Detection of novel skeletogenesis target genes by comprehensive analysis of a Runx2-/- mouse model

Gene Expression Patterns

Volumn 7, Issue 1-2, 2007, Pages 102-112

  Hecht, J ^a,e   Seitz, V ^a   Urban, M ^a   Wagner, F ^b   Robinson, P N ^c   Stiege, A ^a   Dieterich, C ^d   Kornak, U ^c   Wilkening, U ^a   Brieske, N ^a   Zwingman, C ^a   Kidess, A ^a   Stricker, S ^a   Mundlos, S ^a,c  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b German Genome Resource Center RZPD   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Bone; Cartilage; Development; Gene expression; Gene Ontology; Microarray; Osteoclasts; Quantitative RT PCR; Runx2; Skeletogenesis

Indexed keywords

15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ALKALINE PHOSPHATASE; BINDING PROTEIN; CADHERIN; CALPONIN; CALVASCULIN; CATHEPSIN K; CELL ANTIGEN; COLLAGENASE 3; COMPLEMENT FACTOR H; GELATINASE B; GELSOLIN; HOMEODOMAIN PROTEIN; LIPOXYGENASE; MACROPHAGE INFLAMMATORY PROTEIN 2; OSTEOPONTIN; PARATHYROID HORMONE RECEPTOR; PHOSPHOPROTEIN; PROCOLLAGEN C PROTEINASE; PROTEIN KINASE; PROTEIN PATCHED 1; SIALOPROTEIN; SONIC HEDGEHOG PROTEIN; SPHINGOMYELIN PHOSPHODIESTERASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1; VITAMIN D RECEPTOR;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; EXPERIMENTAL MODEL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE TARGETING; GENETIC ANALYSIS; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMERUS; HYBRIDIZATION; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSSIFICATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE; WILD TYPE;

ANIMALS; BONE DEVELOPMENT; CLEIDOCRANIAL DYSPLASIA; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION;

MURINAE;

EID: 33750822719     PISSN: 1567133X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.modgep.2006.05.014     Document Type: Article

References (76)

1. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harris M.A., Hill D.P., Issel-Tarver L., Kasarskis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., and Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology consortium. Nat. Genet. 25 (2000) 25-29
2. Bendall A.J., Hu G., Levi G., and Abate-Shen C. Dlx5 regulates chondrocyte differentiation at multiple stages. Int. J. Dev. Biol. 47 (2003) 335-344
3. Brandenberger R., Schmidt A., Linton J., Wang D., Backus C., Denda S., Muller U., and Reichardt L.F. Identification and characterization of a novel extracellular matrix protein nephronectin that is associated with integrin alpha8beta1 in the embryonic kidney. J. Cell Biol. 154 (2001) 447-458
4. Constam D.B., and Robertson E.J. SPC4/PACE4 regulates a TGFbeta signaling network during axis formation. Genes Dev. 14 (2000) 1146-1155
5. D'Alonzo R.C., Selvamurugan N., Karsenty G., and Partridge N.C. Physical interaction of the activator protein-1 factors c-Fos and c-Jun with Cbfa1 for collagenase-3 promoter activation. J. Biol. Chem. 277 (2002) 816-822
6. de Crombrugghe B., Lefebvre V., and Nakashima K. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr. Opin. Cell Biol. 13 (2001) 721-727
7. de Jong D.S., Vaes B.L., Dechering K.J., Feijen A., Hendriks J.M., Wehrens R., Mummery C.L., van Zoelen E.J., Olijve W., and Steegenga W.T. Identification of novel regulators associated with early-phase osteoblast differentiation. J. Bone Miner. Res. 19 (2004) 947-958
8. Delaisse J.M., Andersen T.L., Engsig M.T., Henriksen K., Troen T., and Blavier L. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc. Res. Tech. 61 (2003) 504-513
9. Duarte W.R., Shibata T., Takenaga K., Takahashi E., Kubota K., Ohya K., Ishikawa I., Yamauchi M., and Kasugai S. S100A4: a novel negative regulator of mineralization and osteoblast differentiation. J. Bone Miner. Res. 18 (2003) 493-501
10. Engelkamp D. Cloning of three mouse Unc5 genes and their expression patterns at mid-gestation. Mech. Dev. 118 (2002) 191-197
11. Engsig M.T., Chen Q.J., Vu T.H., Pedersen A.C., Therkidsen B., Lund L.R., Henriksen K., Lenhard T., Foged N.T., Werb Z., and Delaisse J.M. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J. Cell Biol. 151 (2000) 879-889
12. Erben R.G., Raith S., Eberle J., and Stangassinger M. Ovariectomy augments B lymphopoiesis and generation of monocyte-macrophage precursors in rat bone marrow. Am. J. Physiol. 274 (1998) 476-483
13. Fisher D.A., Smith J.F., Pillar J.S., St Denis S.H., and Cheng J.B. Isolation and characterization of PDE8A, a novel human cAMP-specific phosphodiesterase. Biochem. Biophys. Res. Commun. 246 (1998) 570-577
14. FitzPatrick D.R., Carr I.M., McLaren L., Leek J.P., Wightman P., Williamson K., Gautier P., McGill N., Hayward C., Firth H., Markham A.F., Fantes J.A., and Bonthron D.T. Identification of SATB2 as the cleft palate gene on 2q32-q33. Hum. Mol. Genet. 12 (2003) 2491-2501
15. Fransson L.A. Glypicans. Int. J. Biochem. Cell Biol. 35 (2003) 125-129
16. Friese M.A., Hellwage J., Jokiranta T.S., Meri S., Peter H.H., Eibel H., and Zipfel P.F. FHL-1/reconnectin and factor H: two human complement regulators which are encoded by the same gene are differently expressed and regulated. Mol. Immunol. 36 (1999) 809-818
17. Fukazawa N., Ayukawa K., Nishikawa K., Ohashi H., Ichihara N., Hikawa Y., Abe T., Kudo Y., Kiyama H., Wada K., and Aoki S. Identification and functional characterization of mouse SERINC5 as a myelin membrane protein. Brain Res. 1070 (2006) 1-14
18. Gerbens F., van Erp A.J., Harders F.L., Verburg F.J., Meuwissen T.H., Veerkamp J.H., and te Pas M.F. Effect of genetic variants of the heart fatty acid-binding protein gene on intramuscular fat and performance traits in pigs. J. Anim. Sci. 77 (1999) 846-852
19. Giger R.J., Cloutier J.F., Sahay A., Prinjha R.K., Levengood D.V., Moore S.E., Pickering S., Simmons D., Rastan S., Walsh F.S., Kolodkin A.L., Ginty D.D., and Geppert M. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25 (2000) 29-41
