The emerging role of exosomes in multiple myeloma

Bianchi, 2015, Pathogenesis beyond the cancer clone(s) in multiple myeloma, Blood, 125, 3049, 10.1182/blood-2014-11-568881 Pawlyn, 2019, Toward personalized treatment in multiple myeloma based on molecular characteristics, Blood, 133, 660, 10.1182/blood-2018-09-825331 Rajkumar, 2011, Approach to the treatment of multiple myeloma: a clash of philosophies, Blood, 118, 3205, 10.1182/blood-2011-06-297853 Zhang, 2016, Potential role of exosome-associated microRNA panels and in vivo environment to predict drug resistance for patients with multiple myeloma, Oncotarget, 7, 30876, 10.18632/oncotarget.9021 Gooding, 2016, New approaches to targeting the bone marrow microenvironment in multiple myeloma, Curr Opin Pharmacol, 28, 43, 10.1016/j.coph.2016.02.013 Raimondi, 2015, Involvement of multiple myeloma cell-derived exosomes in osteoclast differentiation, Oncotarget, 6, 13772, 10.18632/oncotarget.3830 Wang, 2014, Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells, Blood, 124, 555, 10.1182/blood-2014-03-562439 Quail, 2013, Microenvironmental regulation of tumor progression and metastasis, Nat Med, 19, 1423, 10.1038/nm.3394 Moloudizargari, 2018, Modifying exosome release in cancer therapy: how can it help?, Pharmacol Res, 134, 246, 10.1016/j.phrs.2018.07.001 Vardaki, 2016, Caspase-3-dependent cleavage of Bcl-xL in the stroma exosomes is required for their uptake by hematological malignant cells, Blood, 128, 2655, 10.1182/blood-2016-05-715961 Otto, 1997, Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development, Cell, 89, 765, 10.1016/S0092-8674(00)80259-7 De Veirman, 2016, Induction of miR-146a by multiple myeloma cells in mesenchymal stromal cells stimulates their pro-tumoral activity, Cancer Lett, 377, 17, 10.1016/j.canlet.2016.04.024 Roccaro, 2013, BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression, J Clin Invest, 123, 1542, 10.1172/JCI66517 Wang, 2013, Kruppel-like factor 8 promotes tumorigenic mammary stem cell induction by targeting miR-146a, Am J Cancer Res, 3, 356 Yaccoby, 2006, Inhibitory effects of osteoblasts and increased bone formation on myeloma in novel culture systems and a myelomatous mouse model, Haematologica, 91, 192 Child, 2003, High-dose chemotherapy with hematopoietic stem-cell rescue for multiple myeloma, N Engl J Med, 348, 1875, 10.1056/NEJMoa022340 Kint, 2019, The treatment of multiple myeloma in an era of precision medicine, Expert Rev Precision Med Drug Dev, 4, 153, 10.1080/23808993.2019.1606672 Nooka, 2015, Treatment options for relapsed and refractory multiple myeloma, Blood, 125, 3085, 10.1182/blood-2014-11-568923 Sponaas, 2015, PDL1 expression on plasma and dendritic cells in myeloma bone marrow suggests benefit of targeted anti PD1-PDL1 therapy, PLoS One, 10, 10.1371/journal.pone.0139867 Kumar, 2017, Emerging options in multiple myeloma: targeted, immune, and epigenetic therapies, Hematol-Am Soc Hematol, 2017, 518, 10.1182/asheducation-2017.1.518 Boyiadzis, 2017, The emerging roles of tumor-derived exosomes in hematological malignancies, Leukemia, 31, 1259, 10.1038/leu.2017.91 Théry, 2002, Exosomes: composition, biogenesis and function, Nat Rev Immunol, 2, 569, 10.1038/nri855 Yáñez-Mó, 2015, Biological properties of extracellular vesicles and their physiological functions, J Extracell, 4, 27066, 10.3402/jev.v4.27066 Canella, 2016, The potential diagnostic