Autophagy and Extracellular Vesicles in Colorectal Cancer: Interactions and Common Actors?
Abstract
:Simple Summary
Abstract
1. Introduction
2. Macroautophagy
2.1. Introducing the Process and Its Main Actors
2.2. Autophagy’s Double-Faceted Role in Carcinogenesis
2.3. Secretory Autophagy and Its Potential Link with Vesicular Trafficking and Secretion
3. Extracellular Vesicles
3.1. EVs Biogenesis and Secretion Mechanisms
3.2. Implications in Cancer Development: Increasing Interest in This Field
4. Autophagy and EVs Trafficking Cooperation: Which Actors
4.1. Common Proteins and Pathways
4.2. An Important Common Organelle: The Versatile and Misunderstood Amphisome
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Klionsky, D.J. Autophagy as a Regulated Pathway of Cellular Degradation. Science 2000, 290, 1717–1721. [Google Scholar] [CrossRef]
- Kroemer, G.; Mariño, G.; Levine, B. Autophagy and the Integrated Stress Response. Mol. Cell 2010, 40, 280–293. [Google Scholar] [CrossRef] [Green Version]
- Ravanan, P.; Srikumar, I.F.; Talwar, P. Autophagy: The spotlight for cellular stress responses. Life Sci. 2017, 188, 53–67. [Google Scholar] [CrossRef]
- Galluzzi, L.; Pietrocola, F.; Pedro, J.M.B.-S.; Amaravadi, R.K.; Baehrecke, E.H.; Cecconi, F.; Codogno, P.; Debnath, J.; Gewirtz, D.A.; Karantza, V.; et al. Autophagy in malignant transformation and cancer progression. EMBO J. 2015, 34, 856–880. [Google Scholar] [CrossRef] [PubMed]
- Mowers, E.E.; Sharifi, M.N.; MacLeod, K.F. Functions of autophagy in the tumor microenvironment and cancer metastasis. FEBS J. 2018, 285, 1751–1766. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kenific, C.M.; Thorburn, A.; Debnath, J. Autophagy and metastasis: Another double-edged sword. Curr. Opin. Cell Biol. 2010, 22, 241–245. [Google Scholar] [CrossRef] [Green Version]
- Mowers, E.; Sharifi, M.N.; MacLeod, K.F. Autophagy in cancer metastasis. Oncogene 2017, 36, 1619–1630. [Google Scholar] [CrossRef]
- Yun, C.W.; Lee, S.H. The Roles of Autophagy in Cancer. Int. J. Mol. Sci. 2018, 19, 3466. [Google Scholar] [CrossRef] [Green Version]
- Mazouffre, C.; Geyl, S.; Perraud, A.; Blondy, S.; Jauberteau, M.-O.; Mathonnet, M.; Verdier, M. Dual inhibition of BDNF/TrkB and autophagy: A promising therapeutic approach for colorectal cancer. J. Cell. Mol. Med. 2017, 21, 2610–2622. [Google Scholar] [CrossRef]
- Mokarram, P.; Albokashy, M.; Zarghooni, M.; Moosavi, M.A.; Sepehri, Z.; Chen, Q.M.; Hudecki, A.; Sargazi, A.; Alizadeh, J.; Moghadam, A.R.; et al. New frontiers in the treatment of colorectal cancer: Autophagy and the unfolded protein response as promising targets. Autophagy 2017, 13, 781–819. [Google Scholar] [CrossRef]
- Koustas, E.; Sarantis, P.; Kyriakopoulou, G.; Papavassiliou, A.G.; Karamouzis, M.V. The Interplay of Autophagy and Tumor Microenvironment in Colorectal Cancer—Ways of Enhancing Immunotherapy Action. Cancers 2019, 11, 533. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.-D.; Fang, Y.-T.; Cheng, Y.-L.; Lin, C.-F.; Hsu, L.-J.; Wang, S.-Y.; Anderson, R.; Chang, C.-P.; Lin, Y.-S. Exophagy of annexin A2 via RAB11, RAB8A and RAB27A in IFN-γ-stimulated lung epithelial cells. Sci. Rep. 2017, 7, 1–13. [Google Scholar] [CrossRef]
