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Original Articles

An Immunosuppressive Effect of Melanoma-derived Exosomes on NY-ESO-1 Antigen-specific Human CD8+ T Cells is Dependent on IL-10 and Independent of BRAFV600E Mutation in Melanoma Cell Lines

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References

  • Ascierto PA, Kirkwood JM, Grob JJ, Simeone E, Grimaldi AM, Maio M, Palmieri G, Testori A, Marincola FM, Mozzillo N. 2012. The role of BRAF V600 mutation in melanoma. J Transl Med. 10(1):85.
  • Brooks DG, Ha SJ, Elsaesser H, Sharpe AH, Freeman GJ, Oldstone MB. 2008. IL-10 and PD-L1 operate through distinct pathways to suppress T-cell activity during persistent viral infection. Proc Natl Acad Sci U S A. 105:20428–33.
  • Chen G, Huang AC, Zhang W, Zhang G, Wu M, Xu W, Yu Z, Yang J, Wang B, Sun H, et al. 2018. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 560(7718):382–86.
  • Ellerhorst JA, Greene VR, Ekmekcioglu S, Warneke CL, Johnson MM, Cooke CP, Wang L-E, Prieto VG, Gershenwald JE, Wei Q, et al. 2011. Clinical correlates of NRAS and BRAF mutations in primary human melanoma. Clin Cancer Res. 17(2):229–35.
  • Emmerich J, Mumm JB, Chan IH, LaFace D, Truong H, McClanahan T, Gorman DM, Oft M. 2012. IL-10 directly activates and expands tumor-resident CD8+ T cells without de novo infiltration from secondary lymphoid organs. Cancer Res. 72(14):3570–81.
  • Feng D, Qin B, Pal K, Sun L, Dutta S, Dong H, Liu X, Mukhopadhyay D, Huang S, Sinicrope FA. 2019. BRAF(V600E)-induced, tumor intrinsic PD-L1 can regulate chemotherapy-induced apoptosis in human colon cancer cells and in tumor xenografts. Oncogene. 38:6752–66.
  • Garcia-Silva S, Benito-Martin A, Sanchez-Redondo S, Hernandez-Barranco A, Ximenez-Embun P, Nogues L, Mazariegos MS, Brinkmann K, Amor López A, Meyer L, et al. 2019. Use of extracellular vesicles from lymphatic drainage as surrogate markers of melanoma progression and BRAF (V600E) mutation. J Exp Med. 216:1061–70.
  • Ikeda H, Old LJ, Schreiber RD. 2002. The roles of IFN gamma in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev. 13:95–109.
  • Ilieva KM, Correa I, Josephs DH, Karagiannis P, Egbuniwe IU, Cafferkey MJ, Spicer JF, Harries M, Nestle FO, Lacy KE, et al. 2014. Effects of BRAF mutations and BRAF inhibition on immune responses to melanoma. Mol Cancer Ther. 13(12):2769–83.
  • Kasahara T, Hooks JJ, Dougherty SF, Oppenheim JJ. 1983. Interleukin 2-mediated immune interferon (IFN-gamma) production by human T cells and T cell subsets. J Immunol. 130:1784–89.
  • Kelleher RJ Jr., Balu-Iyer S, Loyall J, Sacca AJ, Shenoy GN, Peng P, Iyer V, Fathallah AM, Berenson CS, Wallace PK, et al. 2015. Extracellular vesicles present in human ovarian tumor microenvironments induce a phosphatidylserine-dependent arrest in the T-cell signaling cascade. Cancer Immunol Res. 3(11):1269–78.
  • Keller S, Konig AK, Marme F, Runz S, Wolterink S, Koensgen D, Mustea A, Sehouli J, Altevogt P. 2009. Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes. Cancer Lett. 278:73–81.
  • Khalili JS, Liu S, Rodriguez-Cruz TG, Whittington M, Wardell S, Liu C, Zhang M, Cooper ZA, Frederick DT, Li Y, et al. 2012. Oncogenic BRAF(V600E) promotes stromal cell-mediated immunosuppression via induction of interleukin-1 in melanoma. Clin Cancer Res. 18(19):5329–40.
  • Liu S, Matsuzaki J, Wei L, Tsuji T, Battaglia S, Hu Q, Cortes E, Wong L, Yan L, Long M, et al. 2019. Efficient identification of neoantigen-specific T-cell responses in advanced human ovarian cancer. J Immunother Cancer. 7(1):156.
  • Lorre K, Fransen L, Ceuppens JL. 1992. Interleukin-2 induces tumor necrosis factor-alpha production by activated human T cells via a cyclosporin-sensitive pathway. Eur Cytokine Netw. 3(3):321–30.
  • Marleau AM, Chen CS, Joyce JA, Tullis RH. 2012. Exosome removal as a therapeutic adjuvant in cancer. J Transl Med. 10(1):134.
  • Matsumura S, Minamisawa T, Suga K, Kishita H, Akagi T, Ichiki T, Ichikawa Y, Shiba K. 2019. Subtypes of tumour cell-derived small extracellular vesicles having differently externalized phosphatidylserine. J Extracell Vesicles. 8(1):1579541.
  • Matsuzaki J, Gnjatic S, Mhawech-Fauceglia P, Beck A, Miller A, Tsuji T, Eppolito C, Qian F, Lele S, Shrikant P, et al. 2010. Tumor-infiltrating NY-ESO-1–specific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer. Proc Natl Acad Sci U S A. 107:7875–80.
