Mesencephalic astrocyte-derived neurotropic factor is an important factor in chondrocyte ER homeostasis

Cell Stress Chaperones. 2019 Jan;24(1):159-173. doi: 10.1007/s12192-018-0953-7. Epub 2018 Dec 12.

Abstract

Mesencephalic astrocyte-derived neurotrophic factor (MANF) is an endoplasmic reticulum (ER) resident protein that can be secreted due to an imperfect KDEL motif. MANF plays a cytoprotective role in several soft tissues and is upregulated in conditions resulting from intracellular retention of mutant protein, including two skeletal diseases, metaphyseal chondrodysplasia, Schmid type (MCDS) and multiple epiphyseal dysplasia (MED). The role of MANF in skeletal tissue homeostasis is currently unknown. Interestingly, cartilage-specific deletion of Manf in a mouse model of MED resulted in increased disease severity, suggesting its upregulation may be chondroprotective. Treatment of MED chondrocytes with exogenous MANF led to a decrease in the cellular levels of BiP (GRP78), confirming MANF's potential to modulate ER stress responses. However, it did not alleviate the intracellular retention of mutant matrilin-3, suggesting that it is the intracellular MANF that is of importance in the pathobiology of skeletal dysplasias. The Col2Cre-driven deletion of Manf from mouse cartilage resulted in a chondrodysplasia-like phenotype. Interestingly, ablation of MANF in cartilage did not have extracellular consequences but led to an upregulation of several ER-resident chaperones including BiP. This apparent induction of ER stress in turn led to dysregulated chondrocyte apoptosis and decreased proliferation, resulting in reduced long bone growth. We have previously shown that ER stress is an underlying disease mechanism for several skeletal dysplasias. The cartilage-specific deletion of Manf described in this study phenocopies our previously published chondrodysplasia models, further confirming that ER stress itself is sufficient to disrupt skeletal growth and thus represents a potential therapeutic target.

Keywords: Chondrodysplasia; MANF; Skeletal development; UPR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Cartilage / drug effects
  • Cartilage / metabolism
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Chondrocytes / drug effects
  • Chondrocytes / metabolism*
  • Chondrocytes / pathology
  • Embryo Loss / pathology
  • Endoplasmic Reticulum / drug effects
  • Endoplasmic Reticulum / metabolism*
  • Endoplasmic Reticulum Chaperone BiP
  • Endoplasmic Reticulum Stress / drug effects
  • Gene Deletion
  • Growth Plate / drug effects
  • Growth Plate / metabolism
  • Homeostasis* / drug effects
  • Lung / abnormalities
  • Lung / pathology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nerve Growth Factors / metabolism*
  • Organ Specificity / drug effects
  • Osteochondrodysplasias / diagnostic imaging
  • Osteochondrodysplasias / metabolism
  • Osteochondrodysplasias / pathology
  • Osteogenesis / drug effects
  • Protein Binding / drug effects
  • Respiration
  • Tunicamycin / pharmacology
  • Unfolded Protein Response / drug effects

Substances

  • Endoplasmic Reticulum Chaperone BiP
  • Hspa5 protein, mouse
  • MANF protein, mouse
  • Nerve Growth Factors
  • Tunicamycin