- Xu, J.; Camfield, R.; Gorski, S.M. The interplay between exosomes and autophagy—Partners in crime. J. Cell Sci. 2018, 131, jcs215210. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gudbergsson, J.M.; Johnsen, K.B. Exosomes and autophagy: Rekindling the vesicular waste hypothesis. J. Cell Commun. Signal. 2019, 13, 443–450. [Google Scholar] [CrossRef] [PubMed]
- Théry, C. Exosomes: Secreted vesicles and intercellular communications. F1000 Biol. Rep. 2011, 3, 15. [Google Scholar] [CrossRef]
- Record, M.; Carayon, K.; Poirot, M.; Silvente-Poirot, S. Exosomes as new vesicular lipid transporters involved in cell–cell communication and various pathophysiologies. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2014, 1841, 108–120. [Google Scholar] [CrossRef] [PubMed]
- Tkach, M.; Théry, C. Communication by Extracellular Vesicles: Where We Are and Where We Need to Go. Cell 2016, 164, 1226–1232. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- György, B.; Szabó, T.G.; Pásztói, M.; Pál, Z.; Misják, P.; Aradi, B.; László, V.; Pállinger, É.; Pap, E.; Kittel, Á.; et al. Membrane vesicles, current state-of-the-art: Emerging role of extracellular vesicles. Cell. Mol. Life Sci. 2011, 68, 2667–2688. [Google Scholar] [CrossRef] [Green Version]
- Raposo, G.; Stoorvogel, W. Extracellular vesicles: Exosomes, microvesicles, and friends. J. Cell Biol. 2013, 200, 373–383. [Google Scholar] [CrossRef] [Green Version]
- Huotari, J.; Helenius, A. Endosome maturation. EMBO J. 2011, 30, 3481–3500. [Google Scholar] [CrossRef]
- Hurley, J.H. ESCRTs are everywhere. EMBO J. 2015, 34, 2398–2407. [Google Scholar] [CrossRef] [Green Version]
- Raiborg, C.; Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009, 458, 445–452. [Google Scholar] [CrossRef]
- Babst, M. MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr. Opin. Cell Biol. 2011, 23, 452–457. [Google Scholar] [CrossRef] [Green Version]
- Henne, W.M.; Buchkovich, N.J.; Emr, S.D. The ESCRT Pathway. Dev. Cell 2011, 21, 77–91. [Google Scholar] [CrossRef] [Green Version]
- Henne, W.M.; Stenmark, H.; Emr, S.D. Molecular Mechanisms of the Membrane Sculpting ESCRT Pathway. Cold Spring Harb. Perspect. Biol. 2013, 5, a016766. [Google Scholar] [CrossRef] [Green Version]
- Colombo, M.; Moita, C.; Van Niel, G.; Kowal, J.; Vigneron, J.; Benaroch, P.; Manel, N.; Moita, L.F.; Théry, C.; Raposo, G. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci. 2013, 126, 5553–5565. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.; Chen, R.; Kemper, S.; Brigstock, D.R. Pathways of production and delivery of hepatocyte exosomes. J. Cell Commun. Signal. 2017, 12, 343–357. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hessvik, N.P.; Llorente, A. Current knowledge on exosome biogenesis and release. Cell. Mol. Life Sci. 2018, 75, 193–208. [Google Scholar] [CrossRef] [Green Version]
- Ostrowski, M.; Carmo, N.B.; Krumeich, S.; Fanget, I.; Raposo, G.; Savina, A.; Moita, C.F.; Schauer, K.; Hume, A.N.; Freitas, R.P.; et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 2009, 12, 19–30. [Google Scholar] [CrossRef] [Green Version]
- Blanc, L.; Vidal, M. New insights into the function of Rab GTPases in the context of exosomal secretion. Small GTPases 2018, 9, 95–106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baietti, M.F.; Zhang, Z.; Mortier, E.; Melchior, A.; DeGeest, G.; Geeraerts, A.; Ivarsson, Y.; Depoortere, F.; Coomans, C.; Vermeiren, E.; et al. Syndecan–syntenin–ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 2012, 14, 677–685. [Google Scholar] [CrossRef] [PubMed]
- Savina, A.; Fader, C.M.; Damiani, M.T.; Colombo, M.I. Rab11 Promotes Docking and Fusion of Multivesicular Bodies in a Calcium-Dependent Manner. Traffic 2004, 6, 131–143. [Google Scholar] [CrossRef]
- Kowal, J.; Tkach, M.; Théry, C. Biogenesis and secretion of exosomes. Curr. Opin. Cell Biol. 2014, 29, 116–125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fader, C.M.; Sánchez, D.G.; Mestre, M.B.; Colombo, M.I. TI-VAMP/VAMP7 and VAMP3/cellubrevin: Two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta Bioenergy 2009, 1793, 1901–1916. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gross, J.C.; Chaudhary, V.; Bartscherer, K.; Boutros, M. Active Wnt proteins are secreted on exosomes. Nat. Cell Biol. 2012, 14, 1036–1045. [Google Scholar] [CrossRef] [PubMed]
- Tauro, B.J.; Mathias, R.A.; Greening, D.W.; Gopal, S.K.; Ji, H.; Kapp, E.A.; Coleman, B.M.; Hill, A.F.; Kusebauch, U.; Hallows, J.L.; et al. Oncogenic H-Ras Reprograms Madin-Darby Canine Kidney (MDCK) Cell-derived Exosomal Proteins Following Epithelial-Mesenchymal Transition. Mol. Cell. Proteom. 2013, 12, 2148–2159. [Google Scholar] [CrossRef] [Green Version]
- Sung, B.H.; Ketova, T.; Hoshino, D.; Zijlstra, A.; Weaver, A.M. Directional cell movement through tissues is controlled by exosome secretion. Nat. Commun. 2015, 6, 7164. [Google Scholar] [CrossRef] [Green Version]
- Becker, A.; Thakur, B.K.; Weiss, J.M.; Kim, H.S.; Peinado, H.; Lyden, D. Extracellular Vesicles in Cancer: Cell-to-Cell Mediators of Metastasis. Cancer Cell 2016, 30, 836–848. [Google Scholar] [CrossRef] [Green Version]
- Beckler, M.D.; Higginbotham, J.N.; Franklin, J.L.; Ham, A.-J.; Halvey, P.J.; Imasuen, I.E.; Whitwell, C.; Li, M.; Liebler, D.C.; Coffey, R.J. Proteomic Analysis of Exosomes from Mutant KRAS Colon Cancer Cells Identifies Intercellular Transfer of Mutant KRAS. Mol. Cell. Proteom. 2013, 12, 343–355. [Google Scholar] [CrossRef] [Green Version]
- Szvicsek, Z.; Oszvald, Á.; Szabó, L.; Sándor, G.O.; Kelemen, A.; Soós, A.Á.; Pálóczi, K.; Harsányi, L.; Tölgyes, T.; DeDe, K.; et al. Extracellular vesicle release from intestinal organoids is modulated by Apc mutation and other colorectal cancer progression factors. Cell. Mol. Life Sci. 2019, 76, 2463–2476. [Google Scholar] [CrossRef] [Green Version]
- Lugini, L.; Valtieri, M.; Federici, C.; Cecchetti, S.; Meschini, S.; Condello, M.; Signore, M.; Fais, S. Exosomes from human colorectal cancer induce a tumor-like behavior in colonic mesenchymal stromal cells. Oncotarget 2016, 7, 50086–50098. [Google Scholar] [CrossRef] [Green Version]
- Lucchetti, D.; Calapà, F.; Palmieri, V.; Fanali, C.; Carbone, F.; Papa, A.; De Maria, R.; De Spirito, M.; Sgambato, A. Differentiation Affects the Release of Exosomes from Colon Cancer Cells and Their Ability to Modulate the Behavior of Recipient Cells. Am. J. Pathol. 2017, 187, 1633–1647. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mizushima, N. Autophagy: Process and function. Genes Dev. 2007, 21, 2861–2873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mizushima, N.; Yoshimori, T.; Ohsumi, Y. The Role of Atg Proteins in Autophagosome Formation. Annu. Rev. Cell Dev. Biol. 2011, 27, 107–132. [Google Scholar] [CrossRef] [PubMed]
