Home LiteratureArticle Details
PMID: 16199865 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Severe defects in proliferation and differentiation of lens cells in Foxe3 null mice.

Molecular and cellular biology ·Vol. 25 ·No. 20 ·2005-10-00 ·Pages 8854-63

Medina-Martinez O, Brownell I, Amaya-Manzanares F, Hu Q, Behringer RR, Jamrich M

Abstract

During mouse eye development, the correct formation of the lens occurs as a result of reciprocal interactions between the neuroectoderm that forms the retina and surface ectoderm that forms the lens. Although many transcription factors required for early lens development have been identified, the mechanism and genetic interactions mediated by them remain poorly understood. Foxe3 encodes a winged helix-forkhead transcription factor that is initially expressed in the developing brain and in the lens placode and later restricted exclusively to the anterior lens epithelium. Here, we show that targeted disruption of Foxe3 results in abnormal development of the eye. Cells of the anterior lens epithelium show a decreased rate of proliferation, resulting in a smaller than normal lens. The anterior lens epithelium does not properly separate from the cornea and frequently forms an unusual, multilayered tissue. Because of the abnormal differentiation, lens fiber cells do not form properly, and the morphogenesis of the lens is greatly affected. The abnormally differentiated lens cells remain irregular in shape, and the lens becomes vacuolated. The defects in lens development correlate with changes in the expression of growth and differentiation factor genes, including DNase II-like acid DNase, Prox1, p57, and PDGFalpha receptor. As a result of abnormal lens development, the cornea and the retina are also affected. While Foxe3 is also expressed in a distinct region of the embryonic brain, we have not observed abnormal development of the brain in Foxe3(-/-) animals.

