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PMID: 24972088 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Loss of VHL in mesenchymal progenitors of the limb bud alters multiple steps of endochondral bone development.

Developmental biology ·Vol. 393 ·No. 1 ·2014-09-01 ·Pages 124-36

Mangiavini L, Merceron C, Araldi E, Khatri R, Gerard-O'Riley R, Wilson TL, Rankin EB, Giaccia AJ, Schipani E

Abstract

Adaptation to low oxygen tension (hypoxia) is a critical event during development. The transcription factors Hypoxia Inducible Factor-1α (HIF-1α) and HIF-2α are essential mediators of the homeostatic responses that allow hypoxic cells to survive and differentiate. Von Hippel-Lindau protein (VHL) is the E3 ubiquitin ligase that targets HIFs to the proteasome for degradation in normoxia. We have previously demonstrated that the transcription factor HIF-1α is essential for survival and differentiation of growth plate chondrocytes, whereas HIF-2α is not necessary for fetal growth plate development. We have also shown that VHL is important for endochondral bone development, since loss of VHL in chondrocytes causes severe dwarfism. In this study, in order to expand our understanding of the role of VHL in chondrogenesis, we conditionally deleted VHL in mesenchymal progenitors of the limb bud, i.e. in cells not yet committed to the chondrocyte lineage. Deficiency of VHL in limb bud mesenchyme does not alter the timely differentiation of mesenchymal cells into chondrocytes. However, it causes structural collapse of the cartilaginous growth plate as a result of impaired proliferation, delayed terminal differentiation, and ectopic death of chondrocytes. This phenotype is associated to delayed replacement of cartilage by bone. Notably, loss of HIF-2α fully rescues the late formation of the bone marrow cavity in VHL mutant mice, though it does not affect any other detectable abnormality of the VHL mutant growth plates. Our findings demonstrate that VHL regulates bone morphogenesis as its loss considerably alters size, shape and overall development of the skeletal elements.

Keywords
Endochondral bone development Hypoxia Inducible Factor Limb bud mesenchyme Von Hippel–Lindau
MeSH Terms
Animals Basic Helix-Loop-Helix Transcription Factors/genetics Cell Differentiation/genetics Cell Hypoxia Cell Proliferation Cells, Cultured Chondrogenesis/genetics,physiology Growth Plate/embryology,growth & development Hypoxia-Inducible Factor 1, alpha Subunit/genetics Limb Buds/cytology Mesenchymal Stem Cells/cytology Mice Mice, Inbred C57BL Mice, Transgenic Osteogenesis/genetics Von Hippel-Lindau Tumor Suppressor Protein/genetics,physiology
Chemicals
Basic Helix-Loop-Helix Transcription Factors Hif1a protein, mouse Hypoxia-Inducible Factor 1, alpha Subunit endothelial PAS domain-containing protein 1 Von Hippel-Lindau Tumor Suppressor Protein VHL protein, mouse
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Mangiavini Laura
Department of Orthopaedic Surgery, Medical School, University of Michigan, Ann Arbor, MI 48109, USA; Division of Endocrinology, Department of Medicine, School of Medicine, Indiana University, Indianapolis, IN 46202, USA; Endocrine Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Department of Orthopaedic and Traumatology, Milano-Bicocca University, 20900 Monza (MB), Italy.
Merceron Christophe
Department of Orthopaedic Surgery, Medical School, University of Michigan, Ann Arbor, MI 48109, USA; Division of Endocrinology, Department of Medicine, School of Medicine, Indiana University, Indianapolis, IN 46202, USA; Inserm, UMRS 791-LIOAD, Centre for Osteoarticular and Dental Tissue Engineering, Group STEP 'Skeletal Tissue Engineering and Physiopathology', 44042 Nantes, France; LUNAM, Nantes University, Faculty of Dental Surgery, Nantes, France.
Araldi Elisa
Endocrine Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
Khatri Richa
Endocrine Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
Gerard-O'Riley Rita
Division of Endocrinology, Department of Medicine, School of Medicine, Indiana University, Indianapolis, IN 46202, USA.
Wilson Tremika LeShan
Department of Orthopaedic Surgery, Medical School, University of Michigan, Ann Arbor, MI 48109, USA; Division of Endocrinology, Department of Medicine, School of Medicine, Indiana University, Indianapolis, IN 46202, USA; Endocrine Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
Rankin Erinn B
Endocrine Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Division of Radiation and Cancer Biology, Department of Radiation Oncology, Stanford University, Stanford, CA 94303-5152, USA.
Giaccia Amato J
Division of Radiation and Cancer Biology, Department of Radiation Oncology, Stanford University, Stanford, CA 94303-5152, USA.
Schipani Ernestina
Department of Orthopaedic Surgery, Medical School, University of Michigan, Ann Arbor, MI 48109, USA; Division of Endocrinology, Department of Medicine, School of Medicine, Indiana University, Indianapolis, IN 46202, USA; Endocrine Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA; Division of Endocrinology, Department of Medicine, Medical School, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: eschipan@med.umich.edu.
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Article Info
Journal
Developmental biology
Abbr.
Dev Biol
ISSN
1095-564X
Published
2014-09-01
Epub
2014-00-24
Pages
124-36
Language
English
Region
United States
NLM ID
0372762
PMCID
PMC4335807
Subset
IM
Grants
NIAMS NIH HHS · R01 AR065403 · United States
NIAMS NIH HHS · R01AR065403-01 · United States
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