- Tanida, I.; Ueno, T.; Kominami, E. LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 2004, 36, 2503–2518. [Google Scholar] [CrossRef] [PubMed]
- Fujita, N.; Hayashi-Nishino, M.; Fukumoto, H.; Omori, H.; Yamamoto, A.; Noda, T.; Yoshimori, T. An Atg4B Mutant Hampers the Lipidation of LC3 Paralogues and Causes Defects in Autophagosome Closure. Mol. Biol. Cell 2008, 19, 4651–4659. [Google Scholar] [CrossRef] [Green Version]
- Weidberg, H.; Shvets, E.; Elazar, Z. Biogenesis and Cargo Selectivity of Autophagosomes. Annu. Rev. Biochem. 2011, 80, 125–156. [Google Scholar] [CrossRef]
- Itakura, E.; Kishi-Itakura, C.; Mizushima, N. The Hairpin-type Tail-Anchored SNARE Syntaxin 17 Targets to Autophagosomes for Fusion with Endosomes/Lysosomes. Cell 2012, 151, 1256–1269. [Google Scholar] [CrossRef] [Green Version]
- Huang, T.; Song, X.; Yang, Y.; Wan, X.; Alvarez, A.A.; Sastry, N.; Feng, H.; Hu, B.; Cheng, S.-Y. Autophagy and Hallmarks of Cancer. Crit. Rev. Oncog. 2018, 23, 247–267. [Google Scholar] [CrossRef]
- Alers, S.; Löffler, A.S.; Wesselborg, S.; Stork, B. Role of AMPK-mTOR-Ulk1/2 in the Regulation of Autophagy: Cross Talk, Shortcuts, and Feedbacks. Mol. Cell. Biol. 2011, 32, 2–11. [Google Scholar] [CrossRef] [Green Version]
- Torii, S.; Yoshida, T.; Arakawa, S.; Honda, S.; Nakanishi, A.; Shimizu, S. Identification of PPM1D as an essential Ulk1 phosphatase for genotoxic stress-induced autophagy. EMBO Rep. 2016, 17, 1552–1564. [Google Scholar] [CrossRef] [PubMed]
- Mathew, R.; Kongara, S.; Beaudoin, B.; Karp, C.M.; Bray, K.; Degenhardt, K.; Chen, G.; Jin, S.; White, E. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 2007, 21, 1367–1381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levine, B.; Kroemer, G. Autophagy in the Pathogenesis of Disease. Cell 2008, 132, 27–42. [Google Scholar] [CrossRef] [Green Version]
- Singh, S.S.; Vats, S.; Chia, A.Y.-Q.; Tan, T.Z.; Deng, S.; Ong, M.S.; Arfuso, F.; Yap, C.T.; Goh, B.C.; Sethi, G.; et al. Dual role of autophagy in hallmarks of cancer. Oncogene 2018, 37, 1142–1158. [Google Scholar] [CrossRef]
- Mathew, R.; Karantza-Wadsworth, V.; White, E. Role of autophagy in cancer. Nat. Rev. Cancer 2007, 7, 961–967. [Google Scholar] [CrossRef]
- Gong, C.; Bauvy, C.; Tonelli, G.; Yue, W.; Delomenie, C.; Nicolas, V.; Zhu, Y.; Domergue, V.; Marinesteban, V.; Tharinger, H.; et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene 2012, 32, 2261–2272. [Google Scholar] [CrossRef]
- Wolf, J.; Dewi, D.L.; Fredebohm, J.; Müller-Decker, K.; Flechtenmacher, C.; Hoheisel, J.D.; Boettcher, M. A mammosphere formation RNAi screen reveals that ATG4A promotes a breast cancer stem-like phenotype. Breast Cancer Res. 2013, 15, R109. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Yang, B.; Zhou, Q.; Wu, Y.; Shang, D.; Guo, Y.; Song, Z.; Zheng, Q.; Xiong, J. Autophagy promotes hepatocellular carcinoma cell invasion through activation of epithelial–mesenchymal transition. Carcinogenesis 2013, 34, 1343–1351. [Google Scholar] [CrossRef] [Green Version]
