Molecular Mechanisms of Optic Vesicle Development: Complexities, Ambiguities and Controversies ⁎ Ruben Adler A,B, , M

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Molecular Mechanisms of Optic Vesicle Development: Complexities, Ambiguities and Controversies ⁎ Ruben Adler A,B, , M View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Developmental Biology 305 (2007) 1–13 www.elsevier.com/locate/ydbio Review Molecular mechanisms of optic vesicle development: Complexities, ambiguities and controversies ⁎ Ruben Adler a,b, , M. Valeria Canto-Soler a a Department of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, MD, USA b Department of Neuroscience, The Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA Received for publication 22 December 2006; revised 26 January 2007; accepted 30 January 2007 Available online 7 February 2007 Abstract Optic vesicle formation, transformation into an optic cup and integration with neighboring tissues are essential for normal eye formation, and involve the coordinated occurrence of complex cellular and molecular events. Perhaps not surprisingly, these complex phenomena have provided fertile ground for controversial and even contradictory results and conclusions. After presenting an overview of current knowledge of optic vesicle development, we will address conceptual and methodological issues that complicate research in this field. This will be done through a review of the pertinent literature, as well as by drawing on our own experience, gathered through recent studies of both intra- and extra-cellular regulation of optic vesicle development and patterning. Finally, and without attempting to be exhaustive, we will point out some important aspects of optic vesicle development that have not yet received enough attention. © 2007 Elsevier Inc. All rights reserved. Keywords: Epigenetic mechanisms; Extracellular signaling molecules; Eye development; Morphogenetic mechanisms; Lens induction; Optic cup; Optic vesicle; Pattern formation; Retina development; Retinal pigment epithelium; Transcription factors Introduction Comprehensive reviews of the studies done before the year 2000 are available (e.g., Chow and Lang, 2001; Jean et al., This article will present an overview of the complex cellular 1998; Zhang et al., 2002; Lupo et al., 2000) and more recent and molecular mechanisms underlying the formation of the contributions have been partially reviewed (e.g., Bailey et al., optic vesicle (OV), the interactions of the OV with neighbor- 2004; Esteve and Bovolenta, 2006; Lovicu and McAvoy, ing tissues, and its transformation into an optic cup (OC) 2005; Lupo et al., 2006; Sullivan et al., 2004; Wilson and containing three different but interconnected domains (neural Houart, 2004; Yang, 2004; Zaghloul et al., 2005, among retina, retinal pigment epithelium and optic stalk). These others). We will only present here a brief summary of this phenomena have attracted much attention since the early days material, as background for a discussion of problems of of experimental embryology but, despite considerable pro- experimental design and interpretation that are at least partially gress, they remain incompletely understood, and even responsible for controversies in this field. In a closing section, controversial. Space limitations make it impossible to cover we will summarize important aspects of these phenomena that the entire field, or to do justice to the many important have not yet received much experimental analysis. The contributions made by different laboratories over the years. information summarized in this article has been derived from studies on embryos from several different experimental animal species, including amphibians, chick, mouse, and to a lesser extent rat and fish. Although inter-specific differences are only ⁎ Corresponding author. Department of Ophthalmology, Johns Hopkins School of Medicine, 600 N. Wolfe Street, 519 Maumenee, Baltimore, MD considered in some detail in Section V-B, it is not unlikely that 21287-9257, USA. Fax: +1 410 955 0749. they could also be relevant to phenomena described in other E-mail address: [email protected] (R. Adler). parts of the article. 