Mucus-derived exosome-like vesicles from the Spanish slug (Arion vulgaris): taking advantage of invasive pest species in biotechnology
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
36526668
PubMed Central
PMC9870906
DOI
10.1038/s41598-022-26335-3
PII: 10.1038/s41598-022-26335-3
Knihovny.cz E-resources
- MeSH
- Biotechnology MeSH
- Exosomes * metabolism MeSH
- Mucus MeSH
- Humans MeSH
- Gastropoda * MeSH
- Mammals MeSH
- Introduced Species MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The slug Arion vulgaris has attracted major attention as one of the worst invasive herbivore pests in Europe and is renowned for the stiff mucus it secretes for locomotion. In this study we focused on the isolation and characterisation of extracellular vesicles, specifically exosomes and exosome-like vesicles, from Arion secretions. We developed a method for slug mucus collection and subsequent vesicle isolation by ultracentrifugation. The isolated vesicles with an average diameter of ~ 100 nm carry abundant proteins and short RNAs, as well as adhesion molecules similar to mammalian galectins. We demonstrated that the slug extracellular vesicles are internalised by plant cells and human cancer cells in in vitro assays and are loadable by bioactive compounds, which makes them an interesting tool for utilisation in biotechnology.
See more in PubMed
Zemanova MA, Knop E, Heckel G. Introgressive replacement of natives by invading Arion pest slugs. Sci. Rep. 2017;7:14908. doi: 10.1038/s41598-017-14619-y. PubMed DOI PMC
Zemanova MA, Knop E, Heckel G. Phylogeographic past and invasive presence of Arion pest slugs in Europe. Mol. Ecol. 2016;25:5747–5764. doi: 10.1111/mec.13860. PubMed DOI
Lauren, H. Z. G. & Whitlow, W. L. Ecological effects of invasive slugs, Arion rufus, on native cascade oregon grape, Mahonia nervosa. Northwest Sci.86, 1–8, 8 (2012).
Honěk A, Martinková Z. Floral herbivory of an invasive slug on a native weed. Plant Protect. Sci. 2014;50:151–156. doi: 10.17221/75/2013-PPS. DOI
Cunha RL, Patrão C, Castilho R. Different diversity-dependent declines in speciation rate unbalances species richness in terrestrial slugs. Sci. Rep. 2017;7:16198. doi: 10.1038/s41598-017-16417-y. PubMed DOI PMC
Gren IM, Isacs L, Carlsson M. Costs of alien invasive species in Sweden. Ambio. 2009;38:135–140. doi: 10.1579/0044-7447-38.3.135. PubMed DOI
Dörler D, Scheucher A, Zaller JG. Efficacy of chemical and biological slug control measures in response to watering and earthworms. Sci. Rep. 2019;9:2954. doi: 10.1038/s41598-019-39585-5. PubMed DOI PMC
Gismervik K, et al. Invading slugs (Arion vulgaris) can be vectors for Listeria monocytogenes. J. Appl. Microbiol. 2015;118:809–816. doi: 10.1111/jam.12750. PubMed DOI PMC
Gismervik K, Bruheim T, Rørvik LM, Haukeland S, Skaar I. Invasive slug populations (Arion vulgaris) as potential vectors for Clostridium botulinum. Acta Vet. Scand. 2014;56:65. doi: 10.1186/s13028-014-0065-z. PubMed DOI PMC
Patel Z, et al. Molecular identification of novel intermediate host species of Angiostrongylus vasorum in Greater London. Parasitol. Res. 2014;113:4363–4369. doi: 10.1007/s00436-014-4111-6. PubMed DOI
Greistorfer S, et al. Characterization of the Arion vulgaris pedal gland system. J. Morphol. 2020;281:1059–1071. doi: 10.1002/jmor.21231. PubMed DOI PMC
Shirtcliffe NJ, McHale G, Newton MI. Wet adhesion and adhesive locomotion of snails on anti-adhesive non-wetting surfaces. PLoS ONE. 2012;7:e36983. doi: 10.1371/journal.pone.0036983. PubMed DOI PMC
Gural-Sverlova N, Gural R. Morphological, anatomical and behavioural peculiarities of the slugs from the Arion lusitanicus complex in Western Ukraine. Ruthenica Russ. Malacol. J. 2012;21(2):97–111.
Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367:eaau6977. doi: 10.1126/science.aau6977. PubMed DOI PMC
Janouskova O, et al. Conventional and nonconventional sources of exosomes-isolation methods and influence on their downstream biomedical application. Front. Mol. Biosci. 2022;9:846650. doi: 10.3389/fmolb.2022.846650. PubMed DOI PMC
Sritharan S, Sivalingam N. A comprehensive review on time-tested anticancer drug doxorubicin. Life Sci. 2021;278:119527. doi: 10.1016/j.lfs.2021.119527. PubMed DOI
Schuh C, Aguayo S, Zavala G, Khoury M. Exosome-like vesicles in Apis mellifera bee pollen, honey and royal jelly contribute to their antibacterial and pro-regenerative activity. J. Exp. Biol. 2019;222:jeb208702. doi: 10.1242/jeb.208702. PubMed DOI
Schuh C, Cuenca J, Alcayaga-Miranda F, Khoury M. Exosomes on the border of species and kingdom intercommunication. Transl. Res. 2019;210:80–98. doi: 10.1016/j.trsl.2019.03.008. PubMed DOI
Peršurić Ž, Pavelić SK. Bioactives from bee products and accompanying extracellular vesicles as novel bioactive components for wound healing. Molecules. 2021;26:3770. doi: 10.3390/molecules26123770. PubMed DOI PMC
Carregari VC, et al. Snake venom extracellular vesicles (SVEVs) reveal wide molecular and functional proteome diversity. Sci. Rep. 2018;8:12067. doi: 10.1038/s41598-018-30578-4. PubMed DOI PMC
Wu Z, et al. Extracellular vesicle-mediated communication within host–parasite interactions. Front. Immunol. 2019;9:3066. doi: 10.3389/fimmu.2018.03066. PubMed DOI PMC
Nawaz M, Malik MI, Hameed M, Zhou J. Research progress on the composition and function of parasite-derived exosomes. Acta Trop. 2019;196:30–36. doi: 10.1016/j.actatropica.2019.05.004. PubMed DOI
Akuma P, Okagu OD, Udenigwe CC. Naturally occurring exosome vesicles as potential delivery vehicle for bioactive compounds. Front. Sustain. Food Syst. 2019;3:23. doi: 10.3389/fsufs.2019.00023. DOI
Wang M, et al. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants. 2016;2:16151. doi: 10.1038/nplants.2016.151. PubMed DOI PMC
Kessler RJ, Fanestil DD. Interference by lipids in the determination of protein using bicinchoninic acid. Anal. Biochem. 1986;159:138–142. doi: 10.1016/0003-2697(86)90318-0. PubMed DOI
Hueso D, Fontecha J, Gómez-Cortés P. Comparative study of the most commonly used methods for total protein determination in milk of different species and their ultrafiltration products. Front. Nutr. 2022;9:925565. doi: 10.3389/fnut.2022.925565. PubMed DOI PMC
Greistorfer S, et al. Snail mucus—glandular origin and composition in Helix pomatia. Zoology. 2017;122:126–138. doi: 10.1016/j.zool.2017.05.001. PubMed DOI
Newar J, Ghatak A. Studies on the adhesive property of snail adhesive mucus. Langmuir. 2015;31:12155–12160. doi: 10.1021/acs.langmuir.5b03498. PubMed DOI
Gould J, Valdez JW, Upton R. Adhesive defence mucus secretions in the red triangle slug (Triboniophorus graeffei) can incapacitate adult frogs. Ethology. 2019;125:587–591.
Noothuan N, Apitanyasai K, Panha S, Tassanakajon A. Snail mucus from the mantle and foot of two land snails, Lissachatina fulica and Hemiplecta distincta, exhibits different protein profile and biological activity. BMC Res. Notes. 2021;14:138. doi: 10.1186/s13104-021-05557-0. PubMed DOI PMC
Ito S, et al. High molecular weight lectin isolated from the mucus of the giant African snail Achatina fulica. Biosci. Biotechnol. Biochem. 2011;75:20–25. doi: 10.1271/bbb.100389. PubMed DOI
Cilia G, Fratini F. Antimicrobial properties of terrestrial snail and slug mucus. J. Complement. Integr. Med. 2018;15(3):20170168. doi: 10.1515/jcim-2017-0168. PubMed DOI
Dvorak M, et al. Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris. Sci. Rep. 2019;9:20089. doi: 10.1038/s41598-019-56577-7. PubMed DOI PMC
Braun M, Menges M, Opoku F, Smith AM. The relative contribution of calcium, zinc and oxidation-based cross-links to the stiffness of Arion subfuscus glue. J. Exp. Biol. 2013;216:1475–1483. PubMed
