A novel in vivo model to study endochondral bone formation; HIF-1α activation and BMP expression

Bone

Volumn 40, Issue 2, 2007, Pages 409-418

  Emans, Pieter J ^a   Spaapen, Frank ^c   Surtel, Don A M ^a   Reilly, Keryn M ^b   Cremers, Andy ^a   van Rhijn, Lodewijk W ^a   Bulstra, Sjoerd K ^a   Voncken, Jan Willem ^c   Kuijer, Roel ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Chondrogenesis; Endochondral bone formation; Ihh PTHrP; Periostin

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; GENE PRODUCT; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; OSTEOGENIC PROTEIN 1; PARATHYROID HORMONE RELATED PROTEIN; PERIOSTIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CHONDROGENESIS; ENCHONDRAL OSSIFICATION; EVALUATION; FEMALE; GROWTH PLATE; HYPOXIA; IMMUNOHISTOCHEMISTRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGENATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; BONE AND BONES; BONE MORPHOGENETIC PROTEINS; CARTILAGE; CHONDROGENESIS; FEMALE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; OSTEOGENESIS; PERIOSTEUM; RABBITS; RNA, MESSENGER;

EID: 33846028751     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2006.08.005     Document Type: Article

References (47)

1. Zhao Q., Eberspaecher H., Lefebvre V., and De Crombrugghe B. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 209 (1997) 377-386
2. Yoon B.S., and Lyons K.M. Multiple functions of BMPs in chondrogenesis. J. Cell. Biochem. 93 (2004) 93-103
3. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., and de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 16 (2002) 2813-2828
4. Bridgewater L.C., Walker M.D., Miller G.C., Ellison T.A., Holsinger L.D., Potter J.L., et al. Adjacent DNA sequences modulate Sox9 transcriptional activation at paired Sox sites in three chondrocyte-specific enhancer elements. Nucleic Acids Res. 31 (2003) 1541-1553
5. Lefebvre V., Li P., and de Crombrugghe B. A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J. 17 (1998) 5718-5733
6. Lefebvre V., Behringer R.R., and de Crombrugghe B. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthr. Cartil. 9 Suppl A (2001) S69-S75
7. Uusitalo H., Hiltunen A., Ahonen M., Kahari V.M., Aro H., and Vuorio E. Induction of periosteal callus formation by bone morphogenetic protein-2 employing adenovirus-mediated gene delivery. Matrix Biol. 20 (2001) 123-127
8. Robins J.C., Akeno N., Mukherjee A., Dalal R.R., Aronow B.J., Koopman P., et al. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9. Bone 37 (2005) 313-322
9. Schipani E. Hypoxia and HIF-1alpha in chondrogenesis. Semin. Cell Dev. Biol. 16 (2005) 539-546
10. Gersbach C.A., Byers B.A., Pavlath G.K., and Garcia A.J. Runx2/Cbfa1 stimulates transdifferentiation of primary skeletal myoblasts into a mineralizing osteoblastic phenotype. Exp. Cell Res. 300 (2004) 406-417
11. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89 (1997) 765-771
12. Xiao Z.S., Simpson L.G., and Quarles L.D. IRES-dependent translational control of Cbfa1/Runx2 expression. J. Cell. Biochem. 88 (2003) 493-505
13. Li P., Oparil S., Feng W., and Chen Y.F. Hypoxia-responsive growth factors upregulate periostin and osteopontin expression via distinct signaling pathways in rat pulmonary arterial smooth muscle cells. J. Appl. Physiol. 97 (2004) 1550-1558 (discussion 1549)
14. Horiuchi K., Amizuka N., Takeshita S., Takamatsu H., Katsuura M., Ozawa H., et al. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J. Bone Miner. Res. 14 (1999) 1239-1249
15. LeBaron R.G., Bezverkov K.I., Zimber M.P., Pavelec R., Skonier J., and Purchio A.F. Beta IG-H3, a novel secretory protein inducible by transforming growth factor-beta, is present in normal skin and promotes the adhesion and spreading of dermal fibroblasts in vitro. J. Invest. Dermatol. 104 (1995) 844-849
16. Takeshita S., Kikuno R., Tezuka K., and Amann E. Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem. J. 294 Pt 1 (1993) 271-278
17. Wilde J., Terai K., Yokozeki M., Hiura K., Horiuchi K., Kudo A., et al. Compressive mechanical stress increases periostin mRNA expression in the periochondrium. J. Bone Miner. Res. 15 (2000) S348
18. Wilde J., Yokozeki M., Terai K., Kudo A., and Moriyama K. The divergent expression of periostin mRNA in the periodontal ligament during experimental tooth movement. Cell Tissue Res. 312 (2003) 345-351
19. Nakazawa T., Nakajima A., Seki N., Okawa A., Kato M., Moriya H., et al. Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis. J. Orthop. Res. 22 (2004) 520-525
20. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., and de Crombrugghe B. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol. Cell. Biol. 17 (1997) 2336-2346
21. Einhorn T.A. The science of fracture healing. J. Orthop. Trauma 19 (2005) S4-S6
