Targeting CSPG4 for isolation of melanoma cell-derived exosomes from body fluids

Ribas A, Wolchok JD (2018) Cancer immunotherapy using checkpoint blockade. Science 359(6382):1350–1355. https://doi.org/10.1126/science.aar4060 Weiss SA, Wolchok JD, Sznol M (2019) Immunotherapy of melanoma: facts and hopes. Clin Cancer Res 25(17):5191–5201. https://doi.org/10.1158/1078-0432.CCR-18-1550 Pires da Silva I, Lo S, Quek C, Gonzalez M, Carlino MS, Long GV, Menzies AM (2019) Site-specific response patterns, pseudoprogression, and acquired resistance in patients with melanoma treated with ipilimumab combined with anti-PD‑1 therapy. Cancer. https://doi.org/10.1002/cncr.32522 Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S (2000) Escape of human solid tumors from T‑cell recognition: molecular mechanisms and functional significance. Adv Immunol 74:181–273 Cai L, Michelakos T, Yamada T, Fan S, Wang X, Schwab JH, Ferrone CR, Ferrone S (2018) Defective HLA class I antigen processing machinery in cancer. Cancer Immunol Immunother 67(6):999–1009. https://doi.org/10.1007/s00262-018-2131-2 Munn DH, Mellor AL (2016) IDO in the tumor microenvironment: inflammation, counter-regulation, and tolerance. Trends Immunol 37(3):193–207. https://doi.org/10.1016/j.it.2016.01.002 Ohta A (2016) A metabolic immune checkpoint: adenosine in tumor microenvironment. Front Immunol 7:109. https://doi.org/10.3389/fimmu.2016.00109 Hoffmann TK, Dworacki G, Tsukihiro T, Meidenbauer N, Gooding W, Johnson JT, Whiteside TL (2002) Spontaneous apoptosis of circulating T lymphocytes in patients with head and neck cancer and its clinical importance. Clin Cancer Res 8(8):2553–2562 Whiteside TL (2015) The role of regulatory T cells in cancer immunology. Immunotargets Ther 4:159–171. https://doi.org/10.2147/ITT.S55415 Ostrand-Rosenberg S (2018) Myeloid derived-suppressor cells: their role in cancer and obesity. Curr Opin Immunol 51:68–75. https://doi.org/10.1016/j.coi.2018.03.007 Wu Y, Chen W, Xu ZP, Gu W (2019) PD-L1 distribution and perspective for cancer immunotherapy-blockade, knockdown, or inhibition. Front Immunol 10:2022. https://doi.org/10.3389/fimmu.2019.02022 Damgaci S, Ibrahim-Hashim A, Enriquez-Navas PM, Pilon-Thomas S, Guvenis A, Gillies RJ (2018) Hypoxia and acidosis: immune suppressors and therapeutic targets. Immunology 154(3):354–362. https://doi.org/10.1111/imm.12917 Whiteside TL (2017) Exosomes carrying immunoinhibitory proteins and their role in cancer. Clin Exp Immunol 189(3):259–267. https://doi.org/10.1111/cei.12974 Campoli MR, Chang CC, Kageshita T, Wang X, McCarthy JB, Ferrone S (2004) Human high molecular weight-melanoma-associated antigen (HMW-MAA): a melanoma cell surface chondroitin sulfate proteoglycan (MSCP) with biological and clinical significance. Crit Rev Immunol 24:267–296 Campoli M, Ferrone S, Wang X (2010) Functional and clinical relevance of chondroitin sulfate proteoglycan 4. Adv Cancer Res 109:73–121 Ruivo CF, Adem B, Silva M, Melo SA (2017) The biology of cancer exosomes: insights and new perspectives. Cancer Res 77(23):6480–6488. https://doi.org/10.1158/0008-5472.CAN-17-0994 Hessvik NP, Llorente A (2018) Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 75(2):193–208. https://doi.org/10.1007/s00018-017-2595-9 Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, García-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18(6):883–891. https://doi.org/10.1038/nm.2753 Whiteside TL (2017) The effect of tumor-derived exosomes on immune regulation and cancer immunotherapy. Future Oncol 13(28):2583–2592. https://doi.org/10.2217/fon-2017-0343 Mulcahy LA, Pink RC, Carter DR (2014) Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles. https://doi.org/10.3402/jev.v3.24641 Kurywchak P, Tavormina J, Kalluri R (2018) The emerging roles of exosomes in the modulation of immune responses in cancer. Genome Med 10(1):23. https://doi.org/10.1186/s13073-018-0535-4 Chen G, Huang AC, Zhang W, Zhang G, Wu M, Xu W, Yu Z, Yang J, Wang B, Sun H, Xia H, Man Q, Zhong W, Antelo LF, Wu B, Xiong X, Liu X, Guan L, Li T, Liu S, Yang R, Lu Y, Dong L, McGettigan