Transcriptional Characterization of Bone Morphogenetic Proteins (BMPs)-Mediated Osteogenic Signaling

Journal of Cellular Biochemistry

Volumn 90, Issue 6, 2003, Pages 1149-1165

  Peng, Ying ^a,b   Kang, Quan ^a,c   Cheng, Hongwei ^a   Li, Xinmin ^b   Sun, Michael H ^a   Jiang, Wei ^a   Luu, Hue H ^a   Park, Jae Yoon ^a   Haydon, Rex C ^a   He, Tong Chuan ^a,b  

^a UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Bone formation; Expression profiling; Osteoblast differentiation; Osteogenesis; Signal transduction

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 12; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 9; OSTEOGENIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL STIMULATION; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; EMBRYO; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC ANALYSIS; HUMAN; HUMAN CELL; MALE; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION;

ADENOVIRIDAE; ALKALINE PHOSPHATASE; ANIMALS; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, NUDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOGENESIS; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 0345305861     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.10744     Document Type: Article

References (48)

1. Afrakhte M, Moren 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.
2. Aubin JE. 1998. Advances in the osteoblast lineage. Biochem Cell Biol 76:899-910.
3. Aubin JE. 2001. Regulation of osteoblast formation and function. Rev Endocr Metab Disord 2:81-94.
4. Balint E, Lapointe D, Drissi H, Van Der Meijden C, Young DW, Van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2003. Phenotype discovery by gene expression profiling: Mapping of biological processes linked to BMP-2-mediated osteoblast differentiation. J Cell Biochem 89: 401-426.
5. Baltzer AW, Lattermann C, Whalen JD, Ghivizzani S, Wooley P, Krauspe R, Robbins PD, Evans CH. 2000. Potential role of direct adenoviral gene transfer in enhancing fracture repair. Clin Orthop 379:S120-S125.
6. Beck GR, Jr., Zerler B, Moran E. 2001. Gene array analysis of osteoblast differentiation. Cell Growth Differ 12: 61-83.
7. Butte A. 2002. The use and analysis of microarray data. Nat Rev Drug Discov 1:951-960.
8. Cheng H, Jiang W, Phillips FM, Haydon RC, Peng Y, Zhou L, Luu HH, An N, Breyer B, Vanichakarn P, Szatkowski JP, Park JP, He T-C. 2003. Osteogenic activity of the 14 types of human bone morphogenetic proteins (BMPs). J Bone Joint Surg Am 85-A:1544-1552.
9. Daluiski A, Engstrand T, Bahamonde ME, Gamer LW, Agius E, Stevenson SL, Cox K, Rosen V, Lyons KM. 2001. Bone morphogenetic protein-3 is a negative regulator of bone density. Nat Genet 27:84-88.
10. 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.
11. Harris SE, Harris MA. 2001. Gene expression profiling in osteoblast biology: Bioinformatic tools. Mol Biol Rep 28: 139-156.
12. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. 1998a. Identification of c-MYC as a target of the APC pathway. Science 281:1509-1512.
13. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. 1998b. A simplified system for generating recombinant-β adenoviruses. Proc Natl Acad Sci USA 95:2509-2514.
14. Heldin CH, Miyazono K, ten Dijke P. 1997. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465-471.
15. Hoffmann A, Gross G. 2001. BMP signaling pathways in cartilage and bone formation. Crit Rev Eukaryot Gene Expr 11:23-45.
16. Hogan BL. 1996. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev 10:1580-1594.
17. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A. 1999. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 274:19838-19845.
18. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K. 1997. Smad6 inhibits signalling by the TGF-β superfamily. Nature 389:622-626.
19. Itoh S, Itoh F, Goumans MJ, Ten Dijke P. 2000. Signaling of transforming growth factor-β family members through Smad proteins. Eur J Biochem 267:6954-6967.
20. Kang Y, Chen CR, Massague J. 2003. A self-enabling TGF-β response coupled to stress signaling. Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell 11:915-926.