  • Matsuzaki J, Tsuji T, Luescher IF, Shiku H, Mineno J, Okamoto S, Old LJ, Shrikant P, Gnjatic S, Odunsi K. 2015. Direct tumor recognition by a human CD4+ T-cell subset potently mediates tumor growth inhibition and orchestrates anti-tumor immune responses. Sci Rep. 5(1):14896.
  • Maybruck BT, Pfannenstiel LW, Diaz-Montero M, Gastman BR. 2017. Tumor-derived exosomes induce CD8+ T cell suppressors. J Immunother Cancer. 5(1):65.
  • Mortara L, Balza E, Sassi F, Castellani P, Carnemolla B, De Lerma Barbaro A, Fossati S, Tosi G, Accolla RS, Borsi L. 2007. Therapy-induced antitumor vaccination by targeting tumor necrosis factor alpha to tumor vessels in combination with melphalan. Eur J Immunol. 37:3381–92.
  • Mumm JB, Emmerich J, Zhang X, Chan I, Wu L, Mauze S, Blaisdell S, Basham B, Dai J, Grein J, et al. 2011. IL-10 elicits IFNgamma-dependent tumor immune surveillance. Cancer Cell. 20:781–96.
  • Roato I, Brunetti G, Gorassini E, Grano M, Colucci S, Bonello L, Buffoni L, Manfredi R, Ruffini E, Ottaviani D, et al. 2006. IL-7 up-regulates TNF-alpha-dependent osteoclastogenesis in patients affected by solid tumor. PLoS One. 1:e124.
  • Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M, et al. 2015. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med. 372(26):2521–32.
  • Russell AE, Sneider A, Witwer KW, Bergese P, Bhattacharyya SN, Cocks A, Cocucci E, Erdbrügger U, Falcon-Perez JM, Freeman DW, et al. 2019. Biological membranes in EV biogenesis, stability, uptake, and cargo transfer: an ISEV position paper arising from the ISEV membranes and EVs workshop. J Extracell Vesicles. 8(1):1684862.
  • Sa G, Das T, Moon C, Hilston CM, Rayman PA, Rini BI, Tannenbaum CS, Finke JH. 2009. GD3, an overexpressed tumor-derived ganglioside, mediates the apoptosis of activated but not resting T cells. Cancer Res. 69(7):3095–104.
  • Shabaneh TB, Molodtsov AK, Steinberg SM, Zhang P, Torres GM, Mohamed GA, Boni A, Curiel TJ, Angeles CV, Turk MJ. 2018. Oncogenic BRAF V600E governs regulatory T-cell recruitment during melanoma tumorigenesis. Cancer Res. 78(17):5038–49.
  • Sharma P, Diergaarde B, Ferrone S, Kirkwood JM, Whiteside TL. 2020. Melanoma cell-derived exosomes in plasma of melanoma patients suppress functions of immune effector cells. Sci Rep. 10(1):92.
  • Shenoy GN, Loyall J, Berenson CS, Kelleher RJ Jr., Iyer V, Balu-Iyer SV, Odunsi K, Bankert RB. 2018a. Sialic acid-dependent inhibition of T cells by exosomal ganglioside GD3 in ovarian tumor microenvironments. J Immunol. 201:3750–58.
  • Shenoy GN, Loyall J, Maguire O, Iyer V, Kelleher RJ Jr., Minderman H, Wallace PK, Odunsi K, Balu-Iyer SV, Bankert RB. 2018b. Exosomes associated with human ovarian tumors harbor a reversible checkpoint of T-cell responses. Cancer Immunol Res. 6:236–47.
  • Shu S, Yang Y, Allen CL, Hurley E, Tung KH, Minderman H, Wu Y, Ernstoff MS. 2020. Purity and yield of melanoma exosomes are dependent on isolation method. J Extracell Vesicles. 9:1692401.
  • Shu S, Yang Y, Allen CL, Maguire O, Minderman H, Sen A, Ciesielski MJ, Collins KA, Bush PJ, Singh P, et al. 2018. Metabolic reprogramming of stromal fibroblasts by melanoma exosome microRNA favours a pre-metastatic microenvironment. Sci Rep. 8(1):12905.
  • Sumimoto H, Imabayashi F, Iwata T, Kawakami Y. 2006. The BRAF-MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells. J Exp Med. 203:1651–56.
  • Sun Z, Fourcade J, Pagliano O, Chauvin JM, Sander C, Kirkwood JM, Zarour HM. 2015. IL10 and PD-1 cooperate to limit the activity of tumor-specific CD8+ T cells. Cancer Res. 75:1635–44.
  • Tung KH, Ernstoff MS, Allen C, Shu S. 2019. A review of exosomes and their role in the tumor microenvironment and host-tumor “macroenvironment”. J Immunol Sci. 3:4–8.
  • Whipple CA, Boni A, Fisher JL, Hampton TH, Tsongalis GJ, Mellinger DL, Yan S, Tafe LJ, Brinckerhoff CE, Turk MJ, et al. 2016. The mitogen-activated protein kinase pathway plays a critical role in regulating immunological properties of BRAF mutant cutaneous melanoma cells. Melanoma Res. 26(3):223–35.
  • Whiteside TL. 2016. Tumor-derived exosomes and their role in tumor-induced immune suppression. Vaccines (Basel). Dec;4(4): 35. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5192355/
  • Whiteside TL. 2018. The potential of tumor-derived exosomes for noninvasive cancer monitoring: an update. Expert Rev Mol Diagn. 18(12):1029–40.
  • Zhang H-G, Grizzle WE. 2011. Exosomes and cancer: a newly described pathway of immune suppression. Clin Cancer Res. 17(5):959–64.

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