20. Gravallese E.M. Osteopontin: a bridge between bone and the immune system. J. Clin Invest. 112 (2003) 147-149
21. Gurlek A., Pittelkow M.R., and Kumar R. Modulation of growth factor/cytokine synthesis and signaling by 1alpha,25-dihydroxyvitamin D(3): implications in cell growth and differentiation. Endocr. Rev. 23 (2002) 763-786
22. Harroch S., Furtado G.C., Brueck W., Rosenbluth J., Lafaille J., Chao M., Buxbaum J.D., and Schlessinger J. A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat. Genet. 32 (2002) 411-414
23. Hill D.P., Begley D.A., Finger J.H., Hayamizu T.F., McCright I.J., Smith C.M., Beal J.S., Corbani L.E., Blake J.A., Eppig J.T., Kadin J.A., Richardson J.E., and Ringwald M. The mouse gene expression database (GXD): updates and enhancements. Nucleic Acids Res. 32 Database issue (2004) D568-D571
24. Hong H.H., Pischon N., Santana R.B., Palamakumbura A.H., Chase H.B., Gantz D., Guo Y., Uzel M.I., Ma D., and Trackman P.C. A role for lysyl oxidase regulation in the control of normal collagen deposition in differentiating osteoblast cultures. J. Cell. Physiol. 200 (2004) 53-62
25. Inoue K., Zhuang L., Maddox D.M., Smith S.B., and Ganapathy V. Human sodium-coupled citrate transporter, the orthologue of Drosophila Indy, as a novel target for lithium action. Biochem. J. 374 (2003) 21-26
26. Irie S., Hachiya T., Rabizadeh S., Maruyama W., Mukai J., Li Y., Reed J.C., Bredesen D.E., and Sato T.A. Functional interaction of Fas-associated phosphatase-1 (FAP-1) with p75(NTR) and their effect on NF-kappaB activation. FEBS Lett. 460 (1999) 191-198
27. Jakob F., Becker K., Paar E., Ebert-Duemig R., and Schutze N. Expression and regulation of thioredoxin reductases and other selenoproteins in bone. Methods Enzymol. 347 (2002) 168-179
28. Javed A., Barnes G.L., Jasanya B.O., Stein J.L., Gerstenfeld L., Lian J.B., and Stein G.S. runt homology domain transcription factors (Runx, Cbfa, and AML) mediate repression of the bone sialoprotein promoter: evidence for promoter context-dependent activity of Cbfa proteins. Mol. Cell. Biol. 21 (2001) 2891-2905
29. Jiang X.C., Bruce C., Mar J., Lin M., Ji Y., Francone O.L., and Tall A.R. Targeted mutation of plasma phospholipid transfer protein gene markedly reduces high-density lipoprotein levels. J. Clin. Invest. 103 (1999) 907-914
30. Jukkola T., Sinjushina N., and Partanen J. Apcdd1 expression during mouse embryonic development. Gene Expr. Patterns 4 (2004) 755-762
31. Kahler R.A., and Westendorf J.J. Lymphoid enhancer factor-1 and beta-catenin inhibit Runx2-dependent transcriptional activation of the osteocalcin promoter. J. Biol. Chem. 278 (2003) 11937-11944
32. Kalajzic I., Braut A., Guo D., Jiang X., Kronenberg M.S., Mina M., Harris M.A., Harris S.E., and Rowe D.W. Dentin matrix protein 1 expression during osteoblastic differentiation, generation of an osteocyte GFP-transgene. Bone 35 (2004) 74-82
33. Kim G., Lee T.H., Wetzel P., Geers C., Robinson M.A., Myers T.G., Owens J.W., Wehr N.B., Eckhaus M.W., Gros G., Wynshaw-Boris A., and Levine R.L. Carbonic anhydrase III is not required in the mouse for normal growth, development, and life span. Mol. Cell. Biol. 24 (2004) 9942-9947
34. Kim I.S., Otto F., Zabel B., and Mundlos S. Regulation of chondrocyte differentiation by Cbfa1. Mech. Dev. 80 (1999) 159-170
35. Kitching R., Qi S., Li V., Raouf A., Vary C.P., and Seth A. Coordinate gene expression patterns during osteoblast maturation and retinoic acid treatment of MC3T3-E1 cells. J. Bone Miner. Metab. 20 (2002) 269-280
36. Komori T. Regulation of skeletal development by the Runx family of transcription factors. J. Cell. Biochem. 95 (2005) 445-453
37. Lengner C.J., Drissi H., Choi J.Y., van Wijnen A.J., Stein J.L., Stein G.S., and Lian J.B. Activation of the bone-related Runx2/Cbfa1 promoter in mesenchymal condensations and developing chondrocytes of the axial skeleton. Mech. Dev. 114 (2002) 167-170
38. Liu D., Kang J.S., and Derynck R. TGF-beta-activated Smad3 represses MEF2-dependent transcription in myogenic differentiation. EMBO J. 23 (2004) 1557-1566
