Nonstriated Muscle

  1) Nematode Nonstriated (Single Sarcomere) Muscle

Unlike the obliquely striated somatic muscles, which contain several to many sarcomeres repeating in regular order in one cell, nematode nonstriated muscles have either one or a few well-structured sarcomeres or myofilament networks that are less well organized. This group of muscles, also referred to as single-sarcomere muscles, includes pharyngeal, stomatointestinal, anal sphincter, anal depressor, contractile gonadal sheath, and sex-specific muscles. (For more inforamtion, see also Pharynx, Intestine, Rectum and Anus, Male-specific Muscles, Somatic Gonad, Muscle System of the Male and Dauer Pharynx.) In those that contain a single sarcomere, such as pharyngeal, anal depressor, and vulval muscles, the attachment points of the single sarcomere are localized at the ends of the cells as half I bands ending in electron-dense attachments or hemiadherens junctions and connect the myofilaments to epithelium or basal lamina. In other nonstriated muscles where the myofilament network is less well organized, such as uterine muscle um2 and contractile gonadal sheath (see also Egg-laying Apparatus and Somatic Gonad), the filaments seem to be attached to the plasma membrane via randomly localized electron-dense attachments, similar to those found in vertebrate smooth muscle.

  2) Pharyngeal Muscles

This group is comprised of 20 cells located in eight distinct divisions, pm1âpm8, in the pharynx (MusFIG 17; PharynxAtlas). Each pharyngeal muscle (pm) division contains one to three muscle cells (see Alimentary System - Overview) and each division, except the most posterior one, has threefold radial symmetry. Pharyngeal muscle cells are thought to be myoepithelial because, along with arcade cells, they secrete the pharyngeal cuticle. Also, they have clearly defined apical regions adjacent to the lumen cuticle and are bound by zonula adherens junctions. Contraction of pharyngeal muscle cells in general serves to open the lumen. In the first five layers (pm1âpm5), radially oriented filaments attach medially to the cuticle of the lumen and laterally to the pharyngeal basal lamina by hemiadherens junctions (these are labeled âhalf-desmosomesâ in Albertson and Thomson, 1976), which are characterized by an electron-dense deposit on the cytoplasmic face of the plasma membrane (Albertson and Thomson, 1976). pm6 has three posterior projections that extend into pm7, and filaments are excluded from the middle one of these projections. pm7 cells contain both radially and longitudinally oriented filaments that provide a longitudinal, aswell as a radial, component to the motion of the grinder teeth when they contract. Similar to pm1âpm5, pm8 has radially oriented filaments that attach to the lumenal cuticle and the pharyngeal basal lamina at their ends. All muscles except pm8 are innervated by pharyngeal motor neurons. pm8 does not receive any direct  innervation from any of the motor neurons. However, pm8 makes gap junctions to mc3 cells, which are innervated by the M5 neuron (Albertson and Thomson, 1976; White, 1988) (see Alimentary System - Overview and Pharynx, see also Gap Junctions).



  3) Stomatointestinal Muscles

Stomatointestinal (SI) muscles are two sheet-like cells that connect the surfaces of the intestinal cells to the ventral body wall (MusFIG 18; MusMOVIE 3) (Bird and Bird, 1991; Avery and Thomas, 1997). Some longitudinally oriented filaments are located in the ventral regions of the cells, and their attachment structures toward the intestine probably resemble the vertebrate smooth muscle as randomly placed along the cell length (White et al., 1986). Thin, flat processes of these cells wrap around the posterior regions of the intestine on the dorsal side. These processes contain a few vertically oriented myofilaments that attach to the dorsal body wall by  hemiadherens junctions, just lateral to the dorsal body wall muscles. The stomatointestinal muscles send muscle arms to preanal ganglion where they receive synaptic input from DVB (direct input) and AVL (indirect input) neurons. They are electrically coupled to the anal sphincter and anal depressor muscles via gap junctions (see also Gap Junctions). Contraction of these muscles promotes defecation by pressurizing the intestinal contents near the posterior end of the intestine (see also Alimentary System - Intestine).

  4) Anal Depressor Muscle

This is a large, single-sarcomere, H-shaped muscle in hermaphrodites that runs vertically between the dorsal wall of the rectum and the dorsal hypodermis (MusFIG 18 and MusFIG 19) (Thomas, 1990; Avery and Thomas, 1997). This muscle lifts the roof of the rectum when it contracts, allowing the rectum to fill during initial stages of defecation. Later, during defecation it relaxes and the contents of the rectum are expelled (Bird and Bird, 1991). The contractile elements are organized as two parallel sheets of filaments on the right and left sides of this cell, forming two vertically arranged, single sarcomeres. This muscle sends a long muscle arm to the preanal ganglion to be innervated by the DVB (directly) and AVL (indirectly) motor neurons (see also Alimentary System - Intestine).

This muscle is sexually dimorphic between hermaphrodite and male. In males, the contractile apparatus of the anal depressor detaches from the dorsal hypodermis and attaches to the dorsal spicule protractor during the L4 molt, completely reorienting the myofilaments to run anteroposteriorly instead of dorsoventrally (Male-specific Muscles) (Sulston and Horvitz, 1977; Sulston et al., 1980; White, 1988).

