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The Caenorhabditis elegans epidermis as a model skin. II: differentiation and physiological roles

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Abstract The Caenorhabditis elegans epidermis forms one of the principal barrier epithelia of the animal. Differentiation of the epidermis begins in mid embryogenesis and involves apical–basal polarization of the cytoskeletal and secretory systems as well as cellular junction formation. Secretion of the external cuticle layers is one of the major developmental and physiological specializations of the epidermal epithelium. The four post‐embryonic larval stages are separated by periodic moults, in which the epidermis generates a new cuticle with stage‐specific characteristics. The differentiated epidermis also plays key roles in endocrine signaling, fat storage, and ionic homeostasis. The epidermis is intimately associated with the development and function of the nervous system, and may have glial‐like roles in modulating neuronal function. The epidermis provides passive and active defenses against skin‐penetrating pathogens and can repair small wounds. Finally, age‐dependent deterioration of the epidermis is a prominent feature of aging and may affect organismal aging and life span. WIREs Dev Biol 2012 doi: 10.1002/wdev.77 This article is categorized under: Early Embryonic Development > Development to the Basic Body Plan Invertebrate Organogenesis > Worms

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The epidermal basal lamina, and neuronal development. (a) Cross‐section of adult body showing epidermis and adjacent tissues and structures. The external surface is covered by the cuticle; the internal face is covered by basal lamina (BL, red). Neurons (brown) reside on the epidermal side of the BL; the positions of the major nerve tracts relative to the dorsal and ventral epidermal ridges are shown. (b) Biogenesis of BL. The majority of known BL components are synthesized in muscles; the composition of the muscle‐adjacent BL is likely distinct from that of non‐muscle adjacent BL. (c) Developing axons appear to use the epidermis rather than the BL as substrate, as they are seen to pass on the epidermal side of other axons (R. Durbin, Ph.D thesis). (d) Sensory axons have a close relationship with the epidermis. Mechanosensory processes become progressively confined within the epidermis and secrete a specialized extracellular matrix (ECM), the mantle.

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Development of epidermal polarity and cytoskeletal systems. (a) Overview of development of polarity and epidermal features, based on Ref 2. With a few exceptions, the order and dependency of the various polarization processes are not clearly established in the epidermis. All early embryonic blastomeres express classical cadherin/HMP‐1 and LET‐413/Scribble; outer blastomeres are contacted externally by the vitelline envelope. Epithelial differentiation begins with the onset of DLG‐1 and AJM‐1 expression in the premorphogenetic epidermis. In the early epidermis DLG‐1 and AJM‐1 are punctate and localized over the lateral surface. As the epidermis matures, DLG‐1 and AJM‐1 become confined to the subapical region to form adherens junctions (AJs), and LET‐413 becomes basolaterally localized. PAR‐3 and PAR‐6 become apically localized in the epidermis, but are not essential for all aspects of apical–basal polarity. PAR‐6 functions independently of PAR‐3 to promote the assembly (but not localization) of the AJs. (b) Epidermal cytoskeletal systems. Actin filaments (light blue lines) are found in the cortical spectrin cytoskeleton and in large circumferential bundles linking cadherin–catenin junctions. Microtubules (green lines) become polarized circumferentially in the dorsal epidermis during dorsal intercalation. Subsequent nuclear migrations are directed toward microtubule plus ends. Intermediate filaments (pink) such as IFB‐1 are expressed in dorsal and ventral epidermal cells after enclosure and link apical and basal hemidesmosomes in muscle‐adjacent regions of the epidermis.

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Epidermal responses to infection, wounding, and stress. (a) Pathways implicated in responses to infection by Drechmeria coniospora. Drechmeria spores adhere to the cuticle and extend hyphae that penetrate the epidermis.160 A signal transduction pathway involving PKC, the SARM ortholog TIR‐1, and the p38 MAPK cascade is involved in upregulation of transcription of the nlp‐class AMPs.161,162 A G‐protein coupled receptor may be involved early in recognition of damage, as the same pathway is activated by sterile wounding; conversely, the Tribbles‐like kinase is required for the response to infection but not to wounding. The GATA factor ELT‐3 appears to be permissive for nlp upregulation.163 Drechmeria infection also triggers transcription of caenacin AMPs; cnc induction is partly independent of the p38 MAPK cascade and involves a non‐cell‐autonomous TGFβ signal, possibly from neurons.164 (b) Epidermal wounding by microinjection needle or laser irradiation triggers expression of the NLP‐type AMPs, via a pathway similar to that involved in Drechmeria responses, but does not induce the cnc genes.74 A Gαq‐PLCβ‐Ca2+ signaling pathway is involved in wound closure after puncture wounding165; DAPK‐1 can negatively regulate both the innate immune response pathway and the wound closure pathway. (c) Infection by the bacterium M. nematophilum induces swelling of rectal epidermal cells. Genes required for bacterial adhesion are likely involved in biogenesis of the surface coat and/or epicuticle. M. nematophilum infection triggers expression of a variety of genes, some of which are involved in the epidermal swelling response.166 Swelling requires phospholipase C β (EGL‐8)155 and the ERK MAPK cascade167; it is not known if all transcriptional responses are ERK‐dependent. (d) Osmotic stress may be sensed by structures at cuticle furrows coupled to epidermal cell surface receptors. Epidermal responses to hyperosmotic shock include elevated transcription of gpdh‐1 (leading to glycerol accumulation) and expression of a subset of AMPs.168

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Stages, pathways, and tissues involved in molting. (a) Molts have been divided into three main stages: apolysis, cuticle synthesis, and ecdysis. Some genes may be involved in more than one stage. Proteases such as CPZ‐1 are involved in apolysis. Ecdysis (separation of old cuticle) also involves a complex set of motor behaviors not depicted here. (b) Genetic pathways regulating molting. Highly speculative outline of possible regulatory relationships, partly based on Ref 114. Not all regulatory interactions may apply to all molts. (c) Tissue coordination during molts. The focus of LIN‐42A function in molting appears to be in the lateral seam. LIN‐42A might directly or indirectly regulate epidermal quiescence signals such as LIN‐3 and OSM‐7/11, which act on neurons. Quiescence involves decreased muscle contractions, which in turn may affect expression of epidermal molting genes.115

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Cuticle structure and secretory apparatus. (a) Schematic cross‐sections of cuticle in different larval stages and dauer; the surface coat is likely present in all stages but may differ in composition. (b) Aspects of polarized secretion and endocytic pathways in the epidermis. Cuticle collagens are thought to be secreted through classical apical secretory pathway. Large dense‐cored vesicles have been reported in the epidermis prior to molting, but may differ from the dense‐core vesicles characterized in neurons. The epidermis is abundant in MVBs, involved in exosome‐based secretion of hedgehog family proteins such as the WRTs.72 The V0 ATPase subunit VHA‐5 may function in MVB fusion with the apical membrane; VHA‐5 is also localized to the prominent apical membrane stacks, of unknown function. Ellipsoidal organelles dubbed ‘Ward bodies' contain membranous stacks; they have been observed in electron micrographs but are of unknown function.

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