Gene Array Analysis of Bone Morphogenetic Protein Type I Receptor-Induced Osteoblast Differentiation

Journal of Bone and Mineral Research

Volumn 18, Issue 7, 2003, Pages 1177-1185

  Korchynskyi, Olexander ^a   Dechering, Koen J ^b   Sijbers, Anneke M ^b   Olijve, Wiebe ^b,c   Ten Dijke, Peter ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b NV ORGANON   (Netherlands)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Bone morphogenetic proteins; Microarray; Osteoblast; Signal transduction; Smad

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN RECEPTOR; FIBROMODULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMAD PROTEIN; TRANSCRIPTION FACTOR;

ADENOVIRUS; ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; DNA MICROARRAY; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE TRANSFER; GENETIC ANALYSIS; HYBRIDIZATION; MESENCHYME CELL; MOUSE; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; SIGNAL TRANSDUCTION; UNINDEXED SEQUENCE;

ANIMALS; BLOTTING, NORTHERN; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL DIFFERENTIATION; CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; OSTEOBLASTS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, GROWTH FACTOR; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 0142091251     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.2003.18.7.1177     Document Type: Article

References (60)

1. Urist MR 1965 Bone: Formation by autoinduction. Science 150:893-899.
2. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA 1988 Novel regulators of bone formation: Molecular clones and activities. Science 242:1528-1534.
3. Sampath TK, Maliakal JC, Hauschka PV, Jones WK, Sasak H, Tucker RF, White KH, Coughlin JE, Tucker MM, Pang RH 1992 Recombinant human osteogenic protein-1 (hOP-1) induces new bone formation in vivo with a specific activity comparable with natural bovine osteogenic protein and stimulates osteoblast proliferation and differentiation in vitro. J Biol Chem 267:20352-20362.
4. Vukicevic S, Luyten FP, Reddi AH 1989 Stimulation of the expression of osteogenic and chondrogenic phenotypes in vitro by osteogenin. Proc Natl Acad Sci USA 86:8793-8797.
5. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T 1994 Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 127:1755-1766.
6. Yamaguchi A, Katagiri T, Ikeda T, Wozney JM, Rosen V, Wang EA, Kahn AJ, Suda T, Yoshiki S 1991 Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681-687.
7. Chen D, Ji X, Harris MA, Feng JQ, Karsenty G, Celeste AJ, Rosen V, Mundy GR, Harris SE 1998 Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages. J Cell Biol 142:295-305.
8. Yeh LC, Tsai AD, Lee JC 2002 Osteogenic protein-1 (OP-1, BMP-7) induces osteoblastic cell differentiation of the pluripotent mesenchymal cell line C2C12. J Cell Biochem 87:292-304.
9. Kawabata M, Inoue H, Hanyu A, Imamura T, Miyazono K 1998 Smad proteins exist as monomers in vivo and undergo homo- and hetero-oligomerization upon activation by serine/threonine kinase receptors. EMBO J 17:4056-4065.
10. Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J 1994 Mechanism of activation of the TGF-β receptor. Nature 370:341-347.
11. Carcámo J, Weis FM, Ventura F, Wieser R, Wrana JL, Attisano L, Massagué J 1994 Type I receptors specify growth-inhibitory and transcriptional responses to transforming growth factor β and activin. Mol Cell Biol 14:3810-3821.
12. Wieser R, Wrana JL, Massagué J 1995 GS domain mutations that constitutively activate T β R-I, the downstream signaling component in the TGF-β receptor complex. EMBO J 14:2199-2208.
13. Hoodless PA, Haerry T, Abdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL 1996 MADRI, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85:489-500.
14. Kretzschmar M, Liu F, Hata A, Doody J, Massagué J 1997 The TGF-β family mediator Smadl is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev 11:984-995.
15. Derynck R, Zhang Y, Feng XH 1998 Smads: Transcriptional activators of TGF-β responses. Cell 95:737-740.
