MESODERMAL ORGANS- Nonstriated Muscle (Part III)

Nonstriated muscles - Pharyngeal muscles - Stomatointestinal muscles - Anal sphincter muscle- Anal depressor muscle - Vulval muscles - Uterine muscles - Gonadal sheath - Male nonstriated muscles- Cell list - Back to Contents

Nonstriated (single sarcomere) muscles

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 have myofilament networks that are less well organized. This group includes pharyngeal muscles, stomatointestinal muscles, anal sphincter, anal depressor, contractile gonadal sheath and sex-specific muscles. In those that contain a single sarcomere, such as pharyngeal muscle, anal depressor muscle and vulval muscles, the attachment points of the single sarcomere are localized at the ends of the cells as half I bands ending in hemidesmosomes and connect the myofilaments to epithelium or basal lamina (MusFIG13a, 13b, 13c and MusFIG14a, 14b. Also see EggFig14c in Reproductive system Part IVb). In other nonstriated muscles where the myofilament network is less well organized, such as um2 and contractile gonadal sheath, the filaments seem to be attached to the plasma membrane via randomly localized hemidesmosomes similar to those found in vertebrate smooth muscle (See MusFIG11 in Part I).

Pharyngeal muscles

[20 cells]. There are eight distinct muscle divisions in the pharynx, each containing one to three muscle cells (MusFIG16). Each division except the most posterior one has threefold radial symmetry. Pharyngeal muscle cells are thought to be myoepithelial since, along with arcade cells, they secrete the pharyngeal cuticle and they have clearly defined apical regions adjacent to the lumen cuticle and are bound by belt desmosomes. Contraction of pharyngeal muscle cells serves to open the lumen. In the first five layers (pm1-5) radially oriented filaments attach medially to the cuticle of the lumen and laterally to the pharyngeal basal lamina by hemidesmosomes (in Albertson D. J. and Thomson J. N., 1976 these are labeled as "half-desmosomes") which are characterized by enlargement and darkening of the interior margin of the basement membrane (Albertson D. J. and Thomson J. N., 1976)(MusFIG17a, 17b and 17c). 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 as well as longitudinally oriented filaments which provide a longitudinal, as well as a radial component to the motion of the grinder teeth when they contract. Similar to pm1-5, 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 M5 neuron (White J., 1988; Albertson D. J. and Thomson J. N., 1976) (Also see Pharynx Part Ia).

Stomatointestinal muscles

[2 cells]. These are two sheet-like cells that connect the surfaces of the intestinal cells to the ventral epidermis (Bird A. F. and Bird J., 1991; Avery L. and Thomas J. H.,1997)(RectFIG1 and MusFIG18). These muscles have few, longitudinally oriented filaments which are located in the ventral regions of the cells (White J. et al., 1986) and their attachment structures probably resemble the vertebrate smooth muscle as randomly placed along the cell length. Dorsally, thin, flat processes from these cells wrap around the posterior regions of the intestine and contain a few vertically oriented myofilaments which attach to the dorsal body wall by hemidesmosomes, just lateral to the dorsal body wall muscles. The stomatointestinal muscles send muscle arms to preanal ganglion where they receive synaptic input from excitatory GABAergic DVB neuron. They are electrically coupled to the anal sphincter and anal depressor muscles via gap junctions. Contraction of these muscles promote defecation by pressurizing the intestinal contents near the posterior end of the intestine. Also see Alimentary system Part III.

Anal sphincter muscle

[1 cell, sexually dimorphic between hermaphrodite and male]. This is a single toroidal cell that 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 J., 1988). Some filaments from the major contractile ring, however, extend posteriorly and indent into the rectal gland cells. These fibers have hemidesmosomal attachments to the gland cells at the roof and floor of the rectal passageway. The anal sphincter muscle circles the intestine at its junction with the rectum (RectFIG1 and MusFIG19). It is dilated prior to the enteric muscle contractions during defecation and contracts near simultaneously with the other enteric muscles, possibly acting to further squeeze the posterior intestine (Reiner D. J. and Thomas J. H., 1995; Avery L. and Thomas J. H.,1997). A minority of its myofilaments can extend into the cell's four thin processes and become anchored to the body wall. (Also see Alimentary system Part III).
In males, near the end of the L4 stage this muscle goes under a dramatic hypertrophy along with the opening of a cloacal canal. In contrast to hermaphrodites, this modified sphincter must relax in males to permit defecation. During ejaculation it closes off the intestine and pulls it dorsally out of the way of the vas deferens (MusFIG20a and 20b)(Reiner D. J. and Thomas J. H., 1995; Emmons S. W. and Sternberg P. W.,1997). For more information see see MUSCLES OF THE MALE-Part I and Part II.


Anal depressor muscle

[1 cell, sexually dimorphic between hermaphrodite and male]. 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 (Avery L. and Thomas J. H.,1997, Thomas J. H.,1990) (RectFIG1, MusFIG21a, MusFIG21b, MusFIG23a and MusFIG23b). This muscle lifts the roof of the rectum when it contracts, hence allowing the rectum to fill during initial stages of defecation. Later during defecation, it relaxes and the contents of the rectum are expelled (Bird A. F. and Bird J., 1991). The contractile elements are organized as two (left/right) sheets of filaments in this cell forming two vertically arranged, single sarcomeres (MusFIG23a). The center of each sarcomere corresponds to the middle of the cell. The neuromuscular synapse between the muscle arm of the anal depressor muscle and DVB neuron is restricted to the preanal ganglion where DVB also synapses onto the rectal epithelial cell. (Also see Alimentary system Part III).
In males, the anal depressor contractile apparatus detaches from the dorsal hypodermis and attaches to the dorsal spicule protractor during L4 molt, reorienting myofilaments to run anteroposteriorly in this muscle (MusFIG22a and 22b; note that in MusFIG22b only contractile elements are labeled) (Sulston and Horvitz H. R., 1977; Sulston et al., 1980; White J., 1988). For more information see see MUSCLES OF THE MALE-Part I and Part II.

