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Extracellular vesicles from endothelial progenitor cells promote thyroid follicle formation.

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Degosserie, Jonathan [UCL] Heymans, Charlotte [UCL] Spourquet, Catherine [UCL] Halbout, Mathias [UCL] D'Auria, Ludovic [UCL] Van Der Smissen, Patrick [UCL] Vertommen, Didier [UCL] Courtoy, Pierre J. [UCL] Tyteca, Donatienne [UCL] Pierreux, Christophe [UCL]

Organogenesis is a complex and dynamic process requiring reciprocal communication between different cell types. In the thyroid, thyrocyte progenitors secrete the angiocrine factor, VEGFA, to recruit endothelial cells. In return, endothelial cells promote thyrocyte organisation into spherical follicular structures, which are responsible for thyroid hormone synthesis and storage. Medium conditioned by endothelial progenitor cells (EPCs) can promote follicle formation and lumen expansion (i.e. folliculogenesis) in an culture system of thyroid lobes. Here, we postulated that endothelial cells instruct thyrocyte progenitors by producing extracellular vesicles (EVs). We found that medium conditioned by EPCs contain EVs with exosomal characteristics and that these vesicles can be incorporated into thyrocyte progenitors. By mass spectrometry, laminin peptides were abundantly identified in the EV preparations, probably co-sedimenting with EVs. Laminin-α1 silencing in EPC abrogated the folliculogenic effect of EVs. However, density gradient separation of EVs from laminins revealed that both EV-rich and laminin-rich fractions exhibited folliculogenic activity. In conclusion, we suggest that endothelial cells can produce EVs favouring thyrocyte organisation into follicles and lumen expansion, a mechanism promoted by laminin-α1.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2018
Language Anglais
Journal information "Journal of Extracellular Vesicles" - Vol. 7, no.1, p. 1487250 [1-12] (2018)
Peer reviewed yes
Publisher Taylor & Francis ((United States) Philadelphia, PA)
e-issn 2001-3078
Publication status Publié
Affiliations UCL - SSS/DDUV/BCHM - Biochimie-Recherche métabolique
UCL - SSS/DDUV/CELL - Biologie cellulaire
UCL - SSS/DDUV/PHOS - Protein phosphorylation
UCL - SSS/IONS/CEMO - Pôle Cellulaire et moléculaire
Keywords Thyroid ; endothelial cells ; extracellular vesicles ; folliculogenesis ; laminins
Links
  1. Fagman Henrik, Andersson Louise, Nilsson Mikael, The developing mouse thyroid: Embryonic vessel contacts and parenchymal growth pattern during specification, budding, migration, and lobulation, 10.1002/dvdy.20653
  2. Colin Ides M., Denef Jean-François, Lengelé Benoit, Many Marie-Christine, Gérard Anne-Catherine, Recent Insights into the Cell Biology of Thyroid Angiofollicular Units, 10.1210/er.2012-1015
  3. Nilsson Mikael, Fagman Henrik, Development of the thyroid gland, 10.1242/dev.145615
  4. Hick Anne-Christine, Delmarcelle Anne-Sophie, Bouquet Mahé, Klotz Sabrina, Copetti Tamara, Forez Celine, Van Der Smissen Patrick, Sonveaux Pierre, Collet Jean-François, Feron Olivier, Courtoy Pierre J., Pierreux Christophe E., Reciprocal epithelial:endothelial paracrine interactions during thyroid development govern follicular organization and C-cells differentiation, 10.1016/j.ydbio.2013.04.022
  5. Villacorte Mylah, Delmarcelle Anne-Sophie, Lernoux Manon, Bouquet Mahé, Lemoine Pascale, Bolsée Jennifer, Umans Lieve, de Sousa Lopes Susana Chuva, Van Der Smissen Patrick, Sasaki Takako, Bommer Guido, Henriet Patrick, Refetoff Samuel, Lemaigre Frédéric P., Zwijsen An, Courtoy Pierre J., Pierreux Christophe E., Thyroid follicle development requires Smad1/5- and endothelial cell-dependent basement membrane assembly, 10.1242/dev.134171
  6. Raposo Graça, Stoorvogel Willem, Extracellular vesicles: Exosomes, microvesicles, and friends, 10.1083/jcb.201211138
  7. Pan Bin-Tao, Johnstone Rose M., Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor, 10.1016/0092-8674(83)90040-5
