Control of pelvic girdle development by genes of the Pbx family and Emx2

Developmental Dynamics

Volumn 240, Issue 5, 2011, Pages 1173-1189

  Capellini, Terence D ^a   Handschuh, Karen ^a   Quintana, Laura ^b   Ferretti, Elisabetta ^d   Di Giacomo, Giuseppina ^a   Fantini, Sebastian ^c   Vaccari, Giulia ^c   Clarke, Shoa L ^d   Wenger, Aaron M ^e   Bejerano, Gill ^d,e   Sharpe, James ^b,f   Zappavigna, Vincenzo ^c   Selleri, Licia ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^d STANFORD UNIVERSITY   (United States)

^e Stanford University   (United States)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Emx2; Girdle; Ilium; Ischium; Limb; Mouse; Pbx; Pelvis development; Pubis; Somatopleure

Indexed keywords

HOMEODOMAIN PROTEIN; MESSENGER RNA; PROTEIN P300; PROTEIN PAX1; PROTEIN PITX1; PROTEIN PRRX1; PROTEIN TBX15; PROTEIN TWIST1; TRANSCRIPTION FACTOR EMX2; TRANSCRIPTION FACTOR PBX1; TRANSCRIPTION FACTOR PBX2; TRANSCRIPTION FACTOR PBX3; TRANSCRIPTION FACTOR SOX9; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BONE DEVELOPMENT; CONTROLLED STUDY; DNA BINDING; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; FEMALE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE LOCUS; HINDLIMB; ILIAC BONE; IN SITU HYBRIDIZATION; ISCHIUM; MALE; MESENCHYME; MESODERM; MORPHOGENESIS; MOUSE; NONHUMAN; NULL ALLELE; OPTICAL PROJECTION TOMOGRAPHY; PELVIC GIRDLE; PELVIC GIRDLE DEVELOPMENT; POSITION WEIGHT MATRIX; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PUBIC BONE; TOMOGRAPHY; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; COMPUTATIONAL BIOLOGY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MALE; MICE; PAIRED BOX TRANSCRIPTION FACTORS; PELVIS; PROTO-ONCOGENE PROTEINS; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS;

VERTEBRATA;

EID: 79955045629     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22617     Document Type: Article

References (57)

