Loss of AP-2α impacts multiple aspects of ventral body wall development and closure

Developmental Biology

Volumn 267, Issue 2, 2004, Pages 399-417

  Brewer, Stephanie ^a   Williams, Trevor ^a,b  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Abdominal bands; AP 2; Mouse; Omphalocele; Thoracoabdominoschisis; Umbilical ring; Ventral body wall closure

Indexed keywords

TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR AP 2ALPHA; UNCLASSIFIED DRUG; BETA GALACTOSIDASE; DNA BINDING PROTEIN; PRIMER DNA; TCFAP2A PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ABDOMINAL WALL; ABDOMINAL WALL DEFECT; ABDOMINAL WALL MUSCULATURE; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; ECTODERM; EMBRYO; GENE LOSS; MESODERM; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UMBILICUS; ANIMAL; APOPTOSIS; COMPARATIVE STUDY; CROSS BREEDING; GENETIC EPIGENESIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE MUTANT; NICK END LABELING; PHYSIOLOGY; PRENATAL DEVELOPMENT; SILVER STAINING;

MAMMALIA;

ABDOMINAL WALL; ANIMALS; APOPTOSIS; BETA-GALACTOSIDASE; CROSSES, GENETIC; DNA PRIMERS; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HISTOLOGICAL TECHNIQUES; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MESODERM; MICE; MICE, KNOCKOUT; MORPHOGENESIS; SIGNAL TRANSDUCTION; SILVER STAINING; TRANSCRIPTION FACTOR AP-2; TRANSCRIPTION FACTORS;

EID: 1542297350     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.11.021     Document Type: Article

References (96)

