Impaired Autophagy Response in Hepatocellular Carcinomas Enriches Glypican-3 in Exosomes, Not in the Microvesicles

References

• Battistelli M, Falcieri E. Apoptotic bodies: particular extracellular vesicles involved in intercellular communication. Biology. 2020;9(1). doi:10.3390/biology9010021
   PubMed Web of Science ®Google Scholar
• van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228. doi:10.1038/nrm.2017.125
   PubMed Web of Science ®Google Scholar
• Lie PPY, Yoo L, Goulbourne CN, et al. Axonal transport of late endosomes and amphisomes is selectively modulated by local Ca(2+) efflux and disrupted by PSEN1 loss of function. Sci Adv. 2022;8(17):eabj5716. doi:10.1126/sciadv.abj5716
   PubMed Web of Science ®Google Scholar
• Mathieu M, Martin-Jaular L, Lavieu G, Théry C. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol. 2019;21(1):9–17. doi:10.1038/s41556-018-0250-9
   PubMed Web of Science ®Google Scholar
• Malhi H. Emerging role of extracellular vesicles in liver diseases. Am J Physiol Gastrointest Liver Physiol. 2019;317(5):G739–g749. doi:10.1152/ajpgi.00183.2019
   PubMed Web of Science ®Google Scholar
• Leidal AM, Debnath J. Emerging roles for the autophagy machinery in extracellular vesicle biogenesis and secretion. FASEB Bioadv. 2021;3(5):377–386. doi:10.1096/fba.2020-00138
   PubMedGoogle Scholar
• Birgisdottir ÅB, Johansen T. Autophagy and endocytosis - interconnections and interdependencies. J Cell Sci. 2020;133(10). doi:10.1242/jcs.228114
   PubMed Web of Science ®Google Scholar
• Barthet VJA, Brucoli M, Ladds M, et al. Autophagy suppresses the formation of hepatocyte-derived cancer-initiating ductular progenitor cells in the liver. Sci Adv. 2021;7(23). doi:10.1126/sciadv.abf9141
   PubMed Web of Science ®Google Scholar
• Chava S, Lee C, Aydin Y, et al. Chaperone-mediated autophagy compensates for impaired macroautophagy in the cirrhotic liver to promote hepatocellular carcinoma. Oncotarget. 2017;8(25):40019–40036. doi:10.18632/oncotarget.16685
   PubMedGoogle Scholar
• Niture S, Lin M, Rios-Colon L, Qi Q, Moore JT, Kumar D. Emerging roles of impaired autophagy in fatty liver disease and hepatocellular carcinoma. Int J Hepatol. 2021;2021:6675762. doi:10.1155/2021/6675762
   PubMed Web of Science ®Google Scholar
• Lee YA, Noon LA, Akat KM, et al. Autophagy is a gatekeeper of hepatic differentiation and carcinogenesis by controlling the degradation of Yap. Nat Commun. 2018;9(1):4962. doi:10.1038/s41467-018-07338-z
   PubMed Web of Science ®Google Scholar
• Takamura A, Komatsu M, Hara T, et al. Autophagy-deficient mice develop multiple liver tumors. Genes Dev. 2011;25(8):795–800. doi:10.1101/gad.2016211
   PubMed Web of Science ®Google Scholar
• Nakau M, Miyoshi H, Seldin MF, Imamura M, Oshima M, Taketo MM. Hepatocellular carcinoma caused by loss of heterozygosity in Lkb1 gene knockout mice. Cancer Res. 2002;62(16):4549–4553.
   PubMed Web of Science ®Google Scholar
• Qu X, Yu J, Bhagat G, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 2003;112(12):1809–1820. doi:10.1172/jci20039
   PubMed Web of Science ®Google Scholar
• Németh K, Varga Z, Lenzinger D, et al. Extracellular vesicle release and uptake by the liver under normo- and hyperlipidemia. Cell Mol Life Sci. 2021;78(23):7589–7604. doi:10.1007/s00018-021-03969-6
   PubMed Web of Science ®Google Scholar
• Momen-Heravi F, Saha B, Kodys K, Catalano D, Satishchandran A, Szabo G. Increased number of circulating exosomes and their microRNA cargos are potential novel biomarkers in alcoholic hepatitis. J Transl Med. 2015;13:261. doi:10.1186/s12967-015-0623-9
   PubMed Web of Science ®Google Scholar
• Aydin Y, Koksal AR, Reddy V, et al. Extracellular vesicle release promotes viral replication during persistent HCV infection. Cells. 2021;10(5):984. doi:10.3390/cells10050984
   PubMed Web of Science ®Google Scholar
• Xu J, Yang KC, Go NE, et al. Chloroquine treatment induces secretion of autophagy-related proteins and inclusion of Atg8-family proteins in distinct extracellular vesicle populations. Autophagy. 2022:1–14. doi:10.1080/15548627.2022.2039535
   Web of Science ®Google Scholar
• Guo M, Zhang H, Zheng J, Liu Y. Glypican-3: a new target for diagnosis and treatment of hepatocellular carcinoma. J Cancer. 2020;11(8):2008–2021. doi:10.7150/jca.39972
