Anterior eye development and ocular mesenchyme: New insights from mouse models and human diseases

BioEssays

Volumn 26, Issue 4, 2004, Pages 374-386

  Cvekl, Aleš ^a   Tamm, Ernst R ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIRIDIA; ANTERIOR EYE SEGMENT; AXENFELD RIEGER SYNDROME; CELL INTERACTION; CELL TYPE; CONTROLLED STUDY; EPITHELIUM CELL; EYE DEVELOPMENT; EYE DISEASE; HUMAN; HUMAN CELL; MESENCHYME; MOLECULAR MECHANICS; MORPHOGENESIS; MOUSE; NEURAL CREST; NEUROEPITHELIUM; NONHUMAN; PETERS ANOMALY; PHENOTYPE; REVIEW; SYNDROME DELINEATION;

ANIMALS; ANTERIOR EYE SEGMENT; CELL DIFFERENTIATION; EYE; EYE DISEASES; EYE PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICE; MODELS, BIOLOGICAL; OCULAR PHYSIOLOGY; PAIRED BOX TRANSCRIPTION FACTORS; PHENOTYPE; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SYNDROME; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 1842714360     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20009     Document Type: Review

References (94)

1. Duke-Elder S, Cook C, 1963. Normal and Abnormal Development. Part 1. Embryology. Duke-Elder S, editor. London: Henry Kimpton.
2. Haustein J. 1983. On the ultrastructure of the developing and adult mouse corneal stroma. Anat Embryol (Berl) 168:291-305.
3. Pei YF, Rhodin JAG. 1970. The prenatal development of the mouse eye. Anat Rec 168:105-126.
4. Düblin I. 1970. Comparative embryologic studies of the early development of the cornea and the pupillary membrane in reptiles, birds and mammals. Acta Anat (Basel) 76:381-408.
5. Kidson SH, Kume T, Deng K, Winfrey V, Hogan BL. 1999. 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 211:306-322.
6. Reneker LW, Silversides DW, Xu L, Overbeek PA. 2000. Formation of corneal endothelium is essential for anterior segment development. Development 127:533-542.
7. Flügel-Koch C, Ohlmann A, Platigorsky J, Tamm ER. 2002. Overexpression of TGF-b1 alters early development of cornea and lens in transgenic mice. Dev Dyn 225:111-125.
8. Kolmer W. 1936. Entwicklung des Auges. In: Kolmer W, Lauber H, editors. Handbuch der mikroskopischen Anatomie des Menschen, Haut und Siinesorgane. 2. Teil: Auge. Berlin: Verlag von Julius Springer; p 623-676.
9. Ozanics V, Rayborn M, Sagun D. 1977. Observations on the morphology of the developing primate cornea: epithelium, its innervation and anterior stroma. J Morphol 153:263-297.
10. Hay ED. 1980. Development of the vertebrate cornea. Int Rev Cytol 63:263-322.
11. Wulle KG. 1972. The development of the productive and draining system of the aqueous humor in the human eye. Adv Ophthalmol 26:269-355.
12. Smith RS, Zabaleta A, Savinova OV, John SW. 2001. The mouse anterior chamber angle and trabecular meshwork develop without cell death. BMC Dev Biol 1:3.
13. Reme C, d'Epinay SL. 1981. Periods of development of the normal human chamber angle. Doc Ophthalmol 51:241-268.
14. Johnston MC, Noden DM, Hazelton RD, Coulombre JL, Coulombre AJ. 1979. Origins of avian ocular and periocular tissues. Exp Eye Res 29:27-43.
15. Trainor PA, Tam PP. 1995. Cranial paraxial mesoderm and neural crest cells of the mouse embryo: co-distribution in the craniofacial mesenchyme but distinct segregation in branchial arches. Development 121:2569-2582.
16. Coulombre AJ, Coulombre JL. 1964. Lens development. I. Role of the lens in eye growth. J Exp Zool 156:39-48.
17. Genis-Galvez JM. 1966. Role of the lens in the morphogenesis of the iris and cornea. Nature 210:209-210.
18. Jamieson RV, et al. 2002. Domain disruption and mutation of the bZIP transcription factor, MAF, associated with cataract, ocular anterior segment dysgenesis and coloboma. Hum Mo Genet 11:33-42.
19. Ring BZ, Cordes SP, Overbeek PA, Barsh GS. 2000. Regulation of mouse lens fiber cell development and differentiation by the Maf gene. Development 127:307-317.
20. Semina EV, Brownell I, Mintz-Hittner HA, Murray JC, Jamrich M. 2001. Mutations in the human forkhead transcription factor FOXE3 associated with anterior segment ocular dysgenesis and cataracts. Hum Mol Genet 10:231-236.
