The molecular basis of defective lens development in the Iberian mole

BMC Biology

Volumn 6, Issue , 2008, Pages

  David, F David ^a   Jiménez, Rafael ^b   Martin, J Martin ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CRYSTALLIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR C MAF; TRANSCRIPTION FACTOR FOXE3; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PROX1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; EYE DEVELOPMENT; FEMALE; FETUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE LOCATION; GENE REGULATORY NETWORK; LENS FIBER; MOLE (INSECTIVORA); MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PERINATAL PERIOD; SPECIES COMPARISON; VERTEBRATE;

ANIMALIA; MAMMALIA; TALPA OCCIDENTALIS; VERTEBRATA;

EID: 57049145331     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-6-44     Document Type: Article

References (64)

1. Nevo E Adaptive convergence and divergence of subterranean mammals Annu Rev Ecol Syst 1979, 10:269-308. 10.1146/annurev.es.10.110179.001413
2. Strickler AG Yamamoto Y Jeffery WR Early and late changes in Pax6 expression accompany eye degeneration during cavefish development Dev Genes Evol 2001, 211:138-144. 10.1007/s004270000123 11455425
3. Yamamoto Y Stock DW Jeffery WR Hedgehog signalling controls eye degeneration in blind cavefish Nature 2004, 431:844-847. 10.1038/ nature02864 15483612
4. Sweet G Contributions to our knowledge of the anatomy of Notoryctes typhlops, Stirling. Part III, the eye Quart J Microscop Sci 1906, 50:547-571.
5. Gubbay V A comparison of the development of the rudimentary eye of Eremitalpa granti (Broom) with that of the normal eye of Elephantulus myurus jamesoni (Chubb) S Afr J Sci 1956, 52:182-186.
6. Sanyal S Jansen HG de Grip WJ Nevo E de Jong WW The eye of the blind mole rat, Spalax ehrenbergi. Rudiment with hidden function? Invest Ophthalmol Vis Sci 1990, 31:1398-1404. 2142147
7. Quax-Jeuken Y Bruisten S Bloemendal H de Jong WW Nevo E Evolution of crystallins: Expression of lens-specific proteins in the blind mammals mole (Talpa europaea) and mole rat (Spalax ehrenbergi) Mol Biol Evol 1985, 2:279-288. 3870862
8. Nikitina NV Maughan-Brown B O'Riain MJ Kidson SH Postnatal development of the eye in the naked mole rat (Heterocephalus glaber) Anat Rec A Discov Mol Cell Evol Biol 2004, 277:317-337. 10.1002/ar.a.20025 15052660
9. Quilliam AT The problem of vision in the ecology of Talpa europaea Exp Eye Res 1966, 5:63-78. 10.1016/S0014-4835(66)80022-2 5929584
10. Lund RD Lund JS The visual system of the mole. Talpa europaea Exp Neurol 1965, 13:302-316. 10.1016/0014-4886(65)90118-4 5851390
11. Němec P Cveková P Benada O Wielkopolska E Olkowicz S Turlejski K Burda H Bennett NC Peichl L The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): Retina, subcortical visual nuclei and primary visual cortex Brain Res Bull 2008, 75:356-364. 10.1016/j.brainresbull.2007.10.055 18331898
12. Ashery-Padan R Marquardt T Zhou X Gruss P Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye Genes Dev 2000, 14:2701-2711. 317031 11069887 10.1101/gad.184000
13. Coulombre AJ Coulombre JL Lens development. I. Role of the lens in eye growth J Exp Zool 1964, 156:39-47. 10.1002/jez.1401560104 14189921
