Runx1/AML1 hematopoietic transcription factor contributes to skeletal development in vivo

Journal of Cellular Physiology

Volumn 196, Issue 2, 2003, Pages 301-311

  Lian, Jane B ^a   Balint, Eva ^a   Javed, Amjad ^a   Drissi, Hicham ^a   Vitti, Regan ^a   Quinlan, Edward J ^a   Zhang, Lina ^b   Van Wijnen, Andre J ^a   Stein, Janet L ^a   Speck, Nancy ^b   Stein, Gary S ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; EMBRYO; EMBRYO DEVELOPMENT; MOUSE; NEWBORN; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; ANIMALS, NEWBORN; BONE AND BONES; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DNA-BINDING PROTEINS; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; MICE; OSTEOBLASTS; OSTEOGENESIS; PROTO-ONCOGENE PROTEINS; SKELETON; TRANSCRIPTION FACTORS;

EID: 0038460942     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.10316     Document Type: Article

References (59)

1. Alvarez J, Horton J, Sohn P, Serra R. 2001. The perichondrium plays an important role in mediating the effects of TGF-beta1 on endochondral bone formation. Dev Dyn 221:311-321.
2. Bae SC, Ogawa E, Maruyama M, Oka H, Satake M, Shigesada K, Jenkins NA, Gilbert DJ, Copeland NG, Ito Y. 1994. PEBP2 alpha B/mouse AML1 consists of multiple isoforms that possess differential transactivation potentials. Mol Cell Biol 14:3242-3252.
3. Banerjee C, McCabe LR, Choi J-Y, Hiebert SW, Stein JL, Stein GS, Lian JB. 1997. Runt homology domain proteins in osteoblast differentiation: AML-3/CBFA1 is a major component of a bone specific complex. J Cell Biochem 66:1-8.
4. Banerjee C, Javed A, Choi J-Y, Green J, Rosen V, van Wijnen AJ, Stein JL, Lian JB, Stein GS. 2001. Differential regulation of the two principal Runx2/Cbfa1 N-terminal isoforms in response to bone morphogenetic protein-2 during development of the osteoblast phenotype. Endocrinology 142:4026-4039.
5. Bernardin F, Friedman AD. 2002. AML1 stimulates G1 to S progression via its transactivation domain. Oncogene 21:3247-3252.
6. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. 1999. Sox9 is required for cartilage formation. Nat Genet 22:85-89.
7. Bianco P, Gehron RP. 2000. Marrow stromal stem cells. J Clin Invest 105:1663-1668.
8. Bodine PVN, Trailsmith M, Komm BS. 1996. Development and characterization of a conditionally transformed adult human osteoblastic cell line. J Bone Miner Res 11:806-819.
9. Bortell R, Owen TA, Shalhoub V, Heinrichs A, Aronow MA, Rochette-Egly C, Lutz Y, Stein JL, Lian JB, Stein GS. 1993. Constitutive transcription of the osteocalcin gene in osteosarcoma cells is reflected by altered protein-DNA interactions at promoter regulatory elements. Proc Natl Acad Sci USA 90:2300-2304.
10. Bronckers AL, Engelse MA, Cavender A, Gaikwad J, D'Souza RN. 2001. Cell-specific patterns of Cbfa1 mRNA and protein expression in postnatal murine dental tissues. Mech Dev 101:255-258.
11. Burstone MS. 1962. Alkaline phosphatase, naphthol AS-BI phosphate method. In: Burstone MS, editor. Enzyme histochemistry and its application on the study of neoplasm. New York: Academic Press. pp 275-276.
12. Choi J-Y, Lee B-H, Song K-B, Park R-W, Kim I-S, Sohn K-Y, Jo J-S, Ryoo H-M. 1996. Expression patterns of bone-related proteins during osteoblastic differentiation in MC3T3-E1 cells. J Cell Biochem 61:609-618.
13. Choi J-Y, Pratap J, Javed A, Zaidi SK, Xing L, Balint E, Dalamangas S, Boyce B, van Wijnen AJ, Lian JB, Stein JL, Jones SN, Stein GS. 2001. Subnuclear targeting of Runx/Cbfa/AML factors is essential for tissue-specific differentiation during embryonic development. Proc Natl Acad Sci USA 98:8650-8655.
14. Corsetti MT, Calabi F. 1997. Lineage- and stage-specific expression of runt box polypeptides in primitive and definitive hematopoiesis. Blood 89:2359-2368.
15. Crosier PS, Kalev-Zylinska ML, Hall CJ, Flores MV, Horsfield JA, Crosier KE. 2002. Pathways in blood and vessel development revealed through zebrafish genetics. Int J Dev Biol 46:493-502.
16. de Crombrugghe B, Lefebvre V, Nakashima K. 2001. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr Opin Cell Biol 13:721-727.
17. Drissi H, Luc Q, Shakoori R, Chuva de Sousa Lopes S, Choi J-Y, Terry A, Hu M. Jones S. Neil JC. Lian JB. Stein JL. van Wijnen AJ, and Stein GS. 2000. Transcriptional autoregulation of the bone related CBFA1/RUNX2 gene. J Cell Physiol 184:341-350.
18. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. 1997. Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89:747-754.
19. Gutierrez S, Javed A, Tennant D, van Rees M, Montecino M, Stein GS, Stein JL, Lian JB. 2002. CCAAT/enhancer-binding proteins (C/EBP) b and d activate osteocalcin gene transcription and synergize with Runx2 at the C/EBP element to regulate bone-specific expression. J Biol Chem 277:1316-1323.
20. Hou Z, Nguyen Q, Frenkel B, Nilsson SK, Milne M, van Wijnen AJ, Stein JL, Quesenberry P, Lian JB, Stein GS. 1999. Osteoblast-specific gene expression after transplantation of marrow cells: Implications for skeletal gene therapy. Proc Natl Acad Sci USA 96:7294-7299.
21. Huss R. 2000. Perspectives on the morphology and biology of CD34-negative stem cells. J Hematother Stem Cell Res 9:783-793.
22. Javed A, Guo B, Hiebert S, Choi J-Y, Green J, Zhao S-C, Osborne MA, Stifani S, Stein JL, Lian JB, van Wijnen AJ, Stein GS. 2000. Groucho/TLE/R-Esp proteins associate with the nuclear matrix and repress RUNX (CBFa/AML/PEBP2a) dependent activation of tissue-specific gene transcription. J Cell Sci 113:2221-2231.
23. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao Y-H, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
24. Lee MH, Javed A, Kim HJ, Shin HI, Gutierrez S, Choi JY, Rosen V, Stein JL, van Wijnen AJ, Stein GS, Lian JB, Ryoo HM. 1999. Transient upregulation of CBFA1 in response to bone morphogenetic protein-2 and transforming growth factor bl in C2C12 myogenic cells coincides with suppression of the myogenic phenotype but is not sufficient for osteoblast differentiation. J Cell Biochem 73:114-125.
25. 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 beta1 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.
26. Lengner CJ, Drissi H, Choi J-Y, van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2002. Activation of the bone related Runx2/Cbfa1 promoter in mesenchymal condensations and developing chondrocytes of the axial skeleton. Mech Dev 114:167-170.
27. Levanon D, Brenner O, Negreanu V, Bettoun D, Woolf E, Eilam R, Lotem J, Gat U, Otto F, Speck N, Groner Y. 2001. Spatial and temporal expression pattern of Runx3 (Aml2) and Runx1 (Aml1) indicates non-redundant functions during mouse embryogenesis. Mech Dev 109:413-417.
28. Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R, Bernstein Y, Goldenberg D, Xiao C, Fliegauf M, Kremer E, Otto F, Brenner O, Lev-Tov A, Groner Y. 2002. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 21:3454-3463.
29. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ, Lee KY, Nomura S, Lee CW, Han SB, Kim HM, Kim WJ, Yamamoto H, Yamashita N, Yano T, Ikeda T, Itohara S, Inazawa J, Abe T, Hagiwara A, Yamagishi H, Ooe A, Kaneda A, Sugimura T, Ushijima T, Bae SC, Ito Y. 2002. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109:113-124.
30. Lian JB, Stein GS. 2001. Osteoblast biology. In: Marcus R, Feldman D, Kelsey J, editors. Osteoporosis. San Diego: Academic Press. pp 21-71.
31. Lutterbach B, Hiebert SW. 2000. Role of the transcription factor AML-1 in acute leukemia and hematopoietic differentiation. Gene 245:223-235.
32. Marusic A, Grcevic D, Katavic V, Kovacic N, Lukic IK, Kalajzic I, Lorenzo JA. 2000. Role of B lymphocytes in new bone formation. Lab Invest 80:1761-1774.
33. Meyers S, Hiebert SW. 2000. Alterations in subnuclear trafficking of nuclear regulatory factors in acute leukemia. J Cell Biochem 35:93-98.
34. Meyers S, Lenny N, Sun W-H, Hiebert SW. 1996. AML-2 is a potential target for transcriptional regulation by the t(8;21) and t(12;21) fusion proteins in acute leukemia. Oncogene 13:303-312.
35. Mundlos S, Otto F, Mundlos C, Mulliken JB, Aylsworth AS, Albright S, Lindhout D, Cole WG, Henn W, Knoll JHM, Owen MJ, Mertelsmann R, Zabel BU, Olsen BR. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773-779.
36. Nakahara H, Bruder SP, Goldberg VM, Caplan AI. 1990. In vivo osteochondrogenic potential of cultured cells derived from the periosteum. Clin Orthop 259:223-232.
