Emerging roles of tetraspanins in plant inter-cellular and inter-kingdom communication

References

• Garcia-Espana, A, Chung, P-J, Sarkar, IN, Stiner, E, Sun, T-T, Desalle, R. Appearance of new tetraspanin genes during vertebrate evolution. Genom. 2008;91(4):326–334. doi:10.1016/j.ygeno.2007.12.005.
   PubMed Web of Science ®Google Scholar
• Hassuna, N, Monk, PN, Moseley, GW, Partridge, LJ. Strategies for targeting tetraspanin proteins. BioDrugs. 2009;23(6):341–359. doi:10.2165/11315650-000000000-00000.
   PubMed Web of Science ®Google Scholar
• Zhang, X, Muto, A, Van de Velde, J, Neyt, P, Himanen, K, Vandepoele, K. Van Lijsebettens, M, Molecular cloning, expression pattern, and phylogenetic analysis of a tetraspanin CD82-like molecule in lamprey Lampetra japonica. Dev Genes Evol. 2016;226(2):87–98. doi:10.1007/s00427-016-0530-y.
   PubMed Web of Science ®Google Scholar
• Wang F, Vandepoele K, Van Lijsebettens M. Tetraspanin genes in plants. Plant Sci. 2012;190:9–15. doi:10.1016/j.plantsci.2012.03.005.
   PubMed Web of Science ®Google Scholar
• Garcia-Espana, A, Chung, PJ, Zhao, X, Lee, A, Pellicer, A, Yu, J, Sun, TT, DeSalle, R. Origin of the tetraspanin uroplakins and their co-evolution with associated proteins: implications for uroplakin structure and function. Mol Phylogenet Evol. 2006;41(2):355–367. doi:10.1016/j.ympev.2006.04.023.
   PubMed Web of Science ®Google Scholar
• Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol. 2005;6(10):801–811. doi:10.1038/nrm1736.
   PubMed Web of Science ®Google Scholar
• Levy S, Shoham T. Protein-protein interactions in the tetraspanin web. Physiol (Bethesda). 2005;20:218–224. doi:10.1152/physiol.00015.2005.
   PubMed Web of Science ®Google Scholar
• Rubinstein, E, Ziyyat, A, Wolf, J-P, Le Naour, F, Boucheix, C. The molecular players of sperm-egg fusion in mammals. Semin Cell Dev Biol. 2006;17(2):254–263. doi:10.1016/j.semcdb.2006.02.012.
   PubMed Web of Science ®Google Scholar
• Harada, Y, Yoshida, K, Kawano, N, Miyado, K. Critical role of exosomes in sperm-egg fusion and virus-induced cell-cell fusion. Reprod Med Biol. 2013;12(4):117–126. doi:10.1007/s12522-013-0152-2.
   PubMedGoogle Scholar
• Jankovicova, J, Simon, M, Antalíková, J, Cupperová, P, Michalková, K. Role of tetraspanin CD9 molecule in fertilization of mammals. Physiol Res. 2015;64(3):279–293.
   PubMed Web of Science ®Google Scholar
• Jin, L, Wang, J, Guan, F, Zhang, J, Yu, S, Liu, S, Xue, Y, Li, L, Wu, S, Wang, X, Yang, Y. Dominant point mutation in a tetraspanin gene associated with field-evolved resistance of cotton bollworm to transgenic Bt cotton. Proc Natl Acad Sci USA. 2018;115(46):11760–11765. doi:10.1073/pnas.1812138115.
   PubMed Web of Science ®Google Scholar
• Zöller M. Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer. 2009;9(1):40. doi:10.1038/nrc2543.
   PubMed Web of Science ®Google Scholar
• Wang, F, Muto, A, Van de Velde, J, Neyt, P, Himanen, K, Vandepoele, K, Van Lijsebettens, M. Functional analysis of the Arabidopsis tetraspanin gene family in plant growth and development. Plant Physiol. 2015;169(3):2200–2214. doi:10.1104/pp.15.01310.