- Chiarugi, P.; Giannoni, E. Anoikis: A necessary death program for anchorage-dependent cells. Biochem. Pharmacol. 2008, 76, 1352–1364. [Google Scholar] [CrossRef]
- Fung, C.; Lock, R.; Gao, S.; Salas, E.; Debnath, J. Induction of Autophagy during Extracellular Matrix Detachment Promotes Cell Survival. Mol. Biol. Cell 2008, 19, 797–806. [Google Scholar] [CrossRef] [Green Version]
- Hu, Y.-L.; DeLay, M.; Jahangiri, A.; Molinaro, A.M.; Rose, S.D.; Carbonell, W.S.; Aghi, M.K. Hypoxia-Induced Autophagy Promotes Tumor Cell Survival and Adaptation to Antiangiogenic Treatment in Glioblastoma. Cancer Res. 2012, 72, 1773–1783. [Google Scholar] [CrossRef] [Green Version]
- White, E.; Mehnert, J.M.; Chan, C.S. Autophagy, Metabolism, and Cancer. Clin. Cancer Res. 2015, 21, 5037–5046. [Google Scholar] [CrossRef] [Green Version]
- Levy, J.M.M.; Towers, C.G.; Thorburn, A. Targeting autophagy in cancer. Nat. Rev. Cancer 2017, 17, 528–542. [Google Scholar] [CrossRef]
- Onorati, A.V.; Dyczynski, M.; Ojha, R.; Amaravadi, R.K. Targeting autophagy in cancer. Cancer 2018, 124, 3307–3318. [Google Scholar] [CrossRef] [Green Version]
- Devenport, S.N.; Shah, Y.M. Functions and Implications of Autophagy in Colon Cancer. Cells 2019, 8, 1349. [Google Scholar] [CrossRef] [Green Version]
- Seiwert, N.; Neitzel, C.; Stroh, S.; Frisan, T.; Audebert, M.; Toulany, M.; Kaina, B.; Fahrer, J. AKT2 suppresses pro-survival autophagy triggered by DNA double-strand breaks in colorectal cancer cells. Cell Death Dis. 2017, 8, e3019. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, X.; Xu, X.; Zhu, J.; Zhang, S.; Wu, Y.; Wu, Y.; Zhao, K.; Xing, C.; Cao, J.; Zhu, H.; et al. miR-31 affects colorectal cancer cells by inhibiting autophagy in cancer-associated fibroblasts. Oncotarget 2016, 7, 79617–79628. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sasaki, K.; Tsuno, N.H.; Sunami, E.; Tsurita, G.; Kawai, K.; Okaji, Y.; Nishikawa, T.; Shuno, Y.; Hongo, K.; Hiyoshi, M.; et al. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer 2010, 10, 370. [Google Scholar] [CrossRef] [Green Version]
- Lauzier, A.; Normandeau-Guimond, J.; Vaillancourt-Lavigueur, V.; Boivin, V.; Charbonneau, M.; Rivard, N.; Scott, M.S.; Dubois, C.M.; Jean, S. Colorectal cancer cells respond differentially to autophagy inhibition in vivo. Sci. Rep. 2019, 9, 11316. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ponpuak, M.; Mandell, M.A.; Kimura, T.; Chauhan, S.; Cleyrat, C.; Deretic, V. Secretory autophagy. Curr. Opin. Cell Biol. 2015, 35, 106–116. [Google Scholar] [CrossRef] [Green Version]
- Dupont, N.; Jiang, S.; Pilli, M.; Ornatowski, W.; Bhattacharya, D.; Deretic, V. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β. EMBO J. 2011, 30, 4701–4711. [Google Scholar] [CrossRef] [Green Version]
- Migneault, F.; Hébert, M.-J. Autophagy, tissue repair, and fibrosis: A delicate balance. Matrix Biol. 2021. [Google Scholar] [CrossRef]
- Bel, S.; Pendse, M.; Wang, Y.; Li, Y.; Ruhn, K.A.; Hassell, B.; Leal, T.; Winter, S.E.; Xavier, R.J.; Hooper, L.V. Paneth cells secrete lysozyme via secretory autophagy during bacterial infection of the intestine. Science 2017, 357, 1047–1052. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Son, S.M.; Cha, M.-Y.; Choi, H.; Kang, S.; Choi, H.; Lee, M.-S.; Park, S.A.; Mook-Jung, I. Insulin-degrading enzyme secretion from astrocytes is mediated by an autophagy-based unconventional secretory pathway in Alzheimer disease. Autophagy 2016, 12, 784–800. [Google Scholar] [CrossRef] [Green Version]
