Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9

Bone - Tập 37 - Trang 313-322 - 2005
Jared C. Robins1, Nagako Akeno2, Aditi Mukherjee2, Ravi R. Dalal2, Bruce J. Aronow3, Peter Koopman4, Thomas L. Clemens5
1Department of Obstetrics and Gynecology, University of Cincinnati, Cincinnati, OH 45221, USA
2Department of Internal Medicine, and Molecular and Cellular Physiology, University of Cincinnati, Cincinnati, OH 45221, USA
3Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA
4Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia
5Division of Molecular and Cellular Pathology, Department of Pathology, University of Alabama at Birmingham, Volker Hall, G019B, 1530 3rd Avenue S., Birmingham, AL 35294-0019, USA

Tài liệu tham khảo

Akeno, 2001, Hypoxia induces vascular endothelial growth factor gene transcription in human osteoblast-like cells through the hypoxia-inducible factor-2alpha, Endocrinology, 142, 959, 10.1210/en.142.2.959 Millhorn, 2000, Gene regulation during hypoxia in excitable oxygen-sensing cells: depolarization-transcription coupling, Adv. Exp. Med. Biol., 475, 131, 10.1007/0-306-46825-5_13 Zelzer, 1998, Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT, EMBO J., 17, 5085, 10.1093/emboj/17.17.5085 Semenza, 2001, HIF-1 and mechanisms of hypoxia sensing, Curr. Opin. Cell Biol., 13, 167, 10.1016/S0955-0674(00)00194-0 Gerber, 2000, Angiogenesis and bone growth, Trends Cardiovasc. Med., 10, 223, 10.1016/S1050-1738(00)00074-8 Barnes, 1999, Growth factor regulation of fracture repair, J. Bone Miner. Res., 14, 1805, 10.1359/jbmr.1999.14.11.1805 Dennis, 1999, A quadripotential mesenchymal progenitor cell isolated from the marrow of an adult mouse, J. Bone Miner. Res., 14, 700, 10.1359/jbmr.1999.14.5.700 Mackay, 1998, Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow, Tissue Eng., 4, 415, 10.1089/ten.1998.4.415 Pittenger, 1999, Multilineage potential of adult human mesenchymal stem cells, Science, 284, 143, 10.1126/science.284.5411.143 Barry, 2001, Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components, Exp. Cell Res., 268, 189, 10.1006/excr.2001.5278 Lennon, 2001, Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: effects on in vitro and in vivo osteochondrogenesis, J. Cell Physiol., 187, 345, 10.1002/jcp.1081 Bassett, 1961, Influence of oxygen concentration and mechanical factors on differentiation of connective tissues in vitro, Nature, 190, 460, 10.1038/190460a0 Miyazawa, 2002, Two major Smad pathways in TGF-beta superfamily signalling, Genes Cells, 7, 1191, 10.1046/j.1365-2443.2002.00599.x Akiyama, 2002, 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, 2813, 10.1101/gad.1017802 Healy, 1999, Regulation and role of Sox9 in cartilage formation, Dev. Dyn., 215, 69, 10.1002/(SICI)1097-0177(199905)215:1<69::AID-DVDY8>3.0.CO;2-N de Crombrugghe, 2001, Regulatory mechanisms in the pathways of cartilage and bone formation, Curr. Opin. Cell Biol., 13, 721, 10.1016/S0955-0674(00)00276-3 Ogawa, 1988, B cell ontogeny in murine embryo studied by a culture system with the monolayer of a stromal cell clone, ST2: B cell progenitor develops first in the embryonal body rather than in the yolk sac, EMBO J., 7, 1337, 10.1002/j.1460-2075.1988.tb02949.x Wang, 1993, Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells, Growth Factors, 9, 57, 10.3109/08977199308991582 Muller, 2002, Processing of gene expression data generated by quantitative real-time RT-PCR, BioTechniques, 32, 1372 Kanai, 1999, Structural and functional characterization of the mouse Sox9 promoter: implications for campomelic dysplasia, Hum. Mol. Genet., 8, 691, 10.1093/hmg/8.4.691 Scott, 1965, Differential staining of acid glycosaminoglycans (mucopolysaccharides) by alcian blue in salt solutions, Histochemie, 5, 221, 10.1007/BF00306130 Ahmad, 2002, Elevated expression of hexokinase II protects human lung epithelial-like A549 cells against oxidative injury, Am. J. Physiol.: Lung Cell Mol. Physiol., 283, L573, 10.1152/ajplung.00410.2001 Yoon, 2001, Identification of genes differentially induced by hypoxia in pancreatic cancer cells, Biochem. Biophys. Res. Commun., 288, 882, 10.1006/bbrc.2001.5867 Zhong, 1999, Direct comparison of GAPDH, beta-actin, cyclophilin, and 28S rRNA as internal standards for quantifying RNA levels under hypoxia, Biochem. Biophys. Res. Commun., 259, 523, 10.1006/bbrc.1999.0815 Theen, 1982, Liver glycogen synthase and phosphorylase changes in vivo with hypoxia and anesthetics, Am. J. Physiol., 243, E182 Chen, 2001, Hypoxia activates a platelet-derived growth factor receptor/phosphatidylinositol 3-kinase/Akt pathway that results in glycogen synthase kinase-3 inactivation, Cancer Res., 61, 2429 Steinbach, 2003, Hypoxia-induced cell death in human malignant glioma cells: energy deprivation promotes decoupling of mitochondrial cytochrome c release from caspase processing and necrotic cell death, Cell Death Differ., 10, 823, 10.1038/sj.cdd.4401252 Kim, 2003, Hypoxic induction of caspase-11/caspase-1/interleukin-1beta in brain microglia, Brain Res. Mol. Brain Res., 114, 107, 10.1016/S0169-328X(03)00135-9 Khurana, 2002, Effect of hypoxia on caspase-3, -8, and -9 activity and expression in the cerebral cortex of newborn piglets, Neurochem. Res., 27, 931, 10.1023/A:1020347732741 Denko, 2000, Epigenetic regulation of gene expression in cervical cancer cells by the tumor microenvironment, Clin. Cancer Res., 6, 480 Farquharson, 1994, Alterations in glycosaminoglycan concentration and sulfation during chondrocyte maturation, Calcif. Tissue Int., 54, 296, 10.1007/BF00295954 Kawasaki, 1999, Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels, J. Cell. Physiol., 179, 142, 10.1002/(SICI)1097-4652(199905)179:2<142::AID-JCP4>3.0.CO;2-Q Ivkovic, 2003, Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development, Development, 130, 2779, 10.1242/dev.00505 Nishida, 2002, CTGF/Hcs24, a hypertrophic chondrocyte-specific gene product, stimulates proliferation and differentiation, but not hypertrophy of cultured articular chondrocytes, J. Cell. Physiol., 192, 55, 10.1002/jcp.10113 Nishida, 2000, Effects of CTGF/Hcs24, a hypertrophic chondrocyte-specific gene product, on the proliferation and differentiation of osteoblastic cells in vitro, J. Cell. Physiol., 184, 197, 10.1002/1097-4652(200008)184:2<197::AID-JCP7>3.0.CO;2-R Kirsch, 2000, Activation of annexin II and V expression, terminal differentiation, mineralization and apoptosis in human osteoarthritic cartilage, Osteoarthr. Cartil., 8, 294, 10.1053/joca.1999.0304 Kirsch, 1992, Selective binding of anchorin CII (annexin V) to type II and X collagen and to chondrocalcin (C-propeptide of type II collagen). Implications for anchoring function between matrix vesicles and matrix proteins, FEBS Lett., 310, 143, 10.1016/0014-5793(92)81316-E von der, 1997, Annexin V interactions with collagen, Cell. Mol. Life Sci., 53, 539, 10.1007/s000180050069 Wang, 2002, Retinoic acid stimulates annexin-mediated growth plate chondrocyte mineralization, J. Cell Biol., 157, 1061, 10.1083/jcb.200203014 Colnot, 2001, Uncoupling of chondrocyte death and vascular invasion in mouse galectin 3 null mutant bones, Dev. Biol., 229, 203, 10.1006/dbio.2000.9933 Nurminskaya, 1996, Analysis of up-regulated genes during chondrocyte hypertrophy, Ann. N.Y. Acad. Sci., 785, 309, 10.1111/j.1749-6632.1996.tb56293.x Fife, 1994, Studies of