Overcoming the resistance of hepatocellular carcinoma to PD-1/PD-L1 inhibitor and the resultant immunosuppression by CD38 siRNA-loaded extracellular vesicles

References

• Jee BA, Choi JH, Rhee H, Yoon S, Kwon SM, Nahm JH, Yoo JE, Jeon Y, Choi GH, Woo HG, et al. Dynamics of genomic, epigenomic, and transcriptomic aberrations during stepwise hepatocarcinogenesis. Cancer Res. 2019;79:5500–12. doi:10.1158/0008-5472.CAN-19-0991.
   PubMed Web of Science ®Google Scholar
• Villanueva A. Hepatocellular carcinoma. N Engl J Med. 2019;380:1450–1462. doi:10.1056/NEJMra1713263.
   PubMed Web of Science ®Google Scholar
• Sperber AD, Bangdiwala SI, Drossman DA, Ghoshal UC, Simren M, Tack J, Whitehead WE, Dumitrascu DL, Fang X, Fukudo S, et al. Worldwide prevalence and burden of functional gastrointestinal disorders, results of Rome Foundation Global Study. Gastroenterology. 2021;160:99–114 e113. doi:10.1053/j.gastro.2020.04.014.
   PubMed Web of Science ®Google Scholar
• Yang JD, Hainaut P, Gores GJ, Amadou A, Plymoth A, Roberts LR. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol. 2019;16:589–604. doi:10.1038/s41575-019-0186-y.
   PubMed Web of Science ®Google Scholar
• Buonaguro L, Mauriello A, Cavalluzzo B, Petrizzo A, Tagliamonte M. Immunotherapy in hepatocellular carcinoma. Ann Hepatol. 2019;18:291–297. doi:10.1016/j.aohep.2019.04.003.
   PubMed Web of Science ®Google Scholar
• Pegtel DM, Gould SJ. Exosomes. Annu Rev Biochem. 2019;88:487–514. doi:10.1146/annurev-biochem-013118-111902.
   PubMed Web of Science ®Google Scholar
• Barile L, Vassalli G. Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol Ther. 2017;174:63–78. doi:10.1016/j.pharmthera.2017.02.020.
   PubMed Web of Science ®Google Scholar
• El-Andaloussi S, Lee Y, Lakhal-Littleton S, Li J, Seow Y, Gardiner C, Alvarez-Erviti L, Sargent IL, Wood MJ. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc. 2012;7:2112–2126. doi:10.1038/nprot.2012.131.
   PubMed Web of Science ®Google Scholar
• Dwivedi S, Rendon-Huerta EP, Ortiz-Navarrete V, Montano LF. CD38 and regulation of the immune response cells in cancer. J Oncol. 2021;2021:6630295. doi:10.1155/2021/6630295.
   PubMed Web of Science ®Google Scholar
• Lam JH, HHM N, Lim CJ, Sim XN, Malavasi F, Li H, Loh JJH, Sabai K, Kim JK, Ong CCH, et al. Expression of CD38 on macrophages predicts improved prognosis in hepatocellular carcinoma. Front Immunol. 2019;10:2093. doi:10.3389/fimmu.2019.02093.
   PubMed Web of Science ®Google Scholar
• HHM N, Lee RY, Goh S, Tay ISY, Lim X, Lee B, Chew V, Li H, Tan B, Lim S, et al. Immunohistochemical scoring of CD38 in the tumor microenvironment predicts responsiveness to anti-PD-1/PD-L1 immunotherapy in hepatocellular carcinoma. J Immunother Cancer. 2020;8:e000987. doi:10.1136/jitc-2020-000987.
   PubMed Web of Science ®Google Scholar
• Gao L, Liu Y, Du X, Ma S, Ge M, Tang H, Han C, Zhao X, Liu Y, Shao Y, et al. The intrinsic role and mechanism of tumor expressed-CD38 on lung adenocarcinoma progression. Cell Death Dis. 2021;12:680. doi:10.1038/s41419-021-03968-2.
   PubMed Web of Science ®Google Scholar
• Li S, England CG, Ehlerding EB, Kutyreff CJ, Engle JW, Jiang D, Cai W. ImmunoPET imaging of CD38 expression in hepatocellular carcinoma using (64)Cu-labeled daratumumab. Am J Transl Res. 2019;11:6007–6015.
   PubMed Web of Science ®Google Scholar
• Ke M, Zhang Z, Xu B, Zhao S, Ding Y, Wu X, Wu R, Lv Y, Dong J. Baicalein and baicalin promote antitumor immunity by suppressing PD-L1 expression in hepatocellular carcinoma cells. Int Immunopharmacol. 2019;75:105824. doi:10.1016/j.intimp.2019.105824.
   PubMed Web of Science ®Google Scholar
• Pathak R, Pharaon RR, Mohanty A, Villaflor VM, Salgia R, Massarelli E. Acquired resistance to PD-1/PD-L1 blockade in lung cancer: mechanisms and patterns of failure. Cancers (Basel). 2020;12:3851. doi:10.3390/cancers12123851.
