Competence, specification and commitment to an olfactory placode fate

Abstract

Cranial sensory placodes arise as transient thickenings of embryonic head ectoderm (van Wijhe, 1883;von Kupffer, 1891) and invaginate/ingress to form components of the nose, lens and inner ear (Bailey and Streit, 2006; Baker and Bronner-Fraser, 2001;Schlosser, 2006). Of the three sensory placodes, the lens and otic are relatively easy to distinguish and manipulate early in development. Therefore, tissue interactions and signals guiding their induction have been studied extensively (reviewed by Brown et al., 2003;Chow and Lang, 2001;Donner et al., 2006;Grainger, 1992;Noramly and Grainger, 2002;Riley and Phillips, 2003;Saha et al., 1989;Streit, 2001;Torres and Giraldez, 1998).By contrast, development of the olfactory sensory system has been primarily investigated at later stages. An attractive model for studying neurogenesis, its myriad of derivatives include the regenerative odorant sensing olfactory neurons in the olfactory epithelium (Calof et al., 1998;Graziadei and Graziadei, 1979;Graziadei and Metcalf, 1971;Graziadei and Monti Graziadei, 1983), the ingressing gonadotropin-releasing hormone neurons (reviewed by Parhar, 2002;Wray, 2002) [for a contrary view see Whitlock (Whitlock, 2005)], the pheromone-detecting vomeronasal organ (Dulac, 1997) and other neuromodulatory and neuroendocrine cells (Northcutt and Muske, 1994;Tarozzo et al., 1995;Yamamoto et al., 1996). It is the only placode to give rise to glial cells that ingress and migrate along the olfactory nerve towards the brain (Chuah and West, 2002;Ramon-Cueto and Avila, 1998). Cues that guide differentiation along these different pathways and the molecular mechanisms underlying the patterned wiring of olfactory sensory neurons have been examined extensively (reviewed by Baker and Margolis, 2002; Balmer and LaMantia, 2005).Contrasting with this wealth of data, inductive events that initiate olfactory development remain ambiguous, partially because the placode is morphologically invisible until relatively late (HH13+ in birds). Transplantation studies show that precursors straddle the lateral anterior neural folds and adjacent ectoderm in the neurula (Couly and Le Douarin, 1985), but their exact location at intervening stages was unclear. Recent cell marking studies in zebrafish and chick have examined the origin of the olfactory placode at higher resolution and at intervening stages (Bhattacharyya et al., 2004;Whitlock and Westerfield, 2000). Olfactory precursors are initially distributed in a broad region spanning the anterior neural folds and overlapping with lens precursors. Over time, they become progressively restricted to the most anterior ectoderm, finally resolving to a discrete olfactory pit. Knowledge of the location of precursors at different stages has facilitated manipulation of their development.To understand how and when the nasal epithelium is first induced, we examined competence, specification and commitment of ectoderm toward an olfactory fate. This information is a necessary prerequisite for interpreting results of functional perturba...

Novel skeletogenic patterning roles for the olfactory pit

“…A recent study by Bhattacharyya and Bronner-Fraser (Bhattacharyya and Bronner-Fraser, 2008) confirms our results that the olfactory placode is able to form thickened epithelium and neurons in ectopic locations. Our data extend their work by testing the competence of older mesenchyme.…”

The peripheral sensory nervous system in the vertebrate head: A gene regulatory perspective

“…At this point the question remains of whether cells within the PPR are truly multipotent and acquire different fates according to their final location, or whether cells pre-committed to specific fates segregate to their appropriate destinations. Since all placode progenitors initially share common properties (see below) and are only committed to their ultimate fate much later (Baker et al, 1999;Bhattacharyya and Bronner-Fraser, 2008;Gallagher et al, 1996;Groves and Bronner-Fraser, 2000;Henry and Grainger, 1990;Jacobson, 1963a, b, c;Waddington, 1937), it is likely that the PPR represents a territory of multipotent cells. Finally, even after placode formation cells from the surrounding ectoderm continue to be recruited into the placodal epithelium Streit, 2002;Xu et al, 2008).…”

“…At neural plate and early somite stages, competence to respond to signals that induce specific placodes is restricted to the head ectoderm and for some placodes to the PPR itself (Baker et al, 1999;Bhattacharyya and Bronner-Fraser, 2008; At neural plate stages, the pre-placodal territory (pink) surrounds the anterior neural plate (grey); the neural crest territory lies more medial (green). Note: each domain is not yet clearly defined and progenitors for each cell population are intermingled.…”

Mechanisms of cranial placode assembly

“…The classic assay to estimate the timing of specification for a given cell population consists in dissecting small pieces of tissue at different stages and culturing them in isolation, in order to assess whether cells can differentiate according to their normal fate in a neutral environment. The general outcome of these experiments performed for sub-regions of the PPR is that the onset of placode specification is approximately concomitant with the decrease in the overlap between placodal precursors, which makes it difficult to conclude about the precise temporal sequence linking the two events (Baker et al, 1999;Groves and Broner-Fraser, 2000;Baker and Bronner-Fraser, 2001;Bhattacharyya and Bronner-Fraser, 2008).…”