37. Nam S, Jin YH, Li QL, Lee KY, Jeong GB, Ito Y, Lee J, Bae SC. 2002. Expression pattern, regulation, and biological role of runt domain transcription factor, run, in Caenorhabditis elegans. Mol Cell Biol 22:547-554.
38. North T, Gu TL, Stacy T, Wang Q, Howard L, Binder M, Marin-Padilla M, Speck NA. 1999. Cbfa2 is required for the formation of intraaortic hematopoietic clusters. Development 126:2563-2575.
39. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84:321-330.
40. Olsen BR, Reginato AM, Wang W. 2000. Bone development. Annu Rev Cell Dev Biol 16:191-220.
41. Opperman LA. 2000. Cranial sutures as intramembranous bone growth sites. Dev Dyn 219:472-485.
42. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GWH, Beddington RSP, Mundlos S, Olsen BR, Selby PB, Owen MJ. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765-771.
43. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, Kennedy MB, Pockwinse S, Lian JB, Stein GS. 1990. Progressive development of the rat osteoblast phenotype in vitro: Reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 143:420-430.
44. Park MH, Shin HI, Choi JY, Nam SH, Kim YJ, Kim HJ, Ryoo HM. 2001. Differential expression patterns of Runx2 isoforms in cranial suture morphogenesis. J Bone Miner Res 16:885-892.
45. Quarles LD, Yohay DA, Lever LW, Caton R, Wenstrup RJ. 1992. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: An in vitro model of osteoblast development. J Bone Miner Res 7:683-692.
46. Quesenberry P, Habibian H, Dooner M, McAuliffe C, Lambert JF, Colvin G, Miller C, Frimberger A, Becker P. 2001. Physical and physiological plasticity of hematopoietic stem cells. Blood Cells Mol Dis 27:934-937.
47. Rosen V, Nove J, Song JJ, Thies RS, Cox K, Wozney JM. 1994. Responsiveness of clonal limb bud cell lines to bone morphogenetic protein 2 reveals a sequential relationship between cartilage and bone cell phenotypes. J Bone Miner Res 9:1759-1768.
48. Satake M, Nomura S, Yamaguchi-Iwai Y, Takahama Y, Hashimoto Y, Niki M, Kitamura Y, Ito Y. 1995. Expression of the Runt domain-encoding PEBP2 alpha genes in T cells during thymic development. Mol Cell Biol 15:1662-1670.
49. Shevde NK, Bendixen AC, Maruyama M, Li BL, Billmire DA. 2001. Enhanced activity of osteoblast differentiation factor (PEBP2alphaA2/CBFa1) in affected sutural osteoblasts from patients with nonsyndromic craniosynostosis. Cleft Palate Craniofac J 38:606-614.
50. Simeone A, Daga A, Calabi F. 1995. Expression of runt in the mouse embryo. Dev Dyn 203:61-70.
51. Stein GS, van Wijnen AJ, Stein JL, Lian JB, Montecino M, Choi J-Y, Zaidi K, Javed A. 2000. Intranuclear trafficking of transcription factors: Implications for biological control. J Cell Sci 113:2527-2533.
52. Stricker S, Fundele R, Vortkamp A, Mundlos S. 2002. Role of runx genes in chondrocyte differentiation. Dev Biol 245:95-108.
53. Strom DK, Nip J, Westendorf JJ, Linggi B, Lutterbach B, Downing JR, Lenny N, Hiebert SW. 2000. Expression of the AML-1 oncogene shortens the G(1) phase of the cell cycle. J Biol Chem 275:3438-3445.
54. Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, Speck NA. 1996. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci USA 93:3444-3449.
55. Westendorf JJ, Hiebert SW. 1999. Mammalian runt-domain proteins and their roles in hematopoiesis, osteogenesis, and leukemia. J Cell Biochem 33(Suppl 32):51-58.
56. Zaidi SK, Sullivan AJ, van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2002. Integration of Runx and Smad regulatory signals at transcriptionally active subnuclear sites. Proc Natl Acad Sci USA 99:8048-8053.
57. Zeng C, van Wijnen AJ, Stein JL, Meyers S, Sun W, Shopland L, Lawrence JB, Penman S, Lian JB, Stein GS, Hiebert SW. 1997. Identification of a nuclear matrix targeting signal in the leukemia and bone-related AML/CBFa transcription factors. Proc Natl Acad Sci USA 94:6746-6751.
58. Zhang YW, Yasui N, Ito K, Huang G, Fujii M, Hanai J, Nogami H, Ochi T, Miyazono K, Ito Y. 2000. A RUNX2/PEBP2aA/CBFA1 mutation displaying impaired transactivation and Smad interaction in cleidocranial dysplasia. Proc Natl Acad Sci USA 97:10549-10554.
59. Zhou YX, Xu X, Chen L, Li C, Brodie SG, Deng CX. 2000. A Pro250Arg substitution in mouse Fgfr1 causes increased expression of Cbfa1 and premature fusion of calvarial sutures. Hum Mol Genet 9:2001-2008.