Specific ADAM10 inhibitors localize in exosome-like vesicles released by Hodgkin lymphoma and stromal cells and prevent sheddase activity carried to bystander cells

References

• Edwards DR, Handsle MM, Pennington CJ. The ADAM metalloproteinases. Mol Aspects Med. 2008;29(5):258–89. doi: 10.1016/j.mam.2008.08.001. PMID:18762209.
   PubMed Web of Science ®Google Scholar
• Reiss K., and Saftig P. The “A Disintegrin And Metalloprotease” (ADAM) family of sheddases: Physiological and cellular functions. Semin Cell Dev Biol. 2009;20(2):126–37. doi: 10.1016/j.semcdb.2008.11.002. PMID:19049889.
   PubMed Web of Science ®Google Scholar
• Blobel CP. ADAMs: key components in EGFR signalling and development. Nature Rev Cancer. 2005;6(1):32–43. doi: 10.1038/nrm1548. PMID:15688065.
   Google Scholar
• Rocks N, Paulissen G, El Hour M, Quesada F, Crahay C, Gueders M, Foidart JM, Noel A, Cataldo D. Emerging roles of ADAM and ADAMTS metalloproteinases in cancer. Biochimie. 2008;90(2):369–79. doi: 10.1016/j.biochi.2007.08.008. PMID:17920749.
   PubMed Web of Science ®Google Scholar
• Duffy MJ, McKiernan E, O'Donovan N, McGowan P. Role of ADAMs in cancer formation and progression. Clin Cancer Res. 2009;15(4):1140–44. doi: 10.1158/1078-0432.CCR-08-1585. PMID:19228719.
   PubMed Web of Science ®Google Scholar
• Murphy G. The ADAMs: Signalling scissors in the tumor microenvironment. Nature Rev Cancer. 2008;8:929–41. doi: 10.1038/nrc2459. PMID:19005493.
   PubMed Web of Science ®Google Scholar
• Duffy MJ, Mullooly M, O'Donovan N, Sukor S, Crown J, Pierce A, McGowan PM. The ADAMs family of proteases: new biomarkers and therapeutic targets for cancer? Clin Proteomics. 2011;8:9–13. doi: 10.1186/1559-0275-8-9. PMID:21906355.
   PubMedGoogle Scholar
• Saftig P, Reiss K. The “A Disintegrin And Metalloproteases” ADAM10 and ADAM17: novel drug targets with therapeutic potential? Eur J Cell Biol. 2011;90:527–35. doi: 10.1016/j.ejcb.2010.11.005. PMID:21194787.
   PubMed Web of Science ®Google Scholar
• Zhou BB, Peyton M, He B, Liu C, Girard L, Caudler E, Lo Y, Baribaud F, Mikami I, Reguart N, et al. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell. 2006;10(1):39–50. doi: 10.1016/j.ccr.2006.05.024. PMID:16843264.
   PubMed Web of Science ®Google Scholar
• Witters L, Scherle P, Friedman S, Fridman J, Caulder E, Newton R, Lipton A Synergistic inhibition with a dual epidermal growth factor receptor/HER-2/neu tyrosine kinase inhibitor and a disintegrin and metallo proteinase inhibitor. Cancer Res. 2008;68:7082–89. doi: 10.1158/0008-5472.CAN-08-0739. PMID:18757423.
   Web of Science ®Google Scholar
• Moss ML, Stoeck A, Yan W, Dempsey PJ. ADAM10 as a target for anti-cancer therapy. Curr Pharm Biotechnol. 2008;9:2–8. doi:10.2174/138920108783497613. PMID:18289051.
   PubMed Web of Science ®Google Scholar
• Waldhauer I, Steinle A. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res. 2006; 66(5):2520–26. doi:10.1158/0008-5472.CAN-05-2520. PMID:16510567.
   PubMed Web of Science ®Google Scholar
• Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, Stevanovic S, Rammensee HG, Steinle A. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008;68(15):6368–6376. doi: 10.1158/0008-5472.CAN-07-6768. PMID:18676862.
