Chondrocyte phenotype and cell survival are regulated by culture conditions and by specific cytokines through the expression of Sox-9 transcription factor

Rheumatology (Oxford). 2001 Oct;40(10):1146-56. doi: 10.1093/rheumatology/40.10.1146.

Abstract

Objective: To investigate the effects of culture conditions, serum and specific cytokines such as insulin-like growth factor (IGF) 1 and interleukin (IL) 1alpha on phenotype and cell survival in cultures of Syrian hamster embryonic chondrocyte-like cells (DES4(+).2).

Methods: Proteins and RNA extracted from subconfluent and confluent early- and late-passage DES4(+).2 cells cultured in the presence or absence of serum and IL-1alpha or IGF-1 or both cytokines together were analysed for the expression of chondrocyte-specific genes and for the chondrogenic transcription factor Sox-9 by Western and Northern blotting. Apoptosis was assessed by agarose gel electrophoresis of labelled low-molecular weight DNA extracted from DES4(+).2 cells and another Syrian hamster embryonic chondrocyte-like cell line, 10W(+).1, cultured under the different conditions and treatments.

Results: Early passage DES4(+).2 cells expressed chondrocyte-specific molecules such as collagen types alpha1(II) and alpha1(IX), aggrecan, biglycan and link protein and collagen types alpha1(I) and alpha1(X) mRNAs, suggesting a prehypertrophic chondrocyte-like phenotype. The expression of all genes investigated was cell density- and serum-dependent and was low to undetectable in cell populations from later passages. Early-passage DES4(+).2 and 10W(+).1 cells survived when cultured at low cell density, but died by apoptosis when cultured at high cell density in the absence of serum or IGF-1. IGF-1 and IL-1alpha had opposite and antagonistic effects on the chondrocyte phenotype and survival. Whereas IL-1alpha acting alone suppressed cartilage-specific gene expression without significantly affecting cell survival, IGF-1 increased the steady-state mRNA levels and relieved the IL-1alpha-induced suppression of all the chondrocyte-specific genes investigated; it also enhanced chondrocyte survival. Suppression of the chondrocyte phenotype by the inflammatory cytokine IL-1alpha correlated with marked down-regulation of the transcription factor Sox-9, which was relieved by IGF-1. The expression of the Sox9 gene was closely correlated with the expression of the chondrocyte-specific genes under all conditions and treatments.

Conclusions: The results suggest that the effects of cartilage anabolic and catabolic cytokines IGF-1 and IL-1alpha on the expression of the chondrocyte phenotype are mediated by Sox-9. As Sox-9 appears to be essential for matrix production, the potent effect of IL-1alpha in suppressing Sox-9 expression may limit the ability of cartilage to repair during inflammatory joint diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aggrecans
  • Animals
  • Antimetabolites, Antineoplastic / pharmacology
  • Apoptosis / drug effects
  • Apoptosis / immunology
  • Azacitidine / pharmacology
  • Biglycan
  • Cell Line, Transformed
  • Cell Survival / immunology
  • Chondrocytes / cytology*
  • Chondrocytes / immunology*
  • Collagen Type II / genetics
  • Collagen Type IX / genetics
  • Cricetinae
  • Extracellular Matrix Proteins*
  • Fetus / cytology
  • Gene Expression / drug effects
  • Gene Expression / immunology
  • High Mobility Group Proteins / genetics*
  • High Mobility Group Proteins / immunology
  • Insulin-Like Growth Factor I / pharmacology*
  • Interleukin-1 / pharmacology*
  • Lectins, C-Type
  • Mesocricetus
  • Phenotype
  • Proteins / genetics
  • Proteoglycans / genetics
  • RNA, Messenger / analysis
  • SOX9 Transcription Factor
  • Transcription Factors / genetics*
  • Transcription Factors / immunology

Substances

  • Aggrecans
  • Antimetabolites, Antineoplastic
  • Biglycan
  • Collagen Type II
  • Collagen Type IX
  • Extracellular Matrix Proteins
  • High Mobility Group Proteins
  • Interleukin-1
  • Lectins, C-Type
  • Proteins
  • Proteoglycans
  • RNA, Messenger
  • SOX9 Transcription Factor
  • Transcription Factors
  • link protein
  • Insulin-Like Growth Factor I
  • Azacitidine