power of extracellular vesicle analysis for multiple myeloma, Expert Rev Mol Diagn, 16, 277, 10.1586/14737159.2016.1132627 Nomura, 2017, Extracellular vesicles and blood diseases, Int J Hematol, 105, 392, 10.1007/s12185-017-2180-x Gulei, 2018, Exosomes-small players, big sound, Bioconjug Chem, 29, 635, 10.1021/acs.bioconjchem.8b00003 Hessvik, 2016, PIKfyve inhibition increases exosome release and induces secretory autophagy, Cell Mol Life Sci, 73, 4717, 10.1007/s00018-016-2309-8 Colombo, 2013, Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles, J Cell Sci, 126, 5553, 10.1242/jcs.128868 Lange, 2017, Peptidylarginine deiminases—roles in cancer and neurodegeneration and possible avenues for therapeutic intervention via modulation of exosome and microvesicle (EMV) release?, Int J Mol Sci, 18, 10.3390/ijms18061196 Agarwal, 2015, Analysis of exosome release as a cellular response to MAPK pathway inhibition, Langmuir, 31, 5440, 10.1021/acs.langmuir.5b00095 Qu, 2016, Exosome-transmitted lncARSR promotes sunitinib resistance in renal cancer by acting as a competing endogenous RNA, Cancer Cell, 29, 653, 10.1016/j.ccell.2016.03.004 Villarroya-Beltri, 2014, Sorting it out: regulation of exosome loading, Semin Cancer Biol, 28, 3, 10.1016/j.semcancer.2014.04.009 Singh, 2014, Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer, Mol Cancer, 13, 10.1186/1476-4598-13-256 Riches, 2014, Regulation of exosome release from mammary epithelial and breast cancer cells-a new regulatory pathway, Eur J Cancer, 50, 1025, 10.1016/j.ejca.2013.12.019 Baietti, 2012, Syndecan–syntenin–ALIX regulates the biogenesis of exosomes, Nat Cell Biol, 14, 677, 10.1038/ncb2502 Fares, 2017, Syntenin: key player in cancer exosome biogenesis and uptake?, Cell Adh Migr, 11, 124, 10.1080/19336918.2016.1225632 Ghossoub, 2014, Syntenin-ALIX exosome biogenesis and budding into multivesicular bodies are controlled by ARF6 and PLD2, Nat Commun, 5, 10.1038/ncomms4477 Bali, 2014, Olive leaf extracts protect cardiomyocytes against 4-hydroxynonenal-induced toxicity in vitro: comparison with oleuropein, hydroxytyrosol, and quercetin, Planta Med, 80, 984, 10.1055/s-0034-1382881 Guo, 2017, Atg5 disassociates the V1V0-ATPase to promote exosome production and tumor metastasis independent of canonical macroautophagy, Dev Cell, 43, 716, 10.1016/j.devcel.2017.11.018 Moloudizargari, 2017, Autophagy, its mechanisms and regulation: Implications in neurodegenerative diseases, Ageing Res Rev, 40, 64, 10.1016/j.arr.2017.09.005 Purushothaman, 2016, Fibronectin on the surface of myeloma cell-derived exosomes mediates exosome-cell interactions, J Biol Chem, 291, 1652, 10.1074/jbc.M115.686295 Morishita, 2017, Pharmacokinetics of exosomes—an important factor for elucidating the biological roles of exosomes and for the development of exosome-based therapeutics, J Pharm Sci, 106, 2265, 10.1016/j.xphs.2017.02.030 Altevogt, 2014, Novel insights into exosome-induced, tumor-associated inflammation and immunomodulation, Semin Cancer Biol, 28, 51, 10.1016/j.semcancer.2014.04.008 Fan, 2014, Hypoxic exosomes promote angiogenesis, Blood, 124, 3669, 10.1182/blood-2014-10-607846 Li, 2018, Exosome-mediated transfer of lncRUNX2-AS1 from multiple myeloma cells to MSCs contributes to osteogenesis, Oncogene, 1 Braicu, 2015, Exosomes as divine messengers: are they the hermes of modern molecular oncology?, Cell Death Differ, 22, 34, 