   PubMed Web of Science ®Google Scholar
• Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene. 2008;27:5944–58. doi: 10.1038/onc.2008.272. PMID:18836475.
   PubMed Web of Science ®Google Scholar
• Salih HR, Antropius H, Gieseke F, Lutz SZ, Kanz L, Rammensee HG, Steinle A. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood. 2003;102:1389–96. doi: 10.1182/blood-2003-01-0019. PMID:12714493.
   PubMed Web of Science ®Google Scholar
• Poggi A, Venturino C, Catellani S, Clavio M, Miglino M, Gobbi M, Steinle A, Ghia P, Stella S, Caligaris-Cappio F et al. Vδ1 T lymphocytes from B-CLL patients recognize ULBP3 expressed on leukemic B cells and up-regulated by trans-retinoic acid. Cancer Res. 2004;64:9172–9. doi: 10.1158/0008-5472.CAN-04-2417. PMID:15604289.
   PubMed Web of Science ®Google Scholar
• Catellani S, Poggi A., Bruzzone A., Dadati P., Ravetti JL., Gobbi M., Zocchi MR. Expansion of Vdelta1 T lymphocytes producing IL-4 in low-grade non-Hodgkin lymphomas ex pressing UL-16-binding proteins. Blood. 2007;109:2078–85. doi: 10.1182/blood-2006-06-028985. PMID:16973957.
   PubMed Web of Science ®Google Scholar
• Zocchi MR, Catellani S, Canevali P, Tavella S, Garuti A, Villaggio B, Zunino A, Gobbi M, Fraternali-Orcioni G, Kunkl A, et al. High ERp5/ADAM10 expression in lymph node microenvironment and impaired NKG2D-ligands recognition in Hodgkin lymphomas. Blood. 2012; 119:1479–89. doi: 10.1182/blood-2011-07-370841. PMID:22167753.
   PubMed Web of Science ®Google Scholar
• Eichenauer DA, Simhadri VL, von Strandmann EP, Ludwig A, Matthews V, Reiners KS, von Tresckow B, Saftig P, Rose-John S, Engert A, Hansen HP. ADAM10 inhibition of human CD30 shedding increases specificity of targeted immunotherapy in vitro. Cancer Res. 2007;67(1):332–8. doi: 10.1158/0008-5472.CAN-06-2470. PMID:17210715.
   PubMed Web of Science ®Google Scholar
• Zocchi M.R, Camodeca C, Nuti E, Rossello A, Venè R, Tosetti F, Dapino I, Costa D, Musso A, Poggi A. (2016) ADAM10 new selective inhibitors reduce NKG2D ligand release sensitizing Hodgkin lymphoma cells to NKG2D-mediated killing. Oncoimmunology. 2015;5(5):e1123367. doi: 10.1080/2162402X.2015.1123367. PMID:27467923.
   PubMed Web of Science ®Google Scholar
• Camodeca C, Nuti E, Tepshi L, Boero S, Tuccinardi T, Stura E A, Poggi A, Zocchi MR, Rossello A. Discovery of a new selective inhibitor of A Disintegrin And Metalloprotease 10 (ADAM10) able to reduce the shedding of NKG2D ligands in Hodgkin's lymphoma cell models. Eur J Med Chem. 2016;111:193–201. doi: 10.1016/j.ejmech.2016.01.053. PMID:26871660.
   PubMed Web of Science ®Google Scholar
• Stoeck A, Keller S, Riedle S, Sanderson MP, Runz S, Le Naour F Gutwein P, Ludwig A, Rubinstein E, Altevogt P. A role for exosomes in the constitutive and stimulus-induced ectodomain cleavage of L1 and CD44. Biochem J. 2006;393(Pt3):609–18. doi:10.1042/bj20051013. PMID:16229685.