39. Liu Y., Shi Z., Silveira A., Liu J., Sawadogo M., Yang H., and Feng X. Involvement of upstream stimulatory factors 1 and 2 in RANKL-induced transcription of tartrate-resistant acid phosphatase gene during osteoclast differentiation. J. Biol. Chem. 278 (2003) 20603-20611
40. Lockyer P.J., Vanlingen S., Reynolds J.S., McNulty T.J., Irvine R.F., Parys J.B., and Cullen P.J. Tissue-specific expression and endogenous subcellular distribution of the inositol 1,3,4,5-tetrakisphosphate-binding proteins GAP1(IP4BP) and GAP1(m). Biochem. Biophys. Res. Commun. 255 (1999) 421-426
41. Marie P.J. Role of N-cadherin in bone formation. J. Cell. Physiol. 190 (2002) 297-305
42. Mattson M.P., Duan W., Chan S.L., and Camandola S. Par-4: an emerging pivotal player in neuronal apoptosis and neurodegenerative disorders. J. Mol. Neurosci. 13 (1999) 17-30
43. May L.G., and Gay C.V. Multiple G-protein involvement in parathyroid hormone regulation of acid production by osteoclasts. J. Cell. Biochem. 64 (1997) 161-170
44. Miyazawa T., Ogawa Y., Chusho H., Yasoda A., Tamura N., Komatsu Y., Pfeifer A., Hofmann F., and Nakao K. Cyclic GMP-dependent protein kinase II plays a critical role in C-type natriuretic peptide-mediated endochondral ossification. Endocrinology 143 (2002) 3604-3610
45. Miyazono K., Maeda S., and Imamura T. Coordinate regulation of cell growth and differentiation by TGF-beta superfamily and Runx proteins. Oncogene 23 (2004) 4232-4237
46. Mundlos S., Otto F., Mundlos C., Mulliken J.B., Aylsworth A.S., Albright S., Lindhout D., Cole W.G., Henn W., Knoll J.H., Owen M.J., Mertelsmann R., Zabel B.U., and Olsen B.R. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89 (1997) 773-779
47. Ntambi J.M., Miyazaki M., Stoehr J.P., Lan H., Kendziorski C.M., Yandell B.S., Song Y., Cohen P., Friedman J.M., and Attie A.D. Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc. Natl. Acad. Sci. USA 99 (2002) 11482-11486
48. Okamatsu Y., Kim D., Battaglino R., Sasaki H., Spate U., and Stashenko P. MIP-1 gamma promotes receptor-activator-of-NF-kappa-B-ligand-induced osteoclast formation and survival. J. Immunol. 173 (2004) 2084-2090
49. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R., Selby P.B., and Owen M.J. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89 (1997) 765-771
50. Peters T., Dildrop R., Ausmeier K., and Ruther U. Organization of mouse Iroquois homeobox genes in two clusters suggests a conserved regulation and function in vertebrate development. Genome Res. 10 (2000) 1453-1462
51. Pichaud F., Delage-Mourroux R., Frenkian M., Frendo J.L., Roux S., de Vernejoul M.C., and Jullienne A. Type-I 15-hydroxyprostaglandin dehydrogenase: role in macrophage/osteoclast differentiation. Adv. Exp. Med. Biol. 433 (1997) 399-402
52. Pisani D.F., Leclerc L., Jarretou G., Marini J.F., and Dechesne C.A. SMHS1 is involved in oxidative/glycolytic-energy metabolism balance of muscle fibers. Biochem. Biophys. Res. Commun. 326 (2005) 788-793
53. Poliakov A., Cotrina M., and Wilkinson D.G. Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell 7 (2004) 465-480
54. Qin C., Baba O., and Butler W.T. Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit. Rev. Oral. Biol. Med. 15 (2004) 126-136
55. Quarles L.D. FGF23, PHEX, and MEPE regulation of phosphate homeostasis and skeletal mineralization. Am. J. Physiol. Endocrinol. Metab. 285 (2003) 1-9
56. Rescher U., and Gerke V. Annexins-unique membrane binding proteins with diverse functions. J. Cell. Sci. 117 (2004) 2631-2639
57. Reymond A., Marigo V., Yaylaoglu M.B., Leoni A., Ucla C., Scamuffa N., Caccioppoli C., Dermitzakis E.T., Lyle R., Banfi S., Eichele G., Antonarakis S.E., and Ballabio A. Human chromosome 21 gene expression atlas in the mouse. Nature 420 (2002) 582-586
58. Robinson P.N., Wollstein A., Bohme U., and Beattie B. Ontologizing gene-expression microarray data: characterizing clusters with Gene Ontology. Bioinformatics 20 (2004) 979-981