10.1038/cdd.2014.130 Kosaka, 2014, Dark side of the exosome: the role of the exosome in cancer metastasis and targeting the exosome as a strategy for cancer therapy, Future Oncol, 10, 671, 10.2217/fon.13.222 Lu, 2014, Modeling putative therapeutic implications of exosome exchange between tumor and immune cells, Proc Natl Acad Sci U S A, 111, E4165, 10.1073/pnas.1416745111 Gulei, 2018, Exosomes at a glance - common nominators for cancer hallmarks and novel diagnosis tools, Crit Rev Biochem Mol Biol, 53, 564, 10.1080/10409238.2018.1508276 Wang, 2016, Extracellular vesicle cross-talk in the bone marrow microenvironment: implications in multiple myeloma, Oncotarget, 7, 38927, 10.18632/oncotarget.7792 Abdi, 2014, Micro-RNAs, new performers in multiple myeloma bone marrow microenvironment, Biomark Res, 2, 10.1186/2050-7771-2-10 Di Marzo, 2016, Microenvironment drug resistance in multiple myeloma: emerging new players, Oncotarget, 7, 60698, 10.18632/oncotarget.10849 Zingoni, 2018, NKG2D and its ligands: "one for all, all for one", Front Immunol, 9 Iero, 2008, Tumour-released exosomes and their implications in cancer immunity, Cell Death Differ, 15, 80, 10.1038/sj.cdd.4402237 Wang, 2016, Exosomes in tumor microenvironment: novel transporters and biomarkers, J Transl Med, 14, 297, 10.1186/s12967-016-1056-9 Wang, 2015, The bone marrow microenvironment enhances multiple myeloma progression by exosome-mediated activation of myeloid-derived suppressor cells, Oncotarget, 6, 43992, 10.18632/oncotarget.6083 Ghobrial, 2013, Revisiting treatment paradigms in high-risk smoldering multiple myeloma: out with the old, in with the new?, Leuk Lymphoma, 54, 2328, 10.3109/10428194.2013.788699 Basak, 2009, Multiple myeloma bone marrow niche, Curr Pharm Biotechnol, 10, 345, 10.2174/138920109787847493 Mitsiades, 2007, The role of the bone marrow microenvironment in the pathophysiology of myeloma and its significance in the development of more effective therapies, Hematol Oncol Clin North Am, 21, 1007, 10.1016/j.hoc.2007.08.007 Arnulf, 2007, Phenotypic and functional characterization of bone marrow mesenchymal stem cells derived from patients with multiple myeloma, Leukemia, 21, 158, 10.1038/sj.leu.2404466 Corre, 2007, Bone marrow mesenchymal stem cells are abnormal in multiple myeloma, Leukemia, 21, 1079, 10.1038/sj.leu.2404621 Reagan, 2012, Multiple myeloma mesenchymal stem cells: characterization, origin, and tumor-promoting effects, Clin Cancer Res, 18, 342, 10.1158/1078-0432.CCR-11-2212 Xu, 2012, Impaired osteogenic differentiation of mesenchymal stem cells derived from multiple myeloma patients is associated with a blockade in the deactivation of the Notch signaling pathway, Leukemia, 26, 2546, 10.1038/leu.2012.126 Cheng, 2017, Multiple myeloma-derived exosomes regulate the functions of mesenchymal stem cells partially via modulating miR-21 and miR-146a, Stem Cells Int, 2017, 10.1155/2017/9012152 Wang, 2016, Multiple myeloma exosomes establish a favourable bone marrow microenvironment with enhanced angiogenesis and immunosuppression, J Pathol, 239, 162, 10.1002/path.4712 Roccaro, 2013, BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression, J Clin Invest, 123, 1542, 10.1172/JCI66517 Horenstein, 2016, Adenosine generated in the bone marrow niche through a CD38-mediated pathway correlates with progression of human myeloma, Mol Med, 22, 694, 10.2119/molmed.2016.00198 