   PubMed Web of Science ®Google Scholar
• Reimann R, Kost B, Dettmer J. Tetraspanins in plants. Front Plant Sci. 2017;8:545. doi:10.3389/fpls.2017.00545.
   PubMed Web of Science ®Google Scholar
• Boavida, LC, Qin, P., Broz, M., Becker, JD, McCormick, S. Arabidopsis tetraspanins are confined to discrete expression domains and cell types in reproductive tissues and form homo- and heterodimers when expressed in yeast. Plant Physiol. 2013;163(2):696–712. doi:10.1104/pp.113.216598.
   PubMed Web of Science ®Google Scholar
• Berditchevski F, Odintsova E. Characterization of integrin-tetraspanin adhesion complexes: role of tetraspanins in integrin signaling. J Cell Biol. 1999;146:477–492.
   PubMed Web of Science ®Google Scholar
• Berditchevski F, Odintsova E. Tetraspanins as regulators of protein trafficking. Traffic. 2007;8(2):89–96. doi:10.1111/j.1600-0854.2006.00515.x.
   PubMed Web of Science ®Google Scholar
• Kovalenko, OV, Metcalf, DG, DeGrado, WF, Hemler, ME. Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Struct Biol. 2005;5:11. doi:10.1186/1472-6807-5-11.
   PubMed Web of Science ®Google Scholar
• Stipp CS, Kolesnikova TV, Hemler ME. Functional domains in tetraspanin proteins. Trends Biochem Sci. 2003;28(2):106–112. doi:10.1016/S0968-0004(02)00014-2.
   PubMed Web of Science ®Google Scholar
• Termini CM, Gillette JM. Tetraspanins function as regulators of cellular signaling. Front Cell Dev Biol. 2017;5:34. doi:10.3389/fcell.2017.00034.
   PubMed Web of Science ®Google Scholar
• Knepper C, Savory EA, Day B. Arabidopsis NDR1 is an integrin-like protein with a role in fluid loss and plasma membrane-cell wall adhesion. Plant Physiol. 2011;156(1):286–300. doi:10.1104/pp.110.169656.
   PubMed Web of Science ®Google Scholar
• Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 2009;315(9):1584–1592. doi:10.1016/j.yexcr.2008.09.020.
   PubMed Web of Science ®Google Scholar
• van Deventer SJ, Dunlock VE, van Spriel AB. Molecular interactions shaping the tetraspanin web. Biochem Soc Trans. 2017;45(3):741–750. doi:10.1042/BST20160284.
   PubMedGoogle Scholar
• Zimmerman, B., Kelly, B., McMillan, BJ, Seegar, TC, Dror, RO, Kruse, AC, Blacklow, SC. Crystal structure of a full-length human tetraspanin reveals a cholesterol-binding pocket. Cell. 2016;167(4):1041–1051. e11. doi:10.1016/j.cell.2016.09.056.
   PubMed Web of Science ®Google Scholar
• Cnops, G, Neyt, P, Raes, J, Petrarulo, M, Nelissen, H, Malenica, N, Luschnig, C, Tietz, O, Ditengou, F, Palme, K, Azmi, A. The TORNADO1 and TORNADO2 genes function in several patterning processes during early leaf development in Arabidopsis thaliana. Plant Cell. 2006;18(4):852–866. doi:10.1105/tpc.105.040568.
   PubMed Web of Science ®Google Scholar
• Cunha, ES, Sfriso, P, Rojas, AL, Roversi, P, Hospital, A, Orozco, M, Abrescia, NG. Mechanism of structural tuning of the Hepatitis C Virus Human Cellular Receptor CD81 large extracellular loop. Structure. 2018;26(1):181. doi:10.1016/j.str.2018.06.013.