Hermaphrodite vulval muscles

[8 cells, postembryonically born]. There are two sets of vulval muscles, vm1 and vm2, and each contains 4 cells, all of which have single sarcomeres (MusFIG24A-D). The vm1 muscles run between the dorsal edge of the ventral body wall muscle quadrant and the vulC and vulD toroids of vulva and insinuate between rows of ventral body wall muscles (White J. et al., 1986). The vm2 muscles run between the ventral margin of the body wall muscle quadrants and the junction of uterus and the vulva (between the uterus and vulF toroid). The single sarcomeres of vulval muscles stretch along the entire muscle length and attach to discrete zones in the body wall at one end and to the vulval epithelium and vulval cuticle at the other by hemidesmosomes at late L4 stage (White J., 1988)(MusFIG24B-D: Arrowheads indicate hemidesmosomes).  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. vm2s send muscle arms to the neuropil on either side of the hypodermal ridge to receive synaptic input (White J., 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 J. 1988). Nematodes missing all eight vulval muscles are unable to lay eggs. (Bird A. F. and Bird J., 1991). Also see Reproductive system Part IVb.

Hermaphrodite uterine muscles

[8 cells, postembryonically born]. In each half uterus, the distal set of two uterine muscle cells (um2) make a single, full band which wraps around the uterus and attaches to it in a region further from the vulva (Sulston and Horvitz, 1977)(MusFIG26). Each of the proximal set of two muscles (um1), on the other hand, make a half band which wraps around the proximal uterus on the ventral side and attaches to it close to the vulva (MusFIG25). Dorsally they attach to the lateral seam cells (aka uterine seam epidermis at this region) close to the utse-seam attachment sites (Vogel B. E. and Hedgecock E. M. 2001; Woo W.M. et al, 2004). 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 J. E. and Horvitz R. H., 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 (MusFIG12 in Part I). There is no direct innervation of the uterine muscles. Instead they are coupled via gap junctions to vulval muscles (White J. et al., 1986). Also see Reproductive system Part IVb. Nematodes missing all eight uterine muscles are still able to lay eggs as has been shown by ablation studies. (Bird A. F. and Bird J., 1991).

Hermaphrodite contractile gonadal sheath

[10 cells]. There are 5 pairs of gonadal sheath cells which have stereotyped positions along the proximal-distal axis of the gonad and cover the germ line tissue of each gonadal arm (MusFIG27). Sheath cell pairs #3 to #5 abundantly express muscle filament components such as actin and myosin which are organized into dense networks (Hirsh et al., 1976; Strome, 1986; McCarter et al., 1997; Goetinck and Waterston, 1994). Filaments are predominantly longitudinally oriented in pairs #3 and #4, and both longitudinally and circumferentially oriented in pair #5 (GonFig7b). Filaments are also present in the sheath cells #1 and #2 but are much less abundant. The myofilament network of the contractile gonadal sheath is also possibly similar to that of vertebrate smooth muscle in structure. Anchorage points for the myofilament lattice are distributed diffusely over the stretch of cell surface. Each connects to the neraby basal lamina by a hemidesmosome. 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 periodically contracts possibly in response to recurrent intracellular Ca++ transients (see Bui and Sternberg, 2002 and references therein). Also see Reproductive system Part II.

Male nonstriated muscles

C. elegans males have 41 specialized mating muscles all of which are nonstriated. These muscles are:
Diagonal muscles [15 cells - 7 on the left side, 8 on the right, postembryonically born]. All contain 3 sarcomeres per cell.
Longitudinal muscles [10 cells, postembryonically born]. 4 (A/P) outer longitudinal, 4 (A/P) inner longitudinal and 2 caudal outer longitudinal muscles. These contain several, well-structured sarcomeres that appear to orient in tandem to the ventral body wall muscles.
Spicule protractor and retractor muscles [8 cells; 4 protractors and 4 retractors, postembryonically born]. R/L and D/V pairs of spicule retractors and spicule protractors. All are single sarcomeric muscles.
Gubernacular muscles [4 cells, postembryonically born]. 2 gubernacular erectors and 2 gubernacular retractors. All are single sarcomeric muscles.
Postanal oblique muscles [4 cells, postembryonically born]. A/P and L/R pairs. All are single sarcomeric muscles.
For more information see MUSCLES OF THE MALE-Part I and Part II.

Cell List

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 "pharyngeal muscle" (Avery L. and Thomas J. H., 1997)

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

8. Eighth pharyngeal muscle ring

ii. Enteric muscles

1- Stomatointestinal muscle
mu intL
mu intR
2. Anal Sphincter muscle
mu sph
3. Anal depressor muscle
mu anal

ii. Hermaphrodite sex muscles

2. vm2
3. um1
3. um2

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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