21. Ormestad M, Blixt A, Churchill A, Martinsson T, Enerback S, Carlsson P. 2002. Foxe3 haploinsufficiency in mice: a model for Peters' anomaly. Invest Ophthalmol Vis Sci 43:1350-1357.
22. Blixt A, Mahlapuu M, Aitola M, Pelto-Huikko M, Enerback S, Carlsson P. 2000. A forkhead gene, FoxE3, is essential for lens epithelial proliferation and closure of the lens vesicle. Genes Dev 14:245-254.
23. 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.
24. Semina EV, Murray JC, Reiter R, Hrstka RF, Graw J. 2000. Deletion in the promoter region and altered expression of Pitx3 homeobox gene in aphakia mice. Hum Mol Genet 9:1575-1585.
25. Rieger DK, Reichenberger E, McLean W, Sidow A, Olsen BR. 2001. A double-deletion mutation in the Pitx3 gene causes arrested lens development in aphakia mice. Genomics 72:61-72.
26. Varnum DS, Stevens LC. 1968. Aphakia, a new mutation in the mouse. J Hered 59:147-150.
27. Semina EV, Ferrell RE, Mintz-Hittner HA, Bitour P, Alward WL, Reiter RS, Funkhauser C, Daack-Hirsch S, Murray JC. 1998. A novel homeobox gene PITX3 is mutated in families with autosomal-dominant cataracts and ASMD. Nat Genet 19:167-170.
28. Schottenstein EM. 1996. Peters' anomaly. In: Ritch R, Shields MB, Krupin T, editors. The glaucomas 2 ed. St. Louis: Mosby. p 887-897.
29. Lu MF, Pressman C, Dyer R, Johnson RL, Martin JF. 1999. Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401:276-278.
30. Lin CR, Kioussi C, O'Connell S, Briata P, Szeto D, Liu F, Izpisua-Belmonte JC, Rosenfeld MG. 1999. Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401:279-282.
31. Kume T, Deng KY, Winfrey V, Gould DB, Walter MA, Hogan BL. 1998. The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus. Cell 93:985-996.
32. Mears AJ, et al. 1998. Mutations of the forkhead/winged-helix gene, FKHL7, in patients with Axenfeld-Rieger anomaly. Am J Hum Genet 63:1316-1328.
33. Perveen R, et al. 2000. Phenotypic variability and asymmetry of Rieger syndrome associated with PITX2 mutations. Invest Ophthalmol Vis Sci 41:2456-2460.
34. Doward W, Perveen R, Lloyd IC, Ridgway AE, Wilson L, Black GC. 1999. A mutation in the RIEG1 gene associated with Peters' anomaly. J Med Genet 36:152-155.
35. Nishimura DY, et al. 1998. The forkhead transcription factor gene FKHL7 is responsible for glaucoma phenotypes which map to 6p25. Nat Genet 19:140-147.
36. Semina EV, et al. 1996. Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat Genet 14:392-399.
37. Nishimura DY, et al. 2001. A spectrum of FOXC1 mutations suggests gene dosage as a mechanism for developmental defects of the anterior chamber of the eye. Am J Hum Genet 68:364-372.
38. Alward WL. 2000. Axenfeld-Rieger syndrome in the age of molecular genetics. Am J Ophthalmol 130:107-115.
39. Waring GO 3rd, Rodrigues MM, Laibson PR. 1975. Anterior chamber cleavage syndrome A stepladder classification. Surv Ophthalmol 20:3-27.
40. Honkanen RA, Nishimura DY, Swiderski RE, Bennett SR, Hong S, Kwon YH, Stone EM, Sheffield VC, Alward WL. 2003. A family with Axenfeld-Rieger syndrome and Peters Anomaly caused by a point mutation (Phe112Ser) in the FOXC1 gene. Am J Ophthalmol 135:366-375.
41. Gould DB, John SW. 2002. Anterior segment dysgenesis and the developmental glaucomas are complex traits. Hum Mol Genet 11:1185-1193.
42. Smith RS, Zabaleta A, Kume T, Savinova OV, Kidson SH, Martin JE, Nishimura DY, Alward WL, Hogan BL, John SW. 2000. Haploinsufficiency of the transcription factors FOXC1 and FOXC2 results in aberrant ocular development. Hum Mol Genet 9:1021-1032.
43. Gage PJ, Suh H, Camper SA. 1999. Dosage requirement of Pitx2 for development of multiple organs. Development 126:4643-4651.
44. Ashery-Padan R, Gruss P. 2001. Pax6 lights-up the way for eye development. Curr Opin Cell Biol 13:706-714.
45. Gehring WJ, Ikeo K. 1999 Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet 15:371-377.
46. Chow RL, Lang RA. 2001. Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255-296.
47. Ton CC, et al. 1991. Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region. Cell 67:1059-1074.
48. Jordan T, Hanson I, Zaletayev D, Hodgson S, Prosser J, Seawright A, Hastie N, van HV. 1992. The human PAX6 gene is mutated in two patients with aniridia. Nat Genet 1:328-332.