   PubMed Web of Science ®Google Scholar
• Lambou, K, Tharreau, D, Kohler, A, Sirven, C, Marguerettaz, M, Barbisan, C, Sexton, AC, Kellner, EM, Martin, F, Howlett, BJ and Orbach, MJ. Fungi have three tetraspanin families with distinct functions. BMC Genomics. 2008;9:63. doi:10.1186/1471-2164-9-63.
   PubMed Web of Science ®Google Scholar
• Rous, BA, Reaves, BJ, Ihrke, G, Briggs, JAG, Gray, SR, Stephens, DJ, Banting, G, Luzio, JP. Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Mol Biol Cell. 2002;13(3):1071–1082. doi:10.1091/mbc.01-08-0409.
   PubMed Web of Science ®Google Scholar
• Latysheva, N, Muratov, G, Rajesh, S, Padgett, M, Hotchin, NA, Overduin, M, Berditchevski, F. Syntenin-1 is a new component of tetraspanin-enriched microdomains: mechanisms and consequences of the interaction of syntenin-1 with CD63. Mol Cell Biol. 2006;26(20):7707–7718. doi:10.1128/MCB.00849-06.
   PubMed Web of Science ®Google Scholar
• Sala-Valdes, M, Ursa, A, Charrin, S, Rubinstein, E, Hemler, ME, Sánchez-Madrid, F, Yáñez-Mó, M. EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin-radixin-moesin proteins. J Biol Chem. 2006;281(28):19665–19675. doi:10.1074/jbc.M602116200.
   PubMed Web of Science ®Google Scholar
• Olmos E, Reiss B, Dekker K. The ekeko mutant demonstrates a role for tetraspanin-like protein in plant development. Biochem Biophys Res Commun. 2003;310:1054–1061.
   PubMed Web of Science ®Google Scholar
• Clergeot, PH, Gourgues, M, Cots, J, Laurans, F, Latorse, MP, Pepin, R, Tharreau, D, Notteghem, JL, Lebrun, MH. PLS1, a gene encoding a tetraspanin-like protein, is required for penetration of rice leaf by the fungal pathogen Magnaporthe grisea. Proc Natl Acad Sci USA. 2001;98(12):6963–6968. doi:10.1073/pnas.111132998.
   PubMed Web of Science ®Google Scholar
• Moribe H, Mekada E. Co-occurrence of tetraspanin and ROS generators: conservation in protein cross-linking and other developmental processes. Worm. 2013;2(2):e23415. doi:10.4161/worm.23415.
   PubMedGoogle Scholar
• Moribe, H, Konakawa, R, Koga, D, Ushiki, T, Nakamura, K, Mekada, E, Chisholm, AD. Tetraspanin is required for generation of reactive oxygen species by the dual oxidase system in Caenorhabditis elegans. PLoS Genet. 2012;8(9):e1002957. doi:10.1371/journal.pgen.1002957.
   PubMed Web of Science ®Google Scholar
• Charrin, S, Manié, S, Billard, M, Ashman, L, Gerlier, D, Boucheix, C, Rubinstein, E. Multiple levels of interactions within the tetraspanin web. Biochem Biophys Res Commun. 2003;304(1):107–112.
   PubMed Web of Science ®Google Scholar
• Charrin, S, Manié, S, Oualid, M, Billard, M, Boucheix, C, Rubinstein, E. Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Lett. 2002;516(1–3):139–144.
   PubMed Web of Science ®Google Scholar
• Zuidscherwoude, M, et al. Tetraspanin microdomains control localized protein kinase C signaling in B cells. Sci Signal. 2017;10(478):1–15.
   PubMed Web of Science ®Google Scholar
• Espenel, C, Margeat, E, Dosset, P, Arduise, C, Le Grimellec, C, Royer, CA, Boucheix, C, Rubinstein, E, Milhiet, P-E. Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. J Cell Biol. 2008;182(4):765–776. doi:10.1083/jcb.200803010.
   PubMed Web of Science ®Google Scholar
• Zuidscherwoude, M, Göttfert, F, Dunlock, VME, Figdor, CG, Van Den Bogaart, G, Van Spriel, AB. The tetraspanin web revisited by super-resolution microscopy. Sci Rep. 2015;5:12201. doi:10.1038/srep12201.