- Nilsson, P.; Loganathan, K.; Sekiguchi, M.; Matsuba, Y.; Hui, K.; Tsubuki, S.; Tanaka, M.; Iwata, N.; Saito, T.; Saido, T.C. Aβ Secretion and Plaque Formation Depend on Autophagy. Cell Rep. 2013, 5, 61–69. [Google Scholar] [CrossRef] [Green Version]
- Ejlerskov, P.; Rasmussen, I.; Nielsen, T.T.; Bergström, A.-L.; Tohyama, Y.; Jensen, P.H.; Vilhardt, F. Tubulin Polymerization-promoting Protein (TPPP/p25α) Promotes Unconventional Secretion of α-Synuclein through Exophagy by Impairing Autophagosome-Lysosome Fusion. J. Biol. Chem. 2013, 288, 17313–17335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ao, X.; Zou, L.; Wu, Y. Regulation of autophagy by the Rab GTPase network. Cell Death Differ. 2014, 21, 348–358. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kimura, T.; Jia, J.; Kumar, S.; Choi, S.W.; Gu, Y.; Mudd, M.; Dupont, N.; Jiang, S.; Peters, R.; Farzam, F.; et al. Dedicated SNARE s and specialized TRIM cargo receptors mediate secretory autophagy. EMBO J. 2017, 36, 42–60. [Google Scholar] [CrossRef]
- Villarroya-Beltri, C.; Baixauli, F.; Mittelbrunn, M.; Delgado, I.F.; Torralba, D.; Moreno-Gonzalo, O.; Baldanta, S.; Enrich, C.; Guerra, S.; Sánchez-Madrid, F. ISGylation controls exosome secretion by promoting lysosomal degradation of MVB proteins. Nat. Commun. 2016, 7, 13588. [Google Scholar] [CrossRef] [Green Version]
- Levine, B.; Kroemer, G. Biological Functions of Autophagy Genes: A Disease Perspective. Cell 2019, 176, 11–42. [Google Scholar] [CrossRef] [Green Version]
- Trajkovic, K.; Hsu, C.; Chiantia, S.; Rajendran, L.; Wenzel, D.; Wieland, F.; Schwille, P.; Brügger, B.; Simons, M. Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes. Science 2008, 319, 1244–1247. [Google Scholar] [CrossRef]
- Stuffers, S.; Wegner, C.S.; Stenmark, H.; Brech, A. Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic 2009, 10, 925–937. [Google Scholar] [CrossRef] [PubMed]
- Perez-Hernandez, D.; Gutiérrez-Vázquez, C.; Jorge, I.; López-Martín, S.; Ursa, A.; Sánchez-Madrid, F.; Vázquez, J.; Yáñez-Mó, M. The Intracellular Interactome of Tetraspanin-enriched Microdomains Reveals Their Function as Sorting Machineries toward Exosomes. J. Biol. Chem. 2013, 288, 11649–11661. [Google Scholar] [CrossRef] [Green Version]
- Uytterhoeven, V.; Lauwers, E.; Maes, I.; Miskiewicz, K.; Melo, M.N.; Swerts, J.; Kuenen, S.; Wittocx, R.; Corthout, N.; Marrink, S.-J.; et al. Hsc70-4 Deforms Membranes to Promote Synaptic Protein Turnover by Endosomal Microautophagy. Neuron 2015, 88, 735–748. [Google Scholar] [CrossRef] [Green Version]
- Colombo, M.; Raposo, G.; Théry, C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 2014, 30, 255–289. [Google Scholar] [CrossRef] [PubMed]
- Quaglia, M.; Dellepiane, S.; Guglielmetti, G.; Merlotti, G.; Castellano, G.; Cantaluppi, V. Extracellular Vesicles as Mediators of Cellular Crosstalk Between Immune System and Kidney Graft. Front. Immunol. 2020, 11, 74. [Google Scholar] [CrossRef] [PubMed]
