Emergence of sensory structures in the developing epidermis in sepia officinalis and other coleoid cephalopods

Abstract

Embryonic cuttlefish can first respond to a variety of sensory stimuli during early development in the egg capsule. To examine the neural basis of this ability, we investigated the emergence of sensory structures within the developing epidermis. We show that the skin facing the outer environment (not the skin lining the mantle cavity, for example) is derived from embryonic domains expressing the Sepia officinalis ortholog of pax3/7, a gene involved in epidermis specification in vertebrates. On the head, they are confined to discrete brachial regions referred to as "arm pillars" that expand and cover Sof-pax3/7-negative head ectodermal tissues. As revealed by the expression of the S. officinalis ortholog of elav1, an early marker of neural differentiation, the olfactory organs first differentiate at about stage 16 within Sof-pax3/7-negative ectodermal regions before they are covered by the definitive Sof-pax3/7-positive outer epithelium. In contrast, the eight mechanosensory lateral lines running over the head surface and the numerous other putative sensory cells in the epidermis, differentiate in the Sof-pax3/7-positive tissues at stages ∼24-25, after they have extended over the entire outer surfaces of the head and arms. Locations and morphologies of the various sensory cells in the olfactory organs and skin were examined using antibodies against acetylated tubulin during the development of S. officinalis and were compared with those in hatchlings of two other cephalopod species. The early differentiation of olfactory structures and the peculiar development of the epidermis with its sensory cells provide new perspectives for comparisons of developmental processes among molluscs.

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

“…We identified ciliated peripheral sensory neurons in the skin of hatchling O. bimaculoides using α-and β-tubulin antibodies. These cells were similar in morphology and position (Sundermann-Meister, 1978;Sundermann, 1983;Mackie, 2008;Buresi et al, 2014) to cells described as mechanoreceptors in both squid and cuttlefish (Budelmann and Bleckmann, 1988;Bleckmann et al, 1991). It is not yet known whether these peripheral sensory neurons act as mechanoreceptors in the skin of O. bimaculoides.…”

Reversion to developmental pathways underlies rapid arm regeneration in juvenile European cuttlefish, Sepia officinalis (Linnaeus 1758)

“…This study focused on three genes associated with early tissue speciation. Previous studies have identified many genes implicated in cephalopod limb morphogenesis; future experimentation would especially benefit from timepoint‐ and treatment‐specific profiles, with particular emphasis on genes associated with nervous precursor distribution and development of complex sensory and neurological structures (Baratte & Bonnaud, ; Bassaglia et al, ; Buresi, Baratte, Da Silva, & Bonnaud, ; Buresi, Canali, Bonnaud, & Baratte, ; Buresi, Croll, Tiozzo, Bonnaud, & Baratte, ; Focareta, Sesso, & Cole, ; Zhang & Tublitz, ), as well as muscle (Bassaglia et al, ; Fossati et al, ; Navet et al, ; Zullo et al, ) and endothelium (Focareta & Cole, ). Additional genes of interest should be garnered from the available studies in models across taxa (Fei et al, ; Godwin et al, ; Kawakami et al, ; Uygur & Lee, ; Wischin et al, ); ideally strategies utilizing transcriptomic or single‐cell RNA sequencing could be compared on both amputated and regenerated limb tips to provide greater clarity on intraindividual variation in expression based on injury‐naïve and regenerating conditions.…”

Histamine and histidine decarboxylase in the olfactory system and brain of the common cuttlefish Sepia officinalis (Linnaeus, 1758)

“…(d) In situ hybridization against Sof‐elav1 shows some of the nervous structures of the skin: Lateral lines along the arms and left olfactory organ (white arrow). Panel adapted with permission from Buresi, Croll, Tiozzo, Bonnaud, and Baratte (). CNS, central nervous system; Ey, eye; PNS, peripheral nervous system; Sh, shell; y, yolk.…”

“…The embryonic development of S. officinalis is arbitrarily subdivided into 30 stages based on major morphological changes (Lemaire, 1970). Organogenesis and neurogenesis start at around stage 12 and quickly form the nervous system with all of its components (Figure 1c) including the sensory organs and sensory cells (Baratte & Bonnaud, 2009;Buresi et al, 2014;Darmaillacq, Lesimple, & Dickel, 2008;Imarazene, Andouche, Bassaglia, Lopez, & Bonnaud-Ponticelli, 2017;Shigeno, Kidokoro, Tsuchiya, Segawa, & Yamamoto, 2001a;Shigeno, Tsuchiya, & Segawa, 2001b;Yamamoto, Shimazaki, & Shigeno, 2003), the integrative centers (Aroua, Andouche, Martin, Baratte, & Bonnaud, 2011;Buresi et al, 2014), and the connection of motor fibers to their target organs (Baratte & Bonnaud, 2009) early during organogenesis (Romagny, Darmaillacq, Guibe, Bellanger, & Dickel, 2012) soon after the differentiation of the associated sensory neurons ( Figure 1d). As we aimed to describe the distribution of HAergic neurons, this early sensory system development, in addition to the cephalopod's direct development life history, makes late-stage embryos (stages 27-30) a convenient model for sensory system and CNS observations.…”

“…AcTub, a posttranslational modification of α-tubulin, specific to ciliated cells and neurons (Howes, Alushin, Shida, Nachury, & Nogales, 2014), was labeled using a mouse monoclonal antibody (clone 6-11B-1, Sigma-Aldrich Cat# T6793, RRID: AB_477585). This antibody has been used in studies on a variety of invertebrates, including molluscs (Shigeno and Yammamoto, 2002;Todt, Büchinger, & Wanninger, 2008;Baratte & Bonnaud, 2009;Wollesen, Loesel, & Wanninger, 2009;Romagny et al, 2012;Rawlinson, 2010;Buresi et al, 2014). Anti-AcTub was paired with the goat anti-mouse, Alexa Fluor 488 secondary antibody (Thermo Fisher Scientific Cat# A28175, RRID: AB_2536161).…”