   PubMed Web of Science ®Google Scholar
• Cnops, G, Wang, X, Linstead, P, Van Montagu, M, Van Lijsebettens, M, Dolan, L. Tornado1 and tornado2 are required for the specification of radial and circumferential pattern in the Arabidopsis root. Development. 2000;127(15):3385–3394.
   PubMed Web of Science ®Google Scholar
• Lieber, D, Lora, J, Schrempp, S, Lenhard, M, Laux, T. Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate. Curr Biol. 2011;21(12):1009–1017. doi:10.1016/j.cub.2011.05.015.
   PubMed Web of Science ®Google Scholar
• Couto, N, Caja, S, Maia, J, Strano Moraes, MC, Costa-Silva, B. Exosomes as emerging players in cancer biology. Biochimie. 2018. doi:10.1016/j.biochi.2018.03.006.
   PubMed Web of Science ®Google Scholar
• Tucci, M, Mannavola, F, Passarelli, A, Stucci, LS, Cives, M, Silvestris, F. Exosomes in melanoma: a role in tumor progression, metastasis and impaired immune system activity. Oncotarget. 2018;9(29):20826–20837. doi:10.18632/oncotarget.24846.
   PubMedGoogle Scholar
• Huang, CL, Ueno, M., Liu, D, Masuya, D, Nakano, J, Yokomise, H, Nakagawa, T, Miyake, M. MRP-1/CD9 gene transduction regulates the actin cytoskeleton through the downregulation of WAVE2. Oncogene. 2006;25(49):6480–6488. doi:10.1038/sj.onc.1209654.
   PubMed Web of Science ®Google Scholar
• Maecker HT, Todd SC, Levy S. The tetraspanin superfamily: molecular facilitators. FASEB J. 1997;11:428–442.
   PubMed Web of Science ®Google Scholar
• Murk, JL, Humbel, BM, Ziese, U, Griffith, JM, Posthuma, G, Slot, JW, Koster, AJ, Verkleij, AJ, Geuze, HJ, Kleijmeer, MJ. Endosomal compartmentalization in three dimensions: implications for membrane fusion. Proc Natl Acad Sci USA. 2003;100(23):13332–13337. doi:10.1073/pnas.2232379100.
   PubMed Web of Science ®Google Scholar
• Duffield, A, Kamsteeg, E-J, Brown, AN, Pagel, P, Caplan, MJ. The tetraspanin CD63 enhances the internalization of the H,K-ATPase beta-subunit. Proc Natl Acad Sci USA. 2003;100(26):15560–15565.
   PubMed Web of Science ®Google Scholar
• Spoden, G, Freitag, K, Husmann, M, Boller, K, Sapp, M, Lambert, C, Florin, L, Sommer, P. Clathrin- and caveolin-independent entry of human papillomavirus type 16–involvement of tetraspanin-enriched microdomains (TEMs). PLoS One. 2008;3(10):e3313. doi:10.1371/journal.pone.0003313.
   PubMed Web of Science ®Google Scholar
• Guix, FX, et al. Tetraspanin 6: a pivotal protein of the multiple vesicular body determining exosome release and lysosomal degradation of amyloid precursor protein fragments. Mol Neurodegener. 2017;12(1):25. doi:10.1186/s13024-017-0165-0.
   PubMedGoogle Scholar
• Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic. 2008;9(6):871–881. doi:10.1111/j.1600-0854.2008.00734.x.
   PubMed Web of Science ®Google Scholar
• Martin, F, Roth, DM, Jans, DA, Pouton, CW, Partridge, LJ, Monk, PN, Moseley, GW. Tetraspanins in viral infections: a fundamental role in viral biology? J Virol. 2005;79(17):10839–10851. doi:10.1128/JVI.79.17.10839-10851.2005.