copper transport in cultured bovine chondrocytes, Biochim. Biophys. Acta, 1201, 19, 10.1016/0304-4165(94)90145-7 Pecina, 2002, Articular cartilage repair: the role of bone morphogenetic proteins, Int. Orthop., 26, 131, 10.1007/s00264-002-0338-4 Nishihara, 2003, Bone morphogenetic protein signaling in articular chondrocyte differentiation, Biochem. Biophys. Res. Commun., 301, 617, 10.1016/S0006-291X(02)03068-1 Vinall, 2001, The effect of BMP on the expression of cytoskeletal proteins and its potential relevance, J. Bone Joint Surg. Am., 83-A, S63 Gouze, 2001, Interleukin-1beta down-regulates the expression of glucuronosyltransferase I, a key enzyme priming glycosaminoglycan biosynthesis: influence of glucosamine on interleukin-1beta-mediated effects in rat chondrocytes, Arthritis Rheum., 44, 351, 10.1002/1529-0131(200102)44:2<351::AID-ANR53>3.0.CO;2-M Buscher, 1997, Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development, Mech. Dev., 62, 175, 10.1016/S0925-4773(97)00656-4 Iwasaki, 1997, Expression of Indian hedgehog, bone morphogenetic protein 6 and gli during skeletal morphogenesis, Mech. Dev., 69, 197, 10.1016/S0925-4773(97)00145-7 Kawai, 2001, Characterization of human bone morphogenetic protein (BMP)-4 and -7 gene promoters: activation of BMP promoters by Gli, a sonic hedgehog mediator, Bone, 29, 54, 10.1016/S8756-3282(01)00470-7 Chang, 2001, Twisted gastrulation can function as a BMP antagonist, Nature, 410, 483, 10.1038/35068583 Ross, 2001, Twisted gastrulation is a conserved extracellular BMP antagonist, Nature, 410, 479, 10.1038/35068578 Durr, 1996, Identification and immunolocalization of laminin in cartilage, Exp. Cell Res., 222, 225, 10.1006/excr.1996.0028 Bell, 1997, SOX9 directly regulates the type-II collagen gene, Nat. Genet., 16, 174, 10.1038/ng0697-174 Akiyama, 2002, 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, 2813, 10.1101/gad.1017802 Sekiya, 2000, SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6, J. Biol. Chem., 275, 10738, 10.1074/jbc.275.15.10738 Wang, 1993, Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells, Growth Factors, 9, 57, 10.3109/08977199308991582 Semenza, 1994, Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1, J. Biol. Chem., 269, 23757, 10.1016/S0021-9258(17)31580-6 Forsythe, 1996, Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1, Mol. Cell. Biol., 16, 4604, 10.1128/MCB.16.9.4604 Yamaguchi, 1996, Effects of BMP-2, BMP-4, and BMP-6 on osteoblastic differentiation of bone marrow-derived stromal cell lines, ST2 and MC3T3-G2/PA6, Biochem. Biophys. Res. Commun., 220, 366, 10.1006/bbrc.1996.0411 Domm, 2002, Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension, Osteoarthr. Cartil., 10, 13, 10.1053/joca.2001.0477 Murphy, 2001, Effect of oxygen tension and alginate encapsulation on restoration of the differentiated phenotype of passaged chondrocytes, Tissue Eng., 7, 791, 10.1089/107632701753337735 Schipani, 2001, Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival, Genes Dev., 15, 2865 Foster, 1994, Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene, Nature, 372, 525, 10.1038/372525a0 Hageman, 1998, Mutation analysis of the SOX9 gene in a patient with campomelic dysplasia, Hum. Mutat. Suppl., 1, S112, 10.1002/humu.1380110137 Lefebvre, 1997, SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene, Mol. Cell Biol., 17, 2336, 10.1128/MCB.17.4.2336 Pfander, 2003, HIF-1alpha controls extracellular matrix synthesis by epiphyseal chondrocytes, J. Cell Sci., 116, 1819, 10.1242/jcs.00385 Coimbra, 2004, Hypoxia inducible factor-1 alpha expression in human normal and osteoarthritic chondrocytes, Osteoarthr. Cartil., 12, 336, 10.1016/j.joca.2003.12.005