THE CUTICLE

General info - Body cuticle surface morphology - Body cuticle composition and layer organization - Cuticle generated by other tissues - Cuticle production and molting - Cuticle attachment complexes - Back to Contents

General information

The outer surface of the animal is covered by a tough, but flexible, multi-layered, extracellular cuticle (See CutFIG1). The cuticle protects the animal from the environment, maintains body shape and permits motility by acting as an external skeleton. Cuticle is secreted by the epithelial cells covering the body (hypodermis, seam cells) and by interfacial cells lining the four major openings to the exterior (anus, excretory pore, vulva and pharynx). The cuticle surface is covered with a surface coat (glycocalyx) that is thought to be secreted by gland cells (the excretory cell, pharyngeal gland cells or the amphid and phasmid support cells) (Nelson et al., 1983; Jones and Baillie, 1995). At each larval stage an entirely new cuticle is generated and the old cuticle is shed, allowing for growth. Significantly, cuticles of different stages differ in their surface protein expression, layer number, relative thickness and composition, presumably to accommodate for the changing developmental needs and environmental conditions experienced by the animal during its life.

Body cuticle surface morphology

The cuticle surface bears shallow, circumferential-oriented furrows (CutFIG1, 2A, 2B; Chitwood and Chitwood, 1950; Cox et al., 1981a). The cuticular ridges that lie between the furrows are called annuli. In L1, dauer and adult cuticles annulations are interrupted laterally by longitudinally-oriented ridges called alae that are generated by cells of the lateral seam beneath (Specialized epithelial cells Part I - Seam cells) (CutFIG1, 2B). The cuticle surface is also marked by holes and swellings where some neuronal cilia are exposed to the exterior (e.g., amphids (AM) and inner labial (IL) sensory organs CutFIG2A) or lie just beneath the surface, respectively (e.g., the outer labial (OL) sensory organs CutFIG2A or deirids CutFIG2B; see also Sensory Organ Table in Nematode Body Shape) .

Body cuticle composition and layer organization

Layers: The cuticle shows substantial organization into layers or zones that differ in structure and composition. Layers can be distinguished in EM cross-section as well as en face by several modalities (e.g., thin section and deep etching)(CutFIG3, 4A, 4B). The adult cuticle is approximately 0.5 micrometer in thickness (Cox et al., 1981a) and is organized into five major layers or zones: the surface coat (Sc), the epicuticle (Ep) layer and the cortical (Co), medial (Md) and basal (Bs) zones (Cox et al., 1981a; 1981b, Bird and Bird, 1991). The basal zone contains fibril layers (Fl).

Composition: The different layers of the cuticle likely consist of distinct molecular assemblies that impart different qualities. The wide range of phenotypes associated with mutations in cuticle components genes suggests a high degree of functional specialization among cuticle proteins and the layers they contribute to. Mutant phenotypes range from abnormal surface epitope expression (surface antigenicity abnormal phenotype) and pathogen resistance (e.g. bacterially unswollen) to altered body shape (roller, dumpy, squat, long) or abnormal cuticle morphology (blister) (Brenner, 1974; Kusch and Edgar 1986; Higgins and Hirsh, 1977; Kramer and Johnson, 1993; Politz et al., 1990; Link et al., 1992; Hodgkin et al., 2000). The most abundant structural components of cuticle are collagens and the non-collagenous cuticulins (Kramer, 1997;Sebastiano et al., 1991; Lewis et al., 1994). These molecules assemble into the relatively insoluble, higher-order complexes that form the cuticle matrix. Collagens COL-19 (CutFIG4C) and BLI-1(CutFIG4D) localize to the cortical layer (Liu et al., 1995; Thein et al., 2003) and medial layer struts, respectively, of the adult cuticle (Crew and Kramer, 1998); DPY-7(CutFIG4E) localizes to the furrows in cuticles of all stages (McMahon et al., 2003). Though few have been characterized, the cuticle probably also contains many soluble proteins such as enzymes involved in post-secretion modification and cross-linking of matrix proteins or structural proteins associated with the surface coat (e.g. mucins). Lipids and glycolipids are found in the epicuticle layer, an atypical membrane. Carbohydrates are associated with glycosylated proteins of the matrix and of the surface coat (Blaxter and Robertson, 1998).

Larval stage cuticles differ from adult in the type of layers present or their relative thickness (CutFIG5). The dauer cuticle is further distinguished from those of other stages in being less permeable and proportionally thicker (10.2% of the animal's cross sectional area c.f. 4.4% for other stages) due to a reduction in body diameter and an increase in epicuticle layer thickness (Cassada and Russell, 1975; Cox et al., 1981b). Even within a single stage the thickness of certain zones may change with age, for example, the basal zone appears to expand in aging adults (Herndon et al., 2002).

