DLX3 regulates bone mass by targeting genes supporting osteoblast differentiation and mineral homeostasis in vivo

Cell Death and Differentiation

Volumn 21, Issue 9, 2014, Pages 1365-1376

  Isaac, J ^a   Erthal, J ^a   Gordon, J ^b   Duverger, O ^a   Sun, H W ^c   Lichtler, A C ^d   Stein, G S ^b   Lian, J B ^b   Morasso, M I ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF VERMONT   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^d UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISTAL-LESS HOMEOBOX PROTEINS; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; BONE; BONE DENSITY; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; HOMEOSTASIS; MALE; METABOLISM; MOUSE; OSTEOBLAST; TRANSGENIC MOUSE;

ANIMALS; BONE AND BONES; BONE DENSITY; CELL DIFFERENTIATION; HOMEODOMAIN PROTEINS; HOMEOSTASIS; MALE; MICE; MICE, TRANSGENIC; OSTEOBLASTS; TRANSCRIPTION FACTORS;

EID: 84905856510     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.82     Document Type: Article

References (48)

1. Cohen MM Jr. Perspectives on RUNX genes: an update. Am J Med Genet A 2009; 149A: 2629-2646.
2. Jensen ED, Gopalakrishnan R, Westendorf JJ. Regulation of gene expression in osteoblasts. Biofactors 2010; 36: 25-32.
3. Long F. Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 2012; 13: 27-38.
4. Depew MJ, Simpson CA, Morasso M, Rubenstein JL. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J Anat 2005; 207: 501-561.
5. Panganiban G, Rubenstein JL. Developmental functions of the Distal-less/Dlx homeobox genes. Development 2002; 129: 4371-4386.
6. Samee N, de Vernejoul MC, Levi G. Role of DLX regulatory proteins in osteogenesis and chondrogenesis. Crit Rev Eukaryot Gene Expr 2007; 17: 173-186.
7. Shamseldin HE, Faden MA, Alashram W, Alkuraya FS. Identification of a novel DLX5 mutation in a family with autosomal recessive split hand and foot malformation. J Med Genet 2012; 49: 16-20.
8. Haldeman RJ, Cooper LF, Hart TC, Phillips C, Boyd C, Lester GE et al. Increased bone density associated with DLX3 mutation in the tricho-dento-osseous syndrome. Bone 2004; 35: 988-997.
9. Hassan MQ, Javed A, Morasso MI, Karlin J, Montecino M, van Wijnen AJ et al. Dlx3 transcriptional regulation of osteoblast differentiation: temporal recruitment of Msx2, Dlx3, and Dlx5 homeodomain proteins to chromatin of the osteocalcin gene. Mol Cell Biol 2004; 24: 9248-9261.
10. Hassan MQ, Tare RS, Lee SH, Mandeville M, Morasso MI, Javed A et al. BMP2 commitment to the osteogenic lineage involves activation of Runx2 by DLX3 and a homeodomain transcriptional network. J Biol Chem 2006; 281: 40515-40526.
11. Singh M, Del Carpio-Cano FE, Monroy MA, Popoff SN, Safadi FF. Homeodomain transcription factors regulate BMP-2-induced osteoactivin transcription in osteoblasts. J Cell Physiol 2012; 227: 390-399.
12. Duverger O, Isaac J, Zah A, Hwang J, Berdal A, Lian JB et al. In vivo impact of Dlx3 conditional inactivation in neural crest-derived craniofacial bones. J Cell Physiol 2013; 228: 654-664.
13. Choi SJ, Roodman GD, Feng JQ, Song IS, Amin K, Hart PS et al. In vivo impact of a 4 bp deletion mutation in the DLX3 gene on bone development. Dev Biol 2009; 325: 129-137.
14. Lezot F, Thomas BL, Blin-Wakkach C, Castaneda B, Bolanos A, Hotton D et al. Dlx homeobox gene family expression in osteoclasts. J Cell Physiol 2010; 223: 779-787.
15. Doi M, Nagano A, Nakamura Y. Molecular cloning and characterization of a novel gene, EMILIN-5, and its possible involvement in skeletal development. Biochem Biophys Res Commun 2004; 313: 888-893.
16. Li YC, Pirro AE, Amling M, Delling G, Baron R, Bronson R et al. Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci USA 1997; 94: 9831-9835.
17. Mackenzie NC, Zhu D, Milne EM, van 't Hof R, Martin A, Darryl Quarles L et al. Altered bone development and an increase in FGF-23 expression in Enpp1(-/-) mice. PLoS One 2012; 7: e32177.
18. Narisawa S, Frohlander N, Millan JL. Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia. Dev Dyn 1997; 208: 432-446.
19. Staines KA, MacRae VE, Farquharson C. The importance of the SIBLING family of proteins on skeletal mineralisation and bone remodelling. J Endocrinol 2012; 214: 241-255.
20. Wellik DM. Hox genes and vertebrate axial pattern. Curr Top Dev Biol 2009; 88: 257-278.
21. Petersen DN, Tkalcevic GT, Mansolf AL, Rivera-Gonzalez R, Brown TA. Identification of osteoblast/osteocyte factor 45 (OF45), a bone-specific cDNA encoding an RGD-containing protein that is highly expressed in osteoblasts and osteocytes. J Biol Chem 2000; 275: 36172-36180.
22. Chen G, Deng C, Li YP. TGF-beta and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 2012; 8: 272-288.
23. Gazzerro E, Canalis E. Bone morphogenetic proteins and their antagonists. Rev Endocr Metab Disord 2006; 7: 51-65.