  8. Harding C., Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes, 10.1083/jcb.97.2.329
  9. Raposo G., B lymphocytes secrete antigen-presenting vesicles, 10.1084/jem.183.3.1161
  10. Valadi Hadi, Ekström Karin, Bossios Apostolos, Sjöstrand Margareta, Lee James J, Lötvall Jan O, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, 10.1038/ncb1596
  11. Yáñez-Mó María, Siljander Pia R.-M., Andreu Zoraida, Bedina Zavec Apolonija, Borràs Francesc E., Buzas Edit I., Buzas Krisztina, Casal Enriqueta, Cappello Francesco, Carvalho Joana, Colás Eva, Cordeiro-da Silva Anabela, Fais Stefano, Falcon-Perez Juan M., Ghobrial Irene M., Giebel Bernd, Gimona Mario, Graner Michael, Gursel Ihsan, Gursel Mayda, Heegaard Niels H. H., Hendrix An, Kierulf Peter, Kokubun Katsutoshi, Kosanovic Maja, Kralj-Iglic Veronika, Krämer-Albers Eva-Maria, Laitinen Saara, Lässer Cecilia, Lener Thomas, Ligeti Erzsébet, Linē Aija, Lipps Georg, Llorente Alicia, Lötvall Jan, Manček-Keber Mateja, Marcilla Antonio, Mittelbrunn Maria, Nazarenko Irina, Nolte-‘t Hoen Esther N.M., Nyman Tuula A., O'Driscoll Lorraine, Olivan Mireia, Oliveira Carla, Pállinger Éva, del Portillo Hernando A., Reventós Jaume, Rigau Marina, Rohde Eva, Sammar Marei, Sánchez-Madrid Francisco, Santarém N., Schallmoser Katharina, Stampe Ostenfeld Marie, Stoorvogel Willem, Stukelj Roman, Van der Grein Susanne G., Helena Vasconcelos M., Wauben Marca H. M., De Wever Olivier, Biological properties of extracellular vesicles and their physiological functions, 10.3402/jev.v4.27066
  12. Meehan Brian, Rak Janusz, Di Vizio Dolores, Oncosomes – large and small: what are they, where they came from?, 10.3402/jev.v5.33109
  13. Tkach Mercedes, Théry Clotilde, Communication by Extracellular Vesicles: Where We Are and Where We Need to Go, 10.1016/j.cell.2016.01.043
  14. Hayashi Toru, Lombaert Isabelle M.A., Hauser Belinda R., Patel Vaishali N., Hoffman Matthew P., Exosomal MicroRNA Transport from Salivary Mesenchyme Regulates Epithelial Progenitor Expansion during Organogenesis, 10.1016/j.devcel.2016.12.001
  15. Van Deun Jan, , Mestdagh Pieter, Agostinis Patrizia, Akay Özden, Anand Sushma, Anckaert Jasper, Martinez Zoraida Andreu, Baetens Tine, Beghein Els, Bertier Laurence, Berx Geert, Boere Janneke, Boukouris Stephanie, Bremer Michel, Buschmann Dominik, Byrd James B, Casert Clara, Cheng Lesley, Cmoch Anna, Daveloose Delphine, De Smedt Eva, Demirsoy Seyma, Depoorter Victoria, Dhondt Bert, Driedonks Tom A P, Dudek Aleksandra, Elsharawy Abdou, Floris Ilaria, Foers Andrew D, Gärtner Kathrin, Garg Abhishek D, Geeurickx Edward, Gettemans Jan, Ghazavi Farzaneh, Giebel Bernd, Kormelink Tom Groot, Hancock Grace, Helsmoortel Hetty, Hill Andrew F, Hyenne Vincent, Kalra Hina, Kim David, Kowal Joanna, Kraemer Sandra, Leidinger Petra, Leonelli Carina, Liang Yaxuan, Lippens Lien, Liu Shu, Lo Cicero Alessandra, Martin Shaun, Mathivanan Suresh, Mathiyalagan Prabhu, Matusek Támas, Milani Gloria, Monguió-Tortajada Marta, Mus Liselot M, Muth Dillon C, Németh Andrea, Nolte-'t Hoen Esther N M, O'Driscoll Lorraine, Palmulli Roberta, Pfaffl Michael W, Primdal-Bengtson Bjarke, Romano Erminia, Rousseau Quentin, Sahoo Susmita, Sampaio Natalia, Samuel Monisha, Scicluna Benjamin, Soen Bieke, Steels Anneleen, Swinnen Johannes V, Takatalo Maarit, Thaminy Safia, Théry Clotilde, Tulkens Joeri, Van Audenhove Isabel, van der Grein Susanne, Van Goethem Alan, van Herwijnen Martijn J, Van Niel Guillaume, Van Roy Nadine, Van Vliet Alexander R, Vandamme Niels, Vanhauwaert Suzanne, Vergauwen Glenn, Verweij Frederik, Wallaert Annelynn, Wauben Marca, Witwer Kenneth W, Zonneveld Marijke I, De Wever Olivier, Vandesompele Jo, Hendrix An, EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research, 10.1038/nmeth.4185
  16. Delmarcelle AS, J Vis Exp, 6, 88 (2014)
  17. Pierreux Christophe E., Poll Aurélie V., Kemp Caroline R., Clotman Frédéric, Maestro Miguel A., Cordi Sabine, Ferrer Jorge, Leyns Luc, Rousseau Guy G., Lemaigre Frédéric P., The Transcription Factor Hepatocyte Nuclear Factor-6 Controls the Development of Pancreatic Ducts in the Mouse, 10.1053/j.gastro.2005.12.005