14. Griep AE Cell cycle regulation in the developing lens Semin Cell Dev Biol 2006, 17:686-697. 10.1016/j.semcdb.2006.10.004 17218126 2570782
15. Lovicu FJ McAvoy JW Growth factor regulation of lens development Dev Biol 2005, 280:1-14. 10.1016/j.ydbio.2005.01.020 15766743
16. Cvekl A Duncan MK Genetic and epigenetic mechanisms of gene regulation during lens development Prog Retin Eye Res 2007, 26:555-597. 2136409 17905638 10.1016/j.preteyeres.2007.07.002
17. McAvoy JW Induction of the eye lens Differentiation 1980, 17:137-149. 10.1111/j.1432-0436.1980.tb01091.x 7004973
18. Zelenka PS Gao C-Y Rampalli A Arora J Chauthaiwale V He H-Y Cell cycle regulation in the lens: Proliferation, quiescence, apoptosis and differentiation Prog Retin Eye Res 1997, 16:303-322. 10.1016/ S1350-9462(96)00024-9
19. Bozanić D Tafra R Saraga-Babić M Role of apoptosis and mitosis during human eye development Eur J Cell Biol 2003, 82:421-429. 10.1078/0171-9335-00328 14533740
20. Yan Q Liu JP Li DW Apoptosis in lens development and pathology Differentiation 2006, 74:195-211. 10.1111/j.1432-0436.2006.00068.x 16759286
21. Ishizaki Y Jacobson MD Raff MC A role for caspases in lens fiber differentiation J Cell Biol 1998, 140:153-158. 2132591 9425163 10.1083/ jcb.140.1.153
22. Hill RE Favor J Hogan BL Ton CC Saunders GF Hanson IM Prosser J Jordan T Hastie ND van Heyningen V Mouse small eye results from mutations in a paired-like homeobox-containing gene Nature 1991, 354:522-525. 10.1038/ 354522a0 1684639
23. Chow RL Altmann CR Lang RA Hemmati-Brivanlou A Pax6 induces ectopic eyes in a vertebrate Development 1999, 126:4213-4222. 10477290
24. Kozmik Z Pax genes in eye development and evolution Curr Opin Genet Dev 2005, 15:430-438. 10.1016/j.gde.2005.05.001 15950457
25. Walther C Gruss P Pax-6, a murine paired box gene, is expressed in the developing CNS Development 1991, 113:1435-1449. 1687460
26. Grindley JC Davidson DR Hill RE The role of Pax-6 in eye and nasal development Development 1995, 121:1433-1442. 7789273
27. Duncan MK Haynes JI 2nd Cvekl A Piatigorsky J Dual roles for Pax-6: A transcriptional repressor of lens fiber cell-specific beta-crystallin genes Mol Cell Biol 1998, 18:5579-5586. 109142 9710641
28. Duncan MK Xie L David LL Robinson ML Taube JR Cui W Reneker LW Ectopic Pax6 expression disturbs lens fiber cell differentiation Invest Ophthalmol Vis Sci 2004, 45:3589-3598. 10.1167/iovs.04-0151 15452066
29. Cvekl A Piatigorsky J Lens development and crystallin gene expression: many roles for Pax-6 Bioessays 1996, 18:621-630. 10.1002/bies.950180805 8760335
30. Cvekl A Yang Y Chauhan BK Cveklova K Regulation of gene expression by Pax6 in ocular cells: A case of tissue-preferred expression of crystallins in lens Int J Dev Biol 2004, 48:829-844. 2080872 15558475 10.1387/ijdb.041866ac
31. Richardson J Cvekl A Wistow G Pax-6 is essential for lens-specific expression of zeta-crystallin Proc Natl Acad Sci USA 1995, 92:4676-4680. 42007 7753863 10.1073/pnas.92.10.4676
32. Cvekl A Kashanchi F Sax CM Brady JN Piatigorsky J Transcriptional regulation of the mouse alpha A-crystallin gene: Activation dependent on a cyclic AMP-responsive element (DE1/CRE) and a Pax-6-binding site Mol Cell Biol 1995, 15:653-660. 231924 7823934
