A Novel Localization in Human Large Extracellular Vesicles for the EGF-CFC Founder Member CRIPTO and Its Biological and Therapeutic Implications
Open accessAbstract
Tumor growth and metastasis strongly rely on cell-cell communication. One of the mechanisms by which tumor cells communicate involves the release and uptake of lipid membrane encapsulated particles full of bioactive molecules, called extracellular vesicles (EVs). EV exchange between cancer cells may induce phenotype changes in the recipient cells. Our work investigated the effect of EVs released by teratocarcinoma cells on glioblastoma (GBM) cells. EVs were isolated by differential centrifugation and analyzed through Western blot, nanoparticle tracking analysis, and electron microscopy. The effect of large EVs on GBM cells was tested through cell migration, proliferation, and drug-sensitivity assays, and resulted in a specific impairment in cell migration with no effects on proliferation and drug-sensitivity. Noticeably, we found the presence of the EGF-CFC founder member CRIPTO on both small and large EVs, in the latter case implicated in the EV-mediated negative regulation of GBM cell migration. Our data let us propose a novel route and function for CRIPTO during tumorigenesis, highlighting a complex scenario regulating its effect, and paving the way to novel strategies to control cell migration, to ultimately improve the prognosis and quality of life of GBM patients.
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The optimized protocol uses silicone culture inserts to enhance wound homogeneity and reproducibility.
“The protocol incorporates the use of silicone culture inserts to enhance wound homogeneity and reproducibility”
From Optimized Wound Healing Assay to Study Extracellular Vesicle-Driven Glioblastoma Cell Migration (2026) · cites this paper as [43]
Section 2.9 (Wound Healing Assay; page unavailable) says the researchers used Ibidi inserts in a wound-healing assay. It does not identify the inserts as silicone or say they were used to improve wound homogeneity or reproducibility. (LLM, conf=0.85)
Experimental — accuracy not yet measuredExtracellular vesicle isolation and characterization were performed according to MISEV 2018 and 2023.
“EV isolation and characterization were performed according to MISEV 2018 and 2023 [49,50], as previously reported [43].”
From Optimized Wound Healing Assay to Study Extracellular Vesicle-Driven Glioblastoma Cell Migration (2026) · cites this paper as [43]
Materials and Methods §2.2 describes EV isolation by differential centrifugation, and §2.11 says the study followed MISEV2018. Results §3.1 describes EV characterization using markers recommended by MISEV2018. The source does not support the attributed reference to MISEV 2023. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe core methodology was first established in a previous study on the effect of NTERA2 teratocarcinoma-derived extracellular vesicles on U87 glioblastoma cell migration.
“The core methodology was first established in our previous study on the effect of NTERA2 teratocarcinoma-derived EVs on the U87 GB cell migration [43]”
From Optimized Wound Healing Assay to Study Extracellular Vesicle-Driven Glioblastoma Cell Migration (2026) · cites this paper as [43]
Continuous Mitomycin C incubation inhibits cell proliferation.
“continuous Mitomycin C incubation to inhibit cell proliferation without inducing”
From Optimized Wound Healing Assay to Study Extracellular Vesicle-Driven Glioblastoma Cell Migration (2026) · cites this paper as [43]
The identity of the extracellular vesicles was confirmed by showing they possessed specific positive markers CD63 and HSP70, while lacking the negative marker Calnexin.
“The identity of the EVs was confirmed by showing they possessed specific positive markers, such as the CD63 membrane-bound marker and the HSP70 luminal marker, while lacking negative markers specific of intracellular compartments (Calnexin) [43].”
From Optimized Wound Healing Assay to Study Extracellular Vesicle-Driven Glioblastoma Cell Migration (2026) · cites this paper as [43]
Continuous Mitomycin C incubation does not induce cytotoxicity.
“without inducing cytotoxicity, enabling specific assessment of cell migration.”