22. Bostrom M.P., Lane J.M., Berberian W.S., Missri A.A., Tomin E., Weiland A., et al. Immunolocalization and expression of bone morphogenetic proteins 2 and 4 in fracture healing. J. Orthop. Res. 13 (1995) 357-367
23. Emans P.J., Surtel D.A., Frings E.J., Bulstra S.K., and Kuijer R. In vivo generation of cartilage from periosteum. Tissue Eng. 11 (2005) 369-377
24. Zohar R., Sodek J., and McCulloch C.A. Characterization of stromal progenitor cells enriched by flow cytometry. Blood 90 (1997) 3471-3481
25. Ghilzon R., McCulloch C.A., and Zohar R. Stromal mesenchymal progenitor cells. Leuk. Lymphoma 32 (1999) 211-221
26. O'Driscoll S.W., Recklies A.D., and Poole A.R. Chondrogenesis in periosteal explants. An organ culture model for in vitro study. J. Bone Jt. Surg., Am. 76 (1994) 1042-1051
27. Sanyal A., Sarkar G., Saris D.B., Fitzsimmons J.S., Bolander M.E., and O'Driscoll S.W. Initial evidence for the involvement of bone morphogenetic protein-2 early during periosteal chondrogenesis. J. Orthop. Res. 17 (1999) 926-934
28. Sasaki H., Roberts J., Lykins D., Fujii Y., Auclair D., and Chen L.B. Novel chemiluminescence assay for serum periostin levels in women with preeclampsia and in normotensive pregnant women. Am. J. Obstet. Gynecol. 186 (2002) 103-108
29. Sasaki H., Yu C.Y., Dai M., Tam C., Loda M., Auclair D., et al. Elevated serum periostin levels in patients with bone metastases from breast but not lung cancer. Breast Cancer Res. Treat. 77 (2003) 245-252
30. Metzen E., Wolff M., Fandrey J., and Jelkmann W. Pericellular PO2 and O2 consumption in monolayer cell cultures. Respir. Physiol. 100 (1995) 101-106
31. Schipani E., Ryan H.E., Didrickson S., Kobayashi T., Knight M., and Johnson R.S. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 15 (2001) 2865-2876
32. Lee J.W., Bae S.H., Jeong J.W., Kim S.H., and Kim K.W. Hypoxia-inducible factor (HIF-1)alpha: its protein stability and biological functions. Exp. Mol. Med. 36 (2004) 1-12
33. Minchenko A., Bauer T., Salceda S., and Caro J. Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab. Invest. 71 (1994) 374-379
34. Levy N.S., Chung S., Furneaux H., and Levy A.P. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273 (1998) 6417-6423
35. Lu S., Gu X., Hoestje S., and Epner D.E. Identification of an additional hypoxia responsive element in the glyceraldehyde-3-phosphate dehydrogenase gene promoter. Biochim. Biophys. Acta 1574 (2002) 152-156
36. Seagroves T.N., Ryan H.E., Lu H., Wouters B.G., Knapp M., Thibault P., et al. Transcription factor HIF-1 is a necessary mediator of the Pasteur effect in mammalian cells. Mol. Cell. Biol. 21 (2001) 3436-3444
37. Yaoita H., Orimo H., Shirai Y., and Shimada T. Expression of bone morphogenetic proteins and rat distal-less homolog genes following rat femoral fracture. J. Bone Miner. Metab. 18 (2000) 63-70
38. Kloen P., Di Paola M., Borens O., Richmond J., Perino G., Helfet D.L., et al. BMP signaling components are expressed in human fracture callus. Bone 33 (2003) 362-371
39. Simon T.M., Van Sickle D.C., Kunishima D.H., and Jackson D.W. Cambium cell stimulation from surgical release of the periosteum. J. Orthop. Res. 21 (2003) 470-480
40. Koritzinsky M., Magagnin M.G., van den Beucken T., Seigneuric R., Savelkouls K., Dostie J., et al. Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J. 25 (2006) 1114-1125
41. Kronenberg H.M., and Chung U. The parathyroid hormone-related protein and Indian hedgehog feedback loop in the growth plate. Novartis Found. Symp. 232 (2001) 144-152 (discussion 152-7)
42. Chen Y.F., Feng J.A., Li P., Xing D., Ambalavanan N., and Oparil S. Atrial natriuretic peptide-dependent modulation of hypoxia-induced pulmonary vascular remodeling. Life Sci. (2006) 1357-1365
43. Li G., Oparil S., Sanders J.M., Zhang L., Dai M., Chen L.B., et al. Phosphatidylinositol-3-kinase signaling mediates vascular smooth muscle cell expression of periostin in vivo and in vitro. Atherosclerosis (2005) [Electronic publication ahead of print]
44. Yan W., and Shao R. Transduction of a mesenchyme-specific gene periostin into 293T cells induces cell invasive activity through epithelial-mesenchymal transformation. J. Biol. Chem. (2006) 19700-19708
45. Kii I., Amizuka N., Minqi L., Kitajima S., Saga Y., and Kudo A. Periostin is an extracellular matrix protein required for eruption of incisors in mice. Biochem. Biophys. Res. Commun. 342 (2006) 766-772
46. Shao R., Bao S., Bai X., Blanchette C., Anderson R.M., Dang T., et al. Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression. Mol. Cell. Biol. 24 (2004) 3992-4003
47. Gillan L., Matei D., Fishman D.A., Gerbin C.S., Karlan B.Y., and Chang D.D. Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res. 62 (2002) 5358-5364