21. 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.
22. Kreider BL, Benezra R, Rovera G, Kadesch T. 1992. Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science 255:1700-1702.
23. Li C, Wong WH. 2001. Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31-36.
24. Lian JB, Stein GS, Stein JL, van Wijnen AJ. 1998. Transcriptional control of osteoblast differentiation. Biochem Soc Trans 26:14-21.
25. 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.
26. Massague J. 1998. TGF-β signal transduction. Annu Rev Biochem 67:753-791.
27. Merlo GR, Zerega B, Paleari L, Trombino S, Mantero S, Levi G. 2000. Multiple functions of Dlx genes. Int J Dev Biol 44:619-626.
28. Murray SS, Murray EJ, Glackin CA, Urist MR. 1993. Bone morphogenetic protein inhibits differentiation and affects expression of helix-loop-helix regulatory molecules in myoblastic cells. J Cell Biochem 53:51-60.
29. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH, ten Dijke P. 1997. Identification of Smad7, a TGF-β-inducible antagonist of TGF-beta signalling. Nature 389:631-635.
30. Norton JD. 2000. ID helix-loop-helix proteins in cell growth, differentiation, and tumorigenesis. J Cell Sci 113:3897-3905.
31. Ogata T, Wozney JM, Benezra R, Noda M. 1993. Bone morphogenetic protein 2 transiently enhances expression of a gene, Id (inhibitor of differentiation), encoding a helix-loop-helix molecule in osteoblast-like cells. Proc Natl Acad Sci USA 90:9219-9222.
32. Olsen BR, Reginato AM, Wang W. 2000. Bone development. Annu Rev Cell Dev Biol 16:191-220.
33. Panganiban G, Rubenstein JL. 2002. Developmental functions of the Distal-less/Dlx homeobox genes. Development 129:4371-4386.
34. Qiu M, Bulfone A, Ghattas I, Meneses JJ, Christensen L, Sharpe PT, Presley R, Pedersen RA, Rubenstein JL. 1997. Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: Mutations of Dlx-1, Dlx-2, and Dlx-1 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev Biol 185:165-184.
35. Raouf A, Seth A. 2002. Discovery of osteoblast-associated genes using cDNA microarrays. Bone 30:463-471.
36. Reddi AH. 1997. Bone morphogenetic proteins: An unconventionalapproach to isolation of first mammalian morphogens. Cytokine Growth Factor Rev 8:11-20.
37. Reddi AH. 1998. Role of morphogenetic proteins in skeletal tissue engineering and regeneration. Nat Biotechnol 16: 247-252.
38. Roman-Roman S, Garcia T, Jackson A, Theilhaber J, Rawadi G, Connolly T, Spinella-Jaegle S, Kawai S, Courtois B, Bushnell S, Auberval M, Call K, Baron R. 2003. Identification of genes regulated during osteoblastic differentiation by genome-wide expression analysis of mouse calvaria primary osteoblasts in vitro. Bone 32: 474-482.
39. Sun MH, Cheng H, Phillips FM, Peng Y, Kang Q, Haydon RC, He T-C. 2003. Bone morphogenetic proteins and bone regeneration: From biology to clinical applications. Adv Osteoporotic Fracture Manage 2: 70-78.
40. 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.
41. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121.
42. Urist MR. 1997. Bone morphogenetic protein: The molecularization of skeletal system development. J Bone Miner Res 12:343-346.
43. Urist MR, Nilsson O, Rasmussen J, Hirota W, Lovell T, Schmalzreid T, Finerman GA. 1987. Bone regeneration under the influence of a bone morphogenetic protein (BMP) β tricalcium phosphate (TCP) composite in skull trephine defects in dogs. Clin Orthop 214:295-304.
44. Vaes BL, Dechering KJ, Feijen A, Hendriks JM, Lefevre C, Mummery CL, Olijve W, van Zoelen EJ, Steegenga WT. 2002. Comprehensive microarray analysis of bone morphogenetic protein 2-induced osteoblast differentiation resulting in the identification of novel markers for bone development. J Bone Miner Res 17:2106-2118.
45. 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.
46. Wrana JL. 2000. Regulation of Smad activity. Cell 100: 189-192.
47. Zhao GQ. 2003. Consequences of knocking out BMP signaling in the mouse. Genesis 35:43-56.
48. Zou H, Choe KM, Lu Y, Massague J, Niswander L. 1997. BMP signaling and vertebrate limb development. Cold Spring Harb Symp Quant Biol 62:269-272.