skip to main content


Title: Diversity of extracellular matrix morphology in vertebrate skeletal muscle
Abstract

Existing data suggest the extracellular matrix (ECM) of vertebrate skeletal muscle consists of several morphologically distinct layers: an endomysium, perimysium, and epimysium surrounding muscle fibers, fascicles, and whole muscles, respectively. These ECM layers are hypothesized to serve important functional roles within muscle, influencing passive mechanics, providing avenues for force transmission, and influencing dynamic shape changes during contraction. The morphology of the skeletal muscle ECM is well described in mammals and birds; however, ECM morphology in other vertebrate groups including amphibians, fish, and reptiles remains largely unexamined. It remains unclear whether a multilayered ECM is a common feature of vertebrate skeletal muscle, and whether functional roles attributed to the ECM should be considered in mechanical analyses of non‐mammalian and non‐avian muscle. To explore the prevalence of a multilayered ECM, we used a cell maceration and scanning electron microscopy technique to visualize the organization of ECM collagen in muscle from six vertebrates: bullfrogs (Lithobates catesbeianus), turkeys (Meleagris gallopavo), alligators (Alligator mississippiensis), cane toads (Rhinella marina), laboratory mice (Mus musculus), and carp (Cyprinus carpio). All muscles studied contained a collagen‐reinforced ECM with multiple morphologically distinct layers. An endomysium surrounding muscle fibers was apparent in all samples. A perimysium surrounding groups of muscle fibers was apparent in all but carp epaxial muscle; a muscle anatomically, functionally, and phylogenetically distinct from the others studied. An epimysium was apparent in all samples taken at the muscle periphery. These findings show that a multilayered ECM is a common feature of vertebrate muscle and suggest that a functionally relevant ECM should be considered in mechanical models of vertebrate muscle generally. It remains unclear whether cross‐species variations in ECM architecture are the result of phylogenetic, anatomical, or functional differences, but understanding the influence of such variation on muscle mechanics may prove a fruitful area for future research.

 
more » « less
Award ID(s):
1832795
NSF-PAR ID:
10458763
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Journal of Morphology
Volume:
281
Issue:
2
ISSN:
0362-2525
Page Range / eLocation ID:
p. 160-169
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Hypophthalmichthys molitrix,silver carp, is an invasive Asian carp that has become increasingly widespread and ecologically destructive within the upper Mississippi River Basin. Its complex trophic anatomy may help explain the apparent efficiency with which they consume phytoplankton, outcompeting native filter feeders. This cypriniform species is characterized by trophic synapomorphies that include a palatal organ, loss of upper pharyngeal jaws, and a hypertrophied lower pharyngeal jaw. However, in silver carp these structures have become greatly modified and diverge from the more basal condition that characterizes species such as goldfish. The trophic apparatus of silver carp is composed of discrete structures that are functionally coupled: filtering plates, paired epibranchial organs (EBO), a modified palatal organ composed of large muscular folds that interdigitate with the filtering plates, and hypertrophied lower pharyngeal jaws and teeth. The filtering plates fill a significant portion of the buccal cavity, especially since the distal parts of these filtering plates make up a key component of the EBOs. EBOs, food aggregating structures found in many teleosts, are thought to have independently evolved at least six times. Ranging in complexity from small slits on the dorsal wall of the pharyngeal cavity to exceedingly intricate spiraling structures, EBOs are morphologically diverse among filter‐feeding fishes. Despite this morphological diversity and broad taxonomic distribution, little is known regarding the functional anatomy of the EBO. Moreover, the EBO in silver carp is distinct from the organs previously described in other species, being created by four independent pharyngeal involutions (instead of the more typical one or two) that form spiral‐shaped pharyngeal tubes surrounded by circumferential muscle. On each side of the head greatly hypertrophied hyomandibulae and opercles are connected to the anterior cartilaginous caps of the bilateral EBOs via enlarged muscles. Given that these fish are pump filter feeders we hypothesize that the opercula may compress and expand the EBOs during pumping causing food to be moved posteriorly toward the pharyngeal jaws.

     
    more » « less
  2. ABSTRACT

    Dissections of cetacean orbits identified two distinct circular muscle layers that are uniquely more elaborate than the orbitalis muscles described in numerous mammals. The circular orbital muscles in cetaceans form layers that lie both external and internal to the rectus extra ocular muscles (EOMs). A cone‐shaped external circular muscle (ECM) that invests the external surface of the rectus EOMs was found in all cetacean specimens examined. The cetacean ECM corresponds generally to descriptions of themusculus orbitalisin various mammals but is more strongly developed and has more layers than in noncetaceans. A newly identified internal circular muscle (ICM) is located internal to the rectus EOMs and external to the retractor bulbi (RB). The RB is massive in cetaceans and is encased in a connective tissue layer containing convoluted bundles of blood vessels. The most robust ECM and ICM layers were in sperm whale (Physeter macrocephalus) where they form complete rings. Surprisingly, histological analysis showed the sperm whale ECM to contain both smooth and striated (skeletal) muscle layers while the ICM appeared to contain solely skeletal muscle fibers. The extreme development of the ECM (orbitalis) and RB suggest a co‐evolved system mediating high degrees of protrusion and retraction in cetaceans. We know of no homolog of the ICM but its function seems likely related to the complex vascular structures surrounding and deep to the retractor muscle. Skeletal muscle components in orbital circular muscles appear to be highly derived specializations unknown outside of cetaceans. Anat Rec, 2019. © 2019 American Association for Anatomy Anat Rec, 303:1792–1811, 2020. © 2019 American Association for Anatomy