S, Somasundaram R, Radhakrishnan R, Mills G, Lu Y, Kim J, Chen YH, Dong H, Zhao Y, Karakousis GC, Mitchell TC, Schuchter LM, Herlyn M, Wherry EJ, Xu X, Guo W (2018) Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD‑1 response. Nature 560(7718):382–386. https://doi.org/10.1038/s41586-018-0392-8 Wieckowski EU, Visus C, Szajnik M, Szczepanski MJ, Storkus WJ, Whiteside TL (2009) Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J Immunol 183(6):3720–3730. https://doi.org/10.4049/jimmunol.0900970 Sharma P, Diergaarde B, Ferrone S, Kirkwood JM, Whiteside TL (2019) Melanoma cell-derived exosomes in plasma of melanoma patients mediate suppression of immune effector cells. Sci Rep 2020 10(10):92. https://doi.org/10.1038/s41598-019-56542-4 Hong CS, Funk S, Muller L, Boyiadzis M, Whiteside TL (2016) Isolation of biologically active and morphologically intact exosomes from plasma of patients with cancer. J Extracell Vesicles 5:29289. https://doi.org/10.3402/jev.v5.29289 Sharma P, Ludwig S, Muller L, Hong CS, Kirkwood JM, Ferrone S, Whiteside TL (2017) Immunoaffinity-based isolation of melanoma cell-derived exosomes from plasma of patients with melanoma. J Extracell Vesicles 7(1):1435138. https://doi.org/10.1080/20013078.2018.1435138 Wang X, Katayama A, Wang Y, Yu L, Favoino E, Sakakura K, Favole A, Tsuchikawa T, Silver S, Watkins SC, Kageshita T, Ferrone S (2011) Functional characterization of an scFV antibody that immunotherapeutically targets the common cancer cell surface proteoglycan CSPG4. Cancer Res 71:7410–7422 Schlingemann RO, Rietveld FJ, de Waal RM, Ferrone S, Ruiter DJ (1990) Expression of the high molecular weight melanoma associated antigen by pericytes during angiogenesis in tumors and in healing wounds. Am J Pathol 136:1393–1405 Maciag PC, Seavy MM, Pan ZK, Ferrone S, Paterson Y (2008) Cancer immunotherapy targeting the high molecular weight melanoma-associated antigen protein results in a broad antitumor response and reduction of pericytes in the tumor vasculature. Cancer Res 68:8066–8075 Beard RE, Zheng Z, Lagisetty KH, Burns WR, Tran E, Hewitt SM, Abate-Daga D, Rosati SF, Fine HA, Ferrone S, Rosenberg SA, Morgan RA (2014) Multiple chimeric antigen receptors successfully target chondroitin sulfate proteoglycan 4 in several different cancer histologies and cancer stem cells. J Immunother Cancer 2:25 Beard RE, Abate-Daga D, Rosati SF, Zheng Z, Wunderlich JR, Rosenberg SA, Morgan RA (2013) Gene expression profiling using nanostring digital RNA counting to identify potential target antigens for melanoma immunotherapy. Clin Cancer Res 19(18):4941–4950. https://doi.org/10.1158/1078-0432.CCR-13-1253 Wang X, Osada T, Wang Y, Yu L, Sakakura K, Katayama A, McCarthy J, Brufsky A, Chivukula M, Khoury T, Hsu D, Lyerly H, Clay T, Ferrone S (2010) CSPG4 as a new target for antibody-based immunotherapy of triple negative breast cancer. J Natl Cancer Inst 102:1496–1512 Mittelman A, Chen ZJ, Yang H, Wong GY, Ferrone S (1992) Human high molecular weight melanoma-associated antigen (HMW-MAA) mimicry by mouse anti-idiotypic monoclonal antibody MK2-23: induction of humoral anti-HMW-MAA immunity and prolongation of survival in patients with stage IV melanoma. Proc Natl Acad Sci USA 89:466–470 Riccardo F, Iussich S, Maniscalco L, Mayayo SL, Rosa GL, Arigoni M, Maria RD, Gattino F, Lanzardo S, Lardone E, Martano M, Morello E, Prestigio S, Fiore A, Quaglino E, Zabarino S, Ferrone S, Buracco P, Cavallo F (2014) CSPG4-specific immunity and survival prolongation in dogs with oral malignant melanoma immunized with human CSPG4 DNA. Clin Cancer Res 20:3753–3762 Léger O, Johnson-Léger C, Jackson E, Coles B, Dean C (1994) The chondroitin sulfate proteoglycan NG2 is a tumour-specific antigen on the chemically induced rat chondrosarcoma HSN. Int J Cancer 58(5):700–705 Geldres C, Savoldo B, Hoyos V, Caruana I, Zhang M, Yvon E, Del Vecchio M, Creighton CJ, Ittmann MM, Ferrone S, Dotti G (2014) T lymphocytes redirected against the chondroitin sulfate proteoglycan‑4 control the growth of multiple solid tumors both in vitro and in vivo. Clin Cancer Res 20:962–971