Morandi, 2018, Microvesicles released from multiple myeloma cells are equipped with ectoenzymes belonging to canonical and non-canonical adenosinergic pathways and produce adenosine from ATP and NAD, Oncoimmunology, 7 Soriani, 2009, ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype, Blood, 113, 3503, 10.1182/blood-2008-08-173914 Zingoni, 2016, Targeting NKG2D and NKp30 Ligands shedding to improve NK Cell-Based immunotherapy, Crit Rev Immunol, 36, 445, 10.1615/CritRevImmunol.2017020166 Tkach, 2016, Communication by extracellular vesicles: where we are and where we need to go, Cell, 164, 1226, 10.1016/j.cell.2016.01.043 Reiners, 2014, Role of exosomes released by dendritic cells and/or by tumor targets: regulation of NK cell plasticity, Front Immunol, 5, 10.3389/fimmu.2014.00091 Clayton, 2008, Human tumor-derived exosomes down-modulate NKG2D expression, J Immunol, 180, 7249, 10.4049/jimmunol.180.11.7249 Scarlett, 2013, Contribution of bone marrow derived cells to the pancreatic tumor microenvironment, Front Physiol, 4, 56, 10.3389/fphys.2013.00056 Iaccino, 2017, Monitoring multiple myeloma by idiotype-specific peptide binders of tumor-derived exosomes, Mol Cancer, 16, 159, 10.1186/s12943-017-0730-8 Faict, 2018, Exosomes play a role in multiple myeloma bone disease and tumor development by targeting osteoclasts and osteoblasts, Blood Cancer J, 8, 105, 10.1038/s41408-018-0139-7 Bandari, 2018, Chemotherapy induces secretion of exosomes loaded with heparanase that degrades extracellular matrix and impacts tumor and host cell behavior, Matrix Biol, 65, 104, 10.1016/j.matbio.2017.09.001 Wang, 2016, Multiple myeloma exosomes establish a favourable bone marrow microenvironment with enhanced angiogenesis and immunosuppression, J Pathol, 239, 162, 10.1002/path.4712 Ramasamy, 2017, Structure and functions of blood vessels and vascular niches in bone, Stem Cells Int, 2017, 10.1155/2017/5046953 Ohyashiki, 2016, Exosomes promote bone marrow angiogenesis in hematologic neoplasia: the role of hypoxia, Curr Opin Hematol, 23, 268, 10.1097/MOH.0000000000000235 Hu, 2012, Understanding the hypoxic niche of multiple myeloma: therapeutic implications and contributions of mouse models, Dis Model Mech, 5, 763, 10.1242/dmm.008961 Umezu, 2014, Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1, Blood, 124, 3748, 10.1182/blood-2014-05-576116 Umezu, 2017, Replenishing exosomes from older bone marrow stromal cells with miR-340 inhibits myeloma-related angiogenesis, Blood Adv, 1, 812, 10.1182/bloodadvances.2016003251 Giuliani, 2006, Multiple myeloma bone disease: pathophysiology of osteoblast inhibition, Blood, 108, 3992, 10.1182/blood-2006-05-026112 Hameed, 2014, Bone disease in multiple myeloma: pathophysiology and management, Cancer Growth Metastasis, 7, 33, 10.4137/CGM.S16817 Borrelli, 2018, Drug-induced senescent multiple myeloma cells elicit NK cell proliferation by direct or exosome-mediated IL15 trans-presentation, Cancer Immunol Res, 6, 860, 10.1158/2326-6066.CIR-17-0604 Vulpis, 2017, Genotoxic stress modulates the release of exosomes from multiple myeloma cells capable of activating NK cell cytokine production: role of HSP70/TLR2/NF-kB axis, Oncoimmunology, 6, 10.1080/2162402X.2017.1279372 Xiong, 2017, Effect of myeloma-derived exosomes on surface activating receptors of NK cells, Zhongguo Shi Yan Xue Ye Xue Za Zhi, 25, 1713 Zingoni, 2015, Genotoxic stress induces