Distinct roles of maf genes during Xenopus lens development

Abstract

Lens development provides a good model system for studying cellular and molecular mechanisms underlying embryonic induction and morphogenesis. Members of the large Maf family of transcription factors, L-Maf and c-Maf, have been shown to play key roles in chick and mouse lens development. Here we report identification of two Xenopus maf genes, XmafB and XL-maf, which exhibit unique temporal and spatial expression patterns during lens formation. XmafB can first be detected in the presumptive lens-forming ectoderm, when the primary eye vesicle makes contact with the head ectoderm. XL-maf expression appears a little later, just before thickening of the lens placode, and both XmafB and XL-maf can be detected in the lens placode. During lens vesicle formation, the expression domains of XmafB and XL-maf segregated from each other, resulting in restricted expression in lens epithelial and fiber cells, respectively. When the optic cup anlagen was removed, only XmafB expression is detected. Both Mafs can induce the lens fiber cell-specific markers, betaA4- and gamma-crystallins. In animal cap assays, XmafB can induce Pax6, Xlens1 and Sox3 expression, but XL-maf fails to induce Pax6 and Xlens1 expression. These results suggest that these maf genes are involved in the regulation of cell-type specific gene expression and play roles in inductive events during Xenopus lens development.

Characterizing gene expression during lens formation in Xenopus laevis: Evaluating the model for embryonic lens induction

“…Although no examples were found with expression limited solely to the period of specification or com-mitment (i.e, examples II or V in Fig. 1D), several genes are first expressed in the presumptive lens ectoderm at different points during the period of commitment (i.e., XSix3, stage 20;xSOX3, stage 21;XmafB, stage 22;XL-maf and Pitx3, stage 24, see, Pennzel et al, 1997;Zhou et al, 2000;Ishibashi and Yasuda, 2001;Pommereit et al, 2001, and Fig. 4).…”

“…CAK has been shown to play a role in the activation of cdks as well as in the function of TFIIH and RNA polymerase II. Retroviral transduction of antisense Mat1 constructs into fetal human lens (Pannese et al, 1995;Kablar et al, 1996;Hirsch and Harris, 1997;Penzel et al, 1997;Zygar et al, 1998;Schaefer et al, 1999;Kenyon et al, 1999;Hollemann and Pieler, 1999;Zhou et al, 2000;Ishibashi and Yasuda, 2001;Pommereit et al, 2001).…”

Isolation and characterization of a novel gene, xMADML, involved in Xenopus laevis eye development

“…The expression patterns of six different transcription factors Xotx2, xSix3, Sox2, Sox3, Pax6, XLmaf, and lens ␥6-crystallin in xMADML-MO containing eyes were compared with the expression patterns in the contralateral, uninjected eyes, to control, uninjected embryos, and to published expression patterns ( Fig. 8; Pannese et al, 1995;Kablar et al, 1996;Penzel et al, 1997;Mizuseki et al, 1998;Zygar et al, 1998;Schaefer et al, 1999;Zhou et al, 2000;Ishibashi and Yasuda, 2001;Carl et al, 2002). The expression patterns of Xotx2, XL-maf, and ␥6-crystallin were all maintained in the morpholino-injected eyes, although the expression levels were lower compared with the uninjected side (Fig.…”

“…On the other hand, some studies have suggested that Pax6 expression may inhibit maturation of lens fiber cells and expression of certain crystallins Duncan et al, 2004). XLmaf has been shown to be able to induce lens differentiation and crystallin expression, so the persistence of XL-maf expression in the xMADML knockdown could be responsible for the maintenance of ␥6-crystallin expression (Ogino and Yasuda, 1998;Ishibashi and Yasuda, 2001). The data presented here indicate that xMADML is important for the proper differentiation of the eye, either through the direct or indirect downregulation of key genes, including Pax6.…”

“…Among several transcription factors shown to participate in vertebrate eye development are the following: Pax-6, a transcription factor sufficient to cause ectopic eye formation in Drosophila and Xenopus (Halder et al, 1995;Altmann et al, 1997;Chow et al, 1999;Ashery-Padan et al, 2000;Zuber et al, 2003); XL-maf and XMafB, transcription factors able to activate the expression of lens crystallins in Xenopus (Ishibashi and Yasuda, 2001); Prox1 and xSix3, homeodomain transcription factors necessary for proper lens cell development in Xenopus, Drosophila, fish, and mouse (Oliver et al, 1993(Oliver et al, , 1996Tomarev et al, 1996Tomarev et al, , 1998Schaefer et al, 1999;Zhou et al, 2000;Carl et al, 2002;Zuber et al, 2003); Sox2 and Sox3, transcription factors containing an HMG domain, which are important in the regulation of crystallin expression and fiber cell differentiation in Xenopus, mouse, and chick (Kamachi et al, 1995(Kamachi et al, , 1998Uwanogho et al, 1995;Penzel et al, 1997;Schaefer et al, 1999;Kondoh et al, 2004); and Xotx2, a homeobox gene important in patterning the anterior central nervous system (CNS) and placodal structures in Xenopus (Pannese et al, 1995;Kablar et al, 1996;Schaefer et al, 1999). Many of these transcription factors have been shown to interact in a complex network of genes; however, the full complement of genes necessary for embryonic eye development, including hundreds of potential downstream targets, has not been identified.…”