Enhanced bone regeneration associated with decreased apoptosis in mice with partial HIF-1alpha deficiency

J Bone Miner Res. 2007 Mar;22(3):366-74. doi: 10.1359/jbmr.061207.

Abstract

HIF-1alpha activates genes under hypoxia and was hypothesized to regulate bone regeneration. Surprisingly, HIF-1alpha+/- fracture calluses are larger, stronger, and stiffer than HIF-1alpha+/+ calluses because of decreased apoptosis. These data identify apoptosis inhibition as a means to enhance bone regeneration.

Introduction: Bone regeneration subsequent to fracture involves the synergistic activation of multiple signaling pathways. Localized hypoxia after fracture activates hypoxia-inducible factor 1alpha (HIF-1alpha), leading to increased expression of HIF-1 target genes. We therefore hypothesized that HIF-1alpha is a key regulator of bone regeneration.

Materials and methods: Fixed femoral fractures were generated in mice with partial HIF-1alpha deficiency (HIF-1alpha+/-) and wildtype littermates (HIF-1alpha+/+). Fracture calluses and intact contralateral femurs from postfracture days (PFDs) 21 and 28 (N=5-10) were subjected to microCT evaluation and four-point bending to assess morphometric and mechanical properties. Molecular analyses were carried out on PFD 7, 10, and 14 samples (N=3) to determine differential gene expression at both mRNA and protein levels. Finally, TUNEL staining was performed on PFD 14 samples (N=2) to elucidate differential apoptosis.

Results: Surprisingly, fracture calluses from HIF-1alpha+/- mice exhibited greater mineralization and were larger, stronger, and stiffer. Microarray analyses focused on hypoxia-induced genes revealed differential expression (between genotypes) of several genes associated with the apoptotic pathway. Real-time PCR confirmed these results, showing higher expression of proapoptotic protein phosphatase 2a (PP2A) and lower expression of anti-apoptotic B-cell leukemia/lymphoma 2 (BCL2) in HIF-1alpha+/+ calluses. Subsequent TUNEL staining showed that HIF-1alpha+/+ calluses contained larger numbers of TUNEL+ chondrocytes and osteoblasts than HIF-1alpha+/- calluses.

Conclusions: We conclude that partial HIF-1alpha deficiency results in decreased chondrocytic and osteoblastic apoptosis, thereby allowing the development of larger, stiffer calluses and enhancing bone regeneration. Furthermore, apoptosis inhibition may be a promising target for developing new treatments to accelerate bone regeneration.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Apoptosis* / genetics
  • Bone Regeneration* / genetics
  • Bony Callus / metabolism
  • Chondrocytes
  • Female
  • Femoral Fractures / genetics
  • Femoral Fractures / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation* / genetics
  • Hypoxia / genetics
  • Hypoxia / metabolism
  • Hypoxia-Inducible Factor 1, alpha Subunit / deficiency*
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Mice
  • Oligonucleotide Array Sequence Analysis
  • Osteoblasts / metabolism*

Substances

  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit