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Lens Development and Crystallin Gene Expression: Many Roles for Pax-6 Ale5 Cvekl and Joram Piatigorsky

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Lens Development and Crystallin Gene Expression: Many Roles for Pax-6 Ale5 Cvekl and Joram Piatigorsky Review articles e Lens development and crystallin gene expression: many roles for Pax-6 Ale5 Cvekl and Joram Piatigorsky Summary The vertebrate eye lens has been used extensively as a model for developmental processes such as determination, embryonic induction, cellular differentiation, transdifferentiation and regeneration, with the crystallin genes being a prime example of developmentally controlled, tissue-preferred gene expression. Recent studies have shown that Pax-6, a transcription factor containing both a paired domain and homeodomain, is a key protein regulating lens determination and crystallin gene expression in the lens. The use of Pax-6 for expression of different crystallin genes provides a new link at the developmental and transcriptional level among the diverse crystallins and may lead to new insights Accepted into their evolutionary recruitment as refractive proteins. 20 May 1996 Eye development and lens induction inward to form the inner layer of the (secondary) optic cup. Development of a multicellular organism is orchestrated The optic cup gives rise to the neural retina (a thicker inner by the action of specific transcription factors and other layer) and pigmented epithelium (a thin outer layer). The regulatory proteins and molecules, which control the pro- lens vesicle separates from the surface epithelium and gram of embryonic determination and differentiation. The contains a single layer of cells with columnar morphology mechanism of action of the majority of these factors is that differentiate into the posterior lens fiber cells and ante- believed to rely on a synergism between multiple factors. rior lens epithelial cells. Lens development is character- The eye is an advantageous model for studies of transcrip- ized by high, preferential expression of soluble proteins tion factors during development which control organogen- called crystallins (ref. 3; see below). Lens differentiation is esis and tissue-specific gene expression. Vertebrate eye also regulated by growth factors, especially FGFs and development involves a hierarchy of inductive interactions secreted molecules coming from the retina, an area between the embryonic forebrain and surface ecto- beyond the scope of this review. derm(lr2). During the course of gastrulation, a region of Although the identities of transcription factors involved in dorsal ectoderm is induced to form the neural plate, which eye morphogenesis are just beginning to be elucidated, it folds into the neural tube with anterior protrusions and has been shown recently that Pax-6 plays an essential role, gives rise to the future brain. At the end of gastrulation, both in vertebrates and Dr~sophi/a(~-’~).Pax-6 is a complex retinal fields are specified as a thickened zone of the neu- protein with a highly conserved paired domain and homeo- roepithelium, which folds to form the optic sulcus. Enlarge- domain, as described below. Overexpression of Pax-6 from ment of the sulcus generates optic pits in the region of the future forebrain and with the closure of the neural tube, the Drosophila [called eyeless (ey)], mouse [called small eye optic pits are pushed outward. Deepening of the optic pit (Se~)l(’~)or squid (S. Tomarev, P. Callaerts, L. Kos, R. results in the formation of the optic vesicle, which is con- Zinovieva, G. Halder, W. Gehring and J.P., manuscript in nected to the brain cavity by the primitive optic stalk. The preparation), resulted in the formation of ectopic compound first manifestation of lens induction is the appearance of a eyes in the fly, indicating that Pax-6 may have a universal dish-shaped thickening of the surface ectodermal epi- and critical role in eye development. The aim of the present thelium, the lens placode, closely apposed to the anterior review is to summarize recent findings concerning the role surface of the optic vesicle (Fig. 1). The lens placode of Pax-6 in the development and disorders of the eye, in indents to form the lens pit and subsequently the lens vesi- particular to lens induction and transcription of crystallin cle, while the outer part of the optic vesicle collapses genes. BioEssays Vol. 18 no. 8 621 QlCSU Press1996 pp. 621-630 810969 Review art ides Transcription factors implicated in eye development associated with Pax-6 mutations, resulting in a central The molecular events specifying different eye tissues are corneal opacity and physical connection of the lens and being studied by genetic techniques and various gene cornea(33). Other homozygous Pax-6 mutations have selection procedures, with both strategies producing an resulted in the absence of eyes and in brain defects(34). increasing number of candidate genes for involvement in These phenotypes are characterized by severe defects