AP-2α is required after lens vesicle formation to maintain lens integrity

Developmental Dynamics

Volumn 243, Issue 10, 2014, Pages 1298-1309

  Kerr, Christine L ^a   Zaveri, Mizna A ^a   Robinson, Michael L ^b   Williams, Trevor ^c   West Mays, Judith A ^a  

^a MCMASTER UNIVERSITY MEDICAL CENTRE   (Canada)

^b MIAMI UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

AP 2; Differentiation; Lens development; Lens epithelium; Transcription factors

Indexed keywords

TRANSCRIPTION FACTOR AP 2;

ANIMAL; ANIMAL EMBRYO; CATARACT; CELL ADHESION; CELL DIFFERENTIATION; CELL POLARITY; EMBRYOLOGY; EPITHELIUM; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; LENS; METABOLISM; MOUSE; PHENOTYPE; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CATARACT; CELL ADHESION; CELL DIFFERENTIATION; CELL POLARITY; EMBRYO, MAMMALIAN; EPITHELIAL CELLS; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LENS, CRYSTALLINE; MICE; MICE, TRANSGENIC; PHENOTYPE; TRANSCRIPTION FACTOR AP-2;

EID: 84907841711     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24141     Document Type: Article

References (58)

1. Andley UP. 2007. Crystallins in the eye: function and pathology. Prog Retin Eye Res 26:78-98.
2. Ashery-Padan R, Marquardt T, Zhou X, Gruss P. 2000. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev 14:2701-2711.
3. Bassett EA, Korol A, Deschamps PA, Buettner R, Wallace VA, Williams T, West-Mays JA. 2012. Overlapping expression patterns and redundant roles for AP-2 transcription factors in the developing mammalian retina. Dev Dyn 241:814-829.
4. Bassett EA, Pontoriero GF, Feng W, Marquardt T, Fini ME, Williams T, West-Mays JA. 2007. Conditional deletion of activating protein 2alpha (AP-2alpha) in the developing retina demonstrates non-cell-autonomous roles for AP-2alpha in optic cup development. Mol Cell Biol 27:7497-7510.
5. Beebe DC, Vasiliev O, Guo J, Shui YB, Bassnett S. 2001. Changes in adhesion complexes define stages in the differentiation of lens fiber cells. Invest Ophthalmol Vis Sci 42:727-734.
6. Bilder D, Perrimon N. 2000. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403:676-680.
7. Brewer S, Feng W, Huang J, Sullivan S, Williams T. 2004. Wnt1-Cre-mediated deletion of AP-2alpha causes multiple neural crest-related defects. Dev Biol 267:135-152.
8. Brewer S, Jiang X, Donaldson S, Williams T, Sucov HM. 2002. Requirement for AP-2alpha in cardiac outflow tract morphogenesis. Mech Dev 110:139-149.
9. Brownell I, Dirksen M, Jamrich M. 2000. Forkhead Foxe3 maps to the dysgenetic lens locus and is critical in lens development and differentiation. Genesis 27:81-93.
10. Cain S, Martinez G, Kokkinos MI, Turner K, Richardson RJ, Abud HE, Huelsken J, Robinson ML, de Iongh RU. 2008. Differential requirement for beta-catenin in epithelial and fiber cells during lens development. Dev Biol 321:420-433.
11. Carmona FD, Jimenez R, Collinson JM. 2008. The molecular basis of defective lens development in the Iberian mole. BMC Biol 6:44.
12. Carper D, Smith-Gill SJ, Kinoshita JH. 1986. Immunocytochemical localization of the 27K beta-crystallin polypeptide in the mouse lens during development using a specific monoclonal antibody: implications for cataract formation in the Philly mouse. Dev Biol 113:104-109.
13. Chow RL, Lang RA. 2001. Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255-296.
14. Dawes LJ, Sugiyama Y, Lovicu FJ, Harris CG, Shelley EJ, McAvoy JW. 2014. Interactions between lens epithelial and fiber cells reveal an intrinsic self-assembly mechanism. Dev Biol 385:291-303.
15. Dumitrescu AV, Milunsky JM, Longmuir SQ, Drack AV. 2012. A family with branchio-oculo-facial syndrome with primarily ocular involvement associated with mutation of the TFAP2A gene. Ophthal Genet 33:100-106.
16. Duncan MK, Haynes JI Jr, Cvekl A, Piatigorsky J. 1998. Dual roles for Pax-6: a transcriptional repressor of lens fiber cell-specific beta-crystallin genes. Mol Cell Biol 18:5579-5586.