49. Glaser T, Walton DS, Maas RL. 1992. Genomic structure, evolutionary conservation and aniridia mutations in the human PAX6 gene. Nat Genet 2:232-239.
50. Mintz-Hittner HA. 1996. Aniridia. In: Ritch R, Shields MB, Krupin T, editors. The glaucomas. 2 ed. St. Louis: Mosby. p 859-874.
51. Nelson LB, Spaeth GL, Nowinski TS, Margo CE, Jackson L. 1984. Aniridia. A review. Surv Ophthalmol 28:621-642.
52. Prosser J, van Heyningen V. 1998. PAX6 mutations reviewed. Hum Mutat 11:93-108.
53. Baulmann D, Ohlmann A, Flügel-Koch C, Goswami S, Cvekl A, Tamm ER. 2002. Pax6 heterozygous eyes show defects in chamber angle differentiation that are associated with a wide spectrum of other anterior eye segment abnormalities. Mech Dev 118:3-17.
54. Hogan BL, Hirst EM, Horsburgh G, Hetherington CM. 1988. Small eye (Sey): a mouse model for the genetic analysis of craniofacial abnormalities. Development 103(Suppl):115-119.
55. +/- small eye mice mimic human aniridia-related keratopathy. Invest Ophthalmol Vis Sci 44:1871-1878.
56. Davis J, Duncan MK, Robison WG Jr., Piatigorsky J. 2003. Requirement for Pax6 in corneal morphogenesis: a role in adhesion. J Cell Sci 116:2157-2167.
57. Walther C, Gruss P. 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113:1435-1449.
58. Grindley JC, Davidson DR, Hill RE. 1995. The role of pax-6 in eye and nasal development. Development 121:1433-1442.
59. Davis JA, Reed RR. 1996. Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J Neurosci 16:5082-5094.
60. Koroma BM, Yang JM, Sundin OH. 1997. The Pax-6 homeobox gene is expressed throughout the corneal and conjunctival epithelia. Invest Ophthalmol Vis Sci 38:108-120.
61. Collinson JM, Quinn JC, Hill RE, West JD. 2003. The roles of Pax6 in the cornea, retina, and olfactory epithelium of the developing mouse embryo. Dev Biol 255:303-312.
62. Sakai M, Serria MS, Ikeda H, Yoshida K, Imaki J, Nishi S. 2001. Regulation of c-maf gene expression by Pax6 in cultured cells. Nucleic Acids Res 29:1228-1237.
63. 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.
64. Reza HM, Ogino H, Yasuda K. 2002 L-Maf, a downstream target of Pax6, is essential for chick lens development. Mech Dev 116:61-73.
65. Cvekl A, Sax CM, Bresnick EH, Piatigorsky J. 1994. A complex array of positive and negative elements regulates the chicken alpha A-crystallin gene: involvement of Pax-6, USF, CREB and/or CREM, and AP-1 proteins. Mol Cell Biol 14:7363-7376.
66. van Raamsdonk CD, Tilghman SM. 2000. Dosage requirement and allelic expression of PAX6 during lens placode formation. Development 127:5439-5448.
67. Duncan MK, Kozmik Z, Cveklova K, Piatigorsky J, Cvekl A. 2000. Overexpression of PAX6(5a) in lens fiber cells results in cataract and upregulation of (alpha)5(beta)1 integrin expression. J Cell Sci 113:3173-3185.
68. Chauhan BK, Reed NA, Yang Y, Cermak L, Reneker L, Duncan MK, Cvekl A. 2002. A comparative cDNA microarray analysis reveals a spectrum of genes regulated by Pax6 in mouse lens. Genes Cells 7:1267-1283.
69. Collinson JM, Quinn JC, Buchanan MA, Kaufman MH, Wedden SE, West JD, Hill RE. 2001. Primary defects in the lens underlie complex anterior segment abnormalities of the Pax6 heterozygous eye. Proc Natl Acad Sci USA 98:9688-9693.
70. Chang B, et al. 2001. Haploinsufficient Bmp4 ocular phenotypes include anterior segment dysgenesis with elevated intraocular pressure. BMC Genet 2:18.
71. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. 1997. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124:2659-2670.
72. Saika S, Liu CY, Azhar M, Sanford LP, Doetschman T, Gendron RL, Kao CW, Kao WW. 2001. TGFbeta2 in corneal morphogenesis during mouse embryonic development. Dev Biol 240:419-432.
73. Zhou Y, Kato H, Asanoma K, Kondo H, Arima T, Kato K, Matsuda T, Wake N. 2002. Identification of FOXC1 as a TGF-beta1 responsive gene and its involvement in negative regulation of cell growth. Genomics 80:465-472.
