Abstract

In the vertebrate head, central and peripheral components of the sensory nervous system have different embryonic origins, the neural plate and sensory placodes. This raises the question of how they develop in register to form functional sense organs and sensory circuits. Here we show that mutual repression between the homeobox transcription factors Gbx2 and Otx2 patterns the placode territory by influencing regional identity and by segregating inner ear and trigeminal progenitors. Activation of Otx2 targets is necessary for anterior olfactory, lens and trigeminal character, while Gbx2 function is required for the formation of the posterior otic placode. Thus, like in the neural plate antagonistic interaction between Otx2 and Gbx2 establishes positional information thus providing a general mechanism for rostro-caudal patterning of the ectoderm. Our findings support the idea that the Otx/Gbx boundary has an ancient evolutionary origin to which different modules were recruited to specify cells of different fates.

Highlights

  • In the vertebrate head, placodes give rise to crucial parts of the sensory nervous system including the olfactory epithelium, the lens, the inner ear and the sensory neurons of the cranial ganglia (Baker and Bronner-Fraser, 2001; Streit, 2007; Schlosser, 2010)

  • How are central and peripheral components aligned? Here we explore the possibility that a common molecular mechanism allocates anterior-posterior positional information across the entire ectoderm

  • To form a functional nervous system its peripheral and central components must develop in register

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Summary

Introduction

Placodes give rise to crucial parts of the sensory nervous system including the olfactory epithelium, the lens, the inner ear and the sensory neurons of the cranial ganglia (Baker and Bronner-Fraser, 2001; Streit, 2007; Schlosser, 2010). While Gbx is first detected within the posterior neuroectoderm, Otx becomes restricted anteriorly (Simeone et al, 1992, 1993; von Bubnoff et al, 1996; Tour et al, 2001) Both factors mutually repress each other to form a sharp border (Millet et al, 1999; Katahira et al, 2000; Tour et al, 2002a; Glavic et al, 2002) and this interaction establishes the midbrain-hindbrain boundary (MHB) (Wassarman et al, 1997; Acampora et al, 1995, 1997, 1998; Rhinn et al, 1998; Broccoli, et al, 1999; Li et al, 2005). These observations suggest that the Otx2/Gbx interface is primarily important for positioning the MHB (Li and Joyner, 2001; Raible and Brand, 2004)

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