- Lindoso, R.S.; Collino, F.; Vieyra, A. Extracellular vesicles as regulators of tumor fate: Crosstalk among cancer stem cells, tumor cells and mesenchymal stem cells. Stem Cell Investig. 2017, 4, 75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Al-Nedawi, K.; Meehan, B.; Micallef, J.; Lhotak, V.; May, L.; Guha, A.; Rak, J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10, 619–624. [Google Scholar] [CrossRef]
- Pinet, S.; Bessette, B.; Vedrenne, N.; Lacroix, A.; Richard, L.; Jauberteau, M.-O.; Battu, S.; Lalloué, F. TrkB-containing exosomes promote the transfer of glioblastoma aggressiveness to YKL-40-inactivated glioblastoma cells. Oncotarget 2016, 7, 50349–50364. [Google Scholar] [CrossRef] [Green Version]
- Skog, J.; Würdinger, T.; Van Rijn, S.; Meijer, D.H.; Gainche, L.; Curry, W.T.J.; Carter, B.S.; Krichevsky, A.M.; Breakefield, X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10, 1470–1476. [Google Scholar] [CrossRef]
- Webber, J.; Steadman, R.; Mason, M.D.; Tabi, Z.; Clayton, A. Cancer Exosomes Trigger Fibroblast to Myofibroblast Differentiation. Cancer Res. 2010, 70, 9621–9630. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, K.W.; Cho, J.A.; Park, H.; Lim, E.H. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int. J. Oncol. 2011, 40, 130–138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Webber, J.; Spary, L.K.; Sanders, A.J.; Chowdhury, R.; Jiang, W.G.; Steadman, R.; Wymant, J.M.; Jones, A.T.; Kynaston, H.G.; Mason, M.D.; et al. Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes. Oncogene 2015, 34, 290–302. [Google Scholar] [CrossRef]
- Wilson, C.M.; Naves, T.; Vincent, F.; Melloni, B.; Bonnaud, F.; Lalloué, F.; Jauberteau, M.-O. Sortilin mediates the release and transfer of exosomes in concert with two tyrosine kinase receptors. J. Cell Sci. 2014, 127, 3983–3997. [Google Scholar] [CrossRef] [Green Version]
- Steinbichler, T.B.; Dudás, J.; Skvortsov, S.; Ganswindt, U.; Riechelmann, H.; Skvortsova, I.-I. Therapy resistance mediated by exosomes. Mol. Cancer 2019, 18, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Leidal, A.M.; Huang, H.H.; Marsh, T.; Solvik, T.; Zhang, D.; Ye, J.; Kai, F.; Goldsmith, J.; Liu, J.Y.; Huang, Y.-H.; et al. The LC3-conjugation machinery specifies the loading of RNA-binding proteins into extracellular vesicles. Nat. Cell Biol. 2020, 22, 187–199. [Google Scholar] [CrossRef]
- Guo, H.; Chitiprolu, M.; Roncevic, L.; Javalet, C.; Hemming, F.J.; Trung, M.T.; Meng, L.; Latreille, E.; De Souza, C.T.; McCulloch, D.; et al. Atg5 Disassociates the V1V0-ATPase to Promote Exosome Production and Tumor Metastasis Independent of Canonical Macroautophagy. Dev. Cell 2017, 43, 716–730. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guo, H.; Sadoul, R.; Gibbings, D. Autophagy-independent effects of autophagy-related-5 (Atg5) on exosome production and metastasis. Mol. Cell. Oncol. 2018, 5, e1445941. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bader, C.A.; Shandala, T.; Ng, Y.S.; Johnson, I.R.D.; Brooks, D.A. Atg9 is required for intraluminal vesicles in amphisomes and autolysosomes. Biol. Open 2015, 4, 1345–1355. [Google Scholar] [CrossRef] [Green Version]
