BMP-Mediated Functional Cooperation between Dlx5;Dlx6 and Msx1;Msx2 during Mammalian Limb Development

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Vieux Rochas, Maxence ^a,h   Bouhali, Kamal ^a   Mantero, Stefano ^b,i   Garaffo, Giulia ^b   Provero, Paolo ^b   Astigiano, Simonetta ^c   Barbieri, Ottavia ^c,d   Caratozzolo, Mariano F ^e   Tullo, Apollonia ^e   Guerrini, Luisa ^f   Lallemand, Yvan ^g   Robert, Benoît ^g   Levi, Giovanni ^a   Merlo, Giorgio R ^b  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e CNR   (Italy)

^f UNIVERSITY OF MILAN   (Italy)

^g CNRS   (France)

^h EPFL   (Switzerland)

ⁱ HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BONE MORPHOGENETIC PROTEIN 2 GENE; BONE MORPHOGENETIC PROTEIN 4 GENE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DLX5 GENE; DLX6 GENE; DOWN REGULATION; ECTRODACTYLY; EMBRYO; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENETIC ASSOCIATION; LIMB DEVELOPMENT; MESODERM; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; MSX1 GENE; MSX2 GENE; NEWBORN; NONHUMAN; PHENOTYPE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; ECTODERM; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; MESODERM; MICE; MORPHOGENESIS; MSX1 TRANSCRIPTION FACTOR; MUTATION;

EID: 84873864463     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051700     Document Type: Article

References (90)

