FOX and ETS family transcription factors regulate the pigment cell lineage in planarians

Abstract

Many pigment cells acquire unique structural properties and gene expression profiles during animal development. The underlying differentiation pathways have been well characterized in cells formed during embryogenesis, such as the neural crest-derived melanocyte. However, much less is known about the developmental origins of pigment cells produced in adult organisms during tissue homeostasis and repair. Here we report a lineage analysis of ommochrome- and porphyrin-producing cells in the brown, freshwater planarian Using an RNA-sequencing approach, we identified two classes of markers expressed in sequential fashion when new pigment cells are generated during regeneration or in response to pigment cell ablation. We also report roles for FOXF-1 and ETS-1 transcription factors, as well as for an FGFR-like molecule, in the specification and maintenance of this cell type. Together, our results provide insights into mechanisms of adult pigment cell development in the strikingly colorful Platyhelminthes phylum.

foxF-1 Controls Specification of Non-body Wall Muscle and Phagocytic Cells in Planarians

“…foxF-1 was recently shown to be required for the specification of planarian pigment cells [24]. Accordingly, foxF-1 RNAi animals were depigmented (Figure 5B; Figure S7B; [24]).…”

“…foxF-1 had several expression domains (Figure 2D; Figure S4D,E,G): it was expressed in lateral and medial DVM (mp-1 + / mhc-2 + ), in IM cells (mp-1 + / mhc-2 - ), and in pharynx muscle. In addition, foxF-1 was also expressed broadly in a non-muscle subepidermal layer (Figure 2D; [24]). SCS data showed co-expression of foxF-1 with nk4 and gata4/5/6–2 in DVM cells, and with gata4/5/6–3 in IM cells (Figure S4H).…”

“…The cathepsin + cluster contains several cell-type classes, including pigment cells, glia cells, and numerous cells of unknown function [13, 15]. foxF-1 was recently shown to be required for the specification of planarian pigment cells [24]. Accordingly, foxF-1 RNAi animals were depigmented (Figure 5B; Figure S7B; [24]).…”

“…foxF-1 RNAi animals showed significantly decreased expression of cathepsin + -cell subcluster markers, which represent putative different cell types (Figure 6A, Data S2). foxF-1 thus not only regulates pigment cells [24] but also many other cathepsin + cell types. FISH validated these findings in both uninjured and regenerating animals: foxF-1 RNAi animals had significantly fewer cathepsin + cell types expressing the markers dd_10872, acq-1, and dd_582(CTSL2), as well as pigment and glia cells (Figure 6B; Figure 5B,L).…”

“…In addition to the role of FoxF in muscle, we found that foxF-1 was essential for the specification and/or maintenance of a variety of non-muscle cell types, including pigment [24] and glia cells (Figure 7B). These different cell types highly express cathepsin genes [13, 15], lysosomal enzymes essential for processing of extracellular or intracellular particles.…”