THE ORGANIZATION AND MYOFILAMENT ARRAY OF INSECT VISCERAL MUSCLES
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1 J. Cell Sci. i, (1966) Printed in Great Britain THE ORGANIZATION AND MYOFILAMENT ARRAY OF INSECT VISCERAL MUSCLES D. S. SMITH, B. L. GUPTA AND UNA SMITH Department of Biology, University of Virginia, Charlottesville, Virginia, U.S.A. SUMMARY The cytological organization of three insect visceral muscles has been examined in the electron microscope. In each instance, the fibres were found to be striated, and the striation pattern has been shown to reflect the distribution along the sarcomere of two sets of myofilaments. In transverse sections of the fibre at the level of the A band, these muscles have been found to exhibit an unusual myofilament array in which each thick (myosin) filament is surrounded by twelve thin (actin) filaments rather than six, as in insect flight muscle and vertebrate skeletal muscle. The distribution of T-system tubules and cisternae of the sarcoplasmic reticulum in these visceral fibres is described, and compared with the corresponding membrane systems in other striated muscles. INTRODUCTION In anatomical considerations of the insect body, the muscular systems are commonly divided into two general categories: 'skeletal' and 'visceral' fibres. The former act upon the articulated exoskeleton, while the latter invest the various regions of the intestinal tract and other internal organs within the body cavity. Whereas many of the skeletal muscles, notably those concerned with flight and locomotion, may contract rapidly and often at high frequency, the visceral fibres, like their analogues in the vertebrate body, generally exhibit a slower peristaltic or irregular activity. Hitherto, investigations on the cytological organization of insect muscles have mainly been focused upon the fibres involved in the flight mechanism, and these studies have revealed a consistent deviation in the arrangement of the myofilaments of the contractile system from the pattern occurring in vertebrate skeletal muscles. In the latter (Huxley, 1957; Huxley & Hanson, i960) the thick and thin filaments of the sarcomere, respectively containing myosin and actin, are arranged in a double hexagonal array in the A bands, with the actin components situated in the trigonal position with respect to the myosin filaments. In the indirect flight muscles of the blowfly Calliphora, on the other hand, it was found (Huxley & Hanson, 1957) that the thin filaments are relatively more numerous and are situated opposite to, and midway between, adjoining myosin filaments in the hexagonal array. In the former instance, each thin filament is 'shared' by three thick filaments and, in the latter, by two thick filaments. The configuration of myofilaments reported in the asynchronous flight muscle of 4 Cell Sci. 1
2 50 D. S. Smith, B. L. Gupta and U. Smith Calliphora also occurs in the flight muscle fibres of Odonata (Anisoptera and Zygoptera) (D. S. Smith, unpublished), which have synchronous contraction properties, and may be characteristic of insect flight muscles in general. An identical disposition occurs in the tymbal muscle of the cicada Tibicen (D. S. Smith, unpublished), but, in the absence of detailed studies on other insect skeletal muscle fibres, it is not possible to generalize further on the organization of the myofilament array in this category of muscle cells. This report is concerned with the structure of visceral muscle from three locations in the insect body. It has been found that in each instance the contractile material is represented by a double array of thick and thin filaments, occurring in a configuration strikingly different from that of insect flight muscle fibres. In the muscular sheath investing the midgut of Ephestia larvae (Lepidoptera), in that of the spermatheca of Periplaneta (Orthoptera) and of the seminal vesicle of Carausius (Orthoptera), it was found that, while the thick filaments within the A band maintain an hexagonal array, each of these filaments is surrounded by a ring of twelve thin filaments. These visceral muscle fibres were found to be similar not only with respect to their fibrillar organization, but also in their general structure, and, while this account concerns primarily the last of the above examples, the cytological features described are for the most part common to each of these visceral fibres. MATERIALS AND METHODS An adult male specimen of the stick-insect Carausius morosus was found in a laboratory culture of this parthenogenetic species, and was selected for a study of the organization of the seminal vesicle. This paper is concerned mainly with the muscular sheath investing this region of the reproductive tract. The spermatheca was fixed for 2 h in ice-cold 2-5 % glutaraldehyde, maintained at ph 7-4 in 0-05 M cacodylate buffer containing o-i5m sucrose. After overnight washing in cold cacodylate-buffered 0-3 M sucrose, the material was treated with veronal-acetate-buffered 1% osmium tetroxide at the same ph, for 1 h, dehydrated in an ethanol series, and embedded in Araldite. Sections were cut on a Huxley microtome and examined in a Philips EM 200 electron microscope. Contrast in the sections was enhanced by double 'staining', initially with saturated uranyl acetate in 50% ethanol (30 mm) and subsequently with lead citrate (Reynolds, 1963) for 3-5 min. Visceral muscle fibres associated with the midgut of larvae of Ephestia kiihniella, and with the spermatheca of adult Periplaneta americana were also prepared according to the above schedule. RESULTS General organization of the muscle fibres As is frequently the case in organs within the insect body cavity, and also in the body wall of certain invertebrates which lack an exoskeleton (e.g. platyhelminths; annelids) the muscle fibres surrounding the seminal vesicle of Carausius are disposed
