Masticatory myosin unveiled: first determination of contractile parameters of muscle fibers from carnivore jaw muscles

Abstract

Toniolo L, Cancellara P, Maccatrozzo L, Patruno M, Mascarello F, Reggiani C. Masticatory myosin unveiled: first determination of contractile parameters of muscle fibers from carnivore jaw muscles. Am J Physiol Cell Physiol 295: C1535-C1542, 2008. First published October 8, 2008 doi:10.1152/ajpcell.00093.2008.-Masticatory myosin heavy chain (M MyHC) is a myosin subunit isoform with expression restricted to muscles derived from the first branchial arch, such as jaw-closer muscles, with pronounced interspecies variability. Only sparse information is available on the contractile properties of muscle fibers expressing M MyHC (M fibers). In this study, we characterized M fibers isolated from the jaw-closer muscles (temporalis and masseter) of two species of domestic carnivores, the cat and the dog, compared with fibers expressing slow or fast (2A, 2X, and 2B) isoforms. In each fiber, during maximally calcium-activated contractions at 12°C, we determined isometric-specific tension (Po), unloaded shortening velocity (v o) with the slack test protocol, and the rate constant of tension redevelopment (KTR) after a fast shorteningrelengthening cycle. At the end of the mechanical experiment, we identified MyHC isoform composition of each fiber with gel electrophoresis. Electrophoretic migration rate of M MyHC was similar in both species. We found that in both species the kinetic parameters v o and KTR of M fibers were similar to those of 2A fibers, whereas Po values were significantly greater than in any other fiber types. The similarity between 2A and M fibers and the greater tension development of M fibers were confirmed also in mechanical experiments performed at 24°C. Myosin concentration was determined in single fibers and found not different in M fibers compared with slow and fast fibers, suggesting that the higher tension developed by M fibers does not find an explanation in a greater number of force generators. The specific mechanical characteristics of M fibers might be attributed to a diversity in cross-bridge kinetics.

Lion (Panthera leo) and caracal (Caracal caracal) type IIx single muscle fibre force and power exceed that of trained humans

“…The highest specific force in human muscle was achieved by the type IIax fibres (155±8kNm −2 ), whereas the lion and caracal type IIx fibres reached values of 191±8 and 211±22kNm −2 , respectively (Fig.4C). These values were similar to those measured in dog and cat IIx fibres, whereas the absolute force and specific force were lower than those of rat type IIx fibres (Bottinelli et al, 1991;Toniolo et al, 2008). As both absolute force and the CSA of type IIx fibres from cat and dog were similar to those of the lion and caracal, this may suggest a genetic conservation in the MHC IIx isoform functionality.…”

“…The type IIx fibres from both caracal and lion produced less absolute force compared with human type IIax and type IIx fibres from body builders (D'Antona et al, 2006) (Fig.4B). However, the absolute force tended to be the same when compared with type IIx fibres from sedentary human individuals, cats and dogs, although the sedentary humans had larger fibre sizes (Bottinelli et al, 1996;D'Antona et al, 2006;Toniolo et al, 2008).…”

“…From these analyses, it would appear that the same fibre type from different species may possess different contractile properties. For example, force production and unloaded shortening velocity at 12°C of type I, IIa and IIx fibres from cat, rat and dog were found to be higher than those from humans (Bottinelli et al, 1994;Bottinelli, 2001;D'Antona et al, 2006;Toniolo et al, 2007;Toniolo et al, 2008). However, very little is known about the contractile properties of the muscle fibres of wild animal species.…”

Forelimb muscle architecture and myosin isoform composition in the groundhog (Marmota monax)

“…Gels were loaded with a total of ~1 μg protein per lane, stained with silver (Bio-Rad, Hercules, CA, USA) and imaged using a Fluor-Chem E Imaging System (Cell Biosciences, Santa Clara, CA, USA). MHC isoform content was quantified by densitometry in ImageJ (v.1.43, NIH) using the brightness area product method (BAP) similar to Toniolo et al (Toniolo et al, 2008). Band intensity values in each gel lane were summed and used to calculate a percentage for each MHC isoform expressed in a single muscle.…”

Patterns of tropomyosin and troponin-T isoform expression in jaw-closing muscles of mammals and reptiles that express masticatory myosin

“…Whereas rodents typically feed primarily by rapid nibbling of grasses, grains and nuts, many other species that express masticatory myosin, such as most members of Carnivora, typically strangulate prey (requiring sustained force generation), crush bones during feeding and frequently engulf large food items without extensive chewing. Muscle fibers that express masticatory myosin have unusually high force-generating ability (Kato et al, 1985;Saeki et al, 1987;Reiser and Bicer, 2007;Toniolo et al, 2008). It is not clear how masticatory myosin drives mandibular movements associated with food gathering and mastication in species with highly disparate feeding and chewing styles, such as carnivores and rodents.…”