   PubMedGoogle Scholar
• Chitadze G, Lettau M, Bhat J, Wesch D, Steinle A, Fürst D, Mytilineos J, Kalthoff H, Janssen O, Oberg HH, et al. Shedding of endogenous MHC class I-related chain molecules A and B from different human tumor entities: heterogeneous involvement of the “a disintegrin and metalloproteases” 10 and 17. Int J Cancer. 2013;133(7):1557–66. doi: 10.1002/ijc.28174. PMID:23526433.
   PubMed Web of Science ®Google Scholar
• Théry C, Boussac M, Véron P, Ricciardi-Castagnoli P, Raposo G, Garin J, Amigorena S. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001; 166(12):7309–18. doi:10.4049/jimmunol.166.12.7309. PMID:11390481.
   PubMed Web of Science ®Google Scholar
• Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654–9. doi: 10.1038/ncb1596. PMID:17486113.
   PubMed Web of Science ®Google Scholar
• Lundholm M, Schröder M, Nagaeva O, Baranov V, Widmark A, Mincheva-Nilsson L, Wikström P. Prostate tumor-derived exosomes down-regulate NKG2D expression on natural killer cells and CD8+ T cells: mechanism of immune evasion. PLoS One. 2014;9(9):e108925. doi: 10.1371/journal.pone.0108925. PMID:25268476.
   PubMed Web of Science ®Google Scholar
• Filipazzi P, Bürdek M, Villa A, Rivoltini L, Huber V. Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Semin Cancer Biol. 2012;22(4):342–9. doi: 10.1016/j.semcancer.2012.02.005. PMID:22369922.
   PubMed Web of Science ®Google Scholar
• Escrevente C, Morais VA, Keller S, Soares CM, Altevogt P, Costa J. Functional role of N-glycosylation from ADAM10 in processing, localization and activity of the enzyme. Biochim Biophys Acta. 2008;1780(6):905–13. doi: 10.1016/j.bbagen.2008.03.004. PMID:18381078.
   PubMed Web of Science ®Google Scholar
• Waugh MG. Raft-like membranes from the trans-Golgi network and endosomal compartments. Nat Protoc. 2013;8(12):2429–39. doi: 10.1038/nprot.2013.148. PMID:24202556.
   PubMed Web of Science ®Google Scholar
• Camodeca C, Nuti E, Tosetti F, Poggi A, D'Arrigo C, Zocchi MR, Rossello A. Synthesis and in vitro evaluation of ADAM-10 and ADAM-17 selective bioimaging probes. Bioconjugate Chem 2018, Submitted.
   Google Scholar
• Norman LL, Brugués J Sengupta K, Sens P, Aranda-Espinoza H. Cell blebbing and membrane area homeostasis in spreading and retracting cells. Biophys J. 2010 Sep 22;99(6):1726–33. doi: 10.1016/j.bpj.2010.07.031. PMID:20858416.
   PubMed Web of Science ®Google Scholar
• Van Den Berk LC Jansen BJ, Siebers-Vermeulen KG, Roelofs H, Figdor CG, Adema GJ, Torensma R. Mesenchymal stem cells respond to TNF but do not produce TNF. J. Leukoc Biol. 2010;7(2):283–9. doi: 10.1189/jlb.0709467. PMID:19897767.
   Google Scholar
• Hansen HP, Trad A, Dams M, Zigrino P, Moss M, Tator M, Schön G, Grenzi PC, Bachurski D, Aquino B, et al. CD30 on extracellular vesicles from malignant Hodgkin cells supports damaging of CD30 ligand-expressing bystander cells with Brentuximab-Vedotin, in vitro. Oncotarget. 2016;7(21):30523–35. doi: 10.18632/oncotarget.8864. PMID:27105521.
   PubMed Web of Science ®Google Scholar
• Nakayama S, Yokote T, Tsuji M, Akioka T, Miyoshi T, Hirata Y, Hiraoka N, Iwaki K, Takayama A, Nishiwaki U, et al. Expression of tumour necrosis factor-α and its receptors in Hodgkin lymphoma. Br J Haematol. 2014;167(4): 574–77. doi: 10.1111/bjh.13015. PMID:25039986.