  18. Hatzopoulos AK, Development, 125, 1457 (1998)
  19. Kowal Joanna, Arras Guillaume, Colombo Marina, Jouve Mabel, Morath Jakob Paul, Primdal-Bengtson Bjarke, Dingli Florent, Loew Damarys, Tkach Mercedes, Théry Clotilde, Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes, 10.1073/pnas.1521230113
  20. Cominelli Antoine, Gaide Chevronnay Héloïse P., Lemoine Pascale, Courtoy Pierre J., Marbaix Etienne, Henriet Patrick, Matrix metalloproteinase-27 is expressed in CD163+/CD206+ M2 macrophages in the cycling human endometrium and in superficial endometriotic lesions, 10.1093/molehr/gau034
  21. Tyteca D., D'Auria L., Der Smissen P. Van, Medts T., Carpentier S., Monbaliu J.C., de Diesbach P., Courtoy P.J., Three unrelated sphingomyelin analogs spontaneously cluster into plasma membrane micrometric domains, 10.1016/j.bbamem.2010.01.021
  22. Théry C, Curr Protoc Cell Biol (2006)
  23. Witwer Kenneth W., Buzás Edit I., Bemis Lynne T., Bora Adriana, Lässer Cecilia, Lötvall Jan, Nolte-‘t Hoen Esther N., Piper Melissa G., Sivaraman Sarada, Skog Johan, Théry Clotilde, Wauben Marca H., Hochberg Fred, Standardization of sample collection, isolation and analysis methods in extracellular vesicle research, 10.3402/jev.v2i0.20360
  24. Lötvall Jan, Hill Andrew F., Hochberg Fred, Buzás Edit I., Di Vizio Dolores, Gardiner Christopher, Gho Yong Song, Kurochkin Igor V., Mathivanan Suresh, Quesenberry Peter, Sahoo Susmita, Tahara Hidetoshi, Wauben Marca H., Witwer Kenneth W., Théry Clotilde, Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles, 10.3402/jev.v3.26913
  25. Suzuki Keiji, Mitsutake Norisato, Saenko Vladimir, Suzuki Masatoshi, Matsuse Michiko, Ohtsuru Akira, Kumagai Atsushi, Uga Tatsuya, Yano Hiroshi, Nagayama Yuji, Yamashita Shunichi, Dedifferentiation of Human Primary Thyrocytes into Multilineage Progenitor Cells without Gene Introduction, 10.1371/journal.pone.0019354
  26. Lässer C, J Vis Exp, 9, e3037 (2012)
  27. Lobb Richard J., Becker Melanie, Wen Wen Shu, Wong Christina S. F., Wiegmans Adrian P., Leimgruber Antoine, Möller Andreas, Optimized exosome isolation protocol for cell culture supernatant and human plasma, 10.3402/jev.v4.27031
  28. Gardiner Chris, Vizio Dolores Di, Sahoo Susmita, Théry Clotilde, Witwer Kenneth W., Wauben Marca, Hill Andrew F., Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey, 10.3402/jev.v5.32945
  29. Bobrie A., Krumeich S., Reyal F., Recchi C., Moita L. F., Seabra M. C., Ostrowski M., Thery C., Rab27a Supports Exosome-Dependent and -Independent Mechanisms That Modify the Tumor Microenvironment and Can Promote Tumor Progression, 10.1158/0008-5472.can-12-0925
  30. Zabeo Davide, Cvjetkovic Aleksander, Lässer Cecilia, Schorb Martin, Lötvall Jan, Höög Johanna L, Exosomes purified from a single cell type have diverse morphology, 10.1080/20013078.2017.1329476
  31. Willms Eduard, Johansson Henrik J., Mäger Imre, Lee Yi, Blomberg K. Emelie M., Sadik Mariam, Alaarg Amr, Smith C.I. Edvard, Lehtiö Janne, EL Andaloussi Samir, Wood Matthew J.A., Vader Pieter, Cells release subpopulations of exosomes with distinct molecular and biological properties, 10.1038/srep22519
  32. Barington Maria, Brorson Marianne Møller, Hofman-Bang Jacob, Rasmussen Åse Krogh, Holst Birgitte, Feldt-Rasmussen Ulla, Ghrelin-mediated inhibition of the TSH-stimulated function of differentiated human thyrocytes ex vivo, 10.1371/journal.pone.0184992
  33. Roucourt Bart, Meeussen Sofie, Bao Jie, Zimmermann Pascale, David Guido, Heparanase activates the syndecan-syntenin-ALIX exosome pathway, 10.1038/cr.2015.29
Bibliographic reference Degosserie, Jonathan ; Heymans, Charlotte ; Spourquet, Catherine ; Halbout, Mathias ; D'Auria, Ludovic ; et. al. Extracellular vesicles from endothelial progenitor cells promote thyroid follicle formation.. In: Journal of Extracellular Vesicles, Vol. 7, no.1, p. 1487250 [1-12] (2018)
Permanent URL http://hdl.handle.net/2078.1/200505