Interactions between lens epithelial and fiber cells reveal an intrinsic self-assembly mechanism

Developmental Biology

Volumn 385, Issue 2, 2014, Pages 291-303

  Dawes, L J ^a   Sugiyama, Y ^a   Lovicu, F J ^b   Harris, C G ^a   Shelley, E J ^a   McAvoy, J W ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Development and regeneration; FGF; Jagged; Lens epithelial cells; Lens fiber cells; Notch; Planar cell polarity; Wnt

Indexed keywords

JAGGED1; NOTCH RECEPTOR; WNT5A PROTEIN;

ANIMAL TISSUE; ARTICLE; AUTOREGULATION; CELL ASSEMBLY; CELL COMPOSITION; CELL DIFFERENTIATION; CELL GROWTH; CELL INTERACTION; CELL MIGRATION; CELL POLARIZATION; CELL PROLIFERATION; CELLULAR PARAMETERS; CONTROLLED STUDY; EXPLANT; LENS EPITHELIUM; LENS FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; SIGNAL TRANSDUCTION;

DEVELOPMENT AND REGENERATION; FGF; JAGGED; LENS EPITHELIAL CELLS; LENS FIBER CELLS; NOTCH; PLANAR CELL POLARITY; WNT;

ANIMALS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FIBROBLAST GROWTH FACTORS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LENS, CRYSTALLINE; MEMBRANE PROTEINS; RATS; RATS, WISTAR; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84891634650     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.10.030     Document Type: Article

References (41)