Werneke SW, Swann C, Farquharson LA, Hamilton KS, Smith AM. The role of metals in molluscan adhesive gels. J. Exp. Biol. 2007;210:2137–2145. doi: 10.1242/jeb.006098. PubMed DOI
Mair J, Port GR. The influence of mucus production by the slug, Deroceras reticulatum, on predation by Pterostichus madidus and Nebria brevicollis (Coleoptera: Carabidae) Biocontrol Sci. Tech. 2002;12:325–335. doi: 10.1080/09583150220128112. DOI
Deyrup-Olsen I, Louie H, Martin AW, Luchtel DL. Triggering by ATP of product release by mucous granules of the land slug Ariolimax columbianus. Am. J. Physiol. 1992;262:C760–765. doi: 10.1152/ajpcell.1992.262.3.C760. PubMed DOI
Smith AM, Huynh P, Griffin S, Baughn M, Monka P. Strong, non-specific adhesion using C-lectin heterotrimers in a molluscan defensive secretion. Integr. Comp. Biol. 2021;61:1440–1449. doi: 10.1093/icb/icab100. PubMed DOI
Leśków A, Tarnowska M, Szczuka I, Diakowska D. The effect of biologically active compounds in the mucus of slugs Limax maximus and Arion rufus on human skin cells. Sci. Rep. 2021;11:18660. doi: 10.1038/s41598-021-98183-6. PubMed DOI PMC
Gentili V, et al. HelixComplex snail mucus as a potential technology against O3 induced skin damage. PLoS ONE. 2020;15:e0229613. doi: 10.1371/journal.pone.0229613. PubMed DOI PMC
Alogna A, et al. Design of liposomes carrying helixcomplex snail mucus: Preliminary studies. Molecules. 2021;26:4709. doi: 10.3390/molecules26164709. PubMed DOI PMC
Trapella C, et al. HelixComplex snail mucus exhibits pro-survival, proliferative and pro-migration effects on mammalian fibroblasts. Sci. Rep. 2018;8:17665. doi: 10.1038/s41598-018-35816-3. PubMed DOI PMC
Perpelek M, et al. Bioactive snail mucus-slime extract loaded chitosan scaffolds for hard tissue regeneration: The effect of mucoadhesive and antibacterial extracts on physical characteristics and bioactivity of chitosan matrix. Biomed. Mater. 2021;16:065008. doi: 10.1088/1748-605X/ac2352. PubMed DOI
López Angulo DE, do Amaral Sobral PJ. Characterization of gelatin/chitosan scaffold blended with aloe vera and snail mucus for biomedical purpose. Int. J. Biol. Macromol. 2016;92:645–653. doi: 10.1016/j.ijbiomac.2016.07.029. PubMed DOI
Di Filippo MF, et al. Functional properties of chitosan films modified by snail mucus extract. Int. J. Biol. Macromol. 2020;143:126–135. doi: 10.1016/j.ijbiomac.2019.11.230. PubMed DOI
Juncan AM, et al. Advantages of hyaluronic acid and its combination with other bioactive ingredients in cosmeceuticals. Molecules. 2021;26:4429. doi: 10.3390/molecules26154429. PubMed DOI PMC
Thornfeldt C. Cosmeceuticals containing herbs: Fact, fiction, and future. Dermatol. Surg. 2005;31:873–880. doi: 10.1111/j.1524-4725.2005.31734. PubMed DOI
Goyal A, et al. Bioactive-based cosmeceuticals: An update on emerging trends. Molecules. 2022;27:828. doi: 10.3390/molecules27030828. PubMed DOI PMC
Kantawong F, et al. Mucus of Achatina fulica stimulates mineralization and inflammatoryresponse in dental pulp cells. Turk. J. Biol. 2016;40:353–359. doi: 10.3906/biy-1505-29. DOI
Kocholata M, Maly J, Martinec J, Auer Malinska H. Plant extracellular vesicles and their potential in human health research, the practical approach. Physiol. Res. 2022;71:327–339. doi: 10.33549/physiolres.934886. PubMed DOI PMC
Karamanidou T, Tsouknidas A. Plant-derived extracellular vesicles as therapeutic nanocarriers. Int. J. Mol. Sci. 2021;23:191. doi: 10.3390/ijms23010191. PubMed DOI PMC
Rizzo J, Rodrigues ML, Janbon G. Extracellular vesicles in fungi: Past, present, and future perspectives. Front. Cell. Infect. Microbiol. 2020;10:346. doi: 10.3389/fcimb.2020.00346. PubMed DOI PMC
Zhang T, et al. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants. 2016;2:16153. doi: 10.1038/nplants.2016.153. PubMed DOI