MeSH Terms
Animals Base Sequence Brain/embryology,metabolism Cell Differentiation Cell Proliferation Cell Shape DNA/genetics Eye Abnormalities/genetics,metabolism,pathology Female Forkhead Transcription Factors/deficiency,genetics,metabolism Gene Expression Regulation, Developmental Gene Targeting Lens Capsule, Crystalline/abnormalities,embryology,metabolism,pathology Lens, Crystalline/abnormalities,embryology,metabolism,pathology Mice Mice, Knockout Pregnancy
Chemicals
Forkhead Transcription Factors Foxe3 protein, mouse DNA
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Medina-Martinez Olga
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA.
Brownell Isaac
Amaya-Manzanares Felipe
Hu Qiyong
Behringer Richard R
Jamrich Milan
References (50)
50 references, click to expand
  1. Forkhead transcription factors: key players in development and metabolism.
    Dev Biol. 2002 Oct 1;250(1):1-23 PMID: 12297093
  2. Anterior eye development and ocular mesenchyme: new insights from mouse models and human diseases.
    Bioessays. 2004 Apr;26(4):374-86 PMID: 15057935
  3. A forkhead-domain gene is mutated in a severe speech and language disorder.
    Nature. 2001 Oct 4;413(6855):519-23 PMID: 11586359
  4. Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent cell layers of the mouse embryo.
    Development. 1992 Aug;115(4):1045-58 PMID: 1451656
  5. XBF-1, a winged helix transcription factor with dual activity, has a role in positioning neurogenesis in Xenopus competent ectoderm.
    Development. 1998 Dec;125(24):4889-900 PMID: 9811573
  6. The forkhead transcription factor gene FKHL7 is responsible for glaucoma phenotypes which map to 6p25.
    Nat Genet. 1998 Jun;19(2):140-7 PMID: 9620769
  7. Peter's anomaly.
    Ophthalmologica. 1975;171(4-5):318-20 PMID: 1165907
  8. Regulation of proliferation, cell fate specification and differentiation by the homeodomain proteins Prox1, Six3, and Chx10 in the developing retina.
    Cell Cycle. 2003 Jul-Aug;2(4):350-7 PMID: 12851489
  9. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome.
    Nat Genet. 2001 Feb;27(2):159-66 PMID: 11175783
  10. Forkhead Foxe3 maps to the dysgenetic lens locus and is critical in lens development and differentiation.
    Genesis. 2000 Jun;27(2):81-93 PMID: 10890982
  11. A comparative analysis of alphaA- and alphaB-crystallin expression during the cell cycle in primary mouse lens epithelial cultures.
    Exp Eye Res. 2004 Dec;79(6):795-805 PMID: 15642316
  12. Function and regulation of FoxF1 during Xenopus gut development.
    Development. 2004 Aug;131(15):3637-47 PMID: 15229177
  13. Differential expression of fork head genes during early Xenopus and zebrafish development.
    Dev Genet. 1995;17(2):107-16 PMID: 7586752
  14. Regulation of vertebrate eye development by Rx genes.
    Int J Dev Biol. 2004;48(8-9):761-70 PMID: 15558469
  15. Forkhead genes and human disease.
    J Appl Genet. 2001;42(2):211-21 PMID: 14564054
  16. Unified nomenclature for the winged helix/forkhead transcription factors.
    Genes Dev. 2000 Jan 15;14(2):142-6 PMID: 10702024
  17. The forkhead/winged-helix gene, Mf1, is necessary for the normal development of the cornea and formation of the anterior chamber in the mouse eye.
    Dev Biol. 1999 Jul 15;211(2):306-22 PMID: 10395790
  18. Expression of winged helix genes, BF-1 and BF-2, define adjacent domains within the developing forebrain and retina.
    J Neurobiol. 1994 Oct;25(10):1293-309 PMID: 7815060
  19. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres.
    Neuron. 1995 Jun;14(6):1141-52 PMID: 7605629
  20. Prox1 function is crucial for mouse lens-fibre elongation.
    Nat Genet. 1999 Mar;21(3):318-22 PMID: 10080188
  21. Map position of dysgenetic lens (dyl) locus on chromosome 4 in the mouse.
    Genet Res. 1986 Dec;48(3):199-200 PMID: 3569904
  22. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation.
    Cell. 2004 May 14;117(4):421-6 PMID: 15137936
  23. Foxe3 haploinsufficiency in mice: a model for Peters' anomaly.
    Invest Ophthalmol Vis Sci. 2002 May;43(5):1350-7 PMID: 11980846
  24. Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors.
    Neuron. 2004 Sep 16;43(6):795-807 PMID: 15363391
  25. A novel fork head gene mediates early steps during Xenopus lens formation.
    Development. 1999 Nov;126(22):5107-16 PMID: 10529427
  26. The upstream ectoderm enhancer in Pax6 has an important role in lens induction.
    Development. 2001 Nov;128(22):4415-24 PMID: 11714668
  27. Early eye development in vertebrates.
    Annu Rev Cell Dev Biol. 2001;17:255-96 PMID: 11687490
  28. The product of the mouse nude locus, Whn, regulates the balance between epithelial cell growth and differentiation.
    Genes Dev. 1996 Sep 1;10(17):2212-21 PMID: 8804315
  29. Fox (forkhead) genes are involved in the dorso-ventral patterning of the Xenopus mesoderm.
    Int J Dev Biol. 2001;45(1):265-71 PMID: 11291856
  30. Expression of FoxE4 and Rx visualizes the timing and dynamics of critical processes taking place during initial stages of vertebrate eye development.
    Dev Neurosci. 2004;26(5-6):294-307 PMID: 15855758
  31. Ectopic expression of the nude gene induces hyperproliferation and defects in differentiation: implications for the self-renewal of cutaneous epithelia.
    Dev Biol. 1999 Aug 1;212(1):54-67 PMID: 10419685
  32. HNF-3A, a hepatocyte-enriched transcription factor of novel structure is regulated transcriptionally.
    Genes Dev. 1990 Aug;4(8):1427-36 PMID: 2227418
  33. Visual projection map specified by topographic expression of transcription factors in the retina.
    Nature. 1996 Aug 15;382(6592):632-5 PMID: 8757134
  34. Uchida rat (rSey): a new mutant rat with craniofacial abnormalities resembling those of the mouse Sey mutant.
    Differentiation. 1994 Jun;57(1):31-8 PMID: 8070620
  35. Transcription factor haploinsufficiency: when half a loaf is not enough.
    J Clin Invest. 2002 Feb;109(4):451-5 PMID: 11854316
  36. 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 Nov 1;14(21):2701-11 PMID: 11069887
  37. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain.
    Cell. 1990 Sep 21;62(6):1073-85 PMID: 2205396
  38. Five years on the wings of fork head.
    Mech Dev. 1996 Jun;57(1):3-20 PMID: 8817449
  39. Fox's in development and disease.
    Trends Genet. 2003 Jun;19(6):339-44 PMID: 12801727
  40. The fork head domain: a novel DNA binding motif of eukaryotic transcription factors?
    Cell. 1990 Nov 2;63(3):455-6 PMID: 2225060
  41. A forkhead gene, FoxE3, is essential for lens epithelial proliferation and closure of the lens vesicle.
    Genes Dev. 2000 Jan 15;14(2):245-54 PMID: 10652278
  42. A PDGF receptor mutation in the mouse (Patch) perturbs the development of a non-neuronal subset of neural crest-derived cells.
    Development. 1992 May;115(1):133-42 PMID: 1638976
  43. Cooperation between the Cdk inhibitors p27(KIP1) and p57(KIP2) in the control of tissue growth and development.
    Genes Dev. 1998 Oct 15;12(20):3162-7 PMID: 9784491
  44. Haploinsufficiency of the transcription factors FOXC1 and FOXC2 results in aberrant ocular development.
    Hum Mol Genet. 2000 Apr 12;9(7):1021-32 PMID: 10767326
  45. Mutations in the human forkhead transcription factor FOXE3 associated with anterior segment ocular dysgenesis and cataracts.
    Hum Mol Genet. 2001 Feb 1;10(3):231-6 PMID: 11159941
  46. Spectrum of FOXL2 gene mutations in blepharophimosis-ptosis-epicanthus inversus (BPES) families demonstrates a genotype--phenotype correlation.
    Hum Mol Genet. 2001 Jul 15;10(15):1591-600 PMID: 11468277
  47. A novel, activin-inducible, blastopore lip-specific gene of Xenopus laevis contains a fork head DNA-binding domain.
    Genes Dev. 1992 Apr;6(4):599-608 PMID: 1559610
  48. Dysgenetic lens (dyl)--a new gene in the mouse.
    Invest Ophthalmol Vis Sci. 1979 Jun;18(6):642-5 PMID: 109409
  49. Nuclear cataract caused by a lack of DNA degradation in the mouse eye lens.
    Nature. 2003 Aug 28;424(6952):1071-4 PMID: 12944971
  50. The retroviral oncogene qin belongs to the transcription factor family that includes the homeotic gene fork head.
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4490-4 PMID: 8099441
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-10-00
Pages
8854-63
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1265778
Subset
IM
Grants
NCI NIH HHS · P30 CA016672 · United States
NEI NIH HHS · R01 EY012163 · United States
NEI NIH HHS · EY12505 · United States
NCI NIH HHS · CA16672 · United States
NEI NIH HHS · EY12163 · United States
NEI NIH HHS · R01 EY012505 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com