1. Auman H.J., Nottoli T., Lakiza O., Winger Q., Donaldson S., Williams T. Transcription factor AP-2γ is essential in the extra-embryonic lineages for early postimplantation development. Development. 129:2002;2733-2747.
2. Babai F., Musevi-Aghdam J., Schurch W., Royal A., Gabbiani G. Coexpression of alpha-sarcomeric actin, α-smooth muscle actin and desmin during myogenesis in rat and mouse embryos I. Skeletal muscle. Differentiation. 44:1990;132-142.
3. Barbieri O., Ognio E., Rossi O., Astigiano S., Rossi L. Embryotoxicity of benzo(a)pyrene and some of its synthetic derivatives in Swiss mice. Cancer Res. 46:1986;94-98.
4. Bosher J.M., Totty N.F., Hsuan J.J., Williams T., Hurst H.C. A family of AP-2 proteins regulates c-erbB-2 expression in mammary carcinoma. Oncogene. 13:1996;1701-1707.
5. Brewer S., Jiang X., Donaldson S., Williams T., Sucov H.M. Requirement for AP-2α in cardiac outflow tract morphogenesis. Mech. Dev. 110:2002;139-149.
6. Brewer, S., Feng, W., Huang, J., Sullivan, S., and Williams, T. (in press). Wnt1-Cre mediated deletion of AP-2α causes multiple neural crest related defects. Dev Biol.
7. Bryson V. Development of the sternum in screw-tail mice. Anat. Rev. 91:1945;119-138.
8. Byrne C., Tainsky M., Fuchs E. Programming gene expression in developing epidermis. Development. 120:1994;2369-2383.
9. Cantrell J., Haller J., Ravitch M. A syndrome of congenital defects involving the abdominal wall, sternum, diaphragm, pericardium, and heart. Surg. Gynecol. Obstet. 107:1958;602-614.
10. Carmi R., Barbash A., Mares A.J. The thoracoabdominal syndrome (TAS): a new X-linked dominant disorder. Am. J. Med. Genet. 36:1990;109-114.
11. Chazaud C., Oulad-Abdelghani M., Bouillet P., Décimo D., Chambon P., Dollé P. AP-2.2, a novel gene related to AP-2, is expressed in the forebrain, limbs and face during mouse embryogenesis. Mech. Dev. 54:1996;83-94.
12. Chen J.M. Studies on the morphogenesis of the mouse sternum: I. Normal embryonic development. J. Anat. (London). 86:1952;373-386.
13. Chen J.M. Studies on the morphogenesis of the mouse sternum: III. Experiments on the closure and segmentation of the sternal band. J. Anat. 87:1953;130-154.
14. Christ B., Jacob M., Jacob H.J. On the origin and development of the ventrolateral abdominal muscles in the avian embryo. An experimental and ultrastructural study. Anat. Embryol. (Berl). 166:1983;87-101.
15. Duhamel B. Embryology of exomphalos and allied malformations. Arch. Dis. Child. 38:1963;142-147.
16. -/- double knockout mice display severe midline fusion defects and early embryonic lethality. Anat. Embryol. (Berl). 206:2002;73-83.
17. Eggenschwiler J., Ludwig T., Fisher P., Leighton P.A., Tilghman S.M., Efstratiadis A. Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev. 11:1997;3128-3142.
18. Erb R., Jaffe R., Braren V., Jeanty P. Exstrophy of the Cloaca Sequence. 1992;. http://www.thefetus.net/.
19. Fan C.M., Tessier-Lavigne M. Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell. 79:1994;1175-1186.
20. Feng W., Williams T. Cloning and characterization of the mouse AP-2ε gene: a novel family member expressed in the developing olfactory bulb. Mol. Cell. Neurosci. 24:2003;460-475.
21. Ferry J.J.R., Cohen P. Beckwith-Wiedemann Syndrome. 2002;. http://www.emedicine.com/.
22. Fini M.E., Bartlett J.D., Matsubara M., Rinehart W.B., Mody M.K., Girard M.T., Rainville M. The rabbit gene for 92-kDa matrix metalloproteinase. Role of AP1 and AP2 in cell type-specific transcription. J. Biol. Chem. 269:1994;28620-28628.
23. Gage P.J., Camper S.A. Pituitary homeobox 2, a novel member of the bicoid-related family of homeobox genes, is a potential regulator of anterior structure formation. Hum. Mol. Genet. 6:1997;457-464.
24. Gladstone R.J., Wakeley C.P.G. The morphology of the sternum and its relation to the ribs. J. Anat. (London). 66:1932;508-564.
25. Glasser J.G. Omphalocele and Gastroschisis. 2001;. http://www.emedicine. com/.