  5) Anal Sphincter Muscle

This is a single cell with a toroidal region encircling the proximal part of the rectum and about eight thin processes that radiate  medially and laterally from this toroid. These include four long, filament-filled processes that extend laterally to anchor to the body wall on the dorsal and ventral sides (MusFIG 18 and MusFIG 20). The anal sphincter muscle circles the intestine at its junction with the rectum. During defecation, it is dilated before enteric muscle contractions occur to allow waste material to pass into the rectum. It then contracts nearly simultaneously with the other enteric muscles, possibly helping to squeeze the posterior intestine for expulsion of the waste (Reiner and Thomas, 1995; Avery and Thomas, 1997). The toroidal part of the muscle contains a continuous ring of contractile filaments, many of which do not seem to connect to any significant end-point attachment structures. In this aspect, it is thought to be similar to vertebrate smooth muscle (White, 1988). Filaments within the medially projecting, short processes occasionally show electron-dense attachments to the gland cells at the roof and floor of the rectal passageway (MusFIG 20) (see also Alimentary System - Intestine and Rectum and Anus).

This muscle is sexually dimorphic between hermaphrodite and male. In males, near the end of the L4 stage the muscle goes under a dramatic hypertrophy during the opening of a cloacal canal. In contrast to hermaphrodites and larval males, this modified sphincter must relax in males to permit defecation (see Male-specific Muscles) (Reiner and Thomas, 1995; Emmons and Sternberg, 1997).

  6) Vulval Muscles

The two sets of vulval muscles are vm1 and vm2, and each set contains four muscle cells with single sarcomeres (MusFIG 21). Both vulval and uterine muscles in the hermaphrodite are born at the late-L3 stage from two sex myoblasts, M.vlpaa and M.vrpaa. Through three consecutive divisions, each sex myoblast generates two sets (vm and um) of four daughters, with a total of 16 cells located around the developing vulva by the L3 molt. Eight of these comprise the vulval muscles. The four vm1 muscles insinuate between rows of ventral body wall muscles and run between the dorsal edge of the ventral body wall muscle quadrant and the vulC and vulD toroids of vulva (White et al., 1986). The four vm2 muscles run between the ventral margin of the body wall muscle quadrants and the uterusâvulva junction (between the uterus and vulF toroid). Hence, vm1 cells attach to the vulva more ventrally than do vm2 and are more superficial (Sulston and Horvitz, 1977). The single sarcomeres of each vulval muscle stretch along the entire muscle length and attach through hemiadherens junctions to discrete zones in the body wall on one end and to the vulval epithelium and vulval cuticle on the opposite end around the late-L4 stage (White, 1988). The nuclei of the sex muscles also settle into their final positions around the developing gonad at the L4 stage. Among vulval muscles, the vm2s are the only ones that are directly innervated by the VC and HSN neurons of the egg-laying circuitry. The other muscles are either directly or indirectly connected to vm2 by gap junctions (see also Gap Junctions). vm2s send muscle arms to a local neuropil on either side of the hypodermal ridge to receive synaptic input (White, 1988). Coordinated contraction of the vulval muscles expands the uterus and pulls the vulval lips apart, opening the passage for eggs to be expelled (Hodgkin, 1988) (see also Reproductive System - Egg-laying apparatus). Nematodes missing all eight vulval muscles are unable to lay eggs (Bird and Bird, 1991).

  7) Uterine Muscles

There are two sets of uterine muscles, um1 and um2, with four post-embryonically born muscle cells in each set. Each um1 cell makes a quarter of a circle that cups the proximal uterus on the ventral side and attaches to it close to the vulva (MusFIG 22). Dorsally, these cells attach to the lateral seam cells close to the utse-seam attachment sites (Vogel and Hedgecock, 2001; Woo et al., 2004). In each half (left and right sides) uterus, the distal sets of uterine muscle cells (um2) make half circles that wrap around the uterus and attach to it in a region further from the vulva (Sulston and Horvitz, 1977). The filaments of the uterine muscles are circumferentially oriented, which, when the muscle contracts, may move eggs through the uterus by a squeezing action (Sulston and Horvitz, 1977). This myofilament network seems to be anchored to the thin basal lamina on the surface facing the uterus by randomly placed attachment points, similar to the distribution of the dense bodies in vertebrate smooth muscles (MusFIG 1D). There is no direct innervation of the uterine muscles. Instead, they are coupled via gap junctions to vulval muscles (White et al., 1986) (see also Reproductive System - Egg-laying apparatus and Gap Junctions). Nematodes missing all eight uterine muscles are still able to lay eggs, as has been shown by ablation studies (Bird and Bird, 1991).