3 Insect visceral muscles 51 in both longitudinal and circular fashion, perpendicular to one another, over the surface of the organ. This double investment is, however, incomplete, and many fields include fibres oriented in only one direction. Each of these muscle fibres is elongated in transverse section, varying between about 1 and 2-5 fi in width (Figs. 2, 3 and 8), and the contractile material, except in the vicinity of the nucleus, almost fills the cell. The fibrillar system is not divided into lamellar or cylindrical fibrils as in insect skeletal fibres (Tiegs, 1955; Pringle, 1957; Smith, 1962). The nuclei are generally situated laterally in the muscle cell, and, while skeletal fibres are typically multinucleate, these visceral fibres appear to contain only a single nucleus. The sarcoplasm extending from the poles of the nucleus is extensive and free from myofilaments, a circumstance similar to that occurring in vertebrate smooth muscle cells. This region of sarcoplasm contains mitochondria and (Fig. 9) ribosomes, sparse cisternae of the rough-surfaced endoplasmic reticulum and welldefined Golgi complexes. The fibres are linked at frequent intervals by adhesion plates or desmosomes (Fig. 6), exhibiting a layer of dense extracellular material. In skeletal fibres of insects such desmosomes do not occur, and it is interesting to note that in visceral fibres these structures differ from the ' septate desmosomes' generally interpolated in regions of close contact between insect cells (Locke, 1965). Each fibre is surrounded externally by a basement membrane or sarcolemma (Fig. 2) in which, as in other insect muscles (Smith, 1961a), no collagen-like fibrils have been resolved. The cell membrane Each fibre is limited by a typical plasma membrane, underlying the sarcolemma and bounding the contractile material. At intervals, this membrane is inflected or invaginated into the fibre to form blindly ending tubes, generally about A in diameter (Figs. 7, 8) but sometimes (Fig. 11) dilating to form larger cavities, up to 700 A in diameter. In the Carausius and Ephestia material, these invaginations are irregularly disposed, but in the muscle investing the spermatheca of Periplaneta, in which the fibres are larger (up to 15/i in diameter), these derivatives of the cell membrane extend across the radius of the fibre, and are arranged in a more precisely radial pattern. These tubules appear to correspond to the transverse tubular system (T-system) elements which form an array precisely oriented with respect to the myofibrillar striations in insect flight and leg muscle (Smith, 1961 a, b, 1962) and vertebrate skeletal muscle (Porter & Palade, 1957; Andersson-Cedergren, 1959; Fawcett & Revel, 1961; Revel, 1962; Franzini-Armstrong & Porter, 1964; Peachey, 1965), where they are believed to play an important part in contraction, by providing the pathway, electrically coupled with the surface cell membrane, along which excitation may be distributed throughout the fibre. In the visceral muscles so far examined, the sarcoplasmic reticulum cisternae are very reduced in extent, and are apparently represented by flattened vesicles, closely adjoining the invaginated T-system tubules. The close juxtaposition of these two membrane components, in the dyad configuration (corresponding to the 'triads' of vertebrate muscle, see references above), is illustrated in Fig
4 52 D. S. Smith, B. L. Gupta and U. Smith The contractile system As has been described above, the contractile material of each visceral muscle fibre corresponds anatomically to a single fibril. This situation has been described in other invertebrate muscles; for example, in the striated fibres of an ostracod (Fahrenbach, 1964) and a coelenterate (Chapman, Pantin & Robson, 1962). The striated nature of this visceral muscle is readily seen in longitudinal sections of the fibre (Figs. 2,4 and 5). Well-defined Z bands traverse the contractile system, following an irregular course, the sarcomere length defined by adjacent Z bands being about 7 to 8 ft. Each Z band is flanked by similarly irregular I bands, about 0-7 to 1 -o fi in width. It should be noted that, in these longitudinal sections, the light H band, occurring in the central region of the sarcomere in insect and vertebrate skeletal muscles, is not clearly defined. The longitudinal sections (Figs. 4, 5) indicate that both thick (myosin) and thin (actin) filaments occur in the A band, while the former are excluded from the I bands, the situation that obtains in vertebrate skeletal muscle (Huxley & Hanson, i960; Huxley, i960). Further details of the disposition of these myofilaments in visceral fibres are revealed in transverse sections. In transverse profiles of the A band of Carausius visceral muscle (Fig. 7) the double array of thick and thin myofilaments is distinct. At this relatively low magnification, the latter are resolved as rings, surrounding the myosin filaments; the unusual nature of the geometrical relationship between these two sets of filaments becomes apparent at higher magnification. The familiar pattern of six thin filaments surrounding each W (b) W Fig. 1. Diagrammatic representation of the distribution of thick (myosin) and thin (actin)filamentsin the A-band region of: (a) vertebrate skeletal muscle (Huxley, 1957; Huxley, i960; Huxley & Hanson, i960); (6) insect flight muscle fibres (Huxley & Hanson, 1957; Hanson & Lowy, i960; Smith, 1962); (c) insect visceral muscles, described in this paper (compare Fig. 12). thick filament, as in the insect and vertebrate muscles so far described, does not occur; instead, the thin filaments form twelve-membered 'orbitals' around the thick filaments. Very slight distortion in the spacing of this double array is sufficient to obscure the detailed geometry of the double lattice, and the diagram of this configuration shown in Fig. 1 c (and compared with other striated muscles, Fig. 1 a, b) accords with regions of transverse sections of visceral muscle fibres where distortion of the lattice appears to be minimal (Fig. 12). In insect flight muscle and vertebrate skeletal muscle each myosin filament is sur-
5 Insect visceral muscles 53 rounded by six actin filaments but, as Huxley & Hanson (1957) and Smith (1962) noted, the trigonal situation of the actin filaments in vertebrate fibres reduces the ratio of actin to myosin filaments, compared with the flight muscle fibres, in which each actin filament is shared by only two myosin filaments (Fig. 1 a, b). In insect visceral muscles, each thin filament is shared, as in flight muscle, by two thick filaments, but the number of thin filaments is exactly doubled: in flight muscle a myosin filament and its six neighbours are associated with thirty actinfilaments (Fig. 1 b), while in visceral muscle (Fig. 1 c) sixty similar myofilaments occur within the same area. In glutaraldehyde-fixed visceral muscle of Carausius, the diameter of the thick and thin myofilaments is respectively about A, and about A. In osmiumfixed vertebrate muscles, the corresponding values have been measured as no and 50 A (Huxley & Hanson, i960). An increase in the apparent diameter of the myosin filaments after glutaraldehydefixation,to about 150 A, has been described by Franzini- Armstrong & Porter (1964) in fish skeletal muscle. The centre-to-centre spacing of the thick filaments in the A-band array of Carausius visceral muscle is about A; somewhat greater, that is, than the 370-A spacing encountered in osmiumfixed asynchronous insect flight muscle (Smith, 1962). In transverse sections, as in the longitudinal plane, the region of junction between the A and I bands of visceral muscle is clearly demarcated. Fig. 11 illustrates a region of junction between these sarcomere regions in Carausius visceral muscle. An A-band profile, containing both myofilament populations, adjoins a well-defined though irregularly disposed area containing only thin I-band filaments. In the I band, however, the orbital arrangement of the I filaments is lost, and these filaments appear to be closely and irregularly packed. The irregularity of the margin between these bands in precisely transverse sections conforms with their zigzag disposition, viewed in longitudinal section. In longitudinal sections of Carausius seminal vesicle muscle, the Z bands appear as well-defined regions of increased density, in the middle of the span of I filaments, paralleling the contours of the A/I junction. In transverse sections of this muscle (Fig. n) the Z bands are less well defined; however, in the midgut muscle of Ephestia, the I-filament region is divided by an area containing dense structures, perhaps representing aggregates of Z-band material (Fig. 8). The apparent absence of an H zone is a striking feature of longitudinal sections of Carausius visceral muscle. In vertebrate skeletal muscle (Huxley & Hanson, i960) this region of the sarcomere in a relaxed fibre is defined- by the inner extremities of the actinfilaments,and is traversed by the mid-region of the myosinfilaments.although longitudinal sections of insect visceral muscle appear to lack H bands, this region of the sarcomere is more clearly defined in transverse profiles of the fibre, as is illustrated in Fig. 13. At the margin of this band, the thin filaments terminate more or less abruptly, and, as is seen in the case of the A/I junction of these fibres (Figs. 2, 4), the A/H junction appears to be similarly irregular. In their detailed construction, then, these visceral muscles exhibit several points of resemblance with other striated fibres of insects and vertebrates; though, as regards their sarcomere organization, the striation repeat in visceral muscles has been achieved by a hitherto undescribed myofilament configuration.