26. Gomori G.L. A rapid one-step trichrome. Am. J. Clin. Pathol. 20:1950;131.
27. Grange D.K., Arya S., Opitz J.M., Laxova R., Herrmann J., Gilbert E.F. The short umbilical cord. Birth Defects Orig. Artic Ser. 23:1987;191-214.
28. Hall B.K. The role of movement and tissue interactions in the development and growth of bone and secondary cartilage in the clavicle of the embryonic chick. J. Embryol. Exp. Morphol. 93:1986;133-152.
29. Hall B.K. Development of the clavicles in birds and mammals. J. Exp. Zool. 289:2001;153-161.
30. Hartwig N.G., Vermeij-Keers C., De Vries H.E., Kagie M., Kragt H. Limb body wall malformation complex: an embryologic etiology? Hum. Pathol. 20:1989;1071-1077.
31. Hartwig N.G., Steffelaar J.W., Van de Kaa C., Schueler J.A., Vermeij-Keers C. Abdominal wall defect associated with persistent cloaca. The embryologic clues in autopsy. Am. J. Clin. Pathol. 96:1991;640-647.
32. Hasty P., Bradley A., Morris J.H., Edmondson D.G., Venuti J.M., Olson E.N., Klein W.H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature. 364:1993;501-506.
33. Hébert J.M., McConnell S.K. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 222:2000;296-306.
34. Hennig G., Lowrick O., Birchmeier W., Behrens J. Mechanisms identified in the transcriptional control of epithelial gene expression. J. Biol. Chem. 271:1996;595-602.
35. Herva R., Karkinen-Jaaskelainen M. Amniotic adhesion malformation syndrome: fetal and placental pathology. Teratology. 29:1984;11-19.
36. Hillebrandt S., Streffer C., Montagutelli X., Balling R. A locus for radiation-induced gastroschisis on mouse Chromosome 7. Mamm. Genome. 9:1998;995-997.
37. Hirata M., Hall B.K. Temporospatial patterns of apoptosis in chick embryos during the morphogenetic period of development. Int. J. Dev. Biol. 44:2000;757-768.
38. Hogan B., Beddington R., Costantini F., Lacy E. Manipulating the Mouse Embryo: A Laboratory Manual. 1994;Cold Spring Harbor Press, Plainview.
39. Jiang X., Rowitch D.H., Soriano P., McMahon A.P., Sucov H.M. Fate of the mammalian cardiac neural crest. Development. 127:2000;1607-1616.
40. Jorgenson R.J., Levin L.S., Cross H.E., Yoder F., Kelly T.E. The Rieger syndrome. Am. J. Med. Genet. 2:1978;307-318.
41. Kaufman M.H. The Atlas of Mouse Development. 1992;Academic Press Limited, San Diego.
42. Kaufman M.H., Bard J.B.L. The Anatomical Basis of Mouse Development. 1999;Academic Press, San Diego.
43. Kenny-Mobbs T. Myogenic differentiation in early chick wing mesenchyme in the absence of the brachial somites. J. Embryol. Exp. Morphol. 90:1985;415-436.
44. Klima M. Early development of the human sternum and the problem of homologization of the so-called suprasternal structures. Acta Anat. (Basel). 69:1968;473-484.
45. Klima M. Early development of the shoulder girdle and sternum in marsupials (Mammalia: Metatheria). Adv. Anat. Embryol. Cell Biol. 109:1987;1-91.
46. Kuratani S., Martin J.F., Wawersik S., Lilly B., Eichele G., Olson E.N. The expression pattern of the chick homeobox gene gMHox suggests a role in patterning of the limbs and face and in compartmentalization of somites. Dev. Biol. 161:1994;357-369.
47. Leask A., Byrne C., Fuchs E. Transcription factor AP2 and its role in epidermal-specific gene expression. Proc. Natl. Acad. Sci. U. S. A. 88:1991;7948-7952.
48. Lin C.R., Kioussi C., O'Connell S., Briata P., Szeto D., Liu F., Izpisua-Belmonte J.C., Rosenfeld M.G. Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature. 401:1999;279-282.
49. Maher E.R., Reik W. Beckwith-Wiedemann syndrome: imprinting in clusters revisited. J. Clin. Invest. 105:2000;247-252.
50. Manley N.R., Barrow J.R., Zhang T., Capecchi M.R. Hoxb2 and Hoxb4 act together to specify ventral body wall formation. Dev. Biol. 237:2001;130-144.
51. Martin R.A., Cunniff C., Erickson L., Jones K.L. Pentalogy of Cantrell and ectopia cordis, a familial developmental field complex. Am. J. Med. Genet. 42:1992;839-841.
