Mechanism of Supercontraction in a Striated Muscle

Hoyle, Graham; McAlear, James H.; Selverston, Allen I.

doi:10.1083/jcb.26.2.621

Cited by 96 publications

(34 citation statements)

References 13 publications

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“…These modifications, in conjunction with changes in other parts of the motor system, have resulted in muscles that can generate force economically (Twarog, 1967), produce relatively high force over an impressive range of lengths (Hoyle et al, 1965;Lanzavecchia, 1977;Herrel et al, 2002;Woods et al, 2008), shorten with great speed (Rome et al, 1996;Schaeffer et al, 1996;Elemans et al, 2004), act as powerful motors (Lutz and Rome, 1994;Marsh and Olson, 1994), as brakes or shock absorbers (Full et al, 1998), as struts (Roberts et al, 1997;Biewener et al, 1998) or as springs (Tu and Dickinson, 1994). A recognized, but understudied, phenomenon is that muscle fibers can be modified extensively during ontogeny (e.g.…”

Section: Introductionmentioning

confidence: 99%

The ontogeny of muscle structure and locomotory function in the long-finned squidDoryteuthis pealeii

Thompson

Bartol

Baksi

et al. 2010

Journal of Experimental Biology

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SUMMARYUnderstanding the extent to which changes in muscle form and function underlie ontogenetic changes in locomotory behaviors and performance is important in understanding the evolution of musculoskeletal systems and also the ecology of different life stages. We explored ontogenetic changes in the structure, myosin heavy chain (MHC) expression and contractile properties of the circular muscles that provide power for jet locomotion in the long-finned squid Doryteuthis pealeii. The circular muscle fibers of newly hatched paralarvae had different sizes, shapes, thick filament lengths, thin:thick filament ratio, myofilament organization and sarcoplasmic reticulum (SR) distribution than those of adults. Viewed in cross section, most circular muscle cells were roughly triangular or ovoid in shape with a core of mitochondria; however, numerous muscle cells with crescent or other unusual cross-sectional shapes and muscle cells with unequal distributions of mitochondria were present in the paralarvae. The frequency of these muscle cells relative to 'normal' circular muscle cells ranged from 1:6 to 1:10 among the 19 paralarvae we surveyed. The thick filaments of the two types of circular fibers, superficial mitochondria-rich (SMR) and central mitochondria-poor (CMP), differed slightly in length among paralarvae with thick filament lengths of 0.83±0.15 mm and 0.71±0.1 mm for the SMR and CMP fibers, respectively (P 0.05; ANOVA). During ontogeny the thick filament lengths of both the CMP and SMR fibers increased significantly to 1.78±0.27 mm and 3.12±0.56 mm, respectively, in adults (P<0.0001 for both comparisons; ANOVA with Tukey's highly significant difference post hoc tests). When sectioned parallel to their long axes, the SMR and CMP fibers of both paralarvae and adults exhibited the myofilament arrangements typical of obliquely striated muscle cells but the angle of obliquity of the dense bodies was 22.8±2.4 deg. and 4.6±0.87 deg. for paralarvae and adults, respectively. There were also differences in the distribution of the anastomosing network of SR. In paralarvae, the outer and central zones of SR were well developed but the intramyoplasmic zone was greatly reduced in some cells or was scattered non-uniformly across the myoplasm. Whereas in adults the intramyoplasmic SR region was composed primarily of flattened tubules, it was composed primarily of rounded vesicles or tubules when present in the paralarvae. The ontogenetic differences in circular muscle structure were correlated with significant differences in their contractile properties. In brief tetanus at 20°C, the mean unloaded shortening velocity of the paralarval circular muscle preparations was 9.1 L 0 s -1 (where L 0 was the preparation length that generated the peak isometric stress), nearly twice that measured in other studies for the CMP fibers of adults. The mean peak isometric stress was 119±15 mN mm -2 physiological cross section, nearly half that measured for the CMP fibers of adults. Reverse transcriptase-polymerase chain reaction analysis of pa...