   PubMed Web of Science ®Google Scholar
• Borchmann P, Treml JF, Hansen H, Gottstein C, Schnell R, Staak O, Zhang HF, Davis T, Keler T, Diehl V, et al. The human anti-CD30 antibody 5F11 shows in vitro and in vivo activity against malignant lymphoma. Blood. 2003;102(10):3737–42. doi: 10.1182/blood-2003-02-0515. PMID:12881320.
   PubMed Web of Science ®Google Scholar
• Cardarelli P, Moldovan-Loomis MC, Preston B, Black A, Passmore D, Chen T-H, Chen S, Liu J, Kuhne MR, Srinivasan M, et al. In vitro and in vivo characterization of MDX-1401 for therapy of Malignant lymphoma. Clin Cancer Res. 2009;15(10):3376–3383. doi: 10.1158/1078-0432.CCR-08-3222. PMID:19401346.
   PubMed Web of Science ®Google Scholar
• Noy PJ, Yang J, Reyat JS, Matthews AL, Charlton AE, Furmston J, Rogers DA, Rainger GE, Tomlinson MG. TspanC8 Tetraspanins and A Disintegrin and Metalloprotease 10 (ADAM10) Interact via Their Extracellular Regions:evidence for distinct binding mechanisms for different TspanC8 proteins. J Biol Chem. 2016;291(7):3145–57. doi: 10.1074/jbc.M115.703058. PMID:26668317.
   PubMed Web of Science ®Google Scholar
• Borchmann S, von Tresckow B, Engert A. Current developments in the treatment of early-stage classical Hodgkin lymphoma. Curr Opin Oncol. 2016; 28(5):377–83. doi: 10.1097/CCO.0000000000000314. PMID:27455136.
   PubMed Web of Science ®Google Scholar
• Nuti E, Casalini F, Avramova SI, Santamaria S, Fabbi M, Ferrini S, Marinelli L, La Pietra V, Limongelli V, Novellino E, et al. Potent Arylsulfonamide Inhibitors of Tumor Necrosis Factor-α Converting Enzyme Able to Reduce Activated Leukocyte Cell Adhesion Molecule Shedding in Cancer Cell Models. J Med Chem. 2010; 53(6):2622–35. doi: 10.1021/jm901868z. PMID:20180536.
   PubMed Web of Science ®Google Scholar
• Neumann U, Kubota H, Frei K, Ganu V, Leppert D. Characterization of Mca-Lys-Pro-Leu-Gly-Leu-Dpa-Ala-Arg-NH2, a fluorogenic substrate with increased specificity constants for collagenases and tumor necrosis factor converting enzyme. Anal Biochem. 2004;328(2):166–173. doi: 10.1016/j.ab.2003.12.035. PMID:15113693.
   PubMed Web of Science ®Google Scholar
• Benelli R, Monteghirfo S, Balbi C, Barboro P, Ferrari N. Novel antivascular efficacy of metronomic docetaxel therapy in prostate cancer: hnRNP K as a player. Int J Cancer 2009;124:2989–96. doi:10.1002/ijc.24305. PMID:19319982.
   PubMed Web of Science ®Google Scholar
• Colombo MI, Lenhard JM, Mayorga LS, Stahl PD. Reconstitution of endosome fusion: identification of factors necessary for fusion competency. Methods Enzimol. 1992;219:32–44. doi:10.1016/0076-6879(92)19007-S. PMID: 1488005.
   PubMed Web of Science ®Google Scholar
• Waugh MG. Raft-like membranes from the trans-Golgi network and endosomal compartments. Nat Protoc. 2013;8(12):2429–39. doi: 10.1038/nprot.2013.148. PMID:24202556
   PubMed Web of Science ®Google Scholar
• Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;Chapter 3:Unit 3. 22. doi: 10.1002/0471143030.cb0322s30. PMID:18228490.
   Google Scholar