Muscle specialization in the squid motor system

Abstract

SummaryAlthough muscle specialization has been studied extensively in vertebrates, less is known about the mechanisms that have evolved in invertebrate muscle that modulate muscle performance. Recent research on the musculature of squid suggests that the mechanisms of muscle specialization in cephalopods may differ from those documented in vertebrates. Muscle diversity in the development and the evolution of cephalopods appears to be characterized by modulation of the dimensions of the myofilaments, in contrast to the relatively fixed myofilament dimensions of vertebrate muscle. In addition, the arrangement of the myofilaments may also be altered, as has been observed in the extensor muscle fibres of the prey capture tentacles of squid and cuttlefish, which show cross-striation and thus differ from the obliquely striated pattern of most cephalopod locomotor muscle fibres. Although biochemical specializations that reflect differences in aerobic capacity have been documented previously for specific layers of the mantle muscle of squid, comparison of protein profiles of myofilament preparations from the fast crossstriated tentacle fibres and slow obliquely striated fibres from the arms has revealed remarkably few differences in myofilament lattice proteins. In particular, previous studies using a variety of SDS-PAGE techniques and peptide mapping of the myosin heavy chain were unable to resolve differences in the myosin light and heavy chains. Since these techniques cannot exclude the presence of a highly conserved variant that differs in only a few amino acids, in this study semi-quantitative reverse transcription polymerase chain reaction (RT-PCR) analysis of myosin heavy chain messenger RNAs (mRNAs) from the cross-striated tentacle and obliquely striated arm muscle fibres was conducted. This analysis showed that a previously reported alternatively spliced isoform of the squid myosin motor domain is present only in low abundance in both muscle types and therefore differential expression of the two myosins cannot explain the difference in contractile properties. It thus appears that modulation of the contractile properties of the musculature of squid and other cephalopods occurs primarily through variation in the arrangement and dimensions of the myofilaments.

Tuning of shortening speed in coleoid cephalopod muscle: no evidence for tissue‐specific muscle myosin heavy chain isoforms

“…Previous research on loliginid and ommastrephid squids has shown that instead of expressing tissue‐specific myosin heavy chain isoforms, the modulation of shortening velocity occurs through variation in the ultrastructure of the sarcomeres (Kier , ; Kier & Schachat , ; van Leeuwen & Kier ; Shaffer & Kier ). The most important factors are the thick filament and sarcomere length.…”

“…However, Shaffer & Kier () isolated and sequenced myosin heavy chain transcripts and found that D. pealeii does not express tissue‐specific myosin heavy chain isoforms. Although three isoforms were identified (termed A, B, and C), all were found in all muscle tissues studied, and isoforms A and B were observed to be expressed at similar levels in the arm and tentacle musculature (Kier & Schachat ). These results suggest that squid use an alternative mechanism to tune contractile velocities.…”

Comparative morphology of changeable skin papillae in octopus and cuttlefish

“…C,D). Contraction of these muscles not only determines the papilla's flat, truncated shape, but by reducing its cross sectional diameter, it lengthens the papilla away from the dorsal surface of the eye [like the transverse muscles in squid tentacles, (Kier, ; Kier and Schachat, )]. The opposing retractors were parallel with the long axis of the papilla (perpendicular to the horizontal dermal erector muscles); their contraction would shorten the long axis, retracting the papilla (Fig.…”

The Musculature of Coleoid Cephalopod Arms and Tentacles

“…Kier and Schachat ( 2008 ) used semi-quantitative RT-PCR with primers that spanned the alternatively spliced region in order to explore the relative abundance of mRNA for the two myosin heavy chain isoforms in the arm transverse muscle and the tentacle transverse muscle of the squid D. pealeii . The results revealed low levels of mRNA for the alternatively spliced myosin isoform (termed “B”) in both muscle fiber types with isoform “A” much more abundant (90–95%) in both the tentacle transverse muscle and the arm transverse muscle.…”