24. Monroe DG, McGee-Lawrence ME, Oursler MJ, Westendorf JJ. Update on Wnt signaling in bone cell biology and bone disease. Gene 2012; 492: 1-18.
25. Zanotti S, Canalis E. Notch signaling in skeletal health and disease. Eur J Endocrinol 2013; 168: R95-103.
26. Rawlinson SC, McKay IJ, Ghuman M, Wellmann C, Ryan P, Prajaneh S et al. Adult rat bones maintain distinct regionalized expression of markers associated with their development. PLoS One 2009; 4: e8358.
27. Leucht P, Kim JB, Amasha R, James AW, Girod S, Helms JA. Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development 2008; 135: 2845-2854.
28. Hassan MQ, Saini S, Gordon JA, van Wijnen AJ, Montecino M, Stein JL et al. Molecular switches involving homeodomain proteins, HOXA10 and RUNX2 regulate osteoblastogenesis. Cells Tissues Organs 2009; 189: 122-125.
29. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997; 89: 765-771.
30. Nakashima K, Zhou X, Kunkel G, Zhang ZP, Deng JM, Behringer RR et al. The novel zinc finger-containing transcription factor Osterix is required for osteoblast differentiation and bone formation. Cell 2002; 108: 17-29.
31. Ferrari D, Sumoy L, Gannon J, Sun HL, Brown AMC, Upholt WB et al. The expression pattern of the distal-less homeobox-containing gene Dlx-5 in the developing chick limb bud suggests its involvement in apical ectodermal ridge activity, pattern-formation, and cartilage differentiation. Mech Dev 1995; 52: 257-264.
32. Lee MH, Kim YJ, Yoon WJ, Kim JI, Kim BG, Hwang YS et al. Dlx5 specifically regulates Runx2 type II expression by binding to homeodomain-response elements in the Runx2 distal promoter. J Biol Chem 2005; 280: 35579-35587.
33. Samee N, Geoffroy V, Marty C, Schiltz C, Vieux-Rochas M, Levi G et al. Dlx5, a positive regulator of osteoblastogenesis, is essential for osteoblast-osteoclast coupling. Am J Pathol 2008; 173: 773-780.
34. Tadic T, Dodig M, Erceg I, Marijanovic I, Mina M, Kalajzic Z et al. Overexpression of Dlx5 in chicken calvarial cells accelerates osteoblastic differentiation. J Bone Miner Res 2002; 17: 1008-1014.
35. Depew MJ, Lufkin T, Rubenstein JL. Specification of jaw subdivisions by Dlx genes. Science 2002; 298: 381-385.
36. Nam HK, Liu J, Li Y, Kragor A, Hatch NE. Ectonucleotide pyrophosphatase/ phosphodiesterase-1 (ENPP1) protein regulates osteoblast differentiation. J Biol Chem 2011; 286: 39059-39071.
37. Malaval L, Wade-Gueye NM, Boudiffa M, Fei J, Zirngibl R, Chen F et al. Bone sialoprotein plays a functional role in bone formation and osteoclastogenesis. J Exp Med 2008; 205: 1145-1153.
38. Ulsamer A, Ortuno MJ, Ruiz S, Susperregui AR, Osses N, Rosa JL et al. BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J Biol Chem 2008; 283: 3816-3826.
39. Kim Y, Lee M, Wozney JM, Cho J, Ryoo H. BMP2-induced alkaline phosphatase expression is regulated by Dlx5, which is interrupted by Msx2 as a binding competition to the common response element. J Bone Miner Res 2004; 19: S264-S264.
40. Benson MD, Bargeon JL, Xiao G, Thomas PE, Kim A, Cui Y et al. Identification of a homeodomain binding element in the bone sialoprotein gene promoter that is required for its osteoblast-selective expression. J Biol Chem 2000; 275: 13907-13917.
41. Nakayama Y, Nakajima Y, Kato N, Takai H, Kim DS, Arai M et al. Insulin-like growth factor-1 increases bone sialoprotein (BSP) expression through fibroblast growth factor-2 response element and homeodomain protein-binding site in the proximal promoter of the BSP gene. J Cell Physiol 2006; 208: 326-335.
42. Hayashibara T, Hiraga T, Sugita A, Wang L, Hata K, Ooshima T et al. Regulation of osteoclast differentiation and function by phosphate: potential role of osteoclasts in the skeletal abnormalities in hypophosphatemic conditions. J Bone Miner Res 2007; 22: 1743-1751.
43. Kramer I, Halleux C, Keller H, Pegurri M, Gooi JH, Weber PB et al. Osteocyte Wnt/beta-catenin signaling is required for normal bone homeostasis. Mol Cell Biol 2010; 30: 3071-3085.
44. Kulkarni RN, Bakker AD, Everts V, Klein-Nulend J. Inhibition of osteoclastogenesis by mechanically loaded osteocytes: involvement of MEPE. Calcif Tissue Int 2010; 87: 461-468.
45. Liu JC, Lengner CJ, Gaur T, Lou Y, Hussain S, Jones MD et al. Runx2 protein expression utilizes the Runx2 P1 promoter to establish osteoprogenitor cell number for normal bone formation. J Biol Chem 2011; 286: 30057-30070.
46. Aioub M, Lezot F, Molla M, Castaneda B, Robert B, Goubin G et al. Msx2-/- transgenic mice develop compound amelogenesis imperfecta, dentinogenesis imperfecta and periodental osteopetrosis. Bone 2007; 41: 851-859.
47. Grcevic D, Pejda S, Matthews BG, Repic D, Wang L, Li H et al. In vivo fate mapping identifies mesenchymal progenitor cells. Stem Cells 2012; 30: 187-196.
48. Hwang J, Kita R, Kwon HS, Choi EH, Lee SH, Udey MC et al. Epidermal ablation of Dlx3 is linked to IL-17-associated skin inflammation. Proc Natl Acad Sci USA 2011; 108: 11566-11571.