52. Martinez-Frias M.L., Bermejo E., Rodriguez-Pinilla E., Frias J.L. Exstrophy of the cloaca and exstrophy of the bladder: two different expressions of a primary developmental field defect. Am. J. Med. Genet. 99:2001;261-269.
53. Maytin E.V., Lin J.C., Krishnamurthy R., Batchvarova N., Ron D., Mitchell P.J., Habener J.F. Keratin 10 gene expression during differentiation of mouse epidermis requires transcription factors C/EBP and AP-2. Dev. Biol. 216:1999;164-181.
54. Meulemans D., Bronner-Fraser M. Amphioxus and lamprey AP-2 genes: implications for neural crest evolution and migration patterns. Development. 129:2002;4953-4962.
55. Mitchell P.J., Timmons P.M., Hebert J.M., Rigby P.W., Tjian R. Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev. 5:1991;105-119.
56. Moore K.L. The Developing Human. 1982;Saunders, Philadelphia.
57. Moser M., Imhof A., Pscherer A., Bauer R., Amselgruber W., Sinowatz F., Hofstadter F., Schule R., Buettner R. Cloning and characterization of a second AP-2 transcription factor: AP-2β Development. 121:1995;2779-2788.
58. Moser M., Pscherer A., Roth C., Becker J., Mucher G., Zerres K., Dixkens C., Weis J., Guay-Woodford L., Buettner R., Fassler R. Enhanced apoptotic cell death of renal epithelial cells in mice lacking transcription factor AP-2β Genes Dev. 11:1997;1938-1948.
59. Moser M., Ruschoff J., Buettner R. Comparative analysis of AP-2α and AP-2β gene expression during murine embryogenesis. Dev. Dyn. 208:1997;115-124.
60. Munger G.T., Munger B.L. Differentiation of the anterior body wall and truncal epidermis and associated co-migration of cutaneous nerves and mesenchyme. Anat. Rec. 231:1991;261-274.
61. Nabeshima Y., Hanaoka K., Hayasaka M., Esumi E., Li S., Nonaka I. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature. 364:1993;532-535.
62. Nelson, D.K., and Williams, T. (in press). Frontonasal process-specific disruption of AP-2α results in postnatal midfacial hypoplasia, vascular anomalies, and nasal cavity defects. Dev. Biol.
63. Nottoli T., Hagopian-Donaldson S., Zhang J., Perkins A., Williams T. AP-2-null cells disrupt morphogenesis of the eye, face, and limbs in chimeric mice. Proc. Natl. Acad. Sci. U. S. A. 95:1998;13714-13719.
64. Ordahl C.P., Le Douarin N.M. Two myogenic lineages within the developing somite. Development. 114:1992;339-353.
65. Oulad-Abdelghani M., Bouillet P., Chazaud C., Dollé P., Chambon P. AP-2.2: a novel AP-2-related transcription factor induced by retinoic acid during differentiation of P19 embryonal carcinoma cells. Exp. Cell Res. 225:1996;338-347.
66. Padmanabhan R. Retinoic acid-induced caudal regression syndrome in the mouse fetus. Reprod. Toxicol. 12:1998;139-151.
67. Pampfer S., Streffer C. Prenatal death and malformations after irradiation of mouse zygotes with neutrons or X-rays. Teratology. 37:1988;599-607.
68. Parvari R., Weinstein Y., Ehrlich S., Steinitz M., Carmi R. Linkage localization of the thoraco-abdominal syndrome (TAS) gene to Xq25-26. Am. J. Med. Genet. 49:1994;431-434.
69. Price C.J., Kimmel C.A., George J.D., Marr M.C. The developmental toxicity of diethylene glycol dimethyl ether in mice. Fundam. Appl. Toxicol. 8:1987;115-126.
70. Rieger H. Dysgenesis mesodemalis corneal et iridis. Z. Augenheilkd. 86:1935;333.
71. Roebroek A.J., Umans L., Pauli I.G., Robertson E.J., van Leuven F., Van de Ven W.J., Constam D.B. Failure of ventral closure and axial rotation in embryos lacking the proprotein convertase furin. Development. 125:1998;4863-4876.
72. Russo R., D'Armiento M., Angrisani P., Vecchione R. Limb body wall complex: a critical review and a nosological proposal. Am. J. Med. Genet. 47:1993;893-900.
73. Rutledge J.C. Developmental toxicity induced during early stages of mammalian embryogenesis. Mutat. Res. 396:1997;113-127.
74. Schorle H., Meier P., Buchert M., Jaenisch R., Mitchell P.J. Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature. 381:1996;235-238.