6 54 D. S. Smith, B. L. Gupta and U. Smith DISCUSSION The sliding-filament model of striated muscle contraction and relaxation, as proposed by Huxley & Hanson (i960), has been most amply substantiated in the skeletal fibres of vertebrates. However, as Hanson & Lowy (i960) point out, a similar mechanism may operate not only in invertebrate striated fibres, but perhaps also in certain 'smooth' muscles in which two sets of cross-linked myofilaments are present, though not aligned in the sarcomere register characteristic of striated fibres. In vertebrate skeletal muscle fibres it is clear (Huxley & Hanson, i960; Page & Huxley, 1963) that the length of the A and I filaments (the myosin and actin components) remains constant during the activity cycle; furthermore, the length of these filaments is more or less constant in different vertebrate skeletal muscles. In invertebrates, on the other hand, the relaxed sarcomere length, and hence presumably the lengths of the constituent myofilaments, may vary considerably from one muscle to another. The question remains whether invertebrate muscles operate by the same sliding-filament mechanism as occurs in vertebrate fibres, or whether change in filament length is an alternative or additional method of changing sarcomere length. There is no evidence that the length of the A band changes during contraction in insect flight muscle fibres (Hanson, 1956), but such change has been reported elsewhere in invertebrates, as in Limulus skeletal muscle (de Villafranca, 1961) and in femoral muscle of Locusta (Gilmour & Robinson, 1964). While no observations have as yet been made on the changes in band pattern in insect visceral muscle fibres, an important preliminary to such studies is the recognition of the dimensions and distribution of their constituent myofilaments. The Z bands of Carausius visceral muscle, although not precisely aligned transversely to the long axis of the fibre, define a sarcomere length of about 7-8 ju,, that is between three and four times that of insect flight muscle or vertebrate skeletal muscle. In the present material, although no assessment has been made of the degree of contraction or relaxation of the fibres examined, the I-band width is in the range, of o p. Considerably greater sarcomere lengths have been recorded in invertebrate striated muscles; Haswell (1889) described fibres in the pharynx of syllids (Annelida) with a sarcomere length of 33 /i. The apparent absence of an H band in longitudinal sections of visceral muscle fibres deserves further mention. In the relaxed sarcomere of vertebrate muscle, this region is traversed by the medial portions of the myosin filaments, and is delimited by the inner ends of the actin filaments. It has recently been reported (Franzini-Armstrong & Porter, 1964) that in glutaraldehyde-fixed vertebrate muscle the H band may also be traversed by narrow connecting strands linking the inner extremities of the actin filaments. H bands are clearly demarcated in transverse sections of insect visceral fibres, and some indication of similar linking strands traversing this region is evident, and it is possible that this feature, together with the irregularity of this narrow region, serves to obscure this portion of the sarcomere in longitudinal sections. In summary, this preliminary study suggests that the slowly contracting visceral muscles of insects contain contractile material constructed on essentially the same
7 Insect visceral muscles 55 plan as that of vertebrate fibres in that it consists of two morphologically distinct sets of myofilaments which, though differing from those of vertebrate striated muscle in their geometrical arrangement about the long axis, are nevertheless distributed in a comparable fashion along the sarcomere bands. The electron microscope, coupled with biochemical and physiological studies, has contributed much to a more complete understanding of the role of the membrane systems of striated muscle fibres; notably, the function of membranes within the fibre in controlling the phases of the activity cycle. In insect flight muscles, it is known that the plasma membrane at the surface of the fibre is continuous with open tubular invaginations passing radially into the fibre at regular intervals, at a level either midway between the Z and H bands (synchronous fibres) or at other levels (asynchronous fibres) (Smith, 1961a, b, 1962). These tubules correspond to the T-system invaginations that occur in vertebrate striated muscle fibres (H. E. Huxley, 1964; Page, 1964; Franzini-Armstrong & Porter, 1964). Micro-depolarization experiments (A. F. Huxley, 1959, 1964; Huxley & Peachey, 1964) on vertebrate and crab muscle have suggested that these invaginations may be responsible for the triggering of myofibrillar activation by