33. Cvekl A Sax CM Li X McDermott JB Piatigorsky J Pax-6 and lens-specific transcription of the chicken delta 1-crystallin gene Proc Natl Acad Sci USA 1995, 92:4681-4685. 42008 7753864 10.1073/pnas.92.10.4681
34. Gopal-Srivastava R Cvekl A Piatigorsky J Pax-6 and alphaB-crystallin/ small heat shock protein gene regulation in the murine lens: Interaction with the lens-specific regions, LSR1 and LSR2 J Biol Chem 1996, 271:23029-23036. 10.1074/jbc.271.38.23029 8798491
35. Sharon-Friling R Richardson J Sperbeck S Lee D Rauchman M Maas R Swaroop A Wistow G Lens-specific gene recruitment of zeta-crystallin through Pax6, Nrl-Maf, and brain suppressor sites Mol Cell Biol 1998, 18:2067-2076. 121437 9528779
36. Cui W Tomarev SI Piatigorsky J Chepelinsky AB Duncan MK Mafs, Prox1, and Pax6 can regulate chicken betaB1-crystallin gene expression J Biol Chem 2004, 279:11088-11095. 10.1074/jbc.M312414200 14707122
37. Blixt A Mahlapuu M Aitola M Pelto-Huikko M Enerbäck S Carlsson P A forkhead gene, FoxE3, is essential for lens epithelial proliferation and closure of the lens vesicle Genes Dev 2000, 14:245-254. 316354 10652278
38. Blixt A Landgren H Johansson BR Carlsson P Foxe3 is required for morphogenesis and differentiation of the anterior segment of the eye and is sensitive to Pax6 gene dosage Dev Biol 2007, 302:218-229. 10.1016/ j.ydbio.2006.09.021 17064680
39. Kaufman MH The Atlas of Mouse Development London: Academic Press 1992.
40. Duncan MK Cui W Oh DJ Tomarev SI Prox1 is differentially localized during lens development Mech Dev 2002, 112:195-198. 10.1016/ S0925-4773(01)00645-1 11850194
41. Kawauchi S Takahashi S Nakajima O Ogino H Morita M Nishizawa M Yasuda K Yamamoto M Regulation of lens fiber cell differentiation by transcription factor c-Maf J Biol Chem 1999, 274:19254-19260. 10.1074/ jbc.274.27.19254 10383433
42. Ring BZ Cordes SP Overbeek PA Barsh GS Regulation of mouse lens fiber cell development and differentiation by the Maf gene Development 2000, 127:307-317. 10603348
43. Thut CJ Rountree RB Hwa M Kingsley DM A large-scale in situ screen provides molecular evidence for the induction of eye anterior segment structures by the developing lens Dev Biol 2001, 231:63-76. 10.1006/ dbio.2000.0140 11180952
44. Ittner LM Wurdak H Schwerdtfeger K Kunz T Ille F Leveen P Hjalt TA Suter U Karlsson S Hafezi F Born W Sommern L Compound developmental eye disorders following inactivation of TGFβ signaling in neural-crest stem cells J Biol 2005, 4:11. 1414066 16403239 10.1186/jbiol29
45. Gorman ML Stone RD The Natural History of Moles Ithaca: Cornell University Press 1990.
46. Carmona FD Motokawa M Tokita M Tsuchiya K Jiménez R Sánchez-Villagra MR The evolution of female mole ovotestes evidences high plasticity of mammalian gonad development J Exp Zoolog B Mol Dev Evol 2008, 310:259-266. 10.1002/jez.b.21209 18085526
47. Cvekl A Tamm ER Anterior eye development and ocular mesenchyme: New insights from mouse models and human diseases Bioessays 2004, 26:374-386. 2094210 15057935 10.1002/bies.20009