16. Massagué J 1998 TGF-β signal transduction. Annu Rev Biochem 67:753-791.
17. Massagué J, Wotton D 2000 Transcriptional control by the TGF-β/Smad signaling system. EMBO J 19:1745-1754.
18. Korchynskyi O, ten Dijke P 2002 Bone morphogenetic protein receptors and their nuclear effectors in bone formation. In: Vukicevic S, Sampath T (eds.) Bone Morphogenetic Proteins: From Discovery to Clinical Applications. Birkhauser Verlag, Basel, Switzerland, pp. 41-54.
19. Korchynskyi O, ten Dijke P 2002 Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277:4883-4891.
20. Lopez-Rovira T, Chalaux E, Massagué J, Rosa JL, Ventura F 2002 Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J Biol Chem 277:3176-3185.
21. Chalaux E, Lopez-Rovira T, Rosa JL, Bartrons R, Ventura F 1998 JunB is involved in the inhibition of myogenic differentiation by bone morphogenetic protein-2. J Biol Chem 273:537-543.
22. Zou H, Wieser R, Massagué J, Niswander L 1997 Distinct roles of type 1 bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev 11:2191-2203.
23. Panchision DM, Pickel JM, Studer L, Lee SH, Turner PA, Hazel TG, McKay RD 2001 Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev 15:2094-2110.
24. Namiki M, Akiyama S, Katagiri T, Suzuki A, Ueno N, Yamaji N, Rosen V, Wozney JM, Suda T 1997 A kinase domain-truncated type I receptor blocks bone morphogenetic protein-2-induced signal transduction in C2C12 myoblasts. J Biol Chem 272:22046-22052.
25. Fujii M, Takeda K, Imamura T, Aoki H, Sampath TK, Enomoto S, Kawabata M, Kato M, Ichijo H, Miyazono K 1999 Roles of bone morphogenetic protein type 1 receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol Biol Cell 10:3801-3813.
26. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P 1997 TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16:5353-5362.
27. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, Engstrom U, Heldin CH, Funa K, ten Dijke P 1998 The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Lett 434:83-87.
28. Yue H, Eastman PS, Wang BB, Minor J, Doctolero MH, Nuttall RL, Stack R, Becker JW, Montgomery JR, Vainer M, Johnston R 2001 An evaluation of the performance of cDNA microarrays for detecting changes in global mRNA expression. Nucleic Acids Res 29:E41.
29. Venables WN, Ripley BD 1997 Modern Applied Statistics with S-PLUS, 2nd ed. Springer, Basel, Switzerland.
30. Ebisawa T, Tada K, Kitajima I, Tojo K, Sampath TK, Kawabata M, Miyazono K, Imamura T 1999 Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation. J Cell Sci 112:3519-3527.
31. ten Dijke P, Yamashita H, Sampath TK, Reddi AH, Estevez M, Riddle DL, Ichijo H, Heldin CH, Miyazono K 1994 Identification of type I receptors for osteogenic protein-I and bone morphogenetic protein-4. J Biol Chem 269:16985-16988.
32. Afrakhte M, Morén A, Jossan S, Itoh S, Sampath K, Westermark B, Heldin CH, Heldin NE, ten Dijke P 1998 Induction of inhibitory Smad6 and Smad7 mRNA by TGF-β family members. Biochem Biophys Res Commun 249:505-511.
33. Takase M, Imamura T, Sampath TK, Takeda K, Ichijo H, Miyazono K, Kawabata M 1998 Induction of Smad6 mRNA by bone morphogenetic proteins. Biochem Biophys Res Commun 244:26-29.
34. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G 1997 Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89:747-754.
35. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, Wozney JM, Kim EG, Choi JY, Ryoo HM, Bae SC 2000 Runx2 is a common target of transforming growth factor β1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 20:8783-8792.
36. Gori F, Schipani E, Demay MB 2001 Fibromodulin is expressed by both chondrocytes and osteoblasts during fetal bone development. J Cell Biochem 82:46-57.
37. Yeh LC, Adamo ML, Duan C, Lee JC 1998 Osteogenic protein-I regulates insulin-like growth factor-I (IGF-I), IGF-II, and IGF-binding protein-5 (IGFBP-5) gene expression in fetal rat calvaria cells by different mechanisms. J Cell Physiol 175:78-88.
38. Yeh LC, Lee JC 2000 Identification of an osteogenic protein-I (bone morphogenetic protein-7)-responsive element in the promoter of the rat insulin-like growth factor-binding protein-5 gene. Endocrinology 141:3278-3286.
