Clinical Trials Study
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Stem Cells. Jan 26, 2015; 7(1): 223-234
Published online Jan 26, 2015. doi: 10.4252/wjsc.v7.i1.223
Fetal vs adult mesenchymal stem cells achieve greater gene expression, but less osteoinduction
Juan E Santiago-Torres, Rebecca Lovasz, Alicia L Bertone
Juan E Santiago-Torres, Rebecca Lovasz, Alicia L Bertone, Comparative Orthopedic Research Laboratory, Department of Veterinary Clinical Sciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210, United States
Juan E Santiago-Torres, Alicia L Bertone, College of Medicine, The Ohio State University, Columbus, OH 43210, United States
Author contributions: Santiago-Torres JE and Bertone AL designed the research; Santiago-Torres JE and Lovasz R performed the research; Santiago-Torres JE and Bertone AL analyzed the data and wrote the paper.
Supported by The Ohio State University College of Medicine Roessler Research Scholarship (In part); in part by National Cancer Institution of the United States grant No. P30 CA016058 (Our histological examination was performed at The OSU Comparative Pathology and Mouse Phenotyping Shared Resource)
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: Alicia L Bertone, DVM, PhD, Professor, Comparative Orthopedic Research Laboratory, Department of Veterinary Clinical Sciences, College of Veterinary Medicine, The Ohio State University, 601 Tharp St, Columbus, OH 43210, United States. bertone.1@osu.edu
Telephone: +1-614-2927449 Fax: +1-614-6885642
Received: July 31, 2014
Peer-review started: July 31, 2014
First decision: September 28, 2014
Revised: October 14, 2014
Accepted: October 31, 2014
Article in press: December 16, 2014
Published online: January 26, 2015
Processing time: 167 Days and 8 Hours
Abstract

AIM: To investigate adenoviral transduction in mesenchymal stem cells (MSCs) and effects on stemness in vitro and function as a cell therapy in vivo.

METHODS: Bone marrow-derived adult and fetal MSC were isolated from an equine source and expanded in monolayer tissue culture. Polyethylenimine (PEI)-mediated transfection of pcDNA3-eGFP or adenoviral transduction of green fluorescent protein (GFP) was evaluated in fetal MSCs. Adenoviral-mediated transduction was chosen for subsequent experiments. All experiments were carried out at least in triplicate unless otherwise noted. Outcome assessment was obtained by flow cytometry or immunohystochemistry and included transduction efficiency, cell viability, stemness (i.e., cell proliferation, osteogenic and chondrogenic cell differentiation), and quantification of GFP expression. Fetal and adult MSCs were then transduced with an adenoviral vector containing the gene for the bone morphogenic protein 2 (BMP2). In vitro BMP2 expression was assessed by enzyme linked immunosorbent assay. In addition, MSC-mediated gene delivery of BMP2 was evaluated in vivo in an osteoinduction nude mouse quadriceps model. New bone formation was evaluated by microradiography and histology.

RESULTS: PEI provided greater transfection and viability in fetal MSCs than other commercial chemical reagents. Adenoviral transduction efficiency was superior to PEI-mediated transfection of GFP in fetal MSCs (81.3% ± 1.3% vs 35.0% ± 1.6%, P < 0.05) and was similar in adult MSCs (78.1% ± 1.9%). Adenoviral transduction provided significantly greater expression of GFP in fetal than adult MSCs (7.4 ± 0.1 vs 4.4 ± 0.3 millions of mean fluorescence intensity units, P < 0.01) as well as significantly greater in vitro BMP2 expression (0.16 pg/cell-day vs 0.10 pg/cell-day, P < 0.01). Fraction of fetal MSC GFP positive cells decreased significantly faster than adult MSCs (1.15% ± 0.05% vs 11.4% ± 2.1% GFP positive at 2 wk post-transduction, P < 0.05). Cell proliferation and osteogenic differentiation in vitro were not affected by Ad transduction in both fetal and adult MSCs, but fetal MSCs had reduced chondrogenic differentiation in vitro when compared to adult (P < 0.01). Chondrogenic differentiation was also significantly reduced in Ad-GFP transduced cells (P < 0.05). Ad-BMP2 transduced adult MSCs induced new bone formation in more thighs than Ad-BMP2 transduced fetal MSCs (83% vs 17% of the six treated thighs per group, P < 0.05) and resulted in increased femur midshaft diameter due to greater extent of periosteal new bone (1.57 ± 0.35 mm vs 1.27 ± 0.08 mm, P < 0.05).

CONCLUSION: Fetal MSCs may be genetically manipulated ex vivo with adenoviral vectors. Nonetheless, the abbreviated expression of the exogenous gene may limit their applications in vivo.

Keywords: Adenovirus; Bone morphogenic protein 2; Fetal; Green fluorescent protein; Mesenchymal stem cell; Gene transfer technique

Core tip: Fetal mesenchymal stem cells (MSCs) can be genetically manipulated ex vivo with adenoviral vectors without major effects on stemness. Their greater expression of exogenous genes than adult MSCs is promising for MSC-mediated gene therapy. MSC-mediated bone morphogenic protein 2 gene delivery provides osteogenic induction in vivo, which could have clinical applications in bone regeneration. Nonetheless, the abbreviated expression of the exogenous gene provided via adenoviral transduction may limit their applications in vivo.