acting as the pathway along which surface excitation is passively conducted into the fibre. In rapidly contracting synchronous muscles of insects and vertebrates, these T-system tubules are flanked by, and in close association with, cisternae of the sarcoplasmic reticulum in triad or dyad configurations (Smith, 1961a, b, 1962; Porter & Palade, 1957; Andersson-Cedergren, 1959; Fawcett & Revel, 1961; Revel, 1962; Franzini-Armstrong & Porter, 1964; Peachey, 1965). Peachey & Porter (1959) compared the disposition of internal membrane systems in striated and smooth muscle fibres, in the context of the speed of contraction of these muscles, and pointed out that, if some derivative of the cell membrane (now identified as the T-system tubules) is responsible for internal conduction of excitation in striated muscle fibres, then it is possible that the absence of such invaginations in smooth muscle fibres of vertebrates may be correlated with the slowness of their contractile response. Insect visceral muscle fibres appear to represent an intermediate condition between smooth muscle and striated muscles with a highly developed system of transverse tubules (T-system tubules) and associated sarcoplasmic reticulum cisternae. The fibres have a diameter below that of most vertebrate smooth muscle fibres; short T-system invaginations are present, associated in dyad configurations with cisternae of the sarcoplasmic reticulum, which are reduced to small flattened vesicles. The distance across which diffusion of an ' activating substance' must take place to trigger contraction of the fibrillar material in these visceral muscles is of the order of 1 {i; that is, the distance between the cell membrane and tubular derivatives, and the centre of the contractile apparatus. This distance is similar to that separating the centre of the sarcomere from the T-system tubules in the fast-acting fibres of insects and vertebrates, and the speed of contraction of visceral fibres falls well within the limits imposed by the length of the excitation-contraction coupling pathway (compare Peachey & Porter, 1959). Furthermore, if the activating substance in insect visceral muscles represents an influx of calcium ions to the contractile system (Porter, 1961; Ebashi, 1961; Hasselbach, 1964) then it is possible that the slow relaxation of these
8 56 D. S. Smith, B. L. Gupta and U. Smith fibres is mediated by active sequestration of calcium ions within the reduced cisternae of the sarcoplasmic reticulum, perhaps augmented by a calcium-pump mechanism at the cell membrane. The most unusual feature of these visceral muscles is the disposition of the myofilaments within the sarcomere. It should be pointed out that, while comparison has been drawn between the filament array in vertebrate fibres and insect visceral fibres, there is at present no evidence available on the chemical composition of the thick and thin filaments in the latter, and any analogy must therefore be tentative. Nevertheless, the doubling of the number of thin filaments associated with the thick filaments in the A-band region of these muscles divides them sharply from other insect fibres hitherto examined. The extent of occurrence of this pattern of myofilament distribution in insects and other animals, and its physiological significance, remain to be determined. One of us (D. S. S.) gratefully acknowledges support from the National Science Foundation (Grant number GB-1291). REFERENCES ANDERSSON-CEDERGREN, E. (1959). Infrastructure of motor end plate and sarcoplasmic components of mouse skeletal muscle fiber. J. Ultrastruct. Res. (Suppl. 1), CHAPMAN, D. M., PANTIN, C. F. A. & ROBSON, E. A. (1962). Muscle in coelenterates. Revue can. Biol. 21, EBASHI, S. (1961). The role of 'relaxing factor' in contraction-relaxation cycle of muscle. Prog, theor. Phys., Osaka (Suppl. 17), FAHRENBACH, W. H. (1964). A new configuration of the sarcoplasmic reticulum. J. Cell Biol. 22, FAWCETT, D. W. & REVEL, J. P. (1961). The sarcoplasmic reticulum of a fast-acting fish muscle. J. biophys. biochem. Cytol. 10 (Suppl.), FRANZINI-ARMSTRONG, C. & PORTER, K. R. (1964). Sarcolemmal invaginations constituting the T system in fish muscle fibers. J. Cell Biol. 22, GILMOUR, D. & ROBINSON, P. M. (1964). Contraction in glycerinated myofibrils of an insect (Orthoptera, Acrididae). J. Cell Biol. 21, HANSON, J. (1956). Studies on the cross-striation of the indirect flight myofibrils of the blowfly Calliphora. J. biophys. biochem. Cytol. 2, Fig. 2. A low-power electron micrograph of the muscle investing the seminal vesicle in a male Carausius morosus. The fibre is associated with a layer of extracellular basement-membrane material (bm) constituting the sarcolemma. Note the obliquely situated Z bands {Z)flankedby I bands (/) and the apparent absence, in this plane of section, of a mid-sarcomere H band. The contractile material in this muscle consists of a single fibril (fi), bordered on one side by a layer of sarcoplasm (sp). Note the small mitochondria (m). x Fig. 3. A low-power transverse section of Carausius seminal vesicle muscle. Note that in this section the contractile material virtually fills the muscle cell, and that the plasma membrane is invaginated into the fibre at irregular intervals, to form T-system tubules (T). x
