Msx1 and Msx2 in limb mesenchyme modulate digit number and identity

Developmental Dynamics

Volumn 240, Issue 5, 2011, Pages 1190-1202

  Bensoussan Trigano, Vardina ^a,b   Lallemand, Yvan ^a,b   Saint Cloment, Cécile ^a   Robert, Benoît ^a  

^a CNRS   (France)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Anteroposterior axis; Conditional mutation; Limb; Mesenchyme; Msx; Patterning; Shh

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CRE RECOMBINASE; PROTEIN; PROTEIN ETV4; PROTEIN ETV5; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL ECTODERMAL RIDGE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ECTODERM; EMBRYO; FEMALE; FINGER; FORELIMB; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; HINDLIMB; LIMB BUD; LIMB DEVELOPMENT; LOXP SITE; MALE; MESENCHYME; MESODERM; MOUSE; MUTANT; NONHUMAN; NULL ALLELE; POLYDACTYLY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSGENE; UPREGULATION;

ANIMALS; CELL DEATH; CELL PROLIFERATION; EXTREMITIES; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; LIMB BUDS; MESODERM; MICE; MSX1 TRANSCRIPTION FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79954996174     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22619     Document Type: Article

References (54)

1. Ahn K, Mishina Y, Hanks MC, Behringer RR, Crenshaw EB III. 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.
2. Altabef M, Clarke JD, Tickle C. 1997. Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development 124: 4547-4556.
3. 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.
4. Bendall AJ, Abate-Shen C. 2000. Roles for Msx and Dlx homeoproteins in vertebrate development. Gene 247: 17-31.
5. Bensoussan V, Lallemand Y, Moreau J, Cloment CS, Langa F, Robert B. 2008. Generation of an Msx2-GFP conditional null allele. Genesis 46: 276-282.
6. Blanc I, Bach A, Robert B. 2002. Unusual pattern of Sonic hedgehog expression in the polydactylous mouse mutant Hemimelic extra-toes. Int J Dev Biol 46: 969-974.
7. Boehm B, Westerberg H, Lesnicar-Pucko G, Raja S, Rautschka M, Cotterell J, Swoger J, Sharpe J. 2010. The role of spatially controlled cell proliferation in limb bud morphogenesis. PLoS Biol 8: e1000420.
8. Brugger SM, Merrill AE, Torres-Vazquez J, Wu N, Ting MC, Cho JY, Dobias SL, Yi SE, Lyons K, Bell JR, Arora K, Warrior R, Maxson R. 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.
9. Buscher D, Bosse B, Heymer J, Ruther U. 1997. Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Mech Dev 62: 175-182.
10. Chen Y, Bei M, Woo I, Satokata I, Maas R. 1996. Msx1 controls inductive signaling in mammalian tooth morphogenesis. Development 122: 3035-3044.
11. Crossley PH, Martin GR. 1995. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121: 439-451.
12. Dahn RD, Fallon JF. 1999. Limbiting outgrowth: BMPs as negative regulators in limb development. Bioessays 21: 721-725.
13. Davidson D. 1995. The function and evolution of Msx genes: pointers and paradoxes. Trends Genet 11: 405-411.
14. Dunn NR, Winnier GE, Hargett LK, Schrick JJ, Fogo AB, Hogan BL. 1997. Haploinsufficient phenotypes in Bmp4 heterozygous null mice and modification by mutations in Gli3 and Alx4. Dev Biol 188: 235-247.
15. Fernández-Terán MA, Hinchliffe JR, Ros MA. 2006. Birth and death of cells in limb development: a mapping study. Dev Dyn 235: 2521-2537.
16. Ferrari D, Lichtler AC, Pan ZZ, Dealy CN, Upholt WB, Kosher RA. 1998. Ectopic expression of Msx2 in posterior limb bud mesoderm impairs limb morphognesis while inducing Bmp4 expression, inhibiting cell proliferation, and promoting apoptosis. Dev Biol 197: 12-24.
17. Galli A, Robay D, Osterwalder M, Bao X, Benazet JD, Tariq M, Paro R, Mackem S, Zeller R. 2010. Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet 6: e1000901.
18. Gros J, Hu JK, Vinegoni C, Feruglio PF, Weissleder R, Tabin CJ. 2010. WNT5A/JNK and FGF/MAPK pathways regulate the cellular events shaping the vertebrate limb bud. Curr Biol 20: 1993-2002.
19. 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.
20. 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.
21. Knudsen TB, Kochhar DM. 1981. The role of morphogenetic cell death during abnormal limb-bud outgrowth in mice heterozygous for the dominant mutation Hemimelia-extra toe (Hmx). J Embryol Exp Morphol 65(suppl): 289-307.
22. Krabbenhoft KM, Fallon JF. 1992. Talpid2 limb bud mesoderm does not express GHox-8 and has an altered expression pattern of GHox-7. Dev Dyn 194: 52-62.
23. Kraus P, Fraidenraich D, Loomis CA. 2001. Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mech Dev 100: 45-58.
24. Lallemand Y, Nicola MA, Ramos C, Bach A, Cloment CS, Robert B. 2005. Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb development. Development 132: 3003-3014