1. Allard P, Tabin CJ, (2009) Achieving bilateral symmetry during vertebrate limb development. Semin Cell Dev Biol 20: 479-484.
2. Zakany J, Duboule D, (2007) The role of Hox genes during vertebrate limb development. Curr Opin Genet Dev 17: 359-366.
3. Zeller R, (2010) The temporal dynamics of vertebrate limb development, teratogenesis and evolution. Curr Opin Genet Dev 20: 384-390.
4. Bastida MF, Ros MA, (2008) How do we get a perfect complement of digits? Curr Opin Genet Dev 18: 374-380.
5. Riddle RD, Johnson RL, Laufer E, Tabin C, (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401-1416.
6. Zeng X, Goetz JA, Suber LM, Scott WJ Jr, Schreiner CM, et al. (2001) A freely diffusible form of Sonic hedgehog mediates long-range signalling. Nature 411: 716-720.
7. Mariani FV, Ahn CP, Martin GR, (2008) Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 453: 401-405.
8. Sun X, Mariani FV, Martin GR, (2002) Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418: 501-508.
9. Niswander L, Tickle C, Vogel A, Booth I, Martin GR, (1993) FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75: 579-587.
10. Lu P, Yu Y, Perdue Y, Werb Z, (2008) The apical ectodermal ridge is a timer for generating distal limb progenitors. Development 135: 1395-1405.
11. Fernandez-Teran M, Ros MA, (2008) The Apical Ectodermal Ridge: morphological aspects and signaling pathways. Int J Dev Biol 52: 857-871.
12. Loomis CA, Harris E, Michaud J, Wurst W, Hanks M, et al. (1996) The mouse Engrailed-1 gene and ventral limb patterning. Nature 382: 360-363.
13. Parr BA, McMahon AP, (1995) Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374: 350-353.
14. Cygan JA, Johnson RL, McMahon AP, (1997) Novel regulatory interactions revealed by studies of murine limb pattern in Wnt-7a and En-1 mutants. Development 124: 5021-5032.
15. Chen H, Johnson RL, (2002) Interactions between dorsal-ventral patterning genes lmx1b, engrailed-1 and wnt-7a in the vertebrate limb. Int J Dev Biol 46: 937-941.
16. Qiu Q, Chen H, Johnson RL, (2009) Lmx1b-expressing cells in the mouse limb bud define a dorsal mesenchymal lineage compartment. Genesis 47: 224-233.
17. Benazet JD, Zeller R, (2009) Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harb Perspect Biol 1: a001339.
18. Zeller R, Lopez-Rios J, Zuniga A, (2009) Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10: 845-858.
19. Tickle C, (2006) Making digit patterns in the vertebrate limb. Nat Rev Mol Cell Biol 7: 45-53.
20. Pizette S, Abate-Shen C, Niswander L, (2001) BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development 128: 4463-4474.
21. Robert B, (2007) Bone morphogenetic protein signaling in limb outgrowth and patterning. Dev Growth Differ 49: 455-468.
22. Benazet JD, Bischofberger M, Tiecke E, Goncalves A, Martin JF, et al. (2009) A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323: 1050-1053.
23. Wang CK, Omi M, Ferrari D, Cheng HC, Lizarraga G, et al. (2004) Function of BMPs in the apical ectoderm of the developing mouse limb. Dev Biol 269: 109-122.
24. Zuniga A, Haramis AP, McMahon AP, Zeller R, (1999) Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 401: 598-602.
25. Ahn K, Mishina Y, Hanks MC, Behringer RR, Crenshaw EB 3rd (2001) BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development 128: 4449-4461.
26. Tickle C, (2003) Patterning systems-from one end of the limb to the other. Dev Cell 4: 449-458.
27. Robert B, Lallemand Y, (2006) Anteroposterior patterning in the limb and digit specification: contribution of mouse genetics. Dev Dyn 235: 2337-2352.
28. Zeller R, (2004) It takes time to make a pinky: unexpected insights into how SHH patterns vertebrate digits. Sci STKE 2004: pe53.
29. Merlo GR, Paleari L, Mantero S, Genova F, Beverdam A, et al. (2002) Mouse model of split hand/foot malformation type I. Genesis. 33: 97-101.
30. 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.
31. Shamseldin HE, Faden MA, Alashram W, Alkuraya FS, (2012) Identification of a novel DLX5 mutation in a family with autosomal recessive split hand and foot malformation. J Med Genet 49: 16-20.
32. Lallemand Y, Nicola MA, Ramos C, Bach A, Cloment CS, et al. (2005) Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb development. Development 132: 3003-3014.
33. Lallemand Y, Bensoussan V, Cloment CS, Robert B, (2009) Msx genes are important apoptosis effectors downstream of the Shh/Gli3 pathway in the limb. Dev Biol 331: 189-198.
34. Bensoussan-Trigano V, Lallemand Y, Saint Cloment C, Robert B, (2011) Msx1 and Msx2 in limb mesenchyme modulate digit number and identity. Dev Dyn 240: 1190-1202.
35. Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, et al. (1999) Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126: 3795-3809.
36. Beverdam A, Merlo GR, Paleari L, Mantero S, Genova F, et al. (2002) Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: mirror of the past? Genesis 34: 221-227.
37. Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, et al. (1999) Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126: 3831-3846.
38. Depew MJ, Simpson CA, Morasso M, Rubenstein JL, (2005) Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J Anat 207: 501-561.
39. Houzelstein D, Cohen A, Buckingham ME, Robert B, (1997) Insertional mutation of the mouse Msx1 homeobox gene by an nlacZ reporter gene. Mech Dev 65: 123-133.
40. Satokata I, Ma L, Ohshima H, Bei M, Woo I, et al. (2000) Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet 24: 391-395.
41. Satokata I, Maas R, (1994) Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 6: 348-356.
42. Ferrari D, Sumoy L, Gannon J, Sun H, Brown AM, et al. (1995) 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 52: 257-264.
43. Bendall AJ, Abate-Shen C, (2000) Roles for Msx and Dlx homeoproteins in vertebrate development. Gene 247: 17-31.
44. Zhang H, Hu G, Wang H, Sciavolino P, Iler N, et al. (1997) Heterodimerization of Msx and Dlx homeoproteins results in functional antagonism. Mol Cell Biol 17: 2920-2932.
45. Davidson D, (1995) The function and evolution of Msx genes: pointers and paradoxes. Trends Genet 11: 405-411.
46. Panganiban G, Rubenstein JL, (2002) Developmental functions of the Distal-less/Dlx homeobox genes. Development 129: 4371-4386.
47. Merlo GR, Zerega B, Paleari L, Trombino S, Mantero S, et al. (2000) Multiple functions of Dlx genes. Int J Dev Biol 44: 619-626.
48. Liu YH, Tang Z, Kundu RK, Wu L, Luo W, et al. (1999) Msx2 gene dosage influences the number of proliferative osteogenic cells in growth centers of the developing murine skull: a possible mechanism for MSX2-mediated craniosynostosis in humans. Dev Biol 205: 260-274.
49. Odelberg SJ, Kollhoff A, Keating MT, (2000) Dedifferentiation of mammalian myotubes induced by msx1. Cell 103: 1099-1109.
50. Hu G, Lee H, Price SM, Shen MM, Abate-Shen C, (2001) Msx homeobox genes inhibit differentiation through upregulation of cyclin D1. Development 128: 2373-2384.
51. Ishii M, Merrill AE, Chan YS, Gitelman I, Rice DP, et al. (2003) Msx2 and Twist cooperatively control the development of the neural crest-derived skeletogenic mesenchyme of the murine skull vault. Development 130: 6131-6142.
52. Levi G, Puche AC, Mantero S, Barbieri O, Trombino S, et al. (2003) The Dlx5 homeodomain gene is essential for olfactory development and connectivity in the mouse. Mol Cell Neurosci 22: 530-543.
53. Perera M, Merlo GR, Verardo S, Paleari L, Corte G, et al. (2004) Defective neuronogenesis in the absence of Dlx5. Mol Cell Neurosci 25: 153-161.
54. Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, et al. (2007) Dlx-dependent and-independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27: 3230-3243.
55. Merlo GR, Mantero S, Zaghetto AA, Peretto P, Paina S, et al. (2007) The role of Dlx homeogenes in early development of the olfactory pathway. J Mol Histol 38: 347-358.
56. Muraglia A, Perera M, Verardo S, Liu Y, Cancedda R, et al. (2008) DLX5 overexpression impairs osteogenic differentiation of human bone marrow stromal cells. Eur J Cell Biol 87: 751-761.
57. Lo Iacono N, Mantero S, Chiarelli A, Garcia E, Mills AA, et al. (2008) Regulation of Dlx5 and Dlx6 gene expression by p63 is involved in EEC and SHFM congenital limb defects. Development 135: 1377-1388.
58. Radoja N, Guerrini L, Lo Iacono N, Merlo GR, Costanzo A, et al. (2007) Homeobox gene Dlx3 is regulated by p63 during ectoderm development: relevance in the pathogenesis of ectodermal dysplasias. Development 134: 13-18.
59. Chung IH, Han J, Iwata J, Chai Y, (2010) Msx1 and Dlx5 function synergistically to regulate frontal bone development. Genesis 48: 645-655.
60. Levi G, Mantero S, Barbieri O, Cantatore D, Paleari L, et al. (2006) Msx1 and Dlx5 act independently in development of craniofacial skeleton, but converge on the regulation of Bmp signaling in palate formation. Mech Dev 123: 3-16.
61. Han J, Mayo J, Xu X, Li J, Bringas P Jr, et al. (2009) Indirect modulation of Shh signaling by Dlx5 affects the oral-nasal patterning of palate and rescues cleft palate in Msx1-null mice. Development 136: 4225-4233.
62. Pan ZZ, Kronenberg MS, Huang DY, Sumoy L, Rogina B, et al. (2002) MSX2 expression in the apical ectoderm ridge is regulated by an MSX2 and Dlx5 binding site. Biochem Biophys Res Commun 290: 955-961.
