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The ectonucleoside triphosphate diphosphohydrolase-2 (NTPDase2) in human endometrium: a novel marker of basal stroma and mesenchymal stem cells

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Abstract

The human endometrium undergoes repetitive regeneration cycles in order to recover the functional layer, shed during menses. The basal layer, which remains in charge of endometrial regeneration in every cycle, contains adult stem or progenitor cells of epithelial and mesenchymal lineage. Some pathologies such as adenomyosis, in which endometrial tissue develops within the myometrium, originate from this layer. It is well known that the balance between adenosine triphosphate (ATP) and adenosine plays a crucial role in stem/progenitor cell physiology, influencing proliferation, differentiation, and migration. The extracellular levels of nucleotides and nucleosides are regulated by the ectonucleotidases, such as the nucleoside triphosphate diphosphohydrolase 2 (NTPDase2). NTPDase2 is a membrane-expressed enzyme found in cells of mesenchymal origin such as perivascular cells of different tissues and the stem cells of adult neurogenic regions. The aim of this study was to characterize the expression of NTPDase2 in human nonpathological cyclic and postmenopausic endometria and in adenomyosis. We examined proliferative, secretory, and atrophic endometria from women without endometrial pathology and also adenomyotic lesions. Importantly, we identified NTPDase2 as the first marker of basal endometrium since other stromal cell markers such as CD10 label the entire stroma. As expected, NTPDase2 was also found in adenomyotic stroma, thus becoming a convenient tracer of these lesions. We did not record any changes in the expression levels or the localization of NTPDase2 along the cycle, thus suggesting that the enzyme is not influenced by the female sex hormones like other previously studied ectoenzymes. Remarkably, NTPDase2 was expressed by the Sushi Domain containing 2 (SUSD2)+ endometrial mesenchymal stem cells (eMSCs) found perivascularly, rendering it useful as a cell marker to improve the isolation of eMSCs needed for regenerative medicine therapies.

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Acknowledgments

This study was supported by a grant from the Instituto de Salud Carlos III (FIS PI15/00036), co-funded by FEDER funds/European Regional Development Fund (ERDF)-“a Way to Build Europe”-//FONDOS FEDER “una manera de hacer Europa,” and a grant from the Fundación Merck Salud (Ayuda Merck de Investigación 2016-Fertilidad). ARM was awarded a fellowship from the Asociación Española Contra el Cáncer (AECC). JS received support from the Canadian Institutes of Health Research (CIHR) and was the recipient of a “Chercheur National” research award from the Fonds de recherche du Québec – Santé (FRQS). We thank CERCA Programme (Generalitat de Catalunya) for institutional support. We are grateful to Inmaculada Gómez de Aranda for technical support and to Benjamín Torrejón of Serveis Científics I Tecnològics (Campus Bellvitge, Universitat de Barcelona). The authors thank Tom Yohannan for language editing.

Funding

This study was funded by Instituto de Salud Carlos III (grant number FIS PI15/00036); FEDER funds/European Regional Development Fund (ERDF)-“a Way to Build Europe”; Fundación Merck Salud (Ayuda Merck de Investigación 2016-Fertilidad).

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Authors and Affiliations

  1. Departament de Patologia i Terapèutica Experimental, Facultat de Medicina i Ciències de la Salut, Campus Bellvitge, Universitat de Barcelona, Barcelona, Spain

    Carla Trapero, August Vidal, Aitor Rodríguez-Martínez & Mireia Martín-Satué

  2. Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Oncobell Program, CIBERONC, Barcelona, Spain

    Carla Trapero, August Vidal, Aitor Rodríguez-Martínez, Jordi Ponce, Xavier Matias-Guiu & Mireia Martín-Satué

  3. Servei d’Anatomia Patològica, Hospital Universitari de Bellvitge, Barcelona, Spain

    August Vidal & Xavier Matias-Guiu

  4. Centre de Recherche du CHU de Québec, Université Laval, Québec City, QC, Canada

    Jean Sévigny

  5. Départment de Microbiologie-Infectiologie et d’Immunologie, Faculté de Médecine, Université Laval, Quebec City, QC, Canada

    Jean Sévigny

  6. Servei de Ginecologia, Hospital Universitari de Bellvitge, Barcelona, Spain

    Jordi Ponce

  7. Hospital Universitari Quiron Dexeus, Salud de la Mujer Dexeus, Barcelona, Spain

    Buenaventura Coroleu

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  1. Carla Trapero
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Suppl. Fig. 1

Immunolocalization of NTPDase2 in human proliferative (A), secretory (B), and atrophic (C) endometrium. Stroma is labelled in the three cases although labelling is restricted to basal layer in cyclic endometria (A, B). NTPDase2 antibodies used were ALX-215-045 from Enzo (A, C) and H9s from http://ectonucleotidases-ab.com (B). Scale bars 400 μm (A), 300 μm (B), and 100 μm (C) (PNG 2943 kb)

High Resolution Image (TIF 8501 kb) (PNG 1128 kb)

Suppl. Fig. 2

Confocal fluorescence images of some vessels of human atrophic endometrium labeled with NTPDase2 (A), CD146 (B), and PDGFRβ (C). Merged image shows a more external position of NTPDase2+ cells than CD146- and PDGFRβ-positive cells in the perivascular region (D). NTPDase2 antibody used was H9s from http://ectonucleotidases-ab.com. Scale bar 25 μm (D) (PNG 1128 kb) (JPG 216 kb)

High Resolution Image (TIF 6.40 mb) (PNG 1.10 mb)

Suppl. Fig. 3

Confocal fluorescence images of endometrial blood vessels labeled with PECAM-1 (CD31) and NTPDase1 (CD39). Endothelial cells labelled with CD31 (A, E) are also positive for NTPDase1 (B, F) as shown in merge images (D, H). Scale bars 20 μm (PNG 1.01 mb)

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Trapero, C., Vidal, A., Rodríguez-Martínez, A. et al. The ectonucleoside triphosphate diphosphohydrolase-2 (NTPDase2) in human endometrium: a novel marker of basal stroma and mesenchymal stem cells. Purinergic Signalling 15, 225–236 (2019). https://doi.org/10.1007/s11302-019-09656-3

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