   PubMed Web of Science ®Google Scholar
• Zhou W, Zhou Y, Chen X, Ning T, Chen H, Guo Q, Zhang Y, Liu P, Zhang Y, Li C, et al. Pancreatic cancer-targeting exosomes for enhancing immunotherapy and reprogramming tumor microenvironment. Biomaterials. 2021;268:120546. doi:10.1016/j.biomaterials.2020.120546.
   PubMed Web of Science ®Google Scholar
• Zeng Y, Li B, Liang Y, Reeves PM, Qu X, Ran C, Liu Q, Callahan MV, Sluder AE, Gelfand JA, et al. Dual blockade of CXCL12-CXCR4 and PD-1-PD-L1 pathways prolongs survival of ovarian tumor-bearing mice by prevention of immunosuppression in the tumor microenvironment. FASEB J. 2019;33:6596–6608. doi:10.1096/fj.201802067RR.
   PubMed Web of Science ®Google Scholar
• Ogiya D, Liu J, Ohguchi H, Kurata K, Samur MK, Tai YT, Adamia S, Ando K, Hideshima T, Anderson KC. The JAK-STAT pathway regulates CD38 on myeloma cells in the bone marrow microenvironment: therapeutic implications. Blood. 2020;136:2334–2345. doi:10.1182/blood.2019004332.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Bi J, Huang J, Tang Y, Du S, Li P. Exosome: a review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int J Nanomedicine. 2020;15:6917–6934. doi:10.2147/IJN.S264498.
   PubMed Web of Science ®Google Scholar
• Guo S, Perets N, Betzer O, Ben-Shaul S, Sheinin A, Michaelevski I, Popovtzer R, Offen D, Levenberg S. Intranasal delivery of mesenchymal stem cell derived exosomes loaded with phosphatase and tensin homolog siRNA repairs complete spinal cord injury. ACS Nano. 2019;13:10015–10028. doi:10.1021/acsnano.9b01892.
   PubMed Web of Science ®Google Scholar
• Sek K, Molck C, Stewart GD, Kats L, Darcy PK, Beavis PA. Targeting adenosine receptor signaling in cancer immunotherapy. Int J Mol Sci. 2018;19:3837. doi:10.3390/ijms19123837.
   PubMed Web of Science ®Google Scholar
• van de Donk N. Immunomodulatory effects of CD38-targeting antibodies. Immunol Lett. 2018;199:16–22. doi:10.1016/j.imlet.2018.04.005.
   PubMed Web of Science ®Google Scholar
• Chen L, Diao L, Yang Y, Yi X, Rodriguez BL, Li Y, Villalobos PA, Cascone T, Liu X, Tan L, et al. CD38-mediated immunosuppression as a mechanism of tumor cell escape from PD-1/PD-L1 blockade. Cancer Discov. 2018;8:1156–1175. doi:10.1158/2159-8290.CD-17-1033.
   PubMed Web of Science ®Google Scholar
• Lv R, Bao Q, Li Y. Regulation of M1type and M2type macrophage polarization in RAW264.7 cells by Galectin9. Mol Med Rep. 2017;16:9111–9119. doi:10.3892/mmr.2017.7719.
   PubMed Web of Science ®Google Scholar
• Liu W, Yu M, Xie D, Wang L, Ye C, Zhu Q, Liu F, Yang L. Melatonin-stimulated MSC-derived exosomes improve diabetic wound healing through regulating macrophage M1 and M2 polarization by targeting the PTEN/AKT pathway. Stem Cell Res Ther. 2020;11:259. doi:10.1186/s13287-020-01756-x.
   PubMed Web of Science ®Google Scholar
• He G, Zhang H, Zhou J, Wang B, Chen Y, Kong Y, Xie X, Wang X, Fei R, Wei L, et al. Peritumoural neutrophils negatively regulate adaptive immunity via the PD-L1/PD-1 signalling pathway in hepatocellular carcinoma. J Exp Clin Cancer Res. 2015;34:141. doi:10.1186/s13046-015-0256-0.
   PubMed Web of Science ®Google Scholar
• Shi S, Rao Q, Zhang C, Zhang X, Qin Y, Niu Z. Dendritic cells pulsed with exosomes in combination with PD-1 antibody increase the efficacy of sorafenib in hepatocellular carcinoma model. Transl Oncol. 2018;11:250–258. doi:10.1016/j.tranon.2018.01.001.
   PubMed Web of Science ®Google Scholar
• Costa F, Marchica V, Storti P, Malavasi F, Giuliani N. PD-L1/PD-1 axis in multiple myeloma microenvironment and a possible link with CD38-mediated immune-suppression. Cancers (Basel). 2021;13:164. doi:10.3390/cancers13020164.
   PubMed Web of Science ®Google Scholar
• Mittal D, Vijayan D, Smyth MJ. Overcoming acquired PD-1/PD-L1 resistance with CD38 blockade. Cancer Discov. 2018;8:1066–1068. doi:10.1158/2159-8290.CD-18-0798.
   PubMed Web of Science ®Google Scholar