From Optimized Wound Healing Assay to Study Extracellular Vesicle-Driven Glioblastoma Cell Migration (2026) · cites this paper as [43]
The Wound Healing Assay methods (§2.9; page unavailable) say that 2 μg/mL mitomycin C was present to inhibit proliferation while cell migration was assessed. They do not report whether that incubation was cytotoxic; the viability results (§3.2; page unavailable) concern extracellular vesicles, not mitomycin C. Searched for mitomycin C and cell viability or cytotoxicity. (LLM, conf=0.76)
Experimental — accuracy not yet measured
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Cripto haploinsufficiency affects in vivo colon tumor development
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Self-citationRuggiero, D., Nappo, S., Nutile, T., Sorice, R., Talotta, F., Giorgio, E., Bellenguez, C., Leutenegger, A., Liguori, G. L., & Ciullo, M. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1004976 · Cited by 8 · see citing works
Self-citationGudbergsson, J. M., & Duroux, M. C. (2019) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2019.151044 · Cited by 7 · see citing works
From neural stem cells to glioblastoma: A natural history of GBM recapitulated in vitro
Almengló, C., Caamaño, P., Fraga, M., Devesa, J., Costoya, J. A., & Arce, V. M. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30409 · Cited by 5 · see citing works
Conditioned medium from neural stem cells inhibits glioma cell growth.
Li, Z., Zhong, Q., Liu, H., Liu, P., Wu, J., Ma, D.-N., Chen, X., & Yang, X. (2016) · PubMed · doi:10.14715/cmb/2016.62.12.12 · Cited by 3 · see citing works
Flagged first, then by citations
2 of the 84 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Challenges and Promise for Glioblastoma Treatment through Extracellular Vesicle Inquiry
Liguori, G. L. (2024) · Cells · doi:10.3390/cells13040336 · Cited by 24 · see citing works
Self-citationLiguori, G. L., & Kralj‐Iglič, V. (2023) · Cancers · doi:10.3390/cancers15184425 · Cited by 20 · see citing works
Self-citationRomolo, A., Jan, Z., Bedina Zavec, A., Kisovec, M., Arrigler, V., Spasovski, V., Podobnik, M., Iglič, A., Pocsfalvi, G., Kogej, K., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232415801 · Cited by 19 · see citing works
Self-citationMilk derived extracellular vesicle uptake in human microglia regulates the DNA methylation machinery
Wijenayake, S., Eisha, S., Purohit, M. K., & McGowan, P. O. (2024) · Scientific Reports · doi:10.1038/s41598-024-79724-1 · Cited by 19 · see citing works
D’Antonio, C., & Liguori, G. L. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1441914 · Cited by 9 · see citing works
Self-citationExtracellular Vesicles: Hermes between cancers and lymph nodes
Cao, L., Qiu, Y.-Y., Li, Z., Wang, G.-R., Xiao, Y., Luo, H.-Y., Liu, B., Wu, Q., & Bu, L. (2025) · Cancer Letters · doi:10.1016/j.canlet.2025.217735 · Cited by 7 · see citing works
Modeling Glioblastoma for Translation: Strengths and Pitfalls of Preclinical Studies
D’Antonio, C., & Liguori, G. L. (2025) · Biology · doi:10.3390/biology14111490 · Cited by 7 · see citing works
Self-citationJan, Z., Hočevar, M., Kononenko, V., Michelini, S., Repar, N., Caf, M., Kocjančič, B., Dolinar, D., Kralj, S., Makovec, D., et al. (2023) · Materials · doi:10.3390/ma16093287 · Cited by 6 · see citing works
Self-citationSmall Cellular Particles from European Spruce Needle Homogenate
Jeran, M., Romolo, A., Spasovski, V., Hočevar, M., Novak, U., Štukelj, R., Šuštar, V., Kisovec, M., Zavec, A. B., Kogej, K., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054349 · Cited by 5 · see citing works
Self-citationSpasovski, V., Romolo, A., Zagorc, U., Arrigler, V., Kisovec, M., Zavec, A. B., Arko, M., Molnár, A., Schlosser, G., Iglič, A., et al. (2024) · International Journal of Nanomedicine · doi:10.2147/ijn.s432836 · Cited by 4 · see citing works
