Loss of Nmp4 optimizes osteogenic metabolism and secretion to enhance bone quality

Abstract

A goal of osteoporosis therapy is to restore lost bone with structurally sound tissue. Mice lacking the transcription factor nuclear matrix protein 4 ( Nmp4, Zfp384, Ciz, ZNF384) respond to several classes of osteoporosis drugs with enhanced bone formation compared with wild-type (WT) animals. Nmp4−/− mesenchymal stem/progenitor cells (MSPCs) exhibit an accelerated and enhanced mineralization during osteoblast differentiation. To address the mechanisms underlying this hyperanabolic phenotype, we carried out RNA-sequencing and molecular and cellular analyses of WT and Nmp4−/− MSPCs during osteogenesis to define pathways and mechanisms associated with elevated matrix production. We determined that Nmp4 has a broad impact on the transcriptome during osteogenic differentiation, contributing to the expression of over 5,000 genes. Phenotypic anchoring of transcriptional data was performed for the hypothesis-testing arm through analysis of cell metabolism, protein synthesis and secretion, and bone material properties. Mechanistic studies confirmed that Nmp4−/− MSPCs exhibited an enhanced capacity for glycolytic conversion: a key step in bone anabolism. Nmp4−/− cells showed elevated collagen translation and secretion. The expression of matrix genes that contribute to bone material-level mechanical properties was elevated in Nmp4−/− cells, an observation that was supported by biomechanical testing of bone samples from Nmp4−/− and WT mice. We conclude that loss of Nmp4 increases the magnitude of glycolysis upon the metabolic switch, which fuels the conversion of the osteoblast into a super-secretor of matrix resulting in more bone with improvements in intrinsic quality.

Document Details

Document Type
Pub Defense Publication
Publication Date
May 01, 2019
Source ID
10.1152/ajpendo.00343.2018

Entities

People

  • Alexander G. Robling
  • Amber L. Mosley
  • Angela Klunk
  • David B. Burr
  • Deepak Vashishth
  • Emily Wichern
  • Jagannath Misra
  • James M. Hamilton
  • Joseph M. Wallace
  • Joseph P. Bidwell
  • Keith R. Stayrook
  • Kylie Jacobs
  • Matthew R. Allen
  • Michele Adaway
  • Nickolay Brustovetsky
  • Paul J. Childress
  • Ronald C. Wek
  • Yu Shao
  • Yunlong Liu

Organizations

  • Eli Lilly and Company
  • Indiana University
  • Indiana University – Purdue University Indianapolis
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases
  • National Institute of General Medical Sciences
  • National Institutes of Health
  • Rensselaer Polytechnic Institute
  • United States Department of Defense

Tags

Fields of Study

  • Biology

Readers

  • Immunology and Pathology
  • Military Logistics and Supply Chain Management
  • Molecular and Cellular Biology