in eye development. A list of selected eye transcription factors, eye morphogenesis and, in homozygous cases, the preferentially expressed in the developing lens and retina, is absence of the eyes and nose indicate that Pax-6 is an given in Table 1. Additional homeobox genes expressed in essential factor acting early during development and that its vertebrate ocular tissues are compiled elsewhere(11).Thus, loss cannot be readily compensated for by another function- while Pax-6 plays a prominent role in eye and lens develop- ally related gene. ment, it is but one of a growing list of factors that must inter- act in numerous ways. Lens development and Pax-6 During development of the mouse eye, a broad Pax-6 Phenotypes and expression pattern of Pax-6 expression pattern appears in the head surface ectoderm Pax-6 was cloned initially by four groups of investigators and becomes restricted progressively to the area of the from human@),mouse(7), zebrafish@) and The high future lens and cornea(7). Pax-6 mRNA is then detected amino acid sequence conservation (more than 96Oh) of Pax- sequentially in the optic pit, the optic sulcus and the optic 6 indicated that the whole protein is critical for function, con- vesicles. The expression of Pax-6 in the optic vesicle is sistent with the idea that Pax-6 has a very fundamental and associated with development of the inner layers of the specialized role, like other paired domain proteins. There neural retina (Fig. 1). Pax-6 mRNA is also present in the pri- are distinct phenotypes associated with Pax-6. In the mary fiber cells and later in the secondary fiber cells (the mouse, the heterozygous mutations in Pax-6 result in small cortical cells derived at the equatorial margin by division of eye (Sey), a microphthalmia phenotype(4). Homozygous the epithelial cells) of the embryonic len~(~~~~).In addition to Pax-6 mutations (Sey/Sey) are lethal at birth; in addition to the lens, Pax-6 mRNA is found in the surface ectoderm giv- brain defects, the eyes and nose are absent. In the human, ing rise to the cornea and later in the corneal epithelium(7).A a heterozygous Pax-6 phenotype, aniridia (AN), is charac- slightly different pattern of Pax-6 expression occurs in the terized by various ocular malformations including the lens, beginning stages of eye development in the embryonic iris, cornea and retina, leading to cataracts and glau- chicken, where Pax-6 mRNA is limited at first to the coma(6z8).Peters’ anomaly is another rare human disorder prospective lens ectoderm and only later is detected in the Table 1. Examples of transcription factors expressed in the developing vertebrate eye Class/Name Major sites of expression (eye only) Reference Paired domain Pax-6 Optic vesicle, presumptive lens ectoderm, lens, corneal epithelium, 4-7 neuroretina, iris Pax-2 Optic vesicle, optic cup, optic stalk 12-14 Homeodomain Otx-2 Optic cup, RPE, presumptive lens ectoderm 15-17 Msx-1 Mesenchyme between the surface epithelium and the lens, optic cup 18 MSX-2 Optic cup, lens, retina, iris, corneal epithelium 18 Proxl Optic vesicle, lens, retina 19,20 Xlim-3 Inner nuclear layer of the retina 21 ChxlO Optic vesicle, neuroretina 22 Emxl Lens 23 Six3 Optic vesicle, neural retina, lens, optic stalk 24 Optx-l Neural plate, optic vesicle, retina 25 Optx-2 Anterior ectoderm (prospective eye area), optic vesicle, lens/corneal 25 placode, retina, optic nerve Helix-loop-helix mi Pigment layer of retina 26 Forkhead BF-l,2 Asymmetric expression in the retinal neuroepithelium 27 Leucine-zipper sw3-3 Optic cup, lens epithelium, neuroretina 28 Nuclear receptors RARP Pigmented retina, vitreous body, mesenchyme around the eye 29 RXRa Eye 30 HMG sox-1 Lens fibers 31 sox-2 Lens placode, lens, retina 31 622 Vol. 18 no. 8 BioEssays Review articles e Inner Layer B - (Froswtlve Neuroretina) .Newoectcderm Pigment Epithelium) D E Pigmented Layer 'ofRetin0 Fig. 1. Highly schematic diagram of the early events in mouse eye development('*). The developing lens is shown in blue. (A) At embryonic day 9 to 9.5 (E9-9.9, the optic vesicle is attached to the ventral wall of the prosencephalon via the optic stalk. The lens placode (prospective lens) becomes apparent as a thickened area of the surface ectoderm. (6)At E9.5-10, the area of the lens placode has enlarged. (C) At E10.5, the central part of the lens placode indents to form the lens pit and the optic vesicle invaginates to form the optic cup. (D) At about El1.5, the lens pit is converted into the lens vesicle, which is surrounded by a capsule. (E) At E13.5, the lens comprises the anterior cuboidal epithelial cells and the posterior elongationg fiber cells. The neural retina layer behind the lens begins to differentiate and the primitive cornea develops in front of the lens. neural tube(36). In contrast to the situation in mouse The rSey/rSey surface ectoderm never embryos, the olfactory placodes of chicken embryos formed lenses when it was cultivated with rSey/+ or +/+ express little, if any, Pax-6 mRNA.
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