Basic Study
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Transl Med. Dec 12, 2015; 4(3): 113-122
Published online Dec 12, 2015. doi: 10.5528/wjtm.v4.i3.113
Pro- vs anti-stenotic capacities of type-I vs type-II human induced pluripotent-derived endothelial cells
Miwako Nishio, Masako Nakahara, Koichi Saeki, Katsuhito Fujiu, Hiroshi Iwata, Ichiro Manabe, Akira Yuo, Kumiko Saeki
Miwako Nishio, Masako Nakahara, Akira Yuo, Kumiko Saeki, Department of Disease Control, Research Institute, National Center for Global Health and Medicine, Tokyo 162-8655, Japan
Koichi Saeki, Section of Cell Engineering, Department of Basic Research, DNAVEC Center, ID Pharma Co., Ltd., Ibaraki 300-2611, Japan
Katsuhito Fujiu, Hiroshi Iwata, Ichiro Manabe, Department of Cardiovascular Medicine, Graduate School of Medicine, the University of Tokyo, Tokyo 113-8654, Japan
Katsuhito Fujiu, Translational Systems Biology and Medicine Initiative, the University of Tokyo, Tokyo 113-8654, Japan
Katsuhito Fujiu, Kumiko Saeki, PRESTO, Japan Science and Technology Agency, Saitama 332-0012, Japan
Author contributions: Nishio M and Nakahara M performed the experiments and analyzed the data; Saeki K contributed to the establishment of human iPS cells; Fujiu K, Iwata H, Manabe I and Yuo A coordinated the research; Saeki K designed the research and wrote the paper.
Supported by Grant-in-Aid from the Ministry of Health, Labour and Welfare of Japan (KHD1017); and by that from JST, PRESTO.
Institutional review board statement: All experiments including gene recombination experiments and animal experiments were performed after we had obtained permission from the review board of National Center for Global Health and Medicine.
Institutional animal care and use committee statement: All procedures involving animals were reviewed and approved by the Institutional Animal Care and Use Committee of Research Institute, National Center for Global Health and Medicine, Tokyo, Japan (Authorization No. 15014).
Conflict-of-interest statement: None of the authors has any potential financial conflict of interest related to this manuscript.
Data sharing statement: Technical appendix and dataset are available from the corresponding author (saeki@ri.ncgm.go.jp).
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Kumiko Saeki, MD, PhD, Division Chief, Department of Disease Control, Research Institute, National Center for Global Health and Medicine, 1-21-1 Toyama Shinjukuiku, Tokyo 162-8655, Japan. saeki@ri.ncgm.go.jp
Telephone: +81-3-32027181 Fax: +81-3-32027364
Received: June 23, 2015
Peer-review started: June 29, 2015
First decision: August 25, 2015
Revised: October 16, 2015
Accepted: November 10, 2015
Article in press: November 11, 2015
Published online: December 12, 2015
Processing time: 175 Days and 0.4 Hours
Abstract

AIM: To verify in vivo relevance of the categorization of human vascular endothelial cells (VECs) into type-I (pro-proliferative) and type-II (anti-proliferative).

METHODS: Endothelial layers of murine femoral arteries were removed by wire injury (WI) operation, a common technique to induce arteriostenosis. Type-I and type-II VECs produced from human induced pluripotent stem cells (iPSCs), whose characters were previously determined by their effects on the proliferation of vascular smooth muscle cells in in vitro co-culture experiments, were mixed with Matrigel® Matrix. The mixtures were injected into subcutaneous spaces around WI-operated femoral arteries for the transplanted human iPSC-derived VECs (iPSdECs) to take a route to the luminal surface via vasa vasorum, a nutrient microvessel for larger arteries. Histologies of the femoral arteries were examined over time. The presence of human iPSdECs was checked by immunostaining studies using an antibody that specifically recognizes human VECs. Degrees of stenosis of the femoral arteries were calculated after three weeks. To determine the optimal experimental condition, xenotransplantation experiments were performed under various conditions using immunocompromised mice as well as immunocompetent mice with or without administration of immunosuppressants.

RESULTS: Because immunocompromised mice showed unexpected resistance to WI-induced arteriostenosis, we performed xenotransplantation experiments using immunocompetent mice along with immunosuppressant administrations. After one week, luminal surfaces of the WI-operated arteries were completely covered by human iPSdECs, showing the efficacy of our novel transplantation technique. After three weeks, type-I-iPSdECs-transplanted arteries underwent total stenosis, while type-II-iPSdECs-transplanted arteries remained intact. However, untransplanted arteries of immunosuppressant-treated mice also remained intact by unknown reasons. We found that transplanted human VECs had already been replaced by murine endothelial cells by this time, indicating that a transient existence of human type-II-iPSdECs on arterial luminal surfaces can sufficiently prevent the development of stenosis. Thus, we re-performed xenotransplantation experiments using immunocompetent mice without administrating immunosuppressants and found that arteriostenosis was accelerated or prevented by transplantation of type-I or type-II iPSdECs, respectively. Similar results were obtained from the experiments using human embryonic stem cell-derived VECs at early passages (i.e., type-II) and late passages (i.e., type-I).

CONCLUSION: Pro- and anti-stenosis capacities of type-I and type-II human iPSdECs were verified, respectively, promising a therapeutic application of allogenic iPSdECs.

Keywords: Vascular endothelial cells; Vasa vasorum; Arteriostenosis; Wire injury; Human induced pluripotent stem cells

Core tip: We previously reported that human vascular endothelial cells (VECs) were classified into two categories by their in vitro effects on the proliferation of vascular smooth muscle cells: Pro-proliferative VECs (type-I) and anti-proliferative VECs (type-II). Applying our new technique to transplant human VECs onto the luminal surface of endothelial layer-removed murine arteries, the in vivo relevance of the concept for VEC categorization was validated. Transplantation of pro-proliferative VECs (type-I) resulted in total stenosis while that of anti-proliferative VECs (type-II) completely blocked the development of arteriostenosis. Thus, pro-stenosis (type-I) and anti-stenotic (type-II) capacities were verified in vivo.