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A New Method for Xenogeneic Bone Graft Deproteinization: Comparative Study of Radius Defects in a Rabbit Model

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A New Method for Xenogeneic Bone Graft Deproteinization: Comparative Study of Radius Defects in a Rabbit Model RESEARCH ARTICLE A New Method for Xenogeneic Bone Graft Deproteinization: Comparative Study of Radius Defects in a Rabbit Model Pengfei Lei1, Rongxin Sun2, Long Wang1, Jialin Zhou3, Lifei Wan4, Tianjian Zhou5, Yihe Hu1* 1 Department of Orthopedics, Xiangya Hospital, Central South University, Changsha, China, 2 Department of Orthopedics, The Sixth Affiliated Hospital of Xinjiang Medical University, Urumqi, China, 3 Department of Orthopedics, Thoracic hospital of Hunan province, Changsha, China, 4 Department of Orthopedics, Ningxiang People’s Hospital, Ningxiang, China, 5 Department of Orthopedics, The First People’s Hospital of Shenzhen, Shenzhen, China * [email protected] Abstract OPEN ACCESS Background and Objectives Citation: Lei P, Sun R, Wang L, Zhou J, Wan L, Zhou T, et al. (2015) A New Method for Xenogeneic Bone Deproteinization is an indispensable process for the elimination of antigenicity in xenograft Graft Deproteinization: Comparative Study of Radius bones. However, the hydrogen peroxide (H2O2) deproteinized xenograft, which is com- Defects in a Rabbit Model. PLoS ONE 10(12): monly used to repair bone defect, exhibits limited osteoinduction activity. The present study e0146005. doi:10.1371/journal.pone.0146005 was designed to develop a new method for deproteinization and compare the osteogenic Editor: James Cray, Medical University of South capacities of new pepsin deproteinized xenograft bones with those of conventional H2O2 Carolina, UNITED STATES deproteinized ones. Received: March 15, 2015 Accepted: December 12, 2015 Methods Published: December 31, 2015 Bones were deproteinized in H2O2 or pepsin for 8 hours. The morphologies were compared Copyright: © 2015 Lei et al. This is an open access by HE staining. The content of protein and collagen I were measured by the Kjeldahl method article distributed under the terms of the Creative and HPLC-MS, respectively. The physical properties were evaluated by SEM and mechani- Commons Attribution License, which permits cal tests. For in vivo study, X-ray, micro-CT and HE staining were employed to monitor the unrestricted use, distribution, and reproduction in any medium, provided the original author and source are healing processes of radius defects in rabbit models transplanted with different graft credited. materials. Data Availability Statement: All relevant data are in the paper and Supporting Information files. Results Funding: This work was supported by Hunan Compared with H2O2 deproteinized bones, no distinct morphological and physical changes Provincial Foundation for Science and Technology Planning Project (2011FJ6085) to YH, Hunan were observed. However, pepsin deproteinized bones showed a lower protein content, and Provincial Innovation Foundation for Postgraduates a higher collagen content were preserved. In vivo studies showed that pepsin deproteinized (CX2014B072) to PL and The Open-End Fund for the bones exhibited better osteogenic performance than H2O2 deproteinized bones, moreover, Valuable and Precision Instruments of Central South the quantity and quality of the newly formed bones were improved as indicated by micro-CT University (CSUZC2014046) to YH. The funders had no role in study design, data collection and analysis, analysis. From the results of histological examination, the newly formed bones in the pepsin decision to publish, or preparation of the manuscript. group were mature bones. PLOS ONE | DOI:10.1371/journal.pone.0146005 December 31, 2015 1/17 Pepsin for Xenogeneic Bone Graft Deproteinization Competing Interests: The authors have declared Conclusions that no competing interests exist. Pepsin deproteinized xenograft bones show advantages over conventional H2O2 deprotei- nized bones with respect to osteogenic capacity; this new method may hold potential clinical value in the development of new biomaterials for bone grafting. Introduction Bone grafting, as one of the preferred therapeutic methods for long bone defects caused by trauma, infection and tumor resection, can be classified into autogenic and xenogenic grafting based on the sources of the implant materials. Although autogenic bone grafting exhibits a dis- tinct therapeutic effect, its application is greatly limited due to the lack of sufficient bone and the secondary injury to donor sites caused by surgery. Therefore, the drawbacks and limitations make it urgent to explore and develop new biomaterials for bone transplantation. Fortunately, bones from other species possess a tissue structure similar to that of human bones. In addition, these bones also exhibit osteoinduction and osteoconduction activities, potentially satisfying the