1. Abello G., Khatri S., Giraldez F., Alsina B. Early regionalization of the optic placode and its regulation by the Notch signaling pathway. Mech. Dev. 2007, 124:631-634.
2. Ang S.J., Stump R.J., Lovicu F.J., McAvoy J.W. Spatial and temporal expression of Wnt and Dickkopf genes during murine lens development. Gene Expr. Patterns 2004, 4:289-295.
3. Ann E.J., Kim H.Y., Seo M.S., Mo J.S., Kim M.Y., Yoon J.H., Park H.S. Wnt5a controls Notch1 signaling through CaMKII mediated degradation of the SMRT corepressor protein. J. Biol. Chem. 2012, 287:36814-36829.
4. Blakely B.D., Bye C.R., Fernando C.V., Horne M.K., Macheda M.L., Stacker S.A., Arenas E., Parish C.L. Wnt5a regulates midbrain dopaminergic axon growth and guidance. PLoS One 2011, 6:e18373.
5. Chen B., Dodge M.E., Tang W., Lu J., Ma Z., Fan C.W., Wei S., Hao W., Kilgore J., Williams N.S., et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 2009, 5:100-107.
6. Chen Y., Stump R.J., Lovicu F.J., Shimono A., McAvoy J.W. Wnt signaling is required for organization of the lens fiber cell cytoskeleton and development of lens three-dimensional architecture. Dev. Biol. 2008, 324:161-176.
7. Cooper M.T.D., Bray S.J. Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 1999, 397:526-530.
8. Da Forno P.D., Pringle H., Hutchinson P., Osborn J., Huang Q., Potter L., Hancox R.A., Feltcher A., Saldanha G.S. WNT5A expression increases during melanoma progression and correlates with outcome. Clin. Cancer Res. 2008, 14:5825-5832.
9. Dawes L.J., Sugiyama Y., Tanedo A.S., Lovicu F.J., McAvoy J.W. Wnt-frizzled signaling is part of an FGF-induced cascade that promotes lens fiber differentiation. Invest. Ophthalmol. Vis. Sci. 2013, 54:1582-1590.
10. Duncan A.W., Rattis F.M., DiMascio L.N., Congdon K.L., Pazianos G., Zhao C., Yoon K., Cook J.M., Willert K., Gaiano N., Reya T. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 2005, 6:314-322.
11. Eiraku M., Takata N., Ishibashi H., Kawada M., Sakakura E., Okuda S., Sekiguchi K., Adachi T., Sasai Y. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 2011, 472:51-56.
12. Garcia C.M., Yu K., Zhao H., Ashery-Padan R., Ornitz D.M., Robinson M.L., Beebe D.C. Signaling through FGF receptor-2 is required for lens cell survival and for withdrawal from the cell cycle during lens fiber cell differentiation. Dev. Dyn. 2005, 233:516-527.
13. Hayward P., Kalmar T., Arias A.M. Wnt/Notch signalling and information processing during development. Development 2008, 135:411-424.
14. Hing H.K., Sun X., Artavanis-Tsakonas S. Modulation of wingless signaling by Notch in Drosophila. Mech. Dev. 1994, 47:261-268.
15. Ikeya T., Hayashi S. Interplay of Notch and FGF signaling restricts cell fate and MAPK activation in the Drosophila trachea. Development 1999, 126:4455-4463.
16. Jia J., Lin M., Zhang L., York J.P., Zhang P. The Notch signaling pathway controls the size of the ocular lens by directly suppressing p57Kip2 expression. Mol. Cell Biol. 2007, 27:7236-7247.
17. Katoh M., Katoh M. Transcriptional mechanisms of WNT5A based on NF-kappaB, Hedgehog, TGFbeta, and Notch signaling cascades. Int. J. Mol. Med. 2009, 23:763-769.
18. Koyanagi M., Bushoven P., Iwasaki M., Urbich C., Zeiher A.M., Dimmeler S. Notch signaling contributes to the expression of cardiac markers in human circulating progenitor cells. Circ. Res. 2007, 101:1139-1145.
19. Le T.T., Conley K.W., Brown N.L. Jagged 1 is necessary for normal mouse lens formation. Dev. Biol. 2009, 328:118-126.
20. Lovicu F.J., McAvoy J.W. Growth factor regulation of lens development. Dev. Biol. 2005, 280:1-14.
21. Lovicu F.J., McAvoy J.W. Epithelial Explants and their Application to Study Developmental Processes in the Lens. Animal Models in Eye Research 2008, 134-136. Academic Press, Burlington. P.A. Tsonis (Ed.).
22. Lyu J., Joo C.K. Wnt signaling enhances FGF2-triggered lens fiber cell differentiation. Development 2004, 131:1813-1824.
23. Maddala R., Skiba N.P., Lalane R., Sherman D.L., Brophy P.J., Rao P.V. Periaxin is required for hexagonal geometry and membrane organization of mature lens fibers. Dev. Biol. 2011, 357:179-190.
24. McAvoy J.W. Cell division, cell elongation and distribution of α-, β- and γ-crystallins in the rat lens. J. Embryol. Exp. Morphol. 1978, 44:149-165.
25. McAvoy J.W. Cell division, cell elongation and the co-ordination of crystallin gene expression during lens morphogenesis in the rat. J. Embryol. Exp. Morphol. 1978, 45:271-281.
26. Micchelli C.A., Esler W.P., Kimberly W.T., Jack C., Berezovska O., Kornilova A., Hyman B.T., Perrimon N., Wolfe M.S. Gamma-secretase/presenilin inhibitors for Alzheimer's disease phenocopy Notch mutations in Drosophila. FASEB J. 2003, 17:79-81.
27. Nielsen P.A., Baruch A., Shestopalov V.I., Giepmans B.N., Dunia I., Benedetti E.L., Kumar N.M. Lens connexins alpha3C×46 and alpha8C×50 interact with zonula occludens protein-1 (ZO-1). Mol. Biol. Cell 2003, 14:2470-2481.
28. O'Connor M.D., McAvoy J.W. In vitro generation of functional lens-like structures with relevance to age-related nuclear cataract. Invest. Ophthalmol. Vis. Sci. 2007, 48:1245-1252.
29. Peters S., Mix E., Bauer P., Weinelt S., Schubert B., Knoblich R., Bottcher T., Strauss U., Pahnke J., Cattaneo.E., et al. Wnt-5a expression in the rat neuronal progenitor cell line ST14A. Exp. Brain Res. 2004, 158:189-195.
30. Qu X., Hertzler K., Pan Y., Grobe K., Robinson M.L., Zhang X. Genetic epistasis between heparan sulfate and FGF-Ras signaling controls lens development. Dev. Biol. 2011, 355:12-20.
31. Rajagopal R., Dattilo L.K., Kaartinen V., Deng C.X., Umans L., Zwijsen A., Roberts A.B., Bottinger E.P., Beebe D.C. Functions of the type 1 BMP receptor Acvr1 (Alk2) in lens development: cell proliferation, terminal differentiation, and survival. Invest. Ophthalmol. Vis. Sci. 2008, 49:4953-4960.
32. Robinson M.L. An essential role for FGF receptor signaling in lens development. Semin Cell Dev. Biol. 2006, 17:726-740.
33. Rowan S., Conley K.W., Le T.T., Donner A.L., Maas R.L., Brown N.L. Notch signaling regulates growth and differentiation in the mammalian lens. Dev. Biol. 2008, 321:111-122.
34. Saravanamuthu S.S., Gao C.Y., Zelenka P.S. Notch signaling is required for lateral induction of Jagged1 during FGF-induced lens fiber differentiation. Dev. Biol. 2009, 332:166-176.
35. Saravanamuthu S.S., Le T.T., Gao C.Y., Cojocaru R.I., Pandiyan P., Liu C., Zhang J., Zelenka P.S., Brown N.L. Conditional ablation of the Notch2 receptor in the ocular lens. Dev. Biol. 2012, 362:219-229.
36. Small D., Kovalenko D., Soldi R., Mandinova A., Kolev V., Trifonova R., Bagala C., Kacer D., Battelli C., Liaw L., Prudovsky I., Maciag T. Notch activation suppresses fibroblast growth factor-dependent cellular transformation. J. Biol. Chem. 2003, 278:16405-16413.
37. Snyder E.Y., Deitcher D.L., Walsh C., Arnold-Aldea S., Hartwieg E.A., Cepko C.L. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 1992, 68:33-51.
38. Stump R.J., Ang S., Chen Y., von Bahr T., Lovicu F.J., Pinson K., de Iongh R.U., Yamaguchi T.P., Sassoon D.A., McAvoy J.W. A role for Wnt/beta-catenin signaling in lens epithelial differentiation. Dev. Biol. 2003, 259:48-61.
39. Sugiyama Y., Stump R.J., Nguyen A., Wen L., Chen Y., Wang Y., Murdoch J.N., Lovicu F.J., McAvoy J.W. Secreted frizzled-related protein disrupts PCP in eye lens fiber cells that have polarised primary cilia. Dev. Biol. 2010, 338:193-201.
40. Sugiyama Y., Lovicu F.J., McAvoy J.W. Planar cell polarity in the mammalian eye lens. Organogenesis 2011, 7:191-201.
41. Zhao H., Yang.T., Madakashira B.P., Thiels C.A., Bechtle C.A., Garcia C.M., Zhang H., Yu K., Ornitz D.M., Beebe D.C., Robinson M.L. Fibroblast growth factor receptor signaling is essential for lens fiber cell differentiation. Dev. Biol. 2008, 318:276-288.