     
    more » « less
  3. ABSTRACT

    Muscles of the mesopelagic copepodGaussia princeps(Arthropoda, Crustacea, Calanoida) are responsible for repetitive movements of feeding and swimming appendages that are too fast to be followed by eye. This article provides a comparative functional and ultrastructural description of five muscles that have different contraction speeds and are located within different anatomical sites. All are very fast, as indicated by a thick:thin filament ratio of 3:1 and sarcomere lengths that vary between 1 and 3 μm. Measured lengths of thin and thick filaments indicate classification of the muscles into three distinct groups (short, medium, and long) and predict a difference in speed of up to threefold between fibers with the shortest and longest sarcomeres. Indeed, the kicking movement of the posterior legs (with the shortest sarcomere length) is approximately threefold faster than the simultaneous back‐folding of the antennae (with the longest length). Thus, a specific relationship between speed of movement and sarcomere length is established, and we can use the latter to predict the former. Regulatory systems of contraction (sarcoplasmic reticulum [SR] and transverse [T] tubules) match the different contractile properties, varying in frequency of distribution and overall content in parallel to sarcomere variations. All muscles from appendages and body musculature show a unique disposition of contractile material, SR, and T tubules found only in copepod muscles; muscle filaments are grouped in large supermyofibrils that are riddled with frequent cylindrical shafts containing SR and T tubules. This arrangement insures a high spatial frequency of regulatory components. Anat Rec, 301:2164–2176, 2018. © 2018 Wiley Periodicals, Inc.

     
    more » « less
  4. Abstract

    The contractile protein myosinIIis ubiquitous in muscle. It is widely accepted that animals express tissue‐specific myosin isoforms that differ in amino acid sequence andATPase activity in order to tune muscle contractile velocities. Recent studies, however, suggested that the squidDoryteuthis pealeiimight be an exception; members of this species do not express muscle‐specific myosin isoforms, but instead alter sarcomeric ultrastructure to adjust contractile velocities. We investigated whether this alternative mechanism of tuning muscle contractile velocity is found in other coleoid cephalopods. We analyzed myosin heavy chain transcript sequences and expression profiles from muscular tissues of a cuttlefish,Sepia officinalis, and an octopus,Octopus bimaculoides, to determine if these cephalopods express tissue‐specific myosin heavy chain isoforms. We identified transcripts of four and six different myosin heavy chain isoforms inS. officinalisandO. bimaculoidesmuscular tissues, respectively. Transcripts of all isoforms were expressed in all muscular tissues studied, and thusS. officinalisandO. bimaculoidesdo not appear to express tissue‐specific muscle myosin isoforms. We also examined the sarcomeric ultrastructure in the transverse muscle fibers of the arms ofO. bimaculoidesand the arms and tentacles ofS. officinalisusing transmission electron microscopy and found that the fast contracting fibers of the prey capture tentacles ofS. officinalishave shorter thick filaments than those found in the slower transverse muscle fibers of the arms of both species. It thus appears that coleoid cephalopods, including the cuttlefish and octopus, may use ultrastructural modifications rather than tissue‐specific myosin isoforms to adjust contractile velocities.

     
    more » « less
  5. Abstract

    The hypothalamic suprachiasmatic nucleus (SCN), locus of the master circadian clock, bears many neuronal types. At the cellular–molecular level, the clock is comprised of feedback loops involving ‘clock’ genes includingPeriod1andPeriod2,and their protein products,PERIOD1 andPERIOD2 (PER1/2). In the canonical model of circadian oscillation, thePER1/2 proteins oscillate together. While their rhythmic expression in theSCNas a whole has been described, the possibility of regional differences remains unknown. To explore these clock proteins in distinctSCNregions, we assessed their expression through the rostro‐caudal extent of theSCNin sagittal sections. We developed an automated method for tracking three fluorophores in digital images of sections triply labeled forPER1,PER2, and gastrin‐releasing peptide (used to locate the core). In theSCNas a whole, neurons expressing high levels ofPER2 were concentrated in the rostral, rostrodorsal, and caudal portions of the nucleus, and those expressing high levels ofPER1 lay in a broad central area. Within these overall patterns, adjacent cells differed in expression levels of the two proteins. The results demonstrate spatially distinct localization of highPER1 vs.PER2 expression, raising the possibility that their distribution is functionally significant in encoding and communicating temporal information. The findings provoke the question of whether there are fundamental differences inPER1/2 levels amongSCNneurons and/or whether topographical differences in protein expression are a product ofSCNnetwork organization rather than intrinsic differences among neurons.

     
    more » « less