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Section: Introductionmentioning

confidence: 99%

The ontogeny of muscle structure and locomotory function in the long-finned squidDoryteuthis pealeii

Thompson

Bartol

Baksi

et al. 2010

Journal of Experimental Biology

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“…Muscle stored at 2° and sampled 2h hours post-mortem After 2k hours of post-mortem storage at 2°, the muscle observed was supercontracted and was similar to the structure observed in neurallyevoked contraction as described by Hoyle et al (1965). In sectioned muscle, the Z-line appeared to open or become discontinuous and to allow the penetration of filaments.…”

Section: Morphology Of Post-mortem Musclementioning

confidence: 98%

“…As shown by Hoyle et al (1965) If the plane of sectioning showed two thin filaments between adjacent pairs of thick filaments, four thin filaments were seen in the center of the A-band where overlapping of filaments occurred. Thick filaments remained straight indicating that sliding rather than crumpling had occurred.…”

Section: Morphology Of Post-mortem Musclementioning

confidence: 99%

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Ultrastructural and molecular changes in striated muscle during post-mortem shortening

Stromer

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“…9 It is related to the vertebrate Z-band protein, CapZ (36/32)? which not only caps thin filaments, but serves as a Z-band docking site for various signaling molecules. '…”

Section: Capping Proteinmentioning

confidence: 99%

The Insect Z-Band

Saide

Nature’s Versatile Engine: Insect Flight Muscle Inside and Out

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T he Z-band is an electron dense structure that borders sarcomeres in striated muscle. It is a complex assembly of proteins that organizes and stabilizes both thick and thin filament arrays in the contractile apparatus. By anchoring actin filaments and protein extensions of myosin filaments, the Z-band ensures that active as well as passive tensions are transmitted from one sarcomere to the next along the length of muscle.Although Z-bands serve these common functions in all muscles, in insects Z-band ultrastructure is strikingly varied among different types of fibers. It appears fragmented and amorphous in some fibers, solid and geometrically ordered in others.1. This architectural diversity suggests that the Z-band has adapted to specific physiological requirements of different muscle fibers.Although it is not yet possible to describe how proteins are arranged to construct an insect Z-band, there have been significant advances in the field, aided in large part by use of three-dimensional reconstruction techniques, the sequencing of the Drosophila genome, and genetic manipulation of proteins. This chapter will review research that has expanded our understanding of the structure of the insect Z-band and the nature of proteins that are assembled to form it. While the focus will be on the Z-band of indirect flight muscle (IFM), an overview of Z-bands in other muscle types will be presented for comparison. Z-Band Anatomy Unstructured Z-BandsPerhaps the least well organized Z-bands in insects are the larval body wall muscles ' and larval and adult visceral muscles. These fibers require extensive shortening, and the Z-band is designed to allow the penetration of thin and thick filaments of adjacent sarcomeres during contraction. The fibers are described as "supercontracting" ' 9 because they can shorten to less than 40% of rest length, like vertebrate smooth muscle. In fact, normalized length-tension curves of blowfly larval body wall muscle and vertebrate teania coli smooth muscle are nearly identical. 10 In longitudinal sections the Z-bands in these insect fibers appear as discontinuous, poorly aligned, spindle shaped densities that collect and anchor groups of thin filaments. Although in transverse views, cross-sections of thin filaments can sometimes be seen within the Z-band density, they do not have noticeable order. 5 The dense Z material itself is discontinuous and irregularly shaped in cross-section.3 In some muscles the densities appear continuous and form a plate with numerous, large perforations. " Hardie and Hawes, who examined very thick cross sections through Z-bands with high voltage electron microscopy, implied that the perforated Z-structure is more likely to be the rule than the exception in supercontracting insect muscles. Since Z-band material is usually not perfecdy planar in these fibers, thin sections of perforated Z-discs would be expected to appear discontinuous. Sections thick enough to include the entire width of the Z-band allow the interconnectedness of the Z material to be seen (F...

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Mechanism of Supercontraction in a Striated Muscle

Cited by 96 publications

References 13 publications

The ontogeny of muscle structure and locomotory function in the long-finned squidDoryteuthis pealeii

The ontogeny of muscle structure and locomotory function in the long-finned squidDoryteuthis pealeii

Ultrastructural and molecular changes in striated muscle during post-mortem shortening

The Insect Z-Band

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