63. Sumoy L, Wang CK, Lichtler AC, Pierro LJ, Kosher RA, et al. (1995) Identification of a spatially specific enhancer element in the chicken Msx-2 gene that regulates its expression in the apical ectodermal ridge of the developing limb buds of transgenic mice. Dev Biol 170: 230-242.
64. Vieux-Rochas M, Coen L, Sato T, Kurihara Y, Gitton Y, et al. (2007) Molecular dynamics of retinoic acid-induced craniofacial malformations: implications for the origin of gnathostome jaws. PLoS One 2: e510.
65. Jones CM, Lyons KM, Hogan BL, (1991) Involvement of Bone Morphogenetic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111: 531-542.
66. Paina S, Garzotto D, DeMarchis S, Marino M, Moiana A, et al. (2011) Wnt5a is a transcriptional target of Dlx homeogenes and promotes differentiation of interneuron progenitors in vitro and in vivo. J Neurosci 31: 2675-2687.
67. Ala U, Piro RM, Grassi E, Damasco C, Silengo L, et al. (2008) Prediction of human disease genes by human-mouse conserved coexpression analysis. PLoS Comput Biol 4: e1000043.
68. Piro RM, Ala U, Molineris I, Grassi E, Bracco C, et al. (2011) An atlas of tissue-specific conserved coexpression for functional annotation and disease gene prediction. Eur J Hum Genet 19: 1173-1180.
69. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, et al. (2008) Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133: 1266-1276.
70. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, et al. (2010) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105-110.
71. Zerucha T, Stuhmer T, Hatch G, Park BK, Long Q, et al. (2000) A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J Neurosci 20: 709-721.
72. Brugger SM, Merrill AE, Torres-Vazquez J, Wu N, Ting MC, et al. (2004) A phylogenetically conserved cis-regulatory module in the Msx2 promoter is sufficient for BMP-dependent transcription in murine and Drosophila embryos. Development 131: 5153-5165.
73. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM, (2003) Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat Genet 34: 303-307.
74. Michos O, Panman L, Vintersten K, Beier K, Zeller R, et al. (2004) Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131: 3401-3410.
75. Ma L, Lu MF, Schwartz RJ, Martin JF, (2005) Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132: 5601-5611.
76. Matsubara T, Kida K, Yamaguchi A, Hata K, Ichida F, et al. (2008) BMP2 regulates Osterix through Msx2 and Runx2 during osteoblast differentiation. J Biol Chem 283: 29119-29125.
77. Vainio S, Karavanova I, Jowett A, Thesleff I, (1993) Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75: 45-58.
78. Marazzi G, Wang Y, Sassoon D, (1997) Msx2 is a transcriptional regulator in the BMP4-mediated programmed cell death pathway. Dev Biol 186: 127-138.
79. Bei M, Maas R, (1998) FGFs and BMP4 induce both Msx1-independent and Msx1-dependent signaling pathways in early tooth development. Development 125: 4325-4333.
80. 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.
81. Sirard C, Kim S, Mirtsos C, Tadich P, Hoodless PA, et al. (2000) Targeted disruption in murine cells reveals variable requirement for Smad4 in transforming growth factor beta-related signaling. J Biol Chem 275: 2063-2070.
82. Daluiski A, Engstrand T, Bahamonde ME, Gamer LW, Agius E, et al. (2001) Bone morphogenetic protein-3 is a negative regulator of bone density. Nat Genet 27: 84-88.
83. Zhao X, Zhang Z, Song Y, Zhang X, Zhang Y, et al. (2000) Transgenically ectopic expression of Bmp4 to the Msx1 mutant dental mesenchyme restores downstream gene expression but represses Shh and Bmp2 in the enamel knot of wild type tooth germ. Mech Dev 99: 29-38.
84. Zhang Y, Zhang Z, Zhao X, Yu X, Hu Y, et al. (2000) A new function of BMP4: dual role for BMP4 in regulation of Sonic hedgehog expression in the mouse tooth germ. Development 127: 1431-1443.
85. Bei M, Kratochwil K, Maas RL, (2000) BMP4 rescues a non-cell-autonomous function of Msx1 in tooth development. Development 127: 4711-4718.
86. Chen Y, Bei M, Woo I, Satokata I, Maas R, (1996) Msx1 controls inductive signaling in mammalian tooth morphogenesis. Development 122: 3035-3044.
87. Zhang Z, Song Y, Zhao X, Zhang X, Fermin C, et al. (2002) Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development 129: 4135-4146.
88. Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, et al. (2006) Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2: e216.
89. Kraus P, Fraidenraich D, Loomis CA, (2001) Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mech Dev 100: 45-58.
90. Guerrini L, Costanzo A, Merlo GR, (2011) A symphony of regulations centered on p63 to control development of ectoderm-derived structures. J Biomed Biotechnol 2011: 864904.