Human osteoclastogenesis in Epstein-Barr virus-induced erosive arthritis in humanized NOD/Shi-scid/IL-2Rγnull mice

PLoS One. 2021 Apr 1;16(4):e0249340. doi: 10.1371/journal.pone.0249340. eCollection 2021.

Abstract

Many human viruses, including Epstein-Barr virus (EBV), do not infect mice, which is challenging for biomedical research. We have previously reported that EBV infection induces erosive arthritis, which histologically resembles rheumatoid arthritis, in humanized NOD/Shi-scid/IL-2Rγnull (hu-NOG) mice; however, the underlying mechanisms are not known. Osteoclast-like multinucleated cells were observed during bone erosion in this mouse model, and therefore, we aimed to determine whether the human or mouse immune system activated bone erosion and analyzed the characteristics and origin of the multinucleated cells in hu-NOG mice. Sections of the mice knee joint tissues were immunostained with anti-human antibodies against certain osteoclast markers, including cathepsin K and matrix metalloproteinase-9 (MMP-9). Multinucleated cells observed during bone erosion stained positively for human cathepsin K and MMP-9. These results indicate that human osteoclasts primarily induce erosive arthritis during EBV infections. Human osteoclast development from hematopoietic stem cells transplanted in hu-NOG mice remains unclear. To confirm their differentiation potential into human osteoclasts, we cultured bone marrow cells of EBV-infected hu-NOG mice and analyzed their characteristics. Multinucleated cells cultured from the bone marrow cells stained positive for human cathepsin K and human MMP-9, indicating that bone marrow cells of hu-NOG mice could differentiate from human osteoclast progenitor cells into human osteoclasts. These results indicate that the human immune response to EBV infection may induce human osteoclast activation and cause erosive arthritis in this mouse model. Moreover, this study is the first, to our knowledge, to demonstrate human osteoclastogenesis in humanized mice. We consider that this model is useful for studying associations of EBV infections with rheumatoid arthritis and human bone metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthritis / metabolism
  • Arthritis / pathology*
  • Arthritis / virology
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / metabolism
  • Bone Marrow Cells / virology
  • Cathepsin K / immunology
  • Cathepsin K / metabolism
  • Cell Differentiation*
  • Disease Models, Animal
  • Herpesvirus 4, Human / physiology*
  • Humans
  • Interleukin Receptor Common gamma Subunit / deficiency
  • Interleukin Receptor Common gamma Subunit / genetics
  • Knee Joint / diagnostic imaging
  • Knee Joint / pathology
  • Matrix Metalloproteinase 9 / immunology
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Mice, Transgenic
  • Osteoclasts / cytology
  • Osteoclasts / metabolism
  • Osteogenesis*
  • X-Ray Microtomography

Substances

  • Interleukin Receptor Common gamma Subunit
  • Cathepsin K
  • Matrix Metalloproteinase 9

Grants and funding

This work was supported by the MEXT-Supported Program for the Strategic Research Foundation at Private Universities and Nihon University Multidisciplinary Research Grant for 2017. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.