Cuticle generated by other tissue

The major openings of the animal are also cuticle-lined: the buccal cavity and pharynx (ALIMENTARY SYSTEM - (Part I) The Pharynx), the vulva, the rectum (ALIMENTARY SYSTEM - (Part III ) The Rectum & Anus) and the excretory duct and pore (EXCRETORY SYSTEM). These cuticles are secreted by underlying cells that are generally epithelial although, in the case of the buccal cavity and pharynx, other cell types may contribute (hypodermal, arcade and pharyngeal epithelial, muscle and marginal cells). In contrast to body cuticle, cuticles lining the openings do not appear to be composed of layers. However, some contain specialized cuticular elements. The pharyngeal cuticle provides the most striking examples and contains at least four different cuticular element (bridging cuticle, flaps, grinder, sieves and channels) each with potentially specialized roles (for transverse views see CutFIG6A-D; Albertson and Thomson, 1976; Wright and Thomson, 1981).

The excretory duct and pore cuticle also contains regions of distinctive patterning (CutFIG7A, 7B) which may strengthen the pore and help to keep it open.

Cuticle production and molting

The first cuticle, the L1 cuticle, is laid down at the time of embryo elongation. Contraction of circumferential actin filament bundles (AFB), which lie beneath the surface of the hypodermal apical membrane, induce elongation of the embryo and simultaneously produces ridges and furrows in the hypodermis and an overlying lipid layer called the embryonic sheath (Priess and Hirsh, 1986). This surface is thought to serve as a template for cuticle annulations (Costa et al., 1997; CutFIG8A). A similar contractile mechanism may be employed to pattern later stage cuticles and, possibly, the formation of alae.

Following hatching there are four post-embryonic molts whereby an entirely new cuticle is synthesized and the old cuticle is shed. The new cuticle is laid down beneath the existing cuticle - outer layers synthesized first, inner layers last. Seam cells, and to a lesser extent hypodermal cells, acquire large Golgi and have vesicles containing densely-staining material, consistent with the notion that high levels of protein synthesis and secretion occur at this time (Singh and Sulston, 1978). The new cuticle is initially highly convoluted and lies over hypodermal folds known as plicae(CutFIG8B).

Consistent with the cyclic nature of the molting process, synthesis of cuticle components is low between molts and high prior to molts (Cox et al, 1981c). Transcriptional analysis of collagen gene activity reveals multiphasic waves of early (e.g. dpy-7), middle (sqt-1,dpy-13) and late (col-12). It is hypothesized that collagens which are produced co-temporally may be incorporated into the same heteromeric complex or cuticle substructure (Cox et al, 1981c; Cox and Hirsh, 1985; Park and Kramer, 1994; Johnstone and Barry, 1996; McMahon et al., 2003). Some cuticle proteins are synthesized at every molt (e.g. COL-12) while others are stage-specific e.g., adult-specific COL-19 and BLI-1(shown in CutFIG4C, 4D above).

Molting consists of two phases: lethargus, the period of inactivity preceding cuticle shedding, and ecdysis, cuticle shedding (Singh and Sulston, 1978). In the first half of lethargus pumping and locomotion decreases and seam cells lose their granular appearance. Immobility is thought to result from the separation of the basal zone in the old cuticle from the underlying hypodermis. Loosening of the old cuticle begins around the head, then in the buccal cavity and the tail. In the second half of lethargus the worm begins to spin and flip around its long axis. The pharynx contracts and its cuticle lining breaks; the posterior half passes into the intestine and the anterior half is expelled and shed with the body cuticle. Reflactile granules are apparent in the pharyngeal gland cell processes at this time and are thought to play a role in ecdysis. As in insects, molting in C. elegans appears to be regulated by nuclear hormone receptors (Kostrouchova et al., 1998, 2001).

Cuticle attachment complexes

Locomotion requires the transmission of contractile force from body wall muscle to the cuticle. This force is transmitted through a series of mechanical linkages connecting body wall muscle, basement membrane, hypodermis and cuticle (See CutFIG9A-9C). The inner layer of the cuticle is attached to the apical hypodermal membrane through electron-dense attachment complexes called hemidesmosome from which intermediate filaments (MUP-6) extend into the cytoplasm. Similar complexes are also observed on the basal hypodermal membrane and when apical and basal complexes are in register a fibrous organelle (FO) is formed. Anchoring fibrils extend from FOs into the extracellular basal lamina (basement membrane), which is linked, in turn, to muscles through the M line and dense bodies of the sarcomere ( Francis and Waterston, 1991; Hresko et al., 1994, 1999; Bercher et al., 2001; Hong et al., 2001; Hahn and Labouesse, 2001). Similar hemidesmosomal complexes are also associated with non-body wall muscles (e.g. of the vulva and rectum) and with non-muscular cells that also make tight transhypodermal contact with the cuticle such as the excretory pore, touch neuron processes, amphids and phasmids (Bercher et al., 2001).


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