25. 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.
26. Lettice LA, Heaney SJ, Purdie LA, Li L, de Beer P, Oostra BA, Goode D, Elgar G, Hill RE, de Graaff E. 2003. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum Mol Genet 12: 1725-1735.
27. Logan M, Martin JF, Nagy A, Lobe C, Olson EN, Tabin CJ. 2002. Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33: 77-80.
28. Maatouk DM, Choi KS, Bouldin CM, Harfe BD. 2009. In the limb AER Bmp2 and Bmp4 are required for dorsal-ventral patterning and interdigital cell death but not limb outgrowth. Dev Biol 327: 516-523.
29. Mao J, McGlinn E, Huang P, Tabin CJ, McMahon AP. 2009. Fgf-dependent Etv4/5 activity is required for posterior restriction of Sonic Hedgehog and promoting outgrowth of the vertebrate limb. Dev Cell 16: 600-606.
30. 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.
31. Michaud JL, Lapointe F, Le Douarin NM. 1997. The dorsoventral polarity of the presumptive limb is determined by signals produced by the somites and by the lateral somatopleure. Development 124: 1453-1463.
32. Michos O, Panman L, Vintersten K, Beier K, Zeller R, Zuniga A. 2004. Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131: 3401-3410.
33. Nakatomi M, Wang XP, Key D, Lund JJ, Turbe-Doan A, Kist R, Aw A, Chen Y, Maas RL, Peters H. 2010. Genetic interactions between Pax9 and Msx1 regulate lip development and several stages of tooth morphogenesis. Dev Biol 340: 438-449.
34. Neubuser A, Koseki H, Balling R. 1995. Characterization and developmental expression of Pax9, a paired-box-containing gene related to Pax1. Dev Biol 170: 701-716.
35. Ogawa T, Kapadia H, Feng JQ, Raghow R, Peters H, D'souza RN. 2006. Functional consequences of interactions between Pax9 and Msx1 genes in normal and abnormal tooth development. J Biol Chem 281: 18363-18369.
36. Ovchinnikov DA, Selever J, Wang Y, Chen YT, Mishina Y, Martin JF, Behringer RR. 2006. BMP receptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Dev Biol 295: 103-115.
37. Peters H, Neubuser A, Kratochwil K, Balling R. 1998. Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. Genes Dev 12: 2735-2747.
38. Pizette S, Niswander L. 1999. BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126: 883-894.
39. Robert B. 2007. Bone morphogenetic protein signaling in limb outgrowth and patterning. Dev Growth Differ 49: 455-468.
40. Sagai T, Masuya H, Tamura M, Shimizu K, Yada Y, Wakana S, Gondo Y, Noda T, Shiroishi T. 2004. Phylogenetic conservation of a limb-specific, cis-acting regulator of Sonic hedgehog (Shh). Mamm Genome 15: 23-34.
41. Sanz-Ezquerro JJ, Tickle C. 2003. Fgf signaling controls the number of phalanges and tip formation in developing digits. Curr Biol 13: 1830-1836.
42. Satokata I, Maas R. 1994. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 6: 348-356.
43. Satokata I, Ma L, Ohshima H, Bei M, Woo I, Nishizawa K, Maeda T, Takano Y, Uchiyama M, Heaney S, Peters H, Tang Z, Maxson R, Maas R. 2000. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet 24: 391-395.
44. Selever J, Liu W, Lu MF, Behringer RR, Martin JF. 2004. Bmp4 in limb bud mesoderm regulates digit pattern by controlling AER development. Dev Biol 276: 268-279.
45. Sharpe J, Lettice L, Hecksher-Sorensen J, Fox M, Hill R, Krumlauf R. 1999. Identification of sonic hedgehog as a candidate gene responsible for the polydactylous mouse mutant Sasquatch. Curr Biol 9: 97-100.
46. Sun X, Lewandoski M, Meyers EN, Liu YH, Maxson RE, Jr., Martin GR. 2000. Conditional inactivation of Fgf4 reveals complexity of signalling during limb bud development. Nat Genet 25: 83-86.
47. Wang B, Fallon JF, Beachy PA. 2000. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100: 423-434.
48. Wang CK, Omi M, Ferrari D, Cheng HC, Lizarraga G, Chin HJ, Upholt WB, Dealy CN, Kosher RA. 2004. Function of BMPs in the apical ectoderm of the developing mouse limb. Dev Biol 269: 109-122.
49. Wyngaarden LA, Vogeli KM, Ciruna BG, Wells M, Hadjantonakis AK, Hopyan S. 2010. Oriented cell motility and division underlie early limb bud morphogenesis. Development 137: 2551-2558.
50. Xu X, Weinstein M, Li C, Naski M, Cohen RI, Ornitz DM, Leder P, Deng C. 1998. Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125: 753-765.
51. Zhang Z, Song Y, Zhao X, Zhang X, Fermin C, Chen Y. 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.
52. Zhang Z, Verheyden JM, Hassell JA, Sun X. 2009. FGF-regulated Etv genes are essential for repressing Shh expression in mouse limb buds. Dev Cell 16: 607-613.
53. Zhang Z, Sui P, Dong A, Hassell J, Cserjesi P, Chen YT, Behringer RR, Sun X. 2010. Preaxial polydactyly: interactions among ETV, TWIST1 and HAND2 control anterior-posterior patterning of the limb. Development 137: 3417-3426.
54. 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.