75. Semina E.V., Reiter R., Leysens N.J., Alward W.L., Small K.W., Datson N.A., Siegel-Bartelt J., Bierke-Nelson D., Bitoun P., Zabel B.U., Carey J.C., Murray J.C. Cloning and characterization of a novel bicoid-related homeobox transcription factor gene. RIEG, involved in Rieger syndrome. Nat. Genet. 14:1996;392-399.
76. Sevier A.C., Munger B.L. A silverstain for paraffin sections of neural tissue. J. Neuropathol. Exp. Neurol. 24:1965;130-135.
77. Smits-van Prooije A.E., Vermeij-Keers C., Dubbeldam J.A., Mentink M.M., Poelmann R.E. The formation of mesoderm and mesectoderm in presomite rat embryos cultured in vitro, using WGA-Au as a marker. Anat. Embryol. (Berl). 176:1987;71-77.
78. Smits-van Prooije A.E., Vermeij-Keers C., Poelmann R.E., Mentink M.M., Dubbeldam J.A. The formation of mesoderm and mesectoderm in 5- to 41-somite rat embryos cultured in vitro, using WGA-Au as a marker. Anat. Embryol. (Berl). 177:1988;245-256.
79. Stadler H.S. Modelling genitourinary defects in mice: an emerging genetic and developmental system. Nat. Rev., Genet. 4:2003;478-482.
80. Streeter G.L. Focal deficiencies in fetal tissues and their relation to intra-uterine amputation. Contrib. Embryol. Carnegie Inst. 22:1930;1-44.
81. Suzuki N., Labosky P.A., Furuta Y., Hargett L., Dunn R., Fogo A.B., Takahara K., Peters D.M., Greenspan D.S., Hogan B.L. Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development. 122:1996;3587-3595.
82. Thompson J., Bannigan J. Effects of cadmium on formation of the ventral body wall in chick embryos and their prevention by zinc pretreatment. Teratology. 64:2001;87-97.
83. Tremblay P., Dietrich S., Mericskay M., Schubert F.R., Li Z., Paulin D. A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors. Dev. Biol. 203:1998;49-61.
84. Van Allen M.I. Fetal vascular disruptions: mechanisms and some resulting birth defects. Pediatr. Ann. 10:1981;219-233.
85. Van Allen M.I., Curry C., Gallagher L. Limb body wall complex: I. Pathogenesis. Am. J. Med. Genet. 28:1987;529-548.
86. Vasioukhin V., Degenstein L., Wise B., Fuchs E. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc. Natl. Acad. Sci. U. S. A. 96:1999;8551-8556.
87. Vermeij-Keers C., Poelmann R.E. The neural crest: a study on cell degeneration and the improbability of cell migration in mouse embryos. Neth. J. Zool. 30:1980;74-80.
88. Vermeij-Keers C., Hartwig N.G., van der Werff J.F. Embryonic development of the ventral body wall and its congenital malformations. Semin. Pediatr. Surg. 5:1996;82-89.
89. Wei X., Sulik K.K. Pathogenesis of craniofacial and body wall malformations induced by ochratoxin A in mice. Am. J. Med. Genet. 47:1993;862-871.
90. Werling U., Schorle H. Transcription factor gene AP-2γ essential for early murine development. Mol. Cell. Biol. 22:2002;3149-3156.
91. West-Mays J.A., Zhang J., Nottoli T., Hagopian-Donaldson S., Strissel K.J., Libby D., Williams T. AP-2α transcription factor is required for early morphogenesis of the lens vesicle. Dev. Biol. 206:1999;46-62.
92. West-Mays J.A., Sivak J.M., Papagiotas S.S., Kim J., Nottoli T., Williams T., Fini M.E. Positive influence of AP-2α transcription factor on cadherin gene expression and differentiation of the ocular surface. Differentiation. 71:2003;206-216.
93. Williams T., Admon A., Lüscher B., Tjian R. Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Dev. 2:1988;1557-1569.
94. Wu N.F., Kushnick T. The Beckwith-Wiedemann syndrome. The exomphalos-macroglossia-gigantism syndrome. Clin. Pediatr. (Phila). 13:1974;452-457.
95. Zhang J., Hagopian-Donaldson S., Serbedzija G., Elsemore J., Plehn-Dujowich D., McMahon A.P., Flavell R.A., Williams T. Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature. 381:1996;238-241.
96. Zhao F., Satoda M., Licht J.D., Hayashizaki Y., Gelb B.D. Cloning and characterization of a novel mouse AP-2 transcription factor, AP-2δ, with unique DNA binding and transactivation properties. J. Biol. Chem. 276:2001;40755-40760.