Weiberg A, et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science. 2013;342:118–123. doi: 10.1126/science.1239705. PubMed DOI PMC
Divekar PA, et al. Plant secondary metabolites as defense tools against herbivores for sustainable crop protection. Int. J. Mol. Sci. 2022;23:2690. doi: 10.3390/ijms23052690. PubMed DOI PMC
War AR, et al. Mechanisms of plant defense against insect herbivores. Plant Signal. Behav. 2012;7:1306–1320. doi: 10.4161/psb.21663. PubMed DOI PMC
Pakarinen E. The response of terrestrial slugs Arion fasciatus and Deroceras reticulatum to the mucus of stressed conspecifics and heterospecifics. Anim. Behav. 1992;43:1051–1052. doi: 10.1016/S0003-3472(06)80019-9. DOI
Shaheen N, Patel K, Patel P, Moore M, Harrington MA. A predatory snail distinguishes between conspecific and heterospecific snails and trails based on chemical cues in slime. Anim. Behav. 2005;70:1067–1077. doi: 10.1016/j.anbehav.2005.02.017. DOI
Cook A. Mucus trail following by the slug Limax grossui Lupu. Anim. Behav. 1977;25:774–781. doi: 10.1016/0003-3472(77)90127-0. DOI
Cook A. The function of trail following in the pulmonate slug, Limax pseudoflavus. Anim. Behav. 1992;43:813–821. doi: 10.1016/S0003-3472(05)80204-0. DOI
Perocheau D, Touramanidou L, Gurung S, Gissen P, Baruteau J. Clinical applications for exosomes: Are we there yet? Br. J. Pharmacol. 2021;178:2375–2392. doi: 10.1111/bph.15432. PubMed DOI PMC
Shafiei M, Ansari MNM, Razak SIA, Khan MUA. A comprehensive review on the applications of exosomes and liposomes in regenerative medicine and tissue engineering. Polymers. 2021;13:2529. doi: 10.3390/polym13152529. PubMed DOI PMC
Bänfer S, Jacob R. Galectins in intra- and extracellular vesicles. Biomolecules. 2020;10:1232. doi: 10.3390/biom10091232. PubMed DOI PMC
Gonda A, Kabagwira J, Senthil GN, Wall NR. Internalization of exosomes through receptor-mediated endocytosis. Mol. Cancer Res. 2019;17:337–347. doi: 10.1158/1541-7786.MCR-18-0891. PubMed DOI
Kumar P, et al. Neuroprotective effect of placenta-derived mesenchymal stromal cells: Role of exosomes. FASEB J. 2019;33:5836–5849. doi: 10.1096/fj.201800972R. PubMed DOI PMC
Sargent I. Microvesicles and pre-eclampsia. Pregnancy Hypertens. 2013;3:58. doi: 10.1016/j.preghy.2013.04.004. PubMed DOI
Maybruck BT, Pfannenstiel LW, Diaz-Montero M, Gastman BR. Tumor-derived exosomes induce CD8(+) T cell suppressors. J. Immunother. Cancer. 2017;5:65. doi: 10.1186/s40425-017-0269-7. PubMed DOI PMC
Toti A, et al. Activated fibroblasts enhance cancer cell migration by microvesicles-mediated transfer of Galectin-1. J. Cell Commun. Signal. 2021;15:405–419. doi: 10.1007/s12079-021-00624-4. PubMed DOI PMC
Mitry MA, Edwards JG. Doxorubicin induced heart failure: Phenotype and molecular mechanisms. Int. J. Cardiol. Heart Vasc. 2016;10:17–24. PubMed PMC
Meng L, et al. Improving glioblastoma therapeutic outcomes via doxorubicin-loaded nanomicelles modified with borneol. Int. J. Pharm. 2019;567:118485. doi: 10.1016/j.ijpharm.2019.118485. PubMed DOI
Yang T, et al. Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm. Res. 2015;32:2003–2014. doi: 10.1007/s11095-014-1593-y. PubMed DOI PMC
Mehryab F, et al. Exosomes as a next-generation drug delivery system: An update on drug loading approaches, characterization, and clinical application challenges. Acta Biomater. 2020;113:42–62. doi: 10.1016/j.actbio.2020.06.036. PubMed DOI
Tian Y, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials. 2014;35:2383–2390. doi: 10.1016/j.biomaterials.2013.11.083. PubMed DOI
Choi H, et al. Targeted delivery of exosomes armed with anti-cancer therapeutics. Membranes. 2022;12:85. doi: 10.3390/membranes12010085. PubMed DOI PMC
Cheng L, Hill AF. Therapeutically harnessing extracellular vesicles. Nat. Rev. Drug Discov. 2022;21:379–399. doi: 10.1038/s41573-022-00410-w. PubMed DOI
Diversity of extracellular vesicles derived from calli, cell culture and apoplastic fluid of tobacco