Self-citationZhang, X., Zhe, J., Duan, C., Wei, X., He, Z., Shi, C., Yuan, L., Wen, H., Bao, W., & Fan, Q. (2026) · Cell Communication and Signaling · doi:10.1186/s12964-026-02670-0 · Cited by 3 · see citing works
Ejtehadifar, M., Zahedi, S., Gameiro, P., Cabeçadas, J., Rodríguez, M. S., da Silva, M. G., Beck, H. C., Matthiesen, R., & Carvalho, A. S. (2025) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2025.167842 · Cited by 3 · see citing works
Small extracellular vesicles-based drug delivery systems for therapies of gastrointestinal tumours
Luo, L., Wang, D., Xu, W., & Jiang, J. (2025) · Journal of drug targeting · doi:10.1080/1061186x.2025.2535375 · Cited by 2 · see citing works
Cell–Cell Communication and Extracellular Vesicles in Cancer
Lin, L., Zhou, Y., & Hu, K. (2023) · Cancers · doi:10.3390/cancers15092419 · Cited by 2 · see citing works
Short Term Effect of Plant Hybridosomes on Growth of Phaeodactylum Tricornutum Culture
Romolo, A., Hočevar, M., Iglič, A., Bulc, T. G., & Kralj‐Iglič, V. (2023) · Socratic Lectures · doi:10.55295/psl.2023.ii12 · Cited by 1 · see citing works
Self-citationOptimized Wound Healing Assay to Study Extracellular Vesicle-Driven Glioblastoma Cell Migration
D’Antonio, C., Mantile, F., Pocsfalvi, G., & Liguori, G. L. (2026) · Methods and Protocols · doi:10.3390/mps9030081
“[49,50], as previously reported [43].”
InfluentialSelf-citationCRIPTO promotes extracellular vesicle uptake and activation of cancer associated fibroblastsPreprint
Freeman, D. W., Gates, B. L., Spendlove, M. D., Gulbahce, H. E., & Spike, B. T. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.01.583059
Engineered Extracellular Vesicles in Glioma Therapy: Recent Advances and Applications
Xiong, L., Yu, X., Chen, T., Gao, W., Wang, K., Yijin, F., Yin, Y., Zhou, X., Xia, Y., Cui, X., et al. (2026) · International Journal of Nanomedicine · doi:10.2147/ijn.s609673
- Authors
- Mantile, F., Kisovec, M., Adamo, G., Romancino, D. P., Hočevar, M., Božič, D., Bedina Zavec, A., Podobnik, M., Stoppelli, M. P., Kisslinger, A., Bongiovanni, A., Kralj-Iglič, V., & Liguori, G. L.
- Affiliations
- Institute of Genetics and Biophysics (IT)
- National Institute of Chemistry (SI)
- Institute for Biomedical Research and Innovation (IT)
- Institute of Metals and Technology (SI)
- University of Ljubljana (SI)
- Department of Molecular Biology and Nanobiotechnology, National Institute of Chemistry, SI-1000 Ljubljana, Slovenia
- Institute for Experimental Endocrinology and Oncology (IT)
- Faculty of Health Sciences, University of Ljubljana, SI-1000 Ljubljana, Slovenia
- Corresponding author
- Liguori, Giovanna L.
- ORCID
- Venue
- Cancers
- Publisher
- MDPI AG
- Published
- 2022-07-29
- Volume
- 14
- Issue
- 15
- Pages
- 3700
- ISSN
- 2072-6694 (ISSN-L)
- PMC
- PMC9367246
- OpenAlex
- W4289111711
- Cited by
- 18
- References
- 84
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 1
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cancers (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Regione Campania (PO FESR 2014–2020 SATIN, 801338, P3-0388, J1-9162, J3-3066, P2-0132, P1-0391)
- VES4US project (PO FESR 2014–2020 SATIN, 801338, P3-0388, J1-9162, J3-3066, P2-0132, P1-0391)
- Slovenian Research Agency ARRS (PO FESR 2014–2020 SATIN, 801338, P3-0388, J1-9162, J3-3066, P2-0132, P1-0391)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Keywords
- extracellular vesicles, Cripto, glioblastoma, teratocarcinoma cells, cell migration, tumor growth and metastasis, cell proliferation, drug sensitivity, carcinogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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