59. Sanjo H., Kawai T., and Akira S. DRAKs, novel serine/threonine kinases related to death-associated protein kinase that trigger apoptosis. J. Biol. Chem. 273 (1998) 29066-29071
60. Sato M., Morii E., Komori T., Kawahata H., Sugimoto M., Terai K., Shimizu H., Yasui T., Ogihara H., Yasui N., Ochi T., Kitamura Y., Ito Y., and Nomura S. Transcriptional regulation of osteopontin gene in vivo by PEBP2alphaA/CBFA1 and ETS1 in the skeletal tissues. Oncogene 17 (1998) 1517-1525
61. Smith A.N., Borthwick K.J., and Karet F.E. Molecular cloning and characterization of novel tissue-specific isoforms of the human vacuolar H(+)-ATPase C, G and d subunits, and their evaluation in autosomal recessive distal renal tubular acidosis. Gene 297 (2002) 169-177
62. Steiglitz B.M., Keene D.R., and Greenspan D.S. PCOLCE2 encodes a functional procollagen C-proteinase enhancer (PCPE2) that is a collagen-binding protein differing in distribution of expression and post-translational modification from the previously described PCPE1. J. Biol. Chem. 277 (2002) 49820-49830
63. Stein G.S., Lian J.B., van Wijnen A.J., Stein J.L., Montecino M., Javed A., Zaidi S.K., Young D.W., Choi J.Y., and Pockwinse S.M. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene 23 (2004) 4315-4329
64. Stipanuk M.H. Role of the liver in regulation of body cysteine and taurine levels: a brief review. Neurochem. Res. 29 (2004) 105-110
65. Stoffel W., Jenke B., Block B., Zumbansen M., and Koebke J. Neutral sphingomyelinase 2 (smpd3) in the control of postnatal growth and development. Proc. Natl. Acad. Sci. USA 102 (2005) 4554-4559
66. Stricker S., Fundele R., Vortkamp A., and Mundlos S. Role of Runx genes in chondrocyte differentiation. Dev. Biol. 245 (2002) 95-108
67. Suen P.W., Ilic D., Caveggion E., Berton G., Damsky C.H., and Lowell C.A. Impaired integrin-mediated signal transduction, altered cytoskeletal structure and reduced motility in Hck/Fgr deficient macrophages. J. Cell. Sci. 112 (1999) 4067-4078
68. Uchida M., Shima M., Chikazu D., Fujieda A., Obara K., Suzuki H., Nagai Y., Yamato H., and Kawaguchi H. Transcriptional induction of matrix metalloproteinase-13 (collagenase-3) by 1alpha,25-dihydroxyvitamin D3 in mouse osteoblastic MC3T3-E1 cells. J. Bone Miner. Res. 16 (2001) 221-230
69. Wang Q., Xie Y., Du Q.S., Wu X.J., Feng X., Mei L., McDonald J.M., and Xiong W.C. Regulation of the formation of osteoclastic actin rings by proline-rich tyrosine kinase 2 interacting with gelsolin. J. Cell. Biol. 160 (2003) 565-575
70. Wennberg C., Hessle L., Lundberg P., Mauro S., Narisawa S., Lerner U.H., and Millan J.L. Functional characterization of osteoblasts and osteoclasts from alkaline phosphatase knockout mice. J. Bone Miner. Res. 15 (2000) 1879-1888
71. Witke W., Li W., Kwiatkowski D.J., and Southwick F.S. Comparisons of CapG and gelsolin-null macrophages: demonstration of a unique role for CapG in receptor-mediated ruffling, phagocytosis, and vesicle rocketing. J. Cell. Biol. 154 (2001) 775-784
72. Wodicka L., Dong H., Mittmann M., Ho M.H., and Lockhart D.J. Genome-wide expression monitoring in Saccharomyces cerevisiae. Nat. Biotechnol. 15 (1997) 1359-1367
73. Wu W., Glinka A., Delius H., and Niehrs C. Mutual antagonism between dickkopf1 and dickkopf2 regulates Wnt/beta-catenin signalling. Curr. Biol. 10 (2000) 1611-1614
74. Yoshida C.A., Yamamoto H., Fujita T., Furuichi T., Ito K., Inoue K., Yamana K., Zanma A., Takada K., Ito Y., and Komori T. Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev. 18 (2004) 952-963
75. Yu X., Huang Y., Collin-Osdoby P., and Osdoby P. CCR1 chemokines promote the chemotactic recruitment, RANKL development, and motility of osteoclasts and are induced by inflammatory cytokines in osteoblasts. J. Bone Miner. Res. 19 (2004) 2065-2077
76. Zeng W., Yuan W., Wang Y., Jiao W., Zhu Y., Huang C., Li D., Li Y., Zhu C., Wu X., and Liu M. Expression of a novel member of sorting nexin gene family, SNX-L, in human liver development. Biochem. Biophys. Res. Commun. 299 (2002) 542-548