   PubMed Web of Science ®Google Scholar
• Bao L, Chandra PK, Moroz K, et al. Impaired autophagy response in human hepatocellular carcinoma. Exp Mol Pathol. 2014;96(2):149–154. doi:10.1016/j.yexmp.2013.12.002
   PubMed Web of Science ®Google Scholar
• Christianson HC, Belting M. Heparan sulfate proteoglycan as a cell-surface endocytosis receptor. Matrix Biol. 2014;35:51–55. doi:10.1016/j.matbio.2013.10.004
   PubMed Web of Science ®Google Scholar
• Roucourt B, Meeussen S, Bao J, Zimmermann P, David G. Heparanase activates the syndecan-syntenin-ALIX exosome pathway. Cell Res. 2015;25(4):412–428. doi:10.1038/cr.2015.29
   PubMed Web of Science ®Google Scholar
• Zarovni N, Corrado A, Guazzi P, et al. Integrated isolation and quantitative analysis of exosome shuttled proteins and nucleic acids using immunocapture approaches. Methods. 2015;87:46–58. doi:10.1016/j.ymeth.2015.05.028
   PubMed Web of Science ®Google Scholar
• Jeppesen DK, Fenix AM, Franklin JL, et al. Reassessment of Exosome Composition. Cell. 2019;177(2):428–445.e18. doi:10.1016/j.cell.2019.02.029
   PubMed Web of Science ®Google Scholar
• Lane RE, Korbie D, Trau M, Hill MM. Purification protocols for extracellular vesicles. Methods Mol Biol. 2017;1660:111–130. doi:10.1007/978-1-4939-7253-1_10
   PubMedGoogle Scholar
• Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383. doi:10.1083/jcb.201211138
   PubMed Web of Science ®Google Scholar
• Cappello F, Fais S. Extracellular vesicles in cancer pros and cons: the importance of the evidence-based medicine. Semin Cancer Biol. 2022. doi:10.1016/j.semcancer.2022.01.011
   Web of Science ®Google Scholar
• Correll VL, Otto JJ, Risi CM, et al. Optimization of small extracellular vesicle isolation from expressed prostatic secretions in urine for in-depth proteomic analysis. J Extracell Vesicles. 2022;11(2):e12184. doi:10.1002/jev2.12184
   PubMed Web of Science ®Google Scholar
• Davies RT, Kim J, Jang SC, Choi EJ, Gho YS, Park J. Microfluidic filtration system to isolate extracellular vesicles from blood. Lab Chip. 2012;12(24):5202–5210. doi:10.1039/c2lc41006k
   PubMed Web of Science ®Google Scholar
• El-Shennawy L, Hoffmann AD, Dashzeveg NK, et al. Circulating ACE2-expressing extracellular vesicles block broad strains of SARS-CoV-2. Nat Commun. 2022;13(1):405. doi:10.1038/s41467-021-27893-2
   PubMed Web of Science ®Google Scholar
• Jiao Y, Xu P, Shi H, Chen D, Shi H. Advances on liver cell-derived exosomes in liver diseases. J Cell Mol Med. 2021;25(1):15–26. doi:10.1111/jcmm.16123
   PubMed Web of Science ®Google Scholar
• Kanwar SS, Dunlay CJ, Simeone DM, Nagrath S. Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip. 2014;14(11):1891–1900. doi:10.1039/c4lc00136b
   PubMed Web of Science ®Google Scholar
• Aydin Y, Koksal AR, Thevenot P, et al. Experimental validation of novel glypican 3 exosomes for the detection of hepatocellular carcinoma in liver cirrhosis. J Hepatocell Carcinoma. 2021;8:1579–1596. doi:10.2147/jhc.S327339
   PubMed Web of Science ®Google Scholar
• Dalli J, Norling LV, Renshaw D, Cooper D, Leung KY, Perretti M. Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood. 2008;112(6):2512–2519. doi:10.1182/blood-2008-02-140533
   PubMed Web of Science ®Google Scholar
• Dalli J, Serhan CN. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood. 2012;120(15):e60–72. doi:10.1182/blood-2012-04-423525
   PubMed Web of Science ®Google Scholar
• Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA. 2016;113(8):E968–77. doi:10.1073/pnas.1521230113
   PubMed Web of Science ®Google Scholar
• Livshits MA, Khomyakova E, Evtushenko EG, et al. Isolation of exosomes by differential centrifugation: theoretical analysis of a commonly used protocol. Sci Rep. 2015;5:17319. doi:10.1038/srep17319
   PubMed Web of Science ®Google Scholar
• Wang Z, Hj W, Fine D, et al. Ciliated micropillars for the microfluidic-based isolation of nanoscale lipid vesicles. Lab Chip. 2013;13(15):2879–2882. doi:10.1039/c3lc41343h
   PubMed Web of Science ®Google Scholar
• Wunsch BH, Smith JT, Gifford SM, et al. Nanoscale lateral displacement arrays for the separation of exosomes and colloids down to 20 nm. Nat Nanotechnol. 2016;11(11):936–940. doi:10.1038/nnano.2016.134