- Murrow, L.; Malhotra, R.; Debnath, J. ATG12–ATG3 interacts with Alix to promote basal autophagic flux and late endosome function. Nat. Cell Biol. 2015, 17, 300–310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Zhang, Y.; Liu, A.; Wang, J.; Li, L.; Chen, X.; Gao, X.; Xue, Y.; Zhang, X.; Liu, Y. Distinct Dasatinib-Induced Mechanisms of Apoptotic Response and Exosome Release in Imatinib-Resistant Human Chronic Myeloid Leukemia Cells. Int. J. Mol. Sci. 2016, 17, 531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galluzzi, L.; Baehrecke, E.H.; Ballabio, A.; Boya, P.; Pedro, J.M.B.-S.; Cecconi, F.; Choi, A.M.; Chu, C.T.; Codogno, P.; Colombo, M.I.; et al. Molecular definitions of autophagy and related processes. EMBO J. 2017, 36, 1811–1836. [Google Scholar] [CrossRef] [PubMed]
- Adnan, M.; Islam, W.; Zhang, J.; Zheng, W.; Lu, G.-D. Diverse Role of SNARE Protein Sec22 in Vesicle Trafficking, Membrane Fusion, and Autophagy. Cells 2019, 8, 337. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fader, C.M.; Sánchez, D.; Furlán, M.; Colombo, M.I. Induction of Autophagy Promotes Fusion of Multivesicular Bodies with Autophagic Vacuoles in K562 Cells. Traffic 2007, 9, 230–250. [Google Scholar] [CrossRef]
- Patel, K.K.; Miyoshi, H.; Beatty, W.L.; Head, R.D.; Malvin, N.P.; Cadwell, K.; Guan, J.-L.; Saitoh, T.; Akira, S.; Seglen, P.O.; et al. Autophagy proteins control goblet cell function by potentiating reactive oxygen species production. EMBO J. 2013, 32, 3130–3144. [Google Scholar] [CrossRef] [Green Version]
- Zhang, M.; Kenny, S.J.; Ge, L.; Xu, K.; Schekman, R. Translocation of interleukin-1β into a vesicle intermediate in autophagy-mediated secretion. eLife 2015, 4, e11205. [Google Scholar] [CrossRef]
- Kumar, D.; Gupta, D.; Shankar, S.; Srivastava, R.K. Biomolecular characterization of exosomes released from cancer stem cells: Possible implications for biomarker and treatment of cancer. Oncotarget 2015, 6, 3280–3291. [Google Scholar] [CrossRef] [Green Version]
- Sun, W.-L.; Chen, J.; Wang, Y.-P.; Zheng, H. Autophagy protects breast cancer cells from epirubicin-induced apoptosis and facilitates epirubicin-resistance development. Autophagy 2011, 7, 1035–1044. [Google Scholar] [CrossRef] [Green Version]
- Yang, Z.J.; Chee, C.E.; Huang, S.; Sinicrope, F.A. The Role of Autophagy in Cancer: Therapeutic Implications. Mol. Cancer Ther. 2011, 10, 1533–1541. [Google Scholar] [CrossRef] [Green Version]
- Yu, D.; Wu, Y.; Shen, H.; Lv, M.-M.; Chen, W.; Zhang, X.; Zhong, S.; Tang, J.; Zhao, J. Exosomes in development, metastasis and drug resistance of breast cancer. Cancer Sci. 2015, 106, 959–964. [Google Scholar] [CrossRef] [Green Version]
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Auger, C.; Christou, N.; Brunel, A.; Perraud, A.; Verdier, M. Autophagy and Extracellular Vesicles in Colorectal Cancer: Interactions and Common Actors? Cancers 2021, 13, 1039. https://doi.org/10.3390/cancers13051039
Auger C, Christou N, Brunel A, Perraud A, Verdier M. Autophagy and Extracellular Vesicles in Colorectal Cancer: Interactions and Common Actors? Cancers. 2021; 13(5):1039. https://doi.org/10.3390/cancers13051039
Chicago/Turabian StyleAuger, Clément, Niki Christou, Aude Brunel, Aurélie Perraud, and Mireille Verdier. 2021. "Autophagy and Extracellular Vesicles in Colorectal Cancer: Interactions and Common Actors?" Cancers 13, no. 5: 1039. https://doi.org/10.3390/cancers13051039