   PubMed Web of Science ®Google Scholar
• Grove, J, Hu, K, Farquhar, MJ, Goodall, M, Walker, L, Jamshad, M, Drummer, HE, Bill, RM, Balfe, P, McKeating, JA. A new panel of epitope mapped monoclonal antibodies recognising the prototypical tetraspanin CD81. Wellcome Open Res. 2017;2:82. doi:10.12688/wellcomeopenres.12058.1.
   PubMedGoogle Scholar
• Veneault-Fourrey C, Lambou K, Lebrun MH. Fungal Pls1 tetraspanins as key factors of penetration into host plants: a role in re-establishing polarized growth in the appressorium? FEMS Microbiol Lett. 2006;256(2):179–184. doi:10.1111/j.1574-6968.2006.00128.x.
   PubMed Web of Science ®Google Scholar
• Gourgues, M, Brunet-Simon, A, Lebrun, M-H, Levis, C. The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol Microbiol. 2004;51(3):619–629.
   PubMed Web of Science ®Google Scholar
• Bourett TM, Howard RJ. Actin in penetration pegs of the fungal rice blast pathogen, Magnaporthe grisea. Protoplasma. 1992;168:20–26. doi:10.1007/BF01332647.
   Web of Science ®Google Scholar
• Park, G, Bruno, KS, Staiger, CJ, Talbot, NJ, Xu, J-R. Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol Microbiol. 2004;53(6):1695–1707. doi:10.1111/j.1365-2958.2004.04220.x.
   PubMed Web of Science ®Google Scholar
• Gourgues, M, Clergeot, PH, Veneault, C, Cots, J, Sibuet, S, Brunet-Simon, A, Levis, C, Langin, T, Lebrun, MH. A new class of tetraspanins in fungi. Biochem Biophys Res Commun. 2002;297(5):1197–1204.
   PubMed Web of Science ®Google Scholar
• Veneault-Fourrey, C, Parisot, D, Gourgues, M, Laugé, R, Lebrun, M-H, Langin, T. The tetraspanin gene ClPLS1 is essential for appressorium-mediated penetration of the fungal pathogen Colletotrichum lindemuthianum. Fungal Genet Biol. 2005;42(4):306–318. doi:10.1016/j.fgb.2005.01.009.
   PubMed Web of Science ®Google Scholar
• Edens, WA, et al. Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol. 2001;154(4):879–891. doi:10.1083/jcb.200103132.
   PubMed Web of Science ®Google Scholar
• Moribe, H, Yochem, J, Yamada, H, Tabuse, Yo, Fujimoto, T, Mekada, E. Tetraspanin protein (TSP-15) is required for epidermal integrity in Caenorhabditis elegans. J Cell Sci. 2004;117(Pt 22):5209–5220. doi:10.1242/jcs.01403.
   PubMed Web of Science ®Google Scholar
• Siegmund, U, Heller, J, van Kann, JAL, Tudzynski, P, Schmidt, HH. The NADPH oxidase complexes in Botrytis cinerea: evidence for a close association with the ER and the tetraspanin Pls1. PLoS One. 2013;8(2):e55879. doi:10.1371/journal.pone.0055879.
   PubMed Web of Science ®Google Scholar
• Schurmann, J, Buttermann, D, Herrmann, A, Giesbert, S, Tudzynski, P. Molecular characterization of the NADPH oxidase complex in the ergot fungus Claviceps purpurea: cpNox2 and CpPls1 are important for a balanced host-pathogen interaction. Mol Plant Microbe Interact. 2013;26(10):1151–1164. doi:10.1094/MPMI-03-13-0064-R.
   PubMed Web of Science ®Google Scholar
• Charrin, S, Jouannet, S, Boucheix, C, Rubinstein, E. Tetraspanins at a glance. J Cell Sci. 2014;127(Pt 17):3641–3648. doi:10.1242/jcs.154906.
