Increased bone resorption and osteopenia in Dlx5 heterozygous mice

Journal of Cellular Biochemistry

Volumn 107, Issue 5, 2009, Pages 865-872

  Samee, Nadeem ^a,b   Geoffroy, Valérie ^a   Marty, Caroline ^a   Schiltz, Corinne ^a   Vieux Rochas, Maxence ^b   Clément Lacroix, Philippe ^c   Belleville, Cécile ^c   Levi, Giovanni ^b   De Vernejoul, Marie Christine ^a  

^a HÔPITAL LARIBOISIÈRE   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c GALAPAGOS NV   (Belgium)

Author keywords

Bone; Development; Distal less; Dlx5; Homeobox genes; Osteoblasts; Osteoclasts; Remodeling; Resorption

Indexed keywords

DEOXYPYRIDINOLINE; TRANSCRIPTION FACTOR DLX5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE REMODELING; CONTROLLED STUDY; CORTICAL BONE; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMALE; FEMUR SHAFT; GENE EXPRESSION; HETEROZYGOTE; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MALE; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; TRABECULAR BONE; URINALYSIS; URINARY EXCRETION; WILD TYPE;

AMINO ACIDS; ANIMALS; ANIMALS, NEWBORN; BETA-GALACTOSIDASE; BIOLOGICAL MARKERS; BONE DENSITY; BONE DISEASES, METABOLIC; BONE RESORPTION; FEMUR; HAPLOIDY; HETEROZYGOTE; HOMEODOMAIN PROTEINS; MALE; MICE; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; X-RAY MICROTOMOGRAPHY;

MUS;

EID: 67749097679     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22188     Document Type: Article

References (33)

1. Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, Mantero S, Bober E, Barbieri O, Simeone A, Levi G. 1999. Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126:3795-3809.
2. Bendall AJ, Hu G, Levi G, Abate-Shen C. 2003. Dlx5 regulates chondrocyte differentiation at multiple stages. Int J Dev Biol 47:335-344.
3. Benson MD, Bargeon JL, Xiao G, Thomas PE, Kim A, Cui Y, Franceschi RT. 2000. Identification of a homeodomain binding element in the bone sialo-protein gene promoter that is required for its osteoblast-selective expression. J Biol Chem 275:13907-13917.
4. Bousson V, Meunier A, Bergot C, Vicaut E, Rocha MA, Morais MH, Laval-Jeantet AM, Laredo JD. 2001. Distribution of intracortical porosity in human midfemoral cortex by age and gender. J Bone Miner Res 16:1308-1317.
5. Chavassieux P, Seeman E, Delmas PD. 2007. Insights into material and structural basis of bone fragility from diseases associated with fractures: How determinants of the biomechanical properties of bone are compromised by disease. Endocr Rev 28:151-164.
6. Cohen SM, Bronner G, Kuttner F, Jurgens G, Jackle H. 1989. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 338:432-434.
7. Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Amling M, Karsenty G. 1999. A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 13:1025-1036.
8. Hassan MQ, Javed A, Morasso MI, Karlin J, Montecino M, van Wijnen AJ, Stein GS, Stein JL, Lian JB. 2004. Dlx3 transcriptional regulation of osteoblast differentiation: Temporal recruitment of Msx2, Dlx3, and Dlx5 homeodomain proteins to chromatin of the osteocalcin gene. Mol Cell Biol 24:9248-9261.
9. Hassan MQ, Tare RS, Lee SH, Mandeville M, Morasso MI, Javed A, van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2006. BMP2 commitment to the osteogenic lineage involves activation of Runx2 by DLX3 and a homeodomain transcriptional network. J Biol Chem 281:40515-40526.
10. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, 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.
11. Lee MH, Kwon TG, Park HS, Wozney JM, Ryoo HM. 2003. BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2. Biochem Biophys Res Commun 309:689-694.
12. Lee MH, Kim YJ, Yoon WJ, Kim JI, Kim BG, Hwang YS, Wozney JM, Chi XZ, Bae SC, Choi KY, Cho JY, Choi JY, Ryoo HM. 2005. Dlx5 specifically regulates Runx2 type II expression by binding to homeodomain-response elements in the Runx2 distal promoter. J Biol Chem 280:35579-35587.
13. Li H, Marijanovic I, Kronenberg MS, Erceg I, Stover ML, Velonis D, Mina M, Heinrich JG, Harris SE, Upholt WB, Kalajzic I, Lichtler AC. 2008. Expression and function of Dlx genes in the osteoblast lineage. Dev Biol 316:458-470.
14. 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.
15. Miyama K, Yamada G, Yamamoto TS, Takagi C, Miyado K, Sakai M, Ueno N, Shibuya H. 1999. A BMP-inducible gene, dlx5, regulates osteoblast differentiation and mesoderm induction. Dev Biol 208:123-133.
16. Muraglia A, Perera M, Verardo S, Liu Y, Cancedda R, Quarto R, Corte G. 2008. DLX5 overexpression impairs osteogenic differentiation of human bone marrow stromal cells. Eur J Cell Biol 87:751-761.
17. Nishida H, Miyagawa S, Vieux-Rochas M, Morini M, Ogino Y, Suzuki K, Nakagata N, Choi HS, Levi G, Yamada G. 2008. Positive regulation of steroidogenic acute regulatory protein gene expression through the interaction between Dlx and GATA-4 for testicular steroidogenesis. Endocrinology 149:2090-2097.
18. Nissen-Meyer LS, Jemtland R, Gautvik VT, Pedersen ME, Paro R, Fortunati D, Pierroz DD, Stadelmann VA, Reppe S, Reinholt FP, Del Fattore A, Rucci N, Teti A, Ferrari S, Gautvik KM. 2007. Osteopenia, decreased bone formation and impaired osteoblast development in Sox4 heterozygous mice. J Cell Sci 120:2785-2795.
19. O'Hara E, Cohen B, Cohen SM, McGinnisW. 1993. Distal-less is a downstream gene of deformed required for ventral maxillary identity. Development 117:847-856.
20. Olsen BR, Reginato AM, Wang W. 2000. Bone development. Annu Rev Cell Dev Biol 16:191-220.
21. Orestes-Cardoso SM, Nefussi JR, Hotton D, Mesbah M, Orestes-Cardoso MD, Robert B, Berdal A. 2001. Postnatal Msx1 expression pattern in craniofacial, axial, and appendicular skeleton of transgenic mice from the first week until the second year. Dev Dyn 221:1-13.
22. Panganiban G, Rubenstein JL. 2002. Developmental functions of the Distalless/ Dlx homeobox genes. Development 129:4371-4386.
23. Parfitt AM. 1988. Bone histomorphometry: Proposed system for standardization of nomenclature, symbols, and units. Calcif Tissue Int 42:284-286.
24. 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.
25. Robledo RF, Rajan L, Li X, Lufkin T. 2002. The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev 16:1089-1101.
26. Samee N, de Vernejoul MC, Levi G. 2007. Role of DLX regulatory proteins in osteogenesis and chondrogenesis. Crit Rev Eukaryot Gene Expr 17:173-186.
27. Samee N, Geoffroy V, Marty C, Schiltz C, Vieux-Rochas M, Levi G, de Vernejoul MC. 2008. Dlx5, a positive regulator of osteoblastogenesis, is essential for osteoblast-osteoclast coupling. Am J Pathol 173:773-780.
28. Szulc P, Garnero P, Marchand F, Duboeuf F, Delmas PD. 2005. Biochemical markers of bone formation reflect endosteal bone loss in elderly men - MINOS study. Bone 36:13-21.
29. Theoleyre S, Wittrant Y, Tat SK, Fortun Y, Redini F, Heymann D. 2004. The molecular triad OPG/RANK/RANKL: Involvement in the orchestration of pathophysiological bone remodeling. Cytokine Growth Factor Rev 15:457-475.
30. Ulsamer A, Ortuno MJ, Ruiz S, Susperregui AR, Osses N, Rosa JL, Ventura F. 2008. BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J Biol Chem 283:3816-3826.
31. Vanderschueren D, Vandenput L, Boonen S, Lindberg MK, Bouillon R, Ohlsson C. 2004. Androgens and bone. Endocr Rev 25:389-425.
32. Zhang J, Zhu J, Valverde P, Li L, Pageau S, Tu Q, Nishimura R, Yoneda T, Yang P, Zheng W, Ma W, Chen J. 2008. Phenotypic analysis of Dlx5 overexpression in post-natal bone. J Dent Res 87:45-50.
33. Zhao GQ, Zhao S, Zhou X, Eberspaecher H, Solursh M, de Crombrugghe B. 1994. rDlx, a novel distal-less-like homeoprotein is expressed in developing cartilages and discrete neuronal tissues. Dev Biol 164:37-51.