39. Locklin RM, Riggs BL, Hicok KC, Horton HF, Byrne MC, Khosla S 2001 Assessment of gene regulation by bone morphogenetic protein 2 in human marrow stromal cells using gene array technology. J Bone Miner Res 16:2192-2204.
40. Ho NC, Jia L, Driscoll CC, Gutter EM, Francomano CA 2000 A skeletal gene database. J Bone Miner Res 15:2095-2122.
41. Garcia T, Roman-roman S, Jackson A, Theilhaber J, Connolly T, Spinella-jaegle S, Kawai S, Courtois B, Bushnell S, Auberval M, Call K, Baron R 2002 Behavior of osteoblast, adipocyte, and myoblast markers in genome-wide expression analysis of mouse calvaria primary osteoblasts in vitro. Bone 31:205-211.
42. Romano LA, Runyan RB 2000 Slug is an essential target of TGFβ2 signaling in the developing chicken heart. Dev Biol 223:91-102.
43. Aoki H, Fujii M, Imamura T, Yagi K, Takehara K, Kato M, Miyazono K 2001 Synergistic effects of different bone morphogenetic protein type I receptors on alkaline phosphatase induction. J Cell Sci 114:1483-1489.
44. Grimaldi PA, Teboul L, Inadera H, Gaillard D, Amri EZ 1997 Trans-differentiation of myoblasts to adipoblasts: Triggering effects of fatty acids and thiazolidinediones. Prostaglandins Leukot Essent Fatty Acids 57:71-75.
45. Iso T, Chung G, Hamamori Y, Kedes L 2002 HERPI is a cell type-specific primary target of Notch. J Biol Chem 277:6598-6607.
46. Sun J, Kamei CN, Layne MD, Jain MK, Liao JK, Lee ME, Chin MT 2001 Regulation of myogenic terminal differentiation by the hairy-related transcription factor CHF2. J Biol Chem 276:18591-18596.
47. Jen Y, Weintraub H, Benezra R 1992 Overexpression of Id protein inhibits the muscle differentiation program: In vivo association of Id with E2A proteins. Genes Dev 6:1466-1479.
48. Hajra KM, Chen DY, Fearon ER 2002 The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 62:1613-1618.
49. Savagner P, Yamada KM, Thiery JP 1997 The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J Cell Biol 137:1403-1419.
50. Karin M, Ben Neriah Y 2000 Phosphorylation meets ubiquitination: The control of NF-κB activity. Annu Rev Immunol 18:621-663.
51. Bitzer M, von Gersdorff G, Liang D, Dominguez-Rosales A, Beg AA, Rojkind M, Bottinger EP 2000 A mechanism of suppression of TGF-β/SMAD signaling by NF-κB/RelA. Genes Dev 14:187-197.
52. Sidow A, Bulotsky MS, Kerrebrock AW, Birren BW, Altshuler D, Jaenisch R, Johnson KR, Lander ES 1999 A novel member of the F-box/WD40 gene family, encoding dactylin, is disrupted in the mouse dactylaplasia mutant. Nat Genet 23:104-107.
53. Inbal B, Shani G, Cohen O, Kissil JL, Kimchi A 2000 Death-associated protein kinase-related protein 1, a novel serine/ threonine kinase involved in apoptosis. Mol Cell Biol 20:1044-1054.
54. Kawai T, Matsumoto M, Takeda K, Sanjo H, Akira S 1998 ZIP kinase, a novel serine/threonine kinase which mediates apoptosis. Mol Cell Biol 18:1642-1651.
55. Kogel D, Plottner O, Landsberg G, Christian S, Scheidtmann KH 1998 Cloning and characterization of Dlk, a novel serine/threonine kinase that is tightly associated with chromatin and phosphorylates core histones. Oncogene 17:2645-2654.
56. 2+-free smooth muscle contraction via myosin light chain phosphorylation. J Biol Chem 276:29567-29574.
57. Jang CW, Chen CH, Chen CC, Chen JY, Su YH, Chen RH 2002 TGF-β induces apoptosis through Smad-mediated expression of DAP-kinase. Nat Cell Biol 4:51-58.
58. Bachner D, Ahrens M, Schroder D, Hoffmann A, Lauber J, Betat N, Steinert P, Flohe L, Gross G 1998 Bmp-2 downstream targets in mesenchymal development identified by subtractive cloning from recombinant mesenchymal progenitors (C3H10T1/2). Dev Dyn 213:398-411.
59. Contos JJ, Fukushima N, Weiner JA, Kaushal D, Chun J 2000 Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc Natl Acad Sci USA 97:13384-13389.
60. Laing JG, Manley-Markowski RN, Koval M, Civitelli R, Steinberg TH 2001 Connexin45 interacts with zonula occludens-1 and connexin43 in osteoblastic cells. J Biol Chem 276:23051-23055.