   PubMed Web of Science ®Google Scholar
• Lee, Y, Rubio, MC, Alassimone, J, Geldner, N. A mechanism for localized lignin deposition in the endodermis. Cell. 2013;153(2):402–412. doi:10.1016/j.cell.2013.02.045.
   PubMed Web of Science ®Google Scholar
• Foreman, J, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422(6930):442–446. doi:10.1038/nature01485.
   PubMed Web of Science ®Google Scholar
• Takeda, S, Gapper, C, Kaya, H, Bell, E, Kuchitsu, K, Dolan, L. Local positive feedback regulation determines cell shape in root hair cells. Science. 2008;319(5867):1241–1244. doi:10.1126/science.1152505.
   PubMed Web of Science ®Google Scholar
• Coakley G, Maizels RM, Buck AH. Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol. 2015;31(10):477–489. doi:10.1016/j.pt.2015.06.009.
   PubMed Web of Science ®Google Scholar
• Li, Y, Liu, Y, Xiu, F, Wang, J, Cong, H, He, S, Shi, Y, Wang, X, Li, X, Zhou, H. Characterization of exosomes derived from Toxoplasma gondii and their functions in modulating immune responses. Int J Nanomedicine. 2018;13:467–477. doi:10.2147/IJN.S151110.
   PubMed Web of Science ®Google Scholar
• Weidle, UH, Birzele, F, Kollmorgen, G, Rueger, R. The multiple roles of exosomes in metastasis. Cancer Genom Proteom. 2017;14(1):1–15. doi:10.21873/cgp.20015.
   PubMed Web of Science ®Google Scholar
• Zhang, W, Jiang, X, Bao, J, Wang, Y, Liu, H, Tang, L. Exosomes in pathogen infections: A bridge to deliver molecules and link functions. Front Immunol. 2018;9:90. doi:10.3389/fimmu.2018.00090.
   PubMed Web of Science ®Google Scholar
• Cai, Q, Qiao, L, Wang, M, He, B, Lin, FM, Palmquist, J, Huang, SD, Jin, H. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science. 2018;360(6393):1126–1129. doi:10.1126/science.aar4142.
   PubMed Web of Science ®Google Scholar
• Li, Y, Xiu, F, Mou, Z, Xue, Z, Du, H, Zhou, C, Li, Y, Shi, Y, He, S, Zhou, H. Exosomes derived from Toxoplasma gondii stimulate an inflammatory response through JNK signaling pathway. Nanomedicine (Lond). 2018;13(10):1157–1168. doi:10.2217/nnm-2018-0035.
   PubMed Web of Science ®Google Scholar
• Valenzuela, MM, Bennit, HRF, Gonda, A, Osterman, CJD, Hibma, A, Khan, S, Wall, NR. Exosomes secreted from human cancer cell lines contain Inhibitors of Apoptosis (IAP). Cancer Microenviron. 2015;8(2):65–73. doi:10.1007/s12307-015-0167-9.
   PubMed Web of Science ®Google Scholar
• Stahl PD, Raposo G. Exosomes and extracellular vesicles: the path forward. Essays Biochem. 2018;62(2):119–124. doi:10.1042/EBC20170088.
   PubMed Web of Science ®Google Scholar
• Cai, ZY, Xiao, M, Quazi, SH, Ke, ZY. Exosomes: a novel therapeutic target for Alzheimer’s disease? Neural Regen Res. 2018;13(5):930–935. doi:10.4103/1673-5374.232490.
   PubMed Web of Science ®Google Scholar
• Buck, AH, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun. 2014;5:5488. doi:10.1038/ncomms5972.
   PubMed Web of Science ®Google Scholar
• Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010;73(10):1907–1920. doi:10.1016/j.jprot.2010.06.006.
   PubMed Web of Science ®Google Scholar
• Gonzalez JF, Venturi V. A novel widespread interkingdom signaling circuit. Trends Plant Sci. 2013;18(3):167–174. doi:10.1016/j.tplants.2012.09.007.
