The Fos-related antigen Fra-1 is an activator of bone matrix formation

EMBO Journal

Volumn 23, Issue 14, 2004, Pages 2789-2799

  Eferl, Robert ^a   Hoebertz, Astrid ^a   Schilling, Arndt F ^b   Rath, Martina ^a   Karreth, Florian ^a   Kenner, Lukas ^a   Amling, Michael ^b   Wagner, Erwin F ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

AP 1; Bone extracellular matrix; Conditional Fra 1 knockout; Osteoblasts; Osteopenia

Indexed keywords

COLLAGEN TYPE 1; GENE PRODUCT; OSTEOCALCIN; TRANSCRIPTION FACTOR FRA 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MASS; BONE MATRIX; CARTILAGE CELL; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; GENE DELETION; GENE FUNCTION; KNOCKOUT MOUSE; LETHALITY; LONG BONE; MALE; MOUSE; NONHUMAN; OSSIFICATION; OSTEOCLAST; OSTEOPENIA; OSTEOSCLEROSIS; PHENOTYPE; PLACENTA DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN TARGETING; TRANSGENIC MOUSE;

ANIMALS; BONE MATRIX; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; COLLAGEN TYPE I; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; MICE; MICE, TRANSGENIC; OSTEOBLASTS; OSTEOCALCIN; OSTEOCLASTS; OSTEOGENESIS; PROTO-ONCOGENE PROTEINS C-FOS; TRANS-ACTIVATORS;

ANIMALIA; MUS MUSCULUS;

EID: 3543045594     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600282     Document Type: Article

References (39)

