Basic Study
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Mar 28, 2015; 21(12): 3527-3536
Published online Mar 28, 2015. doi: 10.3748/wjg.v21.i12.3527
High persistence rate of hepatitis B virus in a hydrodynamic injection-based transfection model in C3H/HeN mice
Xiu-Hua Peng, Xiao-Nan Ren, Li-Xiang Chen, Bi-Sheng Shi, Chun-Hua Xu, Zhong Fang, Xue Liu, Jie-Liang Chen, Xiao-Nan Zhang, Yun-Wen Hu, Xiao-Hui Zhou
Xiu-Hua Peng, Xiao-Nan Ren, Li-Xiang Chen, Bi-Sheng Shi, Chun-Hua Xu, Zhong Fang, Xue Liu, Jie-Liang Chen, Xiao-Nan Zhang, Yun-Wen Hu, Xiao-Hui Zhou, Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology, Ministry of Education and Health, Fudan University, Shanghai 201508, China
Author contributions: Zhou XH conceived and designed the study; Peng XH, Ren XN, Chen LX, Shi BS, Xu CH, Fang Z, Liu X, Chen JL and Zhang XN performed the experiments; Peng XH, Ren XN, Chen LX and Zhou XH analyzed the data; Zhou XH, Ren XN, Chen LX, Chen JL, Zhang XN and Hu YW wrote and revised the paper.
Supported by Shanghai Municipal Fund for Science and Technology Development, No. 13140902200 and No. 12140900300; National Key Basic Research Development Program (973 Program), No. 2012CB519005.
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: Xiao-Hui Zhou, MD, PhD, Associate Professor, Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology, Ministry of Education and Health, Fudan University, 2901 Caolang Road, Jin Shan District, Shanghai 201508, China. zhouxiaohui@shaphc.org
Telephone: +86-21-37990333 Fax: +86-21-37990333
Received: July 21, 2014
Peer-review started: July 21, 2014
First decision: August 15, 2014
Revised: September 15, 2014
Accepted: October 14, 2014
Article in press: October 15, 2014
Published online: March 28, 2015
Abstract

AIM: To optimize the viral persistence rate in a hydrodynamic injection (HI) based hepatitis B virus (HBV) transfection mouse model.

METHODS: (1) 5-6-wk-old male C3H/HeN and C57BL/6 mice were hydrodynamically injected with 10 μg endotoxin-free pAAV/HBV1.2 plasmid DNA via the tail vein. Hepatitis B surface antigen (HBsAg), hepatitis B e antigen (HBeAg) and HBV DNA, both in the serum and liver, were detected at different time points post HI by ELISA, immunohistochemical staining or quantitative polymerase chain reaction (PCR); (2) male C3H/HeN and C57BL/6 mice, either hydrodynamically injected mice at 10 wk post HI or naïve mice, were all immunized subcutaneously with 5 μg HBsAg formulated in complete Freund’s adjuvant three times at a 2-wk interval. Two weeks after the final immunization, splenocytes were isolated for T cell function analysis by ELISPOT assay; and (3) five weeks post HI, C3H/HeN mice were intragastrically administered 0.1 mg/kg entecavir once a day for 14 d, or were intraperitoneally injected with 1 mg/kg interferon (IFN)-α twice a week for 2 wk, or were treated with PBS as controls. The sera were collected and assayed for HBV DNA on days 0, 7 and 14 after drug treatment.

RESULTS: (1) Approximately 90% (22/25) of the injected C3H/HeN mice were still HBsAg-positive at 46 wk post HI, whereas HBsAg in C57BL/6 mice were completely cleared at 24 wk. Serum levels of HBeAg in C3H/HeN mice were higher than those in C57BL/6 mice from 4 wk to 46 wk. HBV DNA levels in the hydrodynamically injected C3H/HeN mice were higher than those in the C57BL/6 mice, both in the serum (from 4 wk to 46 wk) and in the liver (detected at 8 wk and 46 wk post HI). Histology showed that hepatitis B core antigen and HBsAg were expressed longer in the liver of C3H/HeN mice than in C57BL/6; (2) HBsAg specific T cell responses after HBsAg vaccination in hydrodynamically injected C3H/HeN and C57BL/6 mice, or naive control mice were detected by ELISPOT assay. After stimulation with HBsAg, the frequencies of IFN-γ producing splenocytes in the hydrodynamically injected C3H/HeN mice were significantly lower than those in hydrodynamically injected C57BL/6 mice, control C3H/HeN and control C57BL/6 mice, which were 0, 17 ± 7, 18 ± 10, and 41 ± 10 SFCs/106 splenocytes, respectively, and the mean spot sizes showed the same pattern. Even just stimulated with PMA and ionomysin, T-cell responses elicited in the vaccinated control C3H/HeN were much higher than those in hydrodynamically injected C3H/HeN mice; and (3) For drug treatment experiments on the hydrodynamically injected C3H/HeN mice, serum HBV DNA levels in the entecavir treatment group declined (131.2 folds, P < 0.01) on day 7 after treatment and kept going down. In the group of IFN-α treatment, serum HBV DNA levels declined to a lowest point (6.42 folds, P < 0.05) on 7 d after treatment and then rebounded.

CONCLUSION: We have developed a novel HI-based HBV transfection model using C3H/HeN mice, which had a higher HBV persistence rate than the classic C57BL/6 mouse model.

Keywords: Hepatitis B virus, Hydrodynamic injection, Viral persistence, Liver, Mouse

Core tip: In the classic hepatitis B virus (HBV) hydrodynamic injection (HI) model using C57BL/6 mice, only about 30% of the injected mice carried HBV for more than 12 wk. Here we injected the pAAV-HBV1.2 plasmid into C3H/HeN mice and observed that the hepatitis B surface antigen, hepatitis B e antigen and viral DNA persisted even up to 46 wk in about 90% of the hydrodynamically injected mice. Applying interferon-α or entecavir in this HI model decreased HBV DNA in vivo. Hence, C3H/HeN is a suitable mouse strain for the persistent HBV HI model, which might be useful for chronic hepatitis B research and therapeutic drug development.