0012-1606/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ydbio.2007.01.045 2 R. Adler, M.V. Canto-Soler / Developmental Biology 305 (2007) 1–13 Structural aspects of optic vesicle development Inductive interactions during OV development The initial indication of optic vesicle (OV) formation is the An extensive series of inductive tissue interactions must appearance of symmetrical bilateral evaginations from the occur for the OV to appear, develop, and integrate with diencephalon, which slowly expand through the mesenchyme neighboring tissues. They actually begin well before the first towards the surface ectoderm (Fig. 1A). As contact between morphological indications of OV development, as illustrated by the OV and the ectoderm is established (Fig. 1B), both tissues the induction and regionalization of the neural plate by the undergo complex (and temporally correlated) structural “organizer” (Kessler and Melton, 1994; Streit and Stern, 1999), changes. The ectoderm thickens initially into a “lens placode” and the induction of an “eye field” within the anterior neural (Fig. 1B), which invaginates into a vesicle that eventually plate (Esteve and Bovolenta, 2006; Moore et al., 2004; Zuber et closes and separates completely from the surface ectoderm al., 2003). The eye field is located in the anterior neural plate, (Figs. 1C–D). The concomitant invagination of the OV is more surrounded by telencephalic precursors and by cells that will complex, resulting in the formation of an optic cup (OC) that form the hypothalamus (Esteve and Bovolenta, 2006). The has a double wall, and is connected to the diencephalon by precordal mesoderm plays a key role in determining the eye the optic stalk (Figs. 1C–E). The invagination of the dorsal field and its subdivision into two separate domains, the future aspect of the optic vesicle (Fig. 1C) generates an internal layer bilateral optic vesicles (Li et al., 1997). As the evaginating optic (the neural retina) and an external layer, the retinal pigment vesicles make contact with the mesenchyme and the ectoderm, epithelium (RPE), whereas more ventrally the OV narrows they form a highly interactive system in which numerous considerably into the “choroid fissure” (Figs. 1C′, D). The consecutive, and frequently reciprocal inductive interactions fissure closes completely in normal development, forming the take place. The specification of the neural retina and RPE optic nerve through which retinal ganglion cell axons grow domains within the OV appears to be determined by inductive towards the brain (Fig. 1E); its abnormal persistence is known signals originating in the surface ectoderm and in the as “coloboma”. mesenchyme, respectively (Fuhrmann et al., 2000; Vogel- Fig. 1. Schematic representation of vertebrate eye development. (A) The optic vesicle forms as an evagination from the diencephalon. (B) Upon contact with the surface ectoderm, the optic vesicle becomes patterned into presumptive RPE, neural retina and optic stalk; the surface ectoderm in turn forms the lens placode. (C) The optic vesicle and lens placode invaginate, giving rise to the optic cup and the lens vesicle, respectively. (C′) The ventral region of the invaginating optic vesicle forms the choroid fissure. (D–E) Transition from early to mature optic cup. The lens vesicle loses its cavity and becomes a solid structure; the neural retina and the pigment epithelium become apposed, reducing ependymal cavity to a virtual space; the optic stalk gives riseto the optic nerve, and the surface ectoderm adjacent to the lens gives rise to the corneal epithelium. Abbreviations: C: Cornea; L: lens; LP: lens placode; LV: lens vesicle; MS: mesenchyme; NR: neural retina; ON: optic nerve; OS: optic stalk; OV: optic vesicle; RPE: retinal pigment epithelium; S: sclera; SE: surface ectoderm. R. Adler, M.V. Canto-Soler / Developmental Biology 305 (2007) 1–13 3 Hopker et al., 2000; Zhao et al., 2001). In turn, inductive portant role in regulating Wnt and FGF signaling during the influences from the optic vesicle derivatives influence further early events leading to optic vesicle formation (Filipe et al., development of the lens (Chow and Lang, 2001; Grainger et al., 2006; Yamamoto et al., 2005). One of the factors involved in 1997; Lovicu and McAvoy, 2005). The dorso-ventral patterning splitting the eye field is a secreted Nodal-related member of the of the optic cup is regulated by a balance between opposing TGF-β superfamily encoded by the Cyclops (Cyc) gene (Muller signals originating in the neural tube and/or the optic stalk on et al., 2000; Varga et al., 1999), perhaps acting through the one hand, and in the dorsal region of the optic cup on the other. induction of SHH expression (Chow and Lang, 2001; Ekker The lens also influences the formation of the iris and ciliary et al., 1995; Li et al., 1997; Macdonald et al., 1995; Marti and body, specialized structures at the peripheral margin of the optic Bovolenta, 2002; Muller et al., 2000; Pera and Kessel, 1997; cup (Hyer, 2004). Several aspects of these interactions will be Wilson and Houart, 2004). SHH, in turn, contributes to the discussed in more detail below. normal separation of the eye field into two optic vesicles by regulating its proximo-distal patterning (Chow and Lang, 2001; Extracellular signaling molecules and transcription factors Ekker et al., 1995; Macdonald et al., 1995; Take-uchi et al., involved in OV induction and development 2003; Wilson and Houart, 2004). As already mentioned, patterning of the OV neuroepithelium
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