17. Duncan MK, Xie L, David LL, Robinson ML, Taube JR, Cui W, Reneker LW. 2004. Ectopic Pax6 expression disturbs lens fiber cell differentiation. Invest Ophthalmol Vis Sci 45:3589-3598.
18. Eckert D, Buhl S, Weber S, Jager R, Schorle H. 2005. The AP-2 family of transcription factors. Genome Biol 6:246.
19. Feng W, Williams T. 2003. Cloning and characterization of the mouse AP-2 epsilon gene: a novel family member expressed in the developing olfactory bulb. Mol Cell Neurosci 24:460-475.
20. Ferreira-Cornwell MC, Veneziale RW, Grunwald B, Menko AS. 2000. N-cadherin function is required for differentiation-dependent cytoskeletal reorganization in lens cells in vitro. Exp Cell Res 256:237-247.
21. Gu H, Marth JD, Orban PC, Mossmann H, Rajewsky K. 1994. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265:103-106.
22. Hales AM, Schulz MW, Chamberlain CG, McAvoy JW. 1994. TGF-beta 1 induces lens cells to accumulate alpha-smooth muscle actin, a marker for subcapsular cataracts. Curr Eye Res 13:885-890.
23. Hilger-Eversheim K, Moser M, Schorle H, Buettner R. 2000. Regulatory roles of AP-2 transcription factors in vertebrate development, apoptosis and cell-cycle control. Gene 260:1-12.
24. Hsu CD, Kymes S, Petrash JM. 2006. A transgenic mouse model for human autosomal dominant cataract. Invest Ophthalmol Vis Sci 47:2036-2044.
25. Huang J, Rajagopal R, Liu Y, Dattilo LK, Shaham O, Ashery-Padan R, Beebe DC. 2011. The mechanism of lens placode formation: a case of matrix-mediated morphogenesis. Dev Biol 355:32-42.
26. Kelley PB, Sado Y, Duncan MK. 2002. Collagen IV in the developing lens capsule. Matrix Biol 21:415-423.
27. Kerr CL, Huang J, Williams T, West-Mays JA. 2012. Activation of the Hedgehog signaling pathway in the developing lens stimulates ectopic FoxE3 expression and disruption in fiber cell differentiation. Invest Ophthalmol Vis Sci 53:3316-3330.
28. Loo DT. 2011. In situ detection of apoptosis by the TUNEL assay: an overview of techniques. Methods Mol Biol 682:3-13.
29. Lovicu FJ, McAvoy JW. 2005. Growth factor regulation of lens development. Dev Biol 280:1-14.
30. Lovicu FJ, Steven P, Saika S, McAvoy JW. 2004. Aberrant lens fiber differentiation in anterior subcapsular cataract formation: a process dependent on reduced levels of Pax6. Invest Ophthalmol Vis Sci 45:1946-1953.
31. Lovicu FJ, Robinson ML. 2004. Development of the ocular lens. New York: Cambridge.
32. Maddala R, Chauhan BK, Walker C, Zheng Y, Robinson ML, Lang RA, Rao PV. 2011. Rac1 GTPase-deficient mouse lens exhibits defects in shape, suture formation, fiber cell migration and survival. Dev Biol 360:30-43.
33. Medina-Martinez O, Brownell I, Amaya-Manzanares F, Hu Q, Behringer RR, Jamrich M. 2005. Severe defects in proliferation and differentiation of lens cells in Foxe3 null mice. Mol Cell Biol 25:8854-8863.
34. Milunsky JM, Maher TA, Zhao G, Roberts AE, Stalker HJ, Zori RT, Burch MN, Clemens M, Mulliken JB, Smith R, Lin AE. 2008. TFAP2A mutations result in branchio-oculo-facial syndrome. Am J Hum Genet 82:1171-1177.
35. Min JN, Zhang Y, Moskophidis D, Mivechi NF. 2004. Unique contribution of heat shock transcription factor 4 in ocular lens development and fiber cell differentiation. Genesis 40:205-217.
36. Nielsen PA, Baruch A, Shestopalov VI, Giepmans BN, Dunia I, Benedetti EL, Kumar NM. 2003. Lens connexins alpha3Cx46 and alpha8Cx50 interact with zonula occludens protein-1 (ZO-1). Mol Biol Cell 14:2470-2481.
37. Plageman TF Jr, Chung MI, Lou M, Smith AN, Hildebrand JD, Wallingford JB, Lang RA. 2010. Pax6-dependent Shroom3 expression regulates apical constriction during lens placode invagination. Development 137:405-415.