senescence-associated ADAM10-dependent release of NKG2D MIC ligands in multiple myeloma cells, J Immunol, 195, 736, 10.4049/jimmunol.1402643 Di Noto, 2016, Merging colloidal nanoplasmonics and surface plasmon resonance spectroscopy for enhanced profiling of multiple myeloma-derived exosomes, Biosens Bioelectron, 77, 518, 10.1016/j.bios.2015.09.061 Thuma, 2014, Outsmart tumor exosomes to steal the cancer initiating cell its niche, Semin Cancer Biol, 28, 39, 10.1016/j.semcancer.2014.02.011 Galli, 2018, Phase I study of the heparanase inhibitor roneparstat: an innovative approach for ultiple myeloma therapy, Haematologica, 103, e469, 10.3324/haematol.2017.182865 Rivoltini, 2016, TNF-related apoptosis-inducing ligand (trail)-armed exosomes deliver proapoptotic signals to tumor site, Clin Cancer Res, 22, 3499, 10.1158/1078-0432.CCR-15-2170 Manier, 2017, Prognostic role of circulating exosomal miRNAs in multiple myeloma, Blood, 129, 2429, 10.1182/blood-2016-09-742296 Lia, 2018, Extracellular vesicles as potential biomarkers of acute graft-vs-host disease, Leukemia, 32, 765, 10.1038/leu.2017.277 Robinson, 2018, Dis3 isoforms vary in their endoribonuclease activity and are differentially expressed within haematological cancers, Biochem J, 475, 2091, 10.1042/BCJ20170962 Palumbo, 2011, Multiple myeloma, N Engl J Med, 364, 1046, 10.1056/NEJMra1011442 Meads, 2009, Environment-mediated drug resistance: a major contributor to minimal residual disease, Nat Rev Cancer, 9, A665, 10.1038/nrc2714 Deng, 2018, Exosome-transmitted LINC00461 promotes multiple myeloma cell proliferation and suppresses apoptosis by modulating microRNA/BCL-2 expression, Cytotherapy, 21, 96, 10.1016/j.jcyt.2018.10.006 Sedlarikova, 2018, Circulating exosomal long noncoding RNA PRINS-First findings in monoclonal gammopathies, Hematol Oncol, 36, 786, 10.1002/hon.2554 Leung, 2016, Laboratory testing in monoclonal gammopathy of renal significance (MGRS), Clin Chem Lab Med, 54, 929, 10.1515/cclm-2015-0994 Moore, 2017, The emerging role of exosome and microvesicle- (EMV-) based cancer therapeutics and immunotherapy, Int J Cancer, 141, 428, 10.1002/ijc.30672 Viaud, 2009, Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: a role for NKG2D ligands and IL-15Ralpha, PLoS One, 4, 10.1371/journal.pone.0004942 Soley, 2017, MicroRNA Transfer between bone marrow adipose and multiple myeloma cells, Curr Osteoporos Rep, 15, 162, 10.1007/s11914-017-0360-5 Leaf, 2017, DCOne as an allogeneic cell-based vaccine for multiple myeloma, J Immunother, 40, 315, 10.1097/CJI.0000000000000185 Scheideler, 2008, Comparative transcriptomics of human multipotent stem cells during adipogenesis and osteoblastogenesis, BMC Genomics, 9, 340, 10.1186/1471-2164-9-340 Willis, 2017, Toward exosome-based therapeutics: isolation, heterogeneity, and fit-for-purpose potency, Front Cardiovasc Med, 4, 63, 10.3389/fcvm.2017.00063 Yamashita, 2018, Possibility of exosome-based therapeutics and challenges in production of exosomes eligible for therapeutic application, Biol Pharm Bull, 41, 835, 10.1248/bpb.b18-00133 Cai, 2009, Up-regulation of bone marrow stromal protein 2 (BST2) in breast cancer with bone metastasis, BMC Cancer, 9, 102, 10.1186/1471-2407-9-102 Harshman, 2016, Proteomic characterization of circulating extracellular vesicles identifies novel serum myeloma associated markers, J Proteomics, 136, 89, 10.1016/j.jprot.2015.12.016