requirements of ideal bone graft substitutes. Xenogenic bone grafting overcomes the obstacles of autogenic grafting, but also faces the potential risks of inducing an immune response and trans- mitting infectious diseases in patients [1, 2]. Thus, valid strategies to eliminate the antigenicity of xenograft bones are of vital importance in the development of xenogenic bone graft substitutes. Eliminating the antigens that potentially cause an immune response is a prerequisite for xeno- genicbonegrafting.MHC-IandMHC-IIarethe main sources of antigens which induce an immune response in bone grafting, and they are expressed in osteocytes, osteoblasts, osteoclasts and bone marrow cells. While, antigenicity is not detected in trabecular bone and matrix, but it shows different expression levels in osteocytes, osteoblasts, chondrocytes, chondroblasts, bone marrow cells, blood cells and the adipose tissues in bone lacuna. It has been shown that deprotei- nized bones not only lose their immune reactivity but also retain their osteoinduction and osteo- conduction activities [3–5].Thetrabecularporousarchitectureofdeproteinizedbonesactsasa support structure for blood vessels and bone cell expansion which is extremely important for ossifi- cation. Methods for bone deproteinization have emerged since Martz et al.[6] obtained a deprotei- nized bovine bone by immersing it in hydrogen peroxide, which has been referred to as Kiel bone. Previous studies showed that the bone reparation materials, such as Bio-oss [4, 7, 8], exhibit a rela- tively weak clinical effect by a “creeping substitution” process, which limits their application to large bone defects. Liu et al. reported an optimized method to improve the osteogenesis ability of processed swine ribs, and a large amount of collagen was preserved [9]. Currently, several chemical and physical methods are utilized to deproteinize the bovine bone scaffolds [3, 10]. Strong oxidant such as H2O2 or sodium hypochlorite represents the conventional and most popular methods in previous studies [5, 11–15]. However, with the advancement of bone tissue engineering, improved and convenient methods for bovine bone graft deproteinization have been rarely reported. In this study, we report a new method that utilizes pepsin to deproteinize bovine bones. Comparative studies on the physical, chemical and biological properties of these bones were performed. More importantly, the deproteinized bones showed better therapeutic advantages in the rabbit model of radius defects than bone xenografts treated by conventional method. Materials and Methods Bovine bone graft preparation The cancellous bones of the tibias of 2- to 3-year-old Charolais cattle were collected from pri- vate slaughterhouses in Zhuzhou (A1-3 small industry promotion district of Tianyuan district, PLOS ONE | DOI:10.1371/journal.pone.0146005 December 31, 2015 2/17 Pepsin for Xenogeneic Bone Graft Deproteinization Zhuzhou City, Changsha, China. Geographic coordinates: Lat.27.845°Long.113.091°), by Hengtian Biotechnology Co. Ltd (Zhuzhou, China), then removed soft tissue, bone marrow and cartilage. The bones were cut into cuboid-shaped sticks with dimensions of 0.5 cm × 0.5 cm × 3 cm. The bone sticks were then defatted in a Soxhlet extractor by the petroleum ether extraction method. For hydrogen peroxide deproteinization, the bone sticks were immersed in 30% hydrogen peroxide solution for 8 hours, followed by washing repeatedly with double dis- tilled (ddH2O) water. The bones were allowed to dry before use. For the pepsin deproteiniza- tion procedure, the bones were digested by 0.3 mg/mL pepsin (Sigma, St. Louis, MO, USA) dissolved in pH 2 phosphate buffer (1.97 g NaH2PO4, 1.20 mL H3PO4 in 100 mL ddH2O) at 25°C for 8 hours. The reactions were terminated by adjusting pH to 9 with NaOH to deactivate the pepsin. After 15 min, the bone sticks were washed repeatedly with ddH2O for 30 min and allowed to dry before use. Evaluation of collagen I by high-performance liquid chromatography- mass spectrometry (HPLC-MS) The contents of type I collagen was determined via HPLC-MS by assessing the content of hydroxyproline (Hyp). The chromatographic column selected for analysis was a Luna 5 μ C18 (2) 100A, 150 mm × 2.0 mm, 5 μm column, with nicotinamide (Sigma) as the internal stan- dard, 2% formic acid dissolved in H2O as the mobile phase, and acetonitrile as the solid phase (mobile phase: solid phase = 60: 40). The flow rate was 20 μL/min. The MS operating condi- tions were as follows: ionization mode: ES+, capillary voltage: 3.00 kV, cone voltage: 30.00 V, ion source temperature: 100°C, desolvation gas temperature: 350°C, cone gas flow rate: 50 L/h, desolvation gas flow rate: 400 L/h, ion energy voltage 1: 0.5, ion energy voltage 2: 3.0. The colli- sion pressure was 3.82e-3. The standard curve for hydroxyproline was prepared by the double dilution method with a starting dilution of 497 μg/mL,
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