   PubMed Web of Science ®Google Scholar
• Yang F, Liao X, Tian Y, Li G. Exosome separation using microfluidic systems: size-based, immunoaffinity-based and dynamic methodologies. Biotechnol J. 2017;12(4). doi:10.1002/biot.201600699
   Web of Science ®Google Scholar
• Zhao Z, Yang Y, Zeng Y, He M. A microfluidic ExoSearch chip for multiplexed exosome detection towards blood-based ovarian cancer diagnosis. Lab Chip. 2016;16(3):489–496. doi:10.1039/c5lc01117e
   PubMed Web of Science ®Google Scholar
• Berg Luecke L, Gundry RL. Assessment of streptavidin bead binding capacity to improve quality of streptavidin-based enrichment studies. J Proteome Res. 2021;20(2):1153–1164. doi:10.1021/acs.jproteome.0c00772
   PubMed Web of Science ®Google Scholar
• Campos-Silva C, Suárez H, Jara-Acevedo R, et al. High sensitivity detection of extracellular vesicles immune-captured from urine by conventional flow cytometry. Sci Rep. 2019;9(1):2042. doi:10.1038/s41598-019-38516-8
   PubMedGoogle Scholar
• Kawakami K, Fujita Y, Kato T, et al. Diagnostic potential of serum extracellular vesicles expressing prostate-specific membrane antigen in urologic malignancies. Sci Rep. 2021;11(1):15000. doi:10.1038/s41598-021-94603-9
   PubMed Web of Science ®Google Scholar
• Nakai W, Yoshida T, Diez D, et al. A novel affinity-based method for the isolation of highly purified extracellular vesicles. Sci Rep. 2016;6:33935. doi:10.1038/srep33935
   PubMed Web of Science ®Google Scholar
• Sun N, Lee YT, Zhang RY, et al. Purification of HCC-specific extracellular vesicles on nanosubstrates for early HCC detection by digital scoring. Nat Commun. 2020;11(1):4489. doi:10.1038/s41467-020-18311-0
   PubMed Web of Science ®Google Scholar
• Balaraju AK, Hu B, Rodriguez JJ, Murry M, Glypican LF. 4 regulates planar cell polarity of endoderm cells by controlling the localization of Cadherin 2. Development. 2021;148(14). doi:10.1242/dev.199421
   PubMed Web of Science ®Google Scholar
• Kolluri A, Ho M. The role of glypican-3 in regulating Wnt, YAP, and hedgehog in liver cancer. Front Oncol. 2019;9:708. doi:10.3389/fonc.2019.00708
   PubMed Web of Science ®Google Scholar
• Norman M, Vuilleumier R, Springhorn A, Gawlik J, Pyrowolakis G. Pentagone internalises glypicans to fine-tune multiple signalling pathways. Elife. 2016;5. doi:10.7554/eLife.13301
   Web of Science ®Google Scholar
• Zhou F, Shang W, Yu X, Tian J. Glypican-3: a promising biomarker for hepatocellular carcinoma diagnosis and treatment. Med Res Rev. 2018;38(2):741–767. doi:10.1002/med.21455
   PubMed Web of Science ®Google Scholar
• Qiao D, Yang X, Meyer K, Friedl A. Glypican-1 regulates anaphase promoting complex/cyclosome substrates and cell cycle progression in endothelial cells. Mol Biol Cell. 2008;19(7):2789–2801. doi:10.1091/mbc.e07-10-1025
   PubMed Web of Science ®Google Scholar
• Capurro MI, Shi W, Filmus J. LRP1 mediates Hedgehog-induced endocytosis of the GPC3-Hedgehog complex. J Cell Sci. 2012;125:3380. doi:10.1242/jcs.098889
   PubMed Web of Science ®Google Scholar
• Filmus J. The function of glypicans in the mammalian embryo. Am J Physiol Cell Physiol. 2022;322(4):C694–c698. doi:10.1152/ajpcell.00045.2022
   PubMed Web of Science ®Google Scholar
• Aydin Y, Stephens CM, Chava S, et al. Chaperone-mediated autophagy promotes beclin1 degradation in persistently infected hepatitis C virus cell culture. Am J Pathol. 2018;188(10):2339–2355. doi:10.1016/j.ajpath.2018.06.022
   PubMed Web of Science ®Google Scholar
• Leone P, Solimando AG, Fasano R, et al. The evolving role of immune checkpoint inhibitors in hepatocellular carcinoma treatment. Vaccines. 2021;9(5). doi:10.3390/vaccines9050532
   Web of Science ®Google Scholar
• Ribatti D, Solimando AG, Pezzella F. The anti-VEGF(R) drug discovery legacy: improving attrition rates by breaking the vicious cycle of angiogenesis in cancer. Cancers. 2021;13(14):3433. doi:10.3390/cancers13143433
   PubMed Web of Science ®Google Scholar
• Solimando AG, Susca N, Argentiero A, et al. Second-line treatments for advanced hepatocellular carcinoma: a systematic review and bayesian network meta-analysis. Clin Exp Med. 2022;22(1):65–74. doi:10.1007/s10238-021-00727-7
   PubMed Web of Science ®Google Scholar