1. Akune T, Ogata N, Hoshi K, Kubota N, Terauchi Y, Tobe K, Takagi H, Azuma Y, Kadowaki T, Nakamura K, Kawaguchi H (2002) Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts. J Cell Biol 159: 147-156
2. Amling M, Priemel M, Holzmann T, Chapin K, Rueger JM, Baron R, Demay MB (1999) Rescue of the skeletal phenotype of vitamin D receptor-ablated mice in the setting of normal mineral ion homeostasis: formal histomorphometric and biomechanical analyses. Endocrinology 140: 4982-4987
3. Behrens A, Haigh J, Mechta-Grigoriou F, Nagy A, Yaniv M, Wagner EF (2003) Impaired intervertebral disc formation in the absence of Jun. Development 130: 103-109
4. Boyle WJ, Simonet WS, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423: 337-342
5. Chung KY, Agarwal A, Uitto J, Mauviel A (1996) An AP-1 binding sequence is essential for regulation of the human alpha2(I) collagen (COL1A2) promoter activity by transforming growth factor-beta. J Biol Chem 271: 3272-3278
6. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, Smith E, Bonadio J, Goldstein S, Gundberg C, Bradley A, Karsenty G (1996) Increased bone formation in osteocalcin-deficient mice. Nature 382: 448-452
7. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89: 747-754
8. Eferl R, Wagner EF (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3: 859-868
9. Farzaneh-Far A, Davies JD, Braam LA, Spronk HM, Proudfoot D, Chan SW, O'Shaughnessy KM, Weissberg PL, Vermeer C, Shanahan CM (2001) A polymorphism of the human matrix gamma-carboxyglutamic acid protein promoter alters binding of an activating protein-1 complex and is associated with altered transcription and serum levels. J Biol Chem 276: 32466-32473
10. Fleischmann A, Hafezi F, Elliott C, Reme CE, Ruther U, Wagner EF (2000) Fra-1 replaces c-Fos-dependent functions in mice. Genes Dev 14: 2695-2700
11. 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
12. Grigoriadis AE, Schellander K, Wang ZQ, Wagner EF (1993) Osteoblasts are target cells for transformation in c-fos transgenic mice. J Cell Biol 122: 685-701
13. Grigoriadis AE, Wang ZQ, Cecchini MG, Hofstetter W, Felix R, Fleisch HA, Wagner EF (1994) c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science 266: 443-448
14. Harada S, Rodan GA (2003) Control of osteoblast function and regulation of bone mass. Nature 423: 349-355
15. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M, Kuznetsov SA, Mankani M, Robey PG, Poole AR, Pidoux I, Ward JM, Birkedal-Hansen H (1999) MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99: 81-92
16. Jochum W, David JP, Elliott C, Wutz A, Plenk Jr H, Matsuo K, Wagner EF (2000) Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1. Nat Med 6: 980-984
17. Karsenty G, Wagner EF (2002) Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2: 389-406
18. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass II DA, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, Karsenty G, Chan L (2002) Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 157: 303-314
19. Kenner L, Hoebertz A, Beil T, Keon N, Karreth F, Eferl R, Scheuch H, Szremska A, Amling M, Schorpp-Kistner M, Angel P, Wagner EF (2004) Mice lacking JunB are osteopenic due to cell-autonomous osteoblast and osteoclast defects. J Cell Biol 164: 613-623
20. Li B, Boast S, de los Santos K, Schieren I, Quiroz M, Teitelbaum SL, Tondravi MM, Goff SP (2000) Mice deficient in Abl are osteoporotic and have defects in osteoblast maturation. Nat Genet 24: 304-308
21. Luo G, D'Souza R, Hogue D, Karsenty G (1995) The matrix Gla protein gene is a marker of the chondrogenesis cell lineage during mouse development. J Bone Miner Res 10: 325-334
22. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, Behringer RR, Karsenty G (1997) Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386: 78-81
23. Matsuo K, Owens JM, Tonko M, Elliott C, Chambers TJ, Wagner EF (2000) Fosl1 is a transcriptional target of c-Fos during osteoclast differentiation. Nat Genet 24: 184-187
24. McCabe LR, Banerjee C, Kundu R, Harrison RJ, Dobner PR, Stein JL, Lian JB, Stein GS (1996) Developmental expression and activities of specific fos and jun proteins are functionally related to osteoblast maturation: role of Fra-2 and Jun D during differentiation. Endocrinology 137: 4398-4408
25. McCabe LR, Kockx M, Lian J, Stein J, Stein G (1995) Selective expression of fos- and jun-related genes during osteoblast proliferation and differentiation. Exp Cell Res 218: 255-262
26. Murshed M, Schinke T, McKee MD, Karsenty G (2004) Extracellular matrix mineralization is regulated locally; different roles of two gla-containing proteins. J Cell Biol 165: 625-630
27. Ogata N, Chikazu D, Kubota N, Terauchi Y, Tobe K, Azuma Y, Ohta T, Kadowaki T, Nakamura K, Kawaguchi H (2000) Insulin receptor substrate-1 in osteoblast is indispensable for maintaining bone turnover. J Clin Invest 105: 935-943
28. Owens JM, Matsuo K, Nicholson GC, Wagner EF, Chambers TJ (1999) Fra-1 potentiates osteoclastic differentiation in osteoclast-macrophage precursor cell lines. J Cell Physiol 179: 170-178
29. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610
30. Sabatakos G, Sims NA, Chen J, Aoki K, Kelz MB, Amling M, Bouali Y, Mukhopadhyay K, Ford K, Nestler EJ, Baron R (2000) Overexpression of DeltaFosB transcription factor(s) increases bone formation and inhibits adipogenesis. Nat Med 6: 985-990
31. Schreiber M, Poirier C, Franchi A, Kurzbauer R, Guenet JL, Carle GF, Wagner EF (1997) Structure and chromosomal assignment of the mouse fra-1 gene, and its exclusion as a candidate gene for oc (osteosclerosis). Oncogene 15: 1171-1178
32. Schreiber M, Wang ZQ, Jochum W, Fetka I, Elliott C, Wagner EF (2000) Placental vascularisation requires the AP-1 component fra1. Development 127: 4937-4948
33. Schule R, Umesono K, Mangelsdorf DJ, Bolado J, Pike JW, Evans RM (1990) Jun-Fos and receptors for vitamins A and D recognize a common response element in the human osteocalcin gene. Cell 61: 497-504
34. Tallquist MD, Soriano P (2000) Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function. Genesis 26: 113-115
35. Teitelbaum SL, Ross FP (2003) Genetic regulation of osteoclast development and function. Nat Rev Genet 4: 638-649
36. Thiebaud D, Guenther HL, Porret A, Burckhardt P, Fleisch H, Hofstetter W (1994) Regulation of collagen type I and biglycan mRNA levels by hormones and growth factors in normal and immortalized osteoblastic cell lines. J Bone Miner Res 9: 1347-1354
37. Vidal F, Sage J, Cuzin F, Rassoulzadegan M (1998) Cre expression in primary spermatocytes: a tool for genetic engineering of the germ line. Mol Reprod Dev 51: 274-280
38. Wang ZQ, Ovitt C, Grigoriadis AE, Mohle-Steinlein U, Ruther U, Wagner EF (1992) Bone and haematopoietic defects in mice lacking c-fos. Nature 360: 741-745
39. Yang X, Matsuda K, Bialek P, Jacquot S, Masuoka HC, Schinke T, Li L, Brancorsini S, Sassone-Corsi P, Townes TM, Hanauer A, Karsenty G (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology: implication for Coffin-Lowry syndrome. Cell 117: 387-398