74. Czerny T, Busslinger M. 1995. DNA-binding and transactivation properties of Pax-6: three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5). Mol Cell Biol 15:2858-2871.
75. Goudreau G, Petrou P, Reneker LW, Graw J, Loster J, Gruss P. 2002. Mutually regulated expression of Pax6 and Six3 and its implications for the Pax6 haploinsufficient lens phenotype. Proc Natl Acad Sci USA 99:8719-8724.
76. Planque N, Leconte L, Coquelle FM, Benkhelifa S, Martin P, Felder-Schmittbuhl MP, Saule S. 2001. Interaction of Maf transcription factors with Pax-6 results in synergistic activation of the glucagon promoter. J Biol Chem 276:35751-35760.
77. Mikkola I, Bruun JA, Holm T, Johansen T. 2001. Superactivation of Pax6-mediated transactivation from paired domain-binding sites by dna-independent recruitment of different homeodomain proteins. J Biol Chem 276:4109-4118.
78. Plaza S, Dozier C, Saule S 1993. Quail Pax-6 (Pax-QNR) encodes a transcription factor able to bind and trans-activate its own promoter. Cell Growth Differ 4:1041-1050.
79. Plaza S, Dozier C, Langlois MC, Saule S. 1995. Identification and characterization of a neuroretina-specific enhancer element in the quail Pax-6 (Pax-QNR) gene. Mol Cell Biol 15:892-903.
80. Xu HE, Rould MA, Xu W, Epstein JA, Maas RL, Pabo CO. 1999. Crystal structure of the human Pax6 paired domain-DNA complex reveals specific roles for the linker region and carboxy-terminal subdomain in DNA binding. Genes Dev 13:1263-1275.
81. Chauhan BK, Yang Y, Cveklova K, Cvekl A. 2004 Functional properties of natural human PAX6 and PAX6(5a) mutants. Invest Ophthalmol Vis Sci 45:385-392.
82. Davis A, Cowell JK. 1993. Mutations in the PAX6 gene in patients with hereditary aniridia. Hum Mol Genet 2:2093-2097.
83. Glaser T, Jepeal L, Edwards JG, Young SR, Favor J, Maas RL. 1994. PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat Genet 7:463-471.
84. Singh S, Tang HK, Lee JY, Saunders GF. 1998. Truncation mutations in the transactivation region of PAX6 result in dominant-negative mutants. J Biol Chem 273:21531-21541.
85. Cvekl A, Kashanchi F, Brady JN, Piatigorsky J. 1999. Pax-6 interactions with TATA-box-binding protein and retinoblastoma protein. Invest Ophthalmol Vis Sci 40:1343-1350.
86. Schedl A, Ross A, Lee M, Engelkamp D, Rashbass P, van HV, Hastie ND. 1996. Influence of PAX6 gene dosage on development: overexpression causes severe eye abnormalities. Cell 86:71-82.
87. Hanson IM, Fletcher JM, Jordan T, Brown A, Taylor D, Adams RJ, Punnett HH, van HV. 1994. Mutations at the PAX6 locus are found in heterogeneous anterior segment malformations including Peters' anomaly. Nat Genet 6:168-173.
88. Wolf MT, Lorenz B, Winterpacht A, Drechsler M, Schumacher V, Royer-Pokora B, Blankenagel A, Zabel B, Wildhardt G. 1998. Ten novel mutations found in Aniridia. Hum Mutat 12:304-313.
89. Favor J, Peters H, Hermann T, Schmahl W, Chatterjee B, Neuhauser-Klaus A, Sandulache R. 2001. Molecular characterization of Pax6(2Neu) through Pax6(10Neu): an extension of the Pax6 allelic series and the identification of two possible hypomorph alleles in the mouse Mus musculus. Genetics 159:1689-1700.
90. Andrews GL, Mastick GS. 2003. R-cadherin is a Pax6-regulated, growth-promoting cue for pioneer axons. J Neurosci 23:9873-9880.
91. Chauhan BK, Reed NA, Zhang W, Duncan MK, Kiilmann M, Cvekl A. 2002. Identification of genes downstream of Pax6 in the mouse lens using cDNA microarrays. J Biol Chem 277:11539-11548.
92. Matsuo T, et al. 1993. A mutation in the Pax-6 gene in rat small eye is associated with impaired migration of midbrain crest cells. Nat Genet 3:299-304.
93. Enwright JF 3rd, Grainger RM. 2000. Altered retinoid signaling in the heads of small eye mouse embryos. Dev Biol 221:10-22.
94. Vermot J, Niederreither K, Garnier JM, Chambon P, Dolle P. 2003. Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice. Proc Natl Acad Sci USA 100:1763-1768.