HTLV-1 viral oncogene HBZ drives bone destruction in adult T cell leukemia

JCI Insight. 2019 Oct 3;4(19):e128713. doi: 10.1172/jci.insight.128713.

Abstract

Osteolytic bone lesions and hypercalcemia are common, serious complications in adult T cell leukemia/lymphoma (ATL), an aggressive T cell malignancy associated with human T cell leukemia virus type 1 (HTLV-1) infection. The HTLV-1 viral oncogene HBZ has been implicated in ATL tumorigenesis and bone loss. In this study, we evaluated the role of HBZ on ATL-associated bone destruction using HTLV-1 infection and disease progression mouse models. Humanized mice infected with HTLV-1 developed lymphoproliferative disease and continuous, progressive osteolytic bone lesions. HTLV-1 lacking HBZ displayed only modest delays to lymphoproliferative disease but significantly decreased disease-associated bone loss compared with HTLV-1-infected mice. Gene expression array of acute ATL patient samples demonstrated increased expression of RANKL, a critical regulator of osteoclasts. We found that HBZ regulated RANKL in a c-Fos-dependent manner. Treatment of HTLV-1-infected humanized mice with denosumab, a monoclonal antibody against human RANKL, alleviated bone loss. Using patient-derived xenografts from primary human ATL cells to induce lymphoproliferative disease, we also observed profound tumor-induced bone destruction and increased c-Fos and RANKL gene expression. Together, these data show the critical role of HBZ in driving ATL-associated bone loss through RANKL and identify denosumab as a potential treatment to prevent bone complications in ATL patients.

Keywords: Bone Biology; Bone disease; Oncogenes; Oncology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Basic-Leucine Zipper Transcription Factors / genetics*
  • Basic-Leucine Zipper Transcription Factors / metabolism*
  • Bone Resorption / genetics
  • Bone Resorption / metabolism
  • Bone Resorption / pathology
  • Bone and Bones / pathology
  • Disease Models, Animal
  • Disease Progression
  • Female
  • Gene Expression Regulation, Neoplastic
  • Heterografts
  • Human T-lymphotropic virus 1
  • Humans
  • Kaplan-Meier Estimate
  • Leukemia-Lymphoma, Adult T-Cell / genetics*
  • Leukemia-Lymphoma, Adult T-Cell / metabolism*
  • Leukemia-Lymphoma, Adult T-Cell / pathology
  • Leukemia-Lymphoma, Adult T-Cell / virology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Osteoclasts / metabolism
  • RANK Ligand / genetics
  • RANK Ligand / metabolism
  • Retroviridae Proteins / genetics
  • Retroviridae Proteins / metabolism*
  • Transcriptome

Substances

  • Basic-Leucine Zipper Transcription Factors
  • HBZ protein, human T-cell leukemia virus type I
  • RANK Ligand
  • Retroviridae Proteins
  • TNFSF11 protein, human
  • Tnfsf11 protein, mouse