Human IGF-I propeptide A promotes articular chondrocyte biosynthesis and employs glycosylation-dependent heparin binding

Biochim Biophys Acta Gen Subj. 2018 Mar;1862(3):567-575. doi: 10.1016/j.bbagen.2017.11.017. Epub 2017 Nov 21.

Abstract

Background: Insulin-like growth factor I (IGF-I) is a key regulator of chondrogenesis, but its therapeutic application to articular cartilage damage is limited by rapid elimination from the repair site. The human IGF-I gene gives rise to three IGF-I propeptides (proIGF-IA, proIGF-IB and proIGF-IC) that are cleaved to create mature IGF-I. In this study, we elucidate the processing of IGF-I precursors by articular chondrocytes, and test the hypotheses that proIGF-I isoforms bind to heparin and regulate articular chondrocyte biosynthesis.

Methods: Human IGF-I propeptides and mutants were overexpressed in bovine articular chondrocytes. IGF-I products were characterized by ELISA, western blot and FPLC using a heparin column. The biosynthetic activity of IGF-I products on articular chondrocytes was assayed for DNA and glycosaminoglycan that the cells produced.

Results: Secreted IGF-I propeptides stimulated articular chondrocyte biosynthetic activity to the same degree as mature IGF-I. Of the three IGF-I propeptides, only one, proIGF-IA, strongly bound to heparin. Interestingly, heparin binding of proIGF-IA depended on N-glycosylation at Asn92 in the EA peptide. To our knowledge, this is the first demonstration that N-glycosylation determines the binding of a heparin-binding protein to heparin.

Conclusion: The biosynthetic and heparin binding abilities of proIGF-IA, coupled with its generation of IGF-I, suggest that proIGF-IA may have therapeutic value for articular cartilage repair.

General significance: These data identify human pro-insulin-like growth factor IA as a bifunctional protein. Its combined ability to bind heparin and augment chondrocyte biosynthesis makes it a promising therapeutic agent for cartilage damage due to trauma and osteoarthritis.

Keywords: Biosynthesis; Chondrocyte; E peptide; Glycosylation; Heparin-binding protein; IGF-I propeptide; Insulin-like growth factor (IGF); Protein processing.

Publication types

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

MeSH terms

  • Alternative Splicing
  • Animals
  • Asparagine / metabolism
  • Base Sequence
  • Cartilage, Articular / cytology*
  • Cattle
  • Cells, Cultured
  • Chondrocytes / drug effects*
  • Chondrocytes / metabolism
  • Drug Evaluation, Preclinical
  • Glycosylation
  • Heparin / metabolism*
  • Humans
  • Insulin-Like Growth Factor I / genetics
  • Insulin-Like Growth Factor I / pharmacology
  • Insulin-Like Growth Factor I / physiology*
  • Protein Binding
  • Protein Isoforms / metabolism
  • Protein Precursors / genetics
  • Protein Precursors / pharmacology
  • Protein Precursors / physiology*
  • Protein Processing, Post-Translational*
  • Recombinant Proteins / metabolism

Substances

  • Protein Isoforms
  • Protein Precursors
  • Recombinant Proteins
  • Insulin-Like Growth Factor I
  • Asparagine
  • Heparin