1. Beverdam A, Meijlink FU. 2001. Expression patterns of group-I aristaless-related genes during craniofacial and limb development. Mech Dev 107: 163-167.
2. Bi W, Huang W, Whitworth DJ, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. 2001. Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci U S A 98: 6698-6703.
3. Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G. 2004. A twist code determines the onset of osteoblast differentiation. Dev Cell 6: 423-435.
4. Brendolan A, Ferretti E, Salsi V, Moses K, Quaggin S, Blasi F, Cleary ML, Selleri L. 2005. A Pbx1-dependent genetic and transcriptional network regulates spleen ontogeny. Development 132: 3113-3126.
5. Brent AE, Tabin CJ. 2004. FGF acts directly on the somitic tendon progenitors through the Ets transcription factors Pea3 and Erm to regulate scleraxis expression. Development 131: 3885-3896.
6. Capellini TD, Di Giacomo G, Salsi V, Brendolan A, Ferretti E, Srivastava D, Zappavigna V, Selleri L. 2006. Pbx1/Pbx2 requirement for distal limb patterning is mediated by the hierarchical control of Hox gene spatial distribution and Shh expression. Development 133: 2263-2273.
7. Capellini TD, Zewdu R, Di Giacomo G, Asciutti S, Kugler JE, Di Gregorio A, Selleri L. 2008. Pbx1/Pbx2 govern axial skeletal development by controlling Polycomb and Hox in mesoderm and Pax1/Pax9 in sclerotome. Dev Biol 321: 500-514.
8. Capellini TD, Vaccari G, Ferretti E, Fantini S, He M, Pellegrini M, Quintana L, Di Giacomo G, Sharpe J, Selleri L, Zappavigna V. 2010. Scapula development is governed by genetic interactions of Pbx1 with its family members and with Emx2 via their cooperative control of Alx1. Development 137: 2559-2569.
9. Chalepakis G, Fritsch R, Fickenscher H, Deutsch U, Goulding M, Gruss P. 1991. The molecular basis of the undulated/Pax-1 mutation. Cell 66: 873-884.
10. Cheah KS, Au PK, Lau ET, Little PF, Stubbs L. 1991. The mouse Col2a-1 gene is highly conserved and is linked to Int-1 on chromosome 15. Mamm Genome 1: 171-183.
11. Chevallier A, Kieny M, Mauger A. 1977. Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41: 245-258.
12. Christ B, Huang R, Wilting J. 2000. The development of the avian vertebral column. Anat Embryol (Berl) 202: 179-194.
13. Connell KA, Guess MK, Chen H, Andikyan V, Bercik R, Taylor HS. 2008. HOXA11 is critical for development and maintenance of uterosacral ligaments and deficient in pelvic prolapse. J Clin Invest 118: 1050-1055.
14. Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, Pedersen RA, Rubenstein JL. 1999. Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126: 3831-3846.
15. Di Giacomo G, Koss M, Capellini TD, Brendolan A, Popperl H, Selleri L. 2006. Spatio-temporal expression of Pbx3 during mouse organogenesis. Gene Expr Patterns 6: 747-757.
16. Dudley AT, Ros MA, Tabin CJ. 2002. A re-examination of proximodistal patterning during vertebrate limb development. Nature 418: 539-544.
17. Hostikka SL, Gong J, Carpenter EM. 2009. Axial and appendicular skeletal transformations, ligament alterations, and motor neuron loss in Hoxc10 mutants. Int J Biol Sci 5: 397-410.
18. Huang R, Zhi Q, Patel K, Wilting J, Christ B. 2000. Dual origin and segmental organisation of the avian scapula. Development 127: 3789-3794.
19. Huang R, Christ B, Patel K. 2006. Regulation of scapula development. Anat Embryol (Berl) 211(suppl 1): 65-71.
20. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12: 996-1006.
21. Knezevic V, De Santo R, Schughart K, Huffstadt U, Chiang C, Mahon KA, Mackem S. 1997. Hoxd-12 differentially affects preaxial and postaxial chondrogenic branches in the limb and regulates Sonic hedgehog in a positive feedback loop. Development 124: 4523-4536.
22. Krawchuk D, Weiner SJ, Chen YT, Lu BC, Costantini F, Behringer RR, Laufer E. 2010. Twist1 activity thresholds define multiple functions in limb development. Dev Biol 347: 133-146.
23. Kuijper S, Beverdam A, Kroon C, Brouwer A, Candille S, Barsh G, Meijlink FU. 2005. Genetics of shoulder girdle formation: roles of Tbx15 and aristaless-like genes. Development 132: 1601-1610.
24. Lanctot C, Moreau A, Chamberland M, Tremblay ML, Drouin J. 1999. Hindlimb patterning and mandible development require the Ptx1 gene. Development 126: 1805-1810.
25. Lausch E, Hermanns P, Farin HF, Alanay Y, Unger S, Nikkel S, Steinwender C, Scherer G, Spranger J, Zabel B, Kispert A, Superti-Furga A. 2008. TBX15 mutations cause craniofacial dysmorphism, hypoplasia of scapula and pelvis, and short stature in Cousin syndrome. Am J Hum Genet 83: 649-655.
26. LeClair EE, Bonfiglio L, Tuan RS. 1999. Expression of the paired-box genes Pax-1 and Pax-9 in limb skeleton development. Dev Dyn 214: 101-115.
27. Loebel DA, O'Rourke MP, Steiner KA, Banyer J, Tam PP. 2002. Isolation of differentially expressed genes from wild-type and Twist mutant mouse limb buds. Genesis 33: 103-113.
