Observations on the Variations in Size of the a Region of Arthropod Muscle

Aronson, John F.

doi:10.1083/jcb.19.2.359

Cited by 8 publications

(3 citation statements)

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“…Nonuniform sarcomere lengths are known to occur within single muscle cells in both vertebrate and invertebrate muscles (2,12,13). As Franzini-Armstrong (12) pointed out: "the possibility should be explored that a continuous addition of new sarcomeres underlies the noticeable variabil-ity in A-band length of crustacean fibres.…”

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Transverse sarcomere splitting. A possible means of longitudinal growth in crab muscles.

Jahromi¹,

Charlton²

1979

The Journal of Cell Biology

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Transversely split sarcomeres are seen in mouthpart muscles of the blue crab in the electron microscope. Sarcomeres split only at the H zone. Two new sarcomeres are formed by a Z disk which appears in the H zone of the splitting sarcomere. Splitting may involve breaking of the thick filaments in the H zone, elongation of these filaments, and formation of both new actin filaments and Zdisk materials. Sarcomere splitting would allow longitudinal growth of muscle cells without lengthening of sarcomeres and concomitant changes in contractile properties.KEY WORDS transverse sarcomere splitting growth 9 muscle myofilaments 9 ultrastructure Increase in length of muscle fibers during the growth of animals can involve both lengthening of sarcomeres (I, 5, 6, 13, 15, 23) and addition of sarcomeres (10,13,15,16,26). The mechanism by which sarcomeres are added, however, still remains unclear. Auber (5) suggested that Z disks split transversely and that a new sarcomere grows between the two Z-disk fragments during development of blowfly flight muscles. In vertebrate muscle, the sarcomeres are somewhat shorter near the ends of a muscle cell (13, 14) and protein synthesis is greatest there (16,26). This has led numerous investigators (see reference 14) to suggest that sarcomeres are added at the ends of muscle cells.Nonuniform sarcomere lengths are known to occur within single muscle cells in both vertebrate and invertebrate muscles (2, 12, 13). As FranziniArmstrong (12) pointed out: "the possibility should be explored that a continuous addition of new sarcomeres underlies the noticeable variability in A-band length of crustacean fibres."In this paper we present ultrastructural evidence of transverse splitting of sarcomeres which could underly longitudinal growth as well as nonuniformity of sarcomere length within single muscle cells in blue crabs. MATERIALS AND METHODSBlue crabs, Callinectes sapidus, were obtained from local suppliers in Toronto and kept in tanks of three-quarter strength artificial seawater at ~15~ The maxilliped exopodites were removed, and the flagellum abductor mu~les (muscles 78, 87, and 102 of reference 9) were exposed by removing most of the overlying exoskeleton on one side of th~ appendage. The flagellum joint was immobilized and the muscles were fixed in situ at rest length for 1 h in 2.5% glutaraldehyde containing 0.2% formaldehyde and 0.15 M sodium cacodylate buffer at pH 7.3. Muscles were then placed in cacodylate (0.15 M)-buffered sucrose (0.3 M) wash containing 0.06 M NaCI and 2 mM CaC12 for 2-3 h (H. L. Atwood, unpublished observations). Bundles of fibers were dissected from the exopodite and postfixed in 2% OsO4 (in 0.15 M cacodylate). Other procedures employed were standard for this laboratory. (20). 736J. CELL BIOLOGY 9 The Rockefeller University Press.

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Transverse sarcomere splitting. A possible means of longitudinal growth in crab muscles.

Jahromi¹,

Charlton²

1979

The Journal of Cell Biology

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“…There was no visual evidence of shortening of the A region in fibers which contracted reversibly and apparently completely. Since sarcomere shortening in living mite and in surviving Limulus muscle does not involve appreciable shortening of the A region, the results obtained with glycerinated Limulus muscle would appear to be most clearly explained on the basis of variation in the size of sarcomeres (12) and of undefined effects of the glycerination procedure (13) or of ATP-induced shortening.…”

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Polarized Light Observations on Striated Muscle Contraction in a Mite

Aronson

1967

The Journal of Cell Biology

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Contraction of individual sarcomeres within the living mite Tarsonemus sp. was observed by polarized light microscopy. In unflattened animals the usual range of contraction was such that the minimum sarcomere length approximated the length of the A region, and the maximum sarcomere length was about twice the length of the A region. The central sarcomcres of the dorsal mctapodosomal muscles were observed in detail. The A band length increased slightly with increasing sarcomcre length since the regression of I region length on sarcomere length had an average slope of 0.91. When the A band length in a sarcomere which was shortening was compared with the length when the same sarcomere lengthened, no significant difference was seen. The A band of each sarcomcre seemed to act as a not too rigid limit to further shortening; this agreed with the reversible shortening of a muscle in which the A band had been experimentally shortened. An H region was visible at long sarcomere lengths and was not visible at short sarcomere lengths, even when the muscle was actively shortening. The rate of change of H region length with sarcomere length suggested that I filament length may increase as sarcomere length increases. Despite this effect and the small increase in A length with sarcomere length, the results are considered to be consistent with a model in which shortening occurs by the relative movement of A and I filaments, with little or no change in length of either set of filaments. Sarcomere shortening was clearly associated with an increase in the retardation of the A region.

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“…In muscles of crustaceans, this is achieved by specific variations in the length of the thin and thick filaments and by alterations of sarcomeric structures, without expression of multiple myosin gene products (Jasper and Pézard, 1934;Atwood, 1967;Hoyle, 1967;Franzini-Armstrong, 1970). Fast fibers have shorter thin and thick filaments hence a shorter sarcomere length at rest and a thin/thick filament ratio of 3:1, whereas slower fibers have longer filaments and an increasing ratio of thin/ thick filaments, up to 6:1 (Aronson, 1963;Atwood, 1967Atwood, , 1973Franzini-Armstrong, 1970;Hoyle, 1983). The fibers are typically innervated by axons from several motor neurons (Phillips, 1980) in a way that fast and slow fibers in the same muscle may have a common innervation but respond differentially to the axonal firing frequencies and have differentiated neuromuscular junctions (Atwood, 1967;Davis, 1971;Hinkle and Camhi, 1972;Calabrese, 1989;Fuglevand et al, 1993).…”

Section: Introductionmentioning

confidence: 99%

Functionally Driven Modulation of Sarcomeric Structure and Membrane Systems in the Fast Muscles of a Copepod (Gaussia princeps)

Glaser

Iyer

Gilly

et al. 2018

The Anatomical Record

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Muscles of the mesopelagic copepod Gaussia 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.

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Observations on the Variations in Size of the a Region of Arthropod Muscle

Cited by 8 publications

References 19 publications

Transverse sarcomere splitting. A possible means of longitudinal growth in crab muscles.

Transverse sarcomere splitting. A possible means of longitudinal growth in crab muscles.

Polarized Light Observations on Striated Muscle Contraction in a Mite

Functionally Driven Modulation of Sarcomeric Structure and Membrane Systems in the Fast Muscles of a Copepod (Gaussia princeps)

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