38. Pontoriero GF, Deschamps P, Ashery-Padan R, Wong R, Yang Y, Zavadil J, Cvekl A, Sullivan S, Williams T, West-Mays JA. 2008. Cell autonomous roles for AP-2alpha in lens vesicle separation and maintenance of the lens epithelial cell phenotype. Dev Dyn 237:602-617.
39. Pontoriero GF, Smith AN, Miller LA, Radice GL, West-Mays JA, Lang RA. 2009. Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev Biol 326:403-417.
40. Rivera C, Yamben IF, Shatadal S, Waldof M, Robinson ML, Griep AE. 2009. Cell-autonomous requirements for Dlg-1 for lens epithelial cell structure and fiber cell morphogenesis. Dev Dyn 238:2292-2308.
41. Rungger-Brandle E, Conti A, Leuenberger PM, Rungger D. 2005. Expression of alphasmooth muscle actin in lens epithelia from human donors and cataract patients. Exp Eye Res 81:539-550.
42. Schmitt-Graff A, Pau H, Spahr R, Piper HM, Skalli O, Gabbiani G. 1990. Appearance of alpha-smooth muscle actin in human eye lens cells of anterior capsular cataract and in cultured bovine lens-forming cells. Differentiation 43:115-122.
43. Shaham O, Smith AN, Robinson ML, Taketo MM, Lang RA, Ashery-Padan R. 2009. Pax6 is essential for lens fiber cell differentiation. Development 136:2567-2578.
44. Shin K, Fogg VC, Margolis B. 2006. Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22:207-235.
45. Sinha D, Wyatt MK, Sarra R, Jaworski C, Slingsby C, Thaung C, Pannell L, Robison WG, Favor J, Lyon M, Wistow G. 2001. A temperature-sensitive mutation of Crygs in the murine Opj cataract. J Biol Chem 276:9308-9315.
46. Sivak JM, West-Mays JA, Yee A, Williams T, Fini ME. 2004. Transcription factors Pax6 and AP-2alpha interact to coordinate corneal epithelial repair by controlling expression of matrix metalloproteinase gelatinase B. Mol Cell Biol 24:245-257.
47. Smith AN, Miller LA, Radice G, Ashery-Padan R, Lang RA. 2009. Stage-dependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis. Development 136:2977-2985.
48. Song CW, Okumoto M, Mori N, Yamate J, Sakuma S, Kim JS, Han SS, Hilgers J, Esaki K. 1997. A new hereditary cataract mouse with lens rupture. Lab Anim 31:248-253.
49. Srinivasan Y, Lovicu FJ, Overbeek PA. 1998. Lens-specific expression of transforming growth factor beta1 in transgenic mice causes anterior subcapsular cataracts. J Clin Invest 101:625-634.
50. van Raamsdonk CD, Tilghman SM. 2000. Dosage requirement and allelic expression of PAX6 during lens placode formation. Development 127:5439-5448.
51. Wang X, Garcia CM, Shui YB, Beebe DC. 2004. Expression and regulation of alpha-, beta-, and gamma-crystallins in mammalian lens epithelial cells. Invest Ophthalmol Vis Sci 45:3608-3619.
52. West-Mays JA, Coyle BM, Piatigorsky J, Papagiotas S, Libby D. 2002. Ectopic expression of AP-2alpha transcription factor in the lens disrupts fiber cell differentiation. Dev Biol 245:13-27.
53. West-Mays JA, Sivak JM, Papagiotas SS, Kim J, Nottoli T, Williams T, Fini ME. 2003. Positive influence of AP-2alpha transcription factor on cadherin gene expression and differentiation of the ocular surface. Differentiation 71:206-216.
54. West-Mays JA, Zhang J, Nottoli T, Hagopian-Donaldson S, Libby D, Strissel KJ, Williams T. 1999. AP-2alpha transcription factor is required for early morphogenesis of the lens vesicle. Dev Biol 206:46-62.
55. Wride MA. 2011. Lens fibre cell differentiation and organelle loss: many paths lead to clarity. Philos Trans R Soc Lond 366:1219-1233.
56. Xu L, Overbeek PA, Reneker LW. 2002. Systematic analysis of E-, N- and P-cadherin expression in mouse eye development. Exp Eye Res 74:753-760.
57. Zhang J, Hagopian-Donaldson S, Serbedzija G, Elsemore J, Plehn-Dujowich D, McMahon AP, Flavell RA, Williams T. 1996. Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 381:238-241.
58. Zhao H, Yang Y, Rizo CM, Overbeek PA, Robinson ML. 2004. Insertion of a Pax6 consensus binding site into the alphaA-crystallin promoter acts as a lens epithelial cell enhancer in transgenic mice. Invest Ophthalmol Vis Sci 45:1930-1939.