Vertebrate Cranial Placodes I. Embryonic Induction

Abstract

Cranial placodes are focal regions of thickened ectoderm in the head of vertebrate embryos that give rise to a wide variety of cell types, including elements of the paired sense organs and neurons in cranial sensory ganglia. They are essential for the formation of much of the cranial sensory nervous system. Although relatively neglected today, interest in placodes has recently been reawakened with the isolation of molecular markers for different stages in their development. This has enabled a more finely tuned approach to the understanding of placode induction and development and in some cases has resulted in the isolation of inducing molecules for particular placodes. Both morphological and molecular data support the existence of a preplacodal domain within the cranial neural plate border region. Nonetheless, multiple tissues and molecules (where known) are involved in placode induction, and each individual placode is induced at different times by a different combination of these tissues, consistent with their diverse fates. Spatiotemporal changes in competence are also important in placode induction. Here, we have tried to provide a comprehensive review that synthesises the highlights of a century of classical experimental research, together with more modern evidence for the tissues and molecules involved in the induction of each placode.

21st Century neontology and the comparative development of the vertebrate skull

“…Although extensive effort has been made to understand ectodermal subdivisions within the neural plate, there has been a much less of an effort to understand early regional pattern within the cephalic surface ectoderm outside of those investigations examining the origination of the neural crest, the cranial placodes, and some perhaps generally underappreciated work involving the cement gland in amphibians (Gammill and Sive, 1997, 2000Fang and Elinson, 1999;Baker and Bronner-Fraser, 2001;Schweickert et al, 2001;Sauka-Spengler et al, 2002;Wardle and Sive, 2003;Streit, 2004;Nokhbatolfoghahai and Downie, 2005). Analyses of the development of the early vertebrate epiblast have typically been concerned either with (1) when and how the distinction between neural and non-neural ectoderm is established or (2) how is positional information, i.e., anterior (head) and posterior (trunk), within the neural plate established Stern, 2002Stern, , 2005Wilson and Houart, 2004), and have lead to several questions, including: Is the epiblast ubiquitously competent to become either neurectodermal or surface ectodermal, and if so, is the specification and eventual commitment to neural and surface ectodermal achieved simultaneously, or does one precede the other?…”

Initial specification of the epibranchial placode in zebrafish embryos depends on the fibroblast growth factor signal

“…Therefore, to observe the development of this placode, we tested the possibility that sox3 can be used as a marker, since it is one of the earliest genes expressed specifically in the epibranchial placode in other vertebrates (Baker and Bronner-Fraser, 2001). We previously conducted functional screening of genes affecting zebrafish embryogenesis and found a cDNA clone for sox3 (accession no.…”

“…In vertebrates, the cranial sensory nervous system is derived from two groups of embryonic cells during development: A small portion is derived from neural crest cells, while the majority arises from the sensory placodes (Baker and Bronner-Fraser, 2001). The sensory placode is defined as a focal thickening of epithelium that forms at characteristic positions in the embryonic head (Baker and BronnerFraser, 2001).…”

Characterization of novel GPCR gene coding locus in amphioxus genome: Gene structure, expression, and phylogenetic analysis with implications for its involvement in chemoreception

“…Nevertheless, it is noteworthy that comparison of developmental gene expression between the rostral surface of amphioxus larvae and vertebrate olfactory placode reveals a number of similarities (reviewed by Holland and Holland, 2001; see also Holland and Yu, 2002). For example, the amphioxus counterpart of the Pax6 gene (AmphiPax6), whose expression labels the olfactory placode and its derivatives in vertebrate embryos (see Baker and Bronner-Fraser, 2001), is expressed broadly in the rostral surface of early larvae (Gladon et al, 1998). The Amphi-GPCR1 expression domain, however, is subdivided into two regions by an Amphi-GPCR1-negative domain that may contain distinct sensory neurons called corpuscles of de Quatrefages (see Baatrup, 1982, and references therein).…”

“…The detection and discrimination of chemical stimuli is important for the organization of feeding, mating, and social behavior, and is mediated by peripheral chemosensory organs with varied complexity in almost all metazoans. Vertebrate sensory systems, including the olfactory system, exhibit fairly modest changes over the course of vertebrate evolution (Eisthen, 1997;Hodos and Butler, 1997) due to typical formation of neurogenic placodes in the vertebrate embryo from which nearly all of the cranial sensory cells originate (reviewed by Baker and Bronner-Fraser, 2001). These sensory cells are then interconnected into highly sophisticated circuits that ascend to the brain.…”