   PubMed Web of Science ®Google Scholar
• Yoon YJ, Kim OY, Gho YS. Extracellular vesicles as emerging intercellular communicasomes. BMB Rep. 2014;47(10):531. doi:10.5483/BMBRep.2014.47.10.164.
   PubMed Web of Science ®Google Scholar
• Lakkaraju A, Rodriguez-Boulan E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol. 2008;18(5):199–209. doi:10.1016/j.tcb.2008.03.002.
   PubMed Web of Science ®Google Scholar
• Hassuna, N, Monk, PN, Moseley, GW, Partridge, LJ. Strategies for targeting tetraspanin proteins: potential therapeutic applications in microbial infections. BioDrugs. 2009;23(6):341–359. doi:10.2165/11315650-000000000-00000.
   PubMed Web of Science ®Google Scholar
• Bellavia, D, Raimondi, L, Costa, V, De Luca, A, Carina, V, Maglio, M, Fini, M, Alessandro, R, Giavaresi, G. Engineered exosomes: A new promise for the management of musculoskeletal diseases. Biochim Biophys Acta. 2018;1862:1893–1901.
   Web of Science ®Google Scholar
• Wang, M, Weiberg, A, Lin, FM, Thomma, BP, Huang, HD, Jin, H. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nature Plants. 2016;2(10):16151. doi:10.1038/nplants.2016.151.
   PubMed Web of Science ®Google Scholar
• Weiberg, A, Wang, M, Lin, FM, Zhao, H, Zhang, Z, Kaloshian, I, Huang, HD, Jin, H. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science. 2013;342(6154):118–123. doi:10.1126/science.1239705.
   PubMed Web of Science ®Google Scholar
• Weiberg A, Jin HL. Small RNAs - the secret agents in the plant-pathogen interactions. Curr Opin Plant Biol. 2015;26:87–94. doi:10.1016/j.pbi.2015.05.033.
   PubMed Web of Science ®Google Scholar
• Wang, M, Weiberg, A, Dellota Jr, E, Yamane, D, Jin, H. Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi. RNA Biol. 2017;14(4):421–428. doi:10.1080/15476286.2017.1291112.
   PubMed Web of Science ®Google Scholar
• Gangoda, L, Boukouris, S, Liem, M, Kalra, H, Mathivanan, S. Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics. 2015;15(2–3):260–271. doi:10.1002/pmic.201400234.
   PubMed Web of Science ®Google Scholar
• Regente, M, Pinedo, M, San Clemente, H, Balliau, T, Jamet, E, de la Canal, L. Plant extracellular vesicles are incorporated by a fungal pathogen and inhibit its growth. J Exp Bot. 2017;68(20):5485–5495. doi:10.1093/jxb/erx355.
   PubMed Web of Science ®Google Scholar
• Rutter BD, Innes RW. Extracellular vesicles isolated from the leaf apoplast carry stress-response proteins. Plant Physiol. 2017;173(1):728–741. doi:10.1104/pp.16.01253.
   PubMed Web of Science ®Google Scholar
• Mittelbrunn M, Sanchez-Madrid F. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol. 2012;13(5):328–335. doi:10.1038/nrm3335.
   PubMed Web of Science ®Google Scholar
• Blanc, C, et al. The cuticle mutant eca2 modifies plant defense responses to biotrophic and necrotrophic pathogens and herbivory insects. Mol Plant Microbe Interact. 2018;31(3):344–355. doi:10.1094/MPMI-07-17-0181-R.
   PubMed Web of Science ®Google Scholar
• Serrano, M, Coluccia, F, Torres, M, L’Haridon, F, Métraux, JP. The cuticle and plant defense to pathogens. Front Plant Sci. 2014;5:274. doi:10.3389/fpls.2014.00274.
   PubMed Web of Science ®Google Scholar
• L’Haridon, F, Besson-Bard, A, Binda, M, Serrano, M, Abou-Mansour, E, Balet, F, Schoonbeek, HJ, Hess, S, Mir, R, Léon, J, Lamotte, O. A permeable cuticle is associated with the release of reactive oxygen species and induction of innate immunity. PLoS Pathog. 2011;7(7):e1002148. doi:10.1371/journal.ppat.1002148.
