Cargando…

Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice

BACKGROUND: Neovascularization is necessary for follicular growth. Vascularization is first observed in preantral follicles, and thereafter the vasculature markedly increases in follicles undergoing development. Neovascularization includes angiogenesis and vasculogenesis. Vasculogenesis is the forma...

Descripción completa

Detalles Bibliográficos
Autores principales: Kizuka-Shibuya, Fumie, Tokuda, Nobuko, Takagi, Kiyoshi, Adachi, Yasuhiro, Lee, Lifa, Tamura, Isao, Maekawa, Ryo, Tamura, Hiroshi, Suzuki, Takashi, Owada, Yuji, Sugino, Norihiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3905919/
https://www.ncbi.nlm.nih.gov/pubmed/24444000
http://dx.doi.org/10.1186/1757-2215-7-10
_version_ 1782301406690017280
author Kizuka-Shibuya, Fumie
Tokuda, Nobuko
Takagi, Kiyoshi
Adachi, Yasuhiro
Lee, Lifa
Tamura, Isao
Maekawa, Ryo
Tamura, Hiroshi
Suzuki, Takashi
Owada, Yuji
Sugino, Norihiro
author_facet Kizuka-Shibuya, Fumie
Tokuda, Nobuko
Takagi, Kiyoshi
Adachi, Yasuhiro
Lee, Lifa
Tamura, Isao
Maekawa, Ryo
Tamura, Hiroshi
Suzuki, Takashi
Owada, Yuji
Sugino, Norihiro
author_sort Kizuka-Shibuya, Fumie
collection PubMed
description BACKGROUND: Neovascularization is necessary for follicular growth. Vascularization is first observed in preantral follicles, and thereafter the vasculature markedly increases in follicles undergoing development. Neovascularization includes angiogenesis and vasculogenesis. Vasculogenesis is the formation of new blood vessels by bone marrow-derived endothelial progenitor cells. It is unclear whether vasculogenesis occurs during follicular growth. Blood vessels must be mature to be functional blood vessels. Mature blood vessels are characterized by the recruitment of pericytes. However, it is unclear where pericytes come from and whether they contribute to neovascularization in the follicle during follicular growth. In this study, we investigated whether bone marrow-derived progenitor cells that differentiate into vascular endothelial cells or pericytes contribute to neovascularization during follicular growth. METHODS: A parabiosis model was used in this study. Six-week-old wild-type and transgenic female mice expressing green fluorescent protein (GFP) were conjoined between the lateral abdominal regions to create a shared circulatory system. After 6 weeks, the ovaries were obtained and immunostained for CD31/CD34 (a vascular endothelial cell marker), platelet-derived growth factor receptor-β (PDGFR-β) (a pericyte marker), and GFP (a bone marrow-derived cell marker). RESULTS: Cells that were positive for CD34 and PDGFR-β were observed in the stroma adjacent to the primary or early preantral follicles and in the theca cell layer of the follicles from the late preantral stage to the preovulatory stage. CD31/CD34 and GFP double-positive cells were observed in the theca cell layer of the follicle from the antral stage to the preovulatory stage while the number of double-positive cells in the preovulatory follicles did not increase. PDGFR-β and GFP double-positive cells were observed in the theca cell layer of the preovulatory follicle but not in the smaller follicle. CONCLUSIONS: Locally existing endothelial cells and pericytes in the stroma play a central role in the neovascularization during follicular growth, while bone marrow-derived endothelial cells and pericytes partially contribute to this process.
format Online
Article
Text
id pubmed-3905919
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-39059192014-01-30 Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice Kizuka-Shibuya, Fumie Tokuda, Nobuko Takagi, Kiyoshi Adachi, Yasuhiro Lee, Lifa Tamura, Isao Maekawa, Ryo Tamura, Hiroshi Suzuki, Takashi Owada, Yuji Sugino, Norihiro J Ovarian Res Research BACKGROUND: Neovascularization is necessary for follicular growth. Vascularization is first observed in preantral follicles, and thereafter the vasculature markedly increases in follicles undergoing development. Neovascularization includes angiogenesis and vasculogenesis. Vasculogenesis is the formation of new blood vessels by bone marrow-derived endothelial progenitor cells. It is unclear whether vasculogenesis occurs during follicular growth. Blood vessels must be mature to be functional blood vessels. Mature blood vessels are characterized by the recruitment of pericytes. However, it is unclear where pericytes come from and whether they contribute to neovascularization in the follicle during follicular growth. In this study, we investigated whether bone marrow-derived progenitor cells that differentiate into vascular endothelial cells or pericytes contribute to neovascularization during follicular growth. METHODS: A parabiosis model was used in this study. Six-week-old wild-type and transgenic female mice expressing green fluorescent protein (GFP) were conjoined between the lateral abdominal regions to create a shared circulatory system. After 6 weeks, the ovaries were obtained and immunostained for CD31/CD34 (a vascular endothelial cell marker), platelet-derived growth factor receptor-β (PDGFR-β) (a pericyte marker), and GFP (a bone marrow-derived cell marker). RESULTS: Cells that were positive for CD34 and PDGFR-β were observed in the stroma adjacent to the primary or early preantral follicles and in the theca cell layer of the follicles from the late preantral stage to the preovulatory stage. CD31/CD34 and GFP double-positive cells were observed in the theca cell layer of the follicle from the antral stage to the preovulatory stage while the number of double-positive cells in the preovulatory follicles did not increase. PDGFR-β and GFP double-positive cells were observed in the theca cell layer of the preovulatory follicle but not in the smaller follicle. CONCLUSIONS: Locally existing endothelial cells and pericytes in the stroma play a central role in the neovascularization during follicular growth, while bone marrow-derived endothelial cells and pericytes partially contribute to this process. BioMed Central 2014-01-21 /pmc/articles/PMC3905919/ /pubmed/24444000 http://dx.doi.org/10.1186/1757-2215-7-10 Text en Copyright © 2014 Kizuka-Shibuya et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Kizuka-Shibuya, Fumie
Tokuda, Nobuko
Takagi, Kiyoshi
Adachi, Yasuhiro
Lee, Lifa
Tamura, Isao
Maekawa, Ryo
Tamura, Hiroshi
Suzuki, Takashi
Owada, Yuji
Sugino, Norihiro
Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice
title Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice
title_full Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice
title_fullStr Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice
title_full_unstemmed Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice
title_short Locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice
title_sort locally existing endothelial cells and pericytes in ovarian stroma, but not bone marrow-derived vascular progenitor cells, play a central role in neovascularization during follicular development in mice
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3905919/
https://www.ncbi.nlm.nih.gov/pubmed/24444000
http://dx.doi.org/10.1186/1757-2215-7-10
work_keys_str_mv AT kizukashibuyafumie locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT tokudanobuko locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT takagikiyoshi locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT adachiyasuhiro locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT leelifa locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT tamuraisao locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT maekawaryo locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT tamurahiroshi locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT suzukitakashi locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT owadayuji locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice
AT suginonorihiro locallyexistingendothelialcellsandpericytesinovarianstromabutnotbonemarrowderivedvascularprogenitorcellsplayacentralroleinneovascularizationduringfolliculardevelopmentinmice