Patient-derived iPSCs link elevated mitochondrial respiratory complex I function to osteosarcoma in Rothmund-Thomson syndrome

Abstract

Rothmund-Thomson syndrome (RTS) is an autosomal recessive genetic disorder characterized by poikiloderma, small stature, skeletal anomalies, sparse brows/lashes, cataracts, and predisposition to cancer. Type 2 RTS patients with biallelic RECQL4 pathogenic variants have multiple skeletal anomalies and a significantly increased incidence of osteosarcoma. Here, we generated RTS patient-derived induced pluripotent stem cells (iPSCs) to dissect the pathological signaling leading to RTS patient-associated osteosarcoma. RTS iPSC-derived osteoblasts showed defective osteogenic differentiation and gain of in vitro tumorigenic ability. Transcriptome analysis of RTS osteoblasts validated decreased bone morphogenesis while revealing aberrantly upregulated mitochondrial respiratory complex I gene expression. RTS osteoblast metabolic assays demonstrated elevated mitochondrial respiratory complex I function, increased oxidative phosphorylation (OXPHOS), and increased ATP production. Inhibition of mitochondrial respiratory complex I activity by IACS-010759 selectively suppressed cellular respiration and cell proliferation of RTS osteoblasts. Furthermore, systems analysis of IACS-010759-induced changes in RTS osteoblasts revealed that chemical inhibition of mitochondrial respiratory complex I impaired cell proliferation, induced senescence, and decreased MAPK signaling and cell cycle associated genes, but increased H19 and ribosomal protein genes. In summary, our study suggests that mitochondrial respiratory complex I is a potential therapeutic target for RTS-associated osteosarcoma and provides future insights for clinical treatment strategies.

Document Details

Document Type
Pub Defense Publication
Publication Date
Dec 29, 2021
Source ID
10.1371/journal.pgen.1009971

Entities

People

  • An Xu
  • Benny Abraham Kaipparettu
  • Brittany E Jewell
  • Christopher Vellano
  • Dandan Zhu
  • Danielle Bazer
  • Dung-Fang Lee
  • Erica L. Underwood
  • Holger K. Eltzschig
  • Huihui Fan
  • Jian Tu
  • Julian A. Gingold
  • Jun Hyoung Park
  • Linchao Lu
  • Lisa L. Wang
  • Mo Liu
  • Mo-Fan Huang
  • Nathaniel Berg
  • Nino Rainusso
  • Philip Jones
  • Ruiying Zhao
  • Ruoji Zhou
  • Shu‐Hsia Chen
  • Weidong Jin
  • Ying Liu
  • Yitian Xu
  • Yi‐Hung Chen
  • Zhongming Zhao
  • Zijun Huo

Organizations

  • Amschwand Sarcoma Cancer Foundation
  • Cancer Prevention and Research Institute of Texas
  • Congressionally Directed Medical Research Programs
  • Curtis and Doris K. Hankamer Foundation
  • Doris Duke Charitable Foundation
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development
  • Gillson Longenbaugh Foundation
  • National Cancer Institute
  • National Institutes of Health

Tags

Fields of Study

  • Biology

Readers

  • Immunology and Pathology
  • Molecular Biology and Genetics
  • Molecular and Cellular Biology

Technology Areas

  • Biotechnology