   PubMed Web of Science ®Google Scholar
• Ferrari, S, Galletti, R, Denoux, C, De Lorenzo, G, Ausubel, FM, Dewdney, J. Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol. 2007;144(1):367–379. doi:10.1104/pp.107.095596.
   PubMed Web of Science ®Google Scholar
• Ebine, K, et al. A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol. 2011;13(7):853–859. doi:10.1038/ncb2270.
   PubMed Web of Science ®Google Scholar
• LaMonte, G, et al. Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe. 2012;12(2):187–199. doi:10.1016/j.chom.2012.06.007.
   PubMed Web of Science ®Google Scholar
• An, Q, Ehlers, K, Kogel, KH, Van Bel, AJ, Hückelhoven, R. Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol. 2006;172(3):563–576. doi:10.1111/j.1469-8137.2006.01844.x.
   PubMed Web of Science ®Google Scholar
• An, Q, Hückelhoven, R, Kogel, KH, Van Bel, AJ. Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol. 2006;8(6):1009–1019. doi:10.1111/j.1462-5822.2006.00683.x.
   PubMed Web of Science ®Google Scholar
• An Q, van Bel AJ, Huckelhoven R. Do plant cells secrete exosomes derived from multivesicular bodies? Plant Signal Behav. 2007;2:4–7.
   PubMedGoogle Scholar
• Luginbuehl LH, Oldroyd GED. Understanding the Arbuscule at the Heart of endomycorrhizal symbioses in plants. Curr Biol. 2017;27(17):R952–R963. doi:10.1016/j.cub.2017.06.042.
   PubMed Web of Science ®Google Scholar
• Luginbuehl, LH, Menard, GN, Kurup, S, Van Erp, H, Radhakrishnan, GV, Breakspear, A, Oldroyd, GED, Eastmond, PJ. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science. 2017;356(6343):1175–1178. doi:10.1126/science.aan0081.
   PubMed Web of Science ®Google Scholar
• Choi, D-S, Yang, JS, Choi, EJ, Jang, SC, Park, S., Kim, OY, Hwang, D., Kim, KP, Kim, YK, Kim, S., Gho, YS. The protein interaction network of extracellular vesicles derived from human colorectal cancer cells. J Proteome Res. 2012;11(2):1144–1151. doi:10.1021/pr200842h.
   PubMed Web of Science ®Google Scholar
• Hervera, A, Hervera, A, De Virgiliis, F, Palmisano, I, Zhou, L, Tantardini, E, Kong, G, Hutson, T, Danzi, MC., Perry, RBT, Santos, CX, Kapustin, AN. Reactive oxygen species regulate axonal regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nat Cell Biol. 2018;20(3):307–319. doi:10.1038/s41556-018-0039-x.
   PubMed Web of Science ®Google Scholar
• Krishnamoorthy L, Chang CJ. Exosomal NADPH Oxidase: delivering Redox Signaling for Healing. Biochemistry. 2018. doi:10.1021/acs.biochem.8b00429.
   PubMed Web of Science ®Google Scholar
• Morelli, AE, Larregina, AT, Shufesky, WJ, Sullivan, ML, Stolz, DB, Papworth, GD, Zahorchak, AF, Logar, AJ, Wang, Z, Watkins, SC, Falo, LD. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood. 2004;104(10):3257–3266. doi:10.1182/blood-2004-03-0824.
   PubMed Web of Science ®Google Scholar
• Hernandez-Onate, MA, Esquivel-Naranjo, EU, Mendoza-Mendoza, A, Stewart, A, Herrera-Estrella, AH. An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc Natl Acad Sci USA. 2012;109(37):14918–14923. doi:10.1073/pnas.1209396109.
   PubMed Web of Science ®Google Scholar