballester, B., Sanz, C., Freire, J., Qian, X., Alonso-Garcia, M., Morcillo, E., Cortijo, J., Roflumilast improves corticosteroid resistance COPD bronchial epithelial cells stimulated with toll like receptor 3 agonist. Respir. Res., 16, 2015, 12.
45. Nelson, A.M., Reddy, S.K., Ratliff, T.S., Hossain, M.Z., Katseff, A.S., Zhu, A.S., Chang, E., Resnik, S.R., Page, C., Kim, D., et al. dsRNA released by tissue damage activates TLR3 to drive skin regeneration. Cell Stem Cell 17 (2015), 139–151.
46. Peinado, H., Aleckovic, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., Garcia-Santos, G., Ghajar, C., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18 (2012), 883–891.
47. Pradere, J.P., Dapito, D.H., Schwabe, R.F., The Yin and Yang of toll-like receptors in cancer. Oncogene 33 (2014), 3485–3495.
48. Psaila, B., Lyden, D., The metastatic niche: adapting the foreign soil. Nat. Rev. Cancer 9 (2009), 285–293.
49. Sceneay, J., Smyth, M.J., Moller, A., The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 32 (2013), 449–464.
50. Scheeren, F.A., Kuo, A.H., van Weele, L.J., Cai, S., Glykofridis, I., Sikandar, S.S., Zabala, M., Qian, D., Lam, J.S., Johnston, D., et al. A cell-intrinsic role for TLR2-MYD88 in intestinal and breast epithelia and oncogenesis. Nat. Cell Biol. 16 (2014), 1238–1248.
51. Sistigu, A., Yamazaki, T., Vacchelli, E., Chaba, K., Enot, D.P., Adam, J., Vitale, I., Goubar, A., Baracco, E.E., Remedios, C., et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat. Med. 20 (2014), 1301–1309.
52. Takahashi, H., Ogata, H., Nishigaki, R., Broide, D.H., Karin, M., Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta- and JNK1-dependent inflammation. Cancer Cell 17 (2010), 89–97.
53. Wagner, W.R., Griffith, B.P., Reconstructing the lung. Science 329 (2010), 520–522.
54. Wang, L., Liu, Q., Sun, Q., Zhang, C., Chen, T., Cao, X., TLR4 signaling in cancer cells promotes chemoattraction of immature dendritic cells via autocrine CCL20. Biochem. Biophys. Res. Commun. 366 (2008), 852–856.
55. Wculek, S.K., Malanchi, I., Neutrophils support lung colonization of metastasis-initiating breast cancer cells. Nature 528 (2015), 413–417.
56. Whitsett, J.A., Alenghat, T., Respiratory epithelial cells orchestrate pulmonary innate immunity. Nat. Immunol. 16 (2015), 27–35.
57. Wortham, B.W., Eppert, B.L., Flury, J.L., Morgado Garcia, S., Borchers, M.T., TLR and NKG2D signaling pathways mediate CS-induced pulmonary pathologies. PLoS One, 8, 2013, e78735.
58. Wu, C.F., Andzinski, L., Kasnitz, N., Kroger, A., Klawonn, F., Lienenklaus, S., Weiss, S., Jablonska, J., The lack of type I interferon induces neutrophil-mediated pre-metastatic niche formation in the mouse lung. Int. J. Cancer 137 (2015), 837–847.
59. Zanucco, E., El-Nikhely, N., Gotz, R., Weidmann, K., Pfeiffer, V., Savai, R., Seeger, W., Ullrich, A., Rapp, U.R., Elimination of B-RAF in oncogenic C-RAF-expressing alveolar epithelial type II cells reduces MAPK signal intensity and lung tumor growth. J. Biol. Chem. 289 (2014), 26804–26816.
60. Zhu, W., Jiang, C., Xu, J., Geng, M., Wu, X., Sun, J., Ma, J., Holmdahl, R., Meng, L., Lu, S., Pristane primed rat T cells enhance TLR3 expression of fibroblast-like synoviocytes via TNF-alpha initiated p38 MAPK and NF-kappaB pathways. Clin. Immunol. 156 (2015), 141–153.