28. Malashichev Y, Borkhvardt V, Christ B, Scaal M. 2005. Differential regulation of avian pelvic girdle development by the limb field ectoderm. Anat Embryol (Berl) 210: 187-197.
29. Malashichev Y, Christ B, Prols F. 2008. Avian pelvis originates from lateral plate mesoderm and its development requires signals from both ectoderm and paraxial mesoderm. Cell Tissue Res 331: 595-604.
30. Marcil A, Dumontier E, Chamberland M, Camper SA, Drouin J. 2003. Pitx1 and Pitx2 are required for development of hindlimb buds. Development 130: 45-55.
31. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP, Koentges G. 2005. Neural crest origins of the neck and shoulder. Nature 436: 347-355.
32. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28: 495-501.
33. McLeod M. 1980. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22: 299-301.
34. Moens CB, Selleri L. 2006. Hox cofactors in vertebrate development. Dev Biol 291: 193-206.
35. Naiche LA, Papaioannou VE. 2007. Tbx4 is not required for hindlimb identity or post-bud hindlimb outgrowth. Development 134: 93-103.
36. Niswander L. 2003. Pattern formation: old models out on a limb. Nat Rev Genet 4: 133-143.
37. O'Rourke MP, Soo K, Behringer RR, Hui CC, Tam PP. 2002. Twist plays an essential role in FGF and SHH signal transduction during mouse limb development. Dev Biol 248: 143-156.
38. Pellegrini M, Pantano S, Fumi MP, Lucchini F, Forabosco 2001. Agenesis of the Scapula in Emx2 Homozygous Mutants. Dev Biol 232: 149-156.
39. Perez AV, Perrine M, Brainard N, Vogel KG. 2003. Scleraxis (Scx) directs lacZ expression in tendon of transgenic mice. Mech Dev 120: 1153-1163.
40. Peters H, Wilm B, Sakai N, Imai K, Maas R, Balling R. 1999. Pax1 and Pax9 synergistically regulate vertebral column development. Development 126: 5399-5408.
41. Pomikal C, Streicher J. 2010. 4D-analysis of early pelvic girdle development in the mouse (Mus musculus). J Morphol 271: 116-126.
42. Rhee JW, Arata A, Selleri L, Jacobs Y, Arata S, Onimaru H, Cleary ML. 2004. Pbx3 deficiency results in central hypoventilation. Am J Pathol 165: 1343-1350.
43. Romer AS, Parsons TS. 1986. The vertebrate body. New York: Saunders College Publishing. p iii-679.
44. Sanchez-Villagra MR, Maier W. 2002. Ontogenetic data and the evolutionary origin of the mammalian scapula. Naturwissenschaften 89: 459-461.
45. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, Yagishita N, Matsui D, Koga Y, Itoh N, Kato S. 1999. Fgf10 is essential for limb and lung formation. Nat Genet 21: 138-141.
46. Selleri L, Depew MJ, Jacobs Y, Chanda SK, Tsang KY, Cheah KS, Rubenstein JL, O'Gorman S, Cleary ML. 2001. Requirement for Pbx1 in skeletal patterning and programming chondrocyte proliferation and differentiation. Development 128: 3543-3557.
47. Selleri L, DiMartino J, van Deursen J, Brendolan A, Sanyal M, Boon E, Capellini T, Smith KS, Rhee J, Popperl H, Grosveld G, Cleary ML. 2004. The TALE homeodomain protein Pbx2 is not essential for development and long-term survival. Mol Cell Biol 24: 5324-5331.
48. Sharpe J. 2003. Optical projection tomography as a new tool for studying embryo anatomy. J Anat 202: 175-181.
49. Sharpe J, Ahlgren U, Perry P, Hill B, Ross A, Hecksher-Sorensen J, Baldock R, Davidson D. 2002. Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296: 541-545.
50. Singh MK, Petry M, Haenig B, Lescher B, Leitges M, Kispert AU. 2005. The T-box transcription factor Tbx15 is required for skeletal development. Mech Dev 122: 131-144.
51. ten Berge D, Brouwer A, Korving J, Martin JF, Meijlink F. 1998. Prx1 and Prx2 in skeletogenesis: roles in the craniofacial region, inner ear and limbs. Development 125: 3831-3842.
52. Timmons PM, Wallin J, Rigby PW, Balling R. 1994. Expression and function of Pax 1 during development of the pectoral girdle. Development 120: 2773-2785.
53. Valasek P, Theis S, Krejci E, Grim M, Maina F, Shwartz Y, Otto A, Huang R, Patel K. 2010. Somitic origin of the medial border of the mammalian scapula and its homology to the avian scapula blade. J Anat 216: 482-488.
54. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin EM, Pennacchio LA. 2009. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854-858.
55. Wang B, He L, Ehehalt F, Geetha-Loganathan P, Nimmagadda S, Christ B, Scaal M, Huang R. 2005. The formation of the avian scapula blade takes place in the hypaxial domain of the somites and requires somatopleure-derived BMP signals. Dev Biol 287: 11-18.
56. Wright E, Hargrave MR, Christiansen J, Cooper L, Kun J, Evans T, Gangadharan U, Greenfield A, Koopman P. 1995. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat Genet 9: 15-20.
57. Young NM. 2006. Function, ontogeny and canalization of shape variance in the primate scapula. J Anat 209: 623-636.