48. Vrensen GF Graw J De Wolf A Nuclear breakdown during terminal differentiation of primary lens fibres in mice: A transmission electron microscopic study Exp Eye Res 1991 52 647 659 10.1016/ 0014-4835(91)90017-9 1855541
49. Ashery-Padan R Gruss P Pax6 lights-up the way for eye development Curr Opin Cell Biol 2001, 13:706-714. 10.1016/S0955-0674(00)00274-X 11698186
50. Duncan MK Kozmik Z Cveklova K Piatigorsky J Cvekl A Overexpression of PAX6(5a) in lens fiber cells results in cataract and upregulation of (alpha)5(beta)1 integrin expression J Cell Sci 2000, 113:3173-3785. 10954416
51. Dorà N Ou J Kucerova R Parisi I West JD Collinson JM PAX6 dosage effects on corneal development, growth, and wound healing Dev Dyn 2008, 237:1295-1306. 10.1002/dvdy.21528 18386822
52. Schedl A Ross A Lee M Engelkamp D Rashbass P van Heyningen V Hastie ND Influence of PAX6 gene dosage on development: Overexpression causes severe eye abnormalities Cell 1996, 86:71-82. 10.1016/ S0092-8674(00)80078-1 8689689
53. Sanyal S Hawkins RK Dysgenetic lens (dyl) - a new gene in the mouse Invest Ophthalmol Vis Sci 1979, 18:642-645. 109409
54. Medina-Martinez O Brownell I Amaya-Manzanares F Hu Q Behringer RR Jamrich M Severe defects in proliferation and differentiation of lens cells in Foxe3 null mice Mol Cell Biol 2005, 25:8854-8863. 1265778 16199865 10.1128/MCB.25.20.8854-8863.2005
55. Landgren H Blixt A Carlsson P Persistent FoxE3 expression blocks cytoskeletal remodeling and organelle degradation during lens fiber differentiation Invest Ophthalmol Vis Sci 2008, 49:4269-4277. 10.1167/ iovs.08-2243 18539941
56. Duncan MK Li X Ogino H Yasuda K Piatigorsky J Developmental regulation of the chicken beta B1-crystallin promoter in transgenic mice Mech Dev 1996, 57:79-89. 10.1016/0925-4773(96)00533-3 8817455
57. van Leen RW Breuer ML Lubsen NH Schoenmakers JG Developmental expression of crystallin genes: In situ hybridization reveals a differential localization of specific mRNAs Dev Biol 1987, 123:338-345. 10.1016/ 0012-1606(87)90392-7 3653512
58. van Leen RW van Roozendaal KE Lubsen NH Schoenmakers JG Differential expression of crystallin genes during development of the rat eye lens Dev Biol 1987, 120:457-464. 10.1016/0012-1606(87)90249-1 3030857
59. Chen Q Dowhan DH Liang D Moore DD Overbeek PA CREB-binding protein/p300 co-activation of crystallin gene expression J Biol Chem 2002, 277:24081-24089. 10.1074/jbc.M201821200 11943779
60. Wigle JT Chowdhury K Gruss P Oliver G Prox1 function is crucial for mouse lens-fibre elongation Nat Genet 1999, 21:318-322. 10.1038/6844 10080188
61. Barrionuevo FJ Zurita F Burgos M Jiménez R Testis-like development of gonads in female moles. New insights on mammalian gonad organogenesis Dev Biol 2004, 268:39-52. 10.1016/j.ydbio.2003.11.025 15031103
62. Barrionuevo FJ Zurita F Burgos M Jimenez R Developmental stages and growth rate of the mole Talpa occidentalis (Insectivora, Mammalia) J Mammal 2004, 85:120-125. 10.1644/BPR-010
63. Carmona FD Lupiáñez D Martín E Burgos M Jiménez R Zurita F The spatio-temporal pattern of testis organogenesis in mammals. Insights from the mole Int J Dev Biol 12533024
64. Míšek I Developmental anatomy of mole Talpa europaea (Insectivora, Talpidae). VIII. Ontogeny of visual organ Folia Zool 1988, 37:333-342.