  8) Contractile Gonad Sheath of the Hermaphrodite

Five pairs of gonadal sheath cells have stereotyped positions along the proximalâdistal axis of the gonad and cover the germ-line tissue of each gonadal arm (see MusFIG 17 and Reproductive System - Somatic gonad). Sheath cell pairs 3, 4, and 5 abundantly express muscle filament components such as actin and myosin that are organized into dense networks (Hirsh et al., 1976; Strome, 1986; Goetinck and Waterston, 1994; McCarter et al., 1997; Hall et al., 1999). Filaments are predominantly longitudinally oriented in pairs 3 and 4 and both longitudinally and circumferentially oriented in pair 5 (MusFIG 18). Filaments are also present in sheath cells 1 and 2, but are much less abundant. The myofilament network of the contractile gonadal sheath is possibly similar in organization to that of vertebrate smooth muscle. Anchorage points for the myofilament lattice are distributed diffusely over the outward-facing cell surface. Each connects to the nearby basal lamina by an electron-dense attachment on the plasma membrane. During ovulation, contraction of the proximal sheath pulls the dilated spermatheca over the most proximal oocyte and hence transfers this oocyte into the spermatheca for fertilization. The sheath is not innervated. Instead, it contracts periodically, possibly in response to recurrent intracellular Ca++ transient currents (Bui and Sternberg, 2002, and references therein) (see Reproductive System - Somatic gonad). Gap junctions connect the sheath cells to one another, and transitory gap junctions connect the sheath to the primary oocyte (Hall et al., 1999) (see also Gap Junctions). Thus, signals between the germ line and sheath may coordinate sheath contractions to events in the oocyte and to the presence of sperm (McCarter et al., 1999; Miller et al., 2001; 2003).

  9) List of Nonstriated Muscle Cells

i. Pharyngeal muscles (pm); Note that in earlier publications these cells are labeled as "m"; m1, m2, m3 etc., here they are labeled "pm" for " p haryngeal m uscle" ( Avery L. and Thomas J. H., 1997 )

1. First pharyngeal muscle ring; all fuse into one syncytium around hatching

pm1DL

pm1DR

pm1L

pm1R

pm1VL

pm1VR

2. Second pharyngeal muscle ring

pm2DL; fuses with DR around hatching

pm2DR; fuses with DL around hatching

pm2L; fuses with VL around hatching

pm2R; fuses with VR around hatching

pm2VL; fuses with L around hatching

pm2VR; fuses with R around hatching

3. Third pharyngeal muscle ring

pm3DL; fuses with DR around hatching

pm3DR; fuses with DL around hatching

pm3L; fuses with VL around hatching

pm3R; fuses with VR around hatching

pm3VL; fuses with L around hatching

pm3VR; fuses with R around hatching

4. Fourth pharyngeal muscle ring

pm4DL; fuses with DR around hatching

pm4DR; fuses with DL around hatching

pm4L; fuses with VL around hatching

pm4R; fuses with VR around hatching

pm4VL; fuses with L around hatching

pm4VR; fuses with R around hatching

5.Fifth pharyngeal muscle ring

pm5DL; fuses with DR around hatching

pm5DR; fuses with DL around hatching

pm5L; fuses with VL around hatching

pm5R; fuses with VR around hatching

pm5VL; fuses with L around hatching

pm5VR; fuses with R around hatching

6. Sixth pharyngeal muscle ring

pm6D

pm6VL

pm6VR

7. Seventh pharyngeal muscle ring

pm7D

pm7VL

pm7VR

8. Eighth pharyngeal muscle ring

pm8

ii. Enteric muscles

1. Stomatointestinal muscle

mu intL; ABplpppppaa

mu intR; MSppaapp

2. Anal sphincter muscle 

mu sph; ABprpppppap

3. Anal depressor muscle

mu anal; ABplpppppap

iii. Hermaphrodite sex muscles

1. vm1

M.vrpaapaa

M.vrpaaapp

M.vlpaapaa

M.vlpaaapp

2. vm2 

M.vrpaapap

M.vrpaaapa

M.vlpaapap

M.vlpaaapa

3. um1 

M.vrpaappa

M.vrpaaaap

M.vlpaappa

M.vlpaaaap

3. um2

M.vrpaappp

M.vrpaaaaa

M.vlpaappp

M.vlpaaaaa

iv. Hermaphrodite contractile gonadal sheath

1. Somatic Sheath (10 cells/5 pairs) of anterior gonad arm: Z1.apa (sheath cell 1) 

Z1.appaaa (sheath cell 2) 

Z1.appaap (sheath cell 3) 

Z1.appapa (sheath cell 4) 

Z1.appapp (sheath cell 5) 

Z1.paaa (sheath cell 1) 

Z1.paapaaa (sheath cell 2) 

Z1.paapaap (sheath cell 3) 

Z1.paapapa (sheath cell 4) 

Z1.paapapp (sheath cell 5)

2. Somatic Sheath (10 cells/5 pairs) of posterior gonad arm: Z4.pap (sheath cell 1) 

Z4.paappp (sheath cell 2) 

Z4.paappa (sheath cell 3) 

Z4.paapap (sheath cell 4) 

Z4.paapaa (sheath cell 5) 

Z4.appp (sheath cell 1) 

Z4.appappp (sheath cell 2) 

Z4.appappa (sheath cell 3) 

Z4.appapap (sheath cell 4) 

Z4.appapaa (sheath cell 5)

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