9 journal of Cell Science, Vol. i, No. i bm wmm D. S. SMITH, B. L. GUPTA AND U. SMITH {Facing p. 56)
10 Fig. 4. Longitudinal section of Carausius visceral muscle, including a Z band and the adjoining regions of the sarcomere. Note the irregular disposition of this band (Z), and the adjoining I bands containing only thin filaments (about 50 A in diameter) (/). From the edge of the I bands extend the A bands of the sarcomere, in which thick and thin filaments interdigitate (A). The dense particles present in the I-band region probably represent glycogen deposits (g). x
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12 Fig. 5. Longitudinal section of Caraushis visceral muscle, including a Z band (Z) flanked by A regions (A). Note that the I region extending from the Z band contains only thin filaments (2) but that the neighbouring A band contains both thick (1) and thin (2) myofilaments. x Fig. 6. The intercellular linkage between muscle fibres investing the seminal vesicle of Caraushis. In these regions of close apposition the cell membranes are separated by an intercellular gap containing a layer of dense material (arrows), a situation resembling that occurring in the 'desmosomes' or adhesion plates between many epithelial cells. Note that a layer of dense material occurs within the muscle cells in the desmosome region, and that I filaments (/) appear to terminate beside the cell membrane in this region. It is possible that the dense sarcoplasm bordering the desmosome represents Z-band material, and that the Z bands traversing the fibre may sometimes terminate at the cell surface, x
13 Journal of Cell Science, Vol. i, No. i D. S. SMITH, B. L. GUPTA AND U. SMITH
14 Fig. 7. Transverse section of visceral muscle of Carausius, through an A-band region. Note the two sets of myofilaments, and the invaginated T-system tubules (T); also the microtubules (mf) situated near the surface of the fibre, x
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16 Fig. 8. Transverse section of visceral muscle investing the midgut of larval Ephestia. Note the A-band profiles (A) containing thick and thin myofilaments, the I bands containing only thin filaments (/) and the aggregations of dense material in the middle of the I bands, apparently representing Z-band material (Z). As in Carausius visceral muscle, the plasma membrane of these fibres is invaginated into the cell at irregular intervals, to form T-system tubules (T). x
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18 Fig. 9. Longitudinal section of Carausius visceral muscle, including a portion of the nucleus («) and the adjoining sarcoplasm. The latter contains sparsely distributed cisternae of the rough-surfaced endoplasmic reticulum (er) and well-developed smooth-membraned Golgi complexes (go), x Fig. 10. Longitudinal section of Carausius visceral muscle, illustrating the disposition of membrane systems within the fibre. A profile of the plasma membrane is included at left (pm). Within the fibre, a portion of a T-system tubule (T) invaginated from the surface plasma membrane (compare Fig. 7) lies alongside the fibrillar material (fi), and is closely associated with a flattened vesicle or cisterna of the sarcoplasmic reticulum (sr) containing electron-dense material, x
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20 Fig. II. The distribution of myofilaments at the junction of A and I bands in Caraitsius visceral muscle. In the A bands (.-?) the thick filaments are surrounded by orbitals of thin filaments, while in the I bands (/) only thin filaments occur. Dense material, probably representing the Z band (Z) is also included in this section. Note the invaginated tubules of the T-system (T): the mouth of the upper tubule contains a layer of extracellular material (indicated by an asterisk), bordered by regions of increased density (arrows) within the sarcoplasm, possibly confluent with the Z bands (compare Fig. 6). x noooo.
21 Journal of Cell Science, Vol. i, No. i z *» -» * * D. S. SMITH, 13. L. GUPTA AND U. SMITH
22 Fig. 12. The disposition of myofilaments in the A band of Caraiisius visceral muscle. The thick filaments form a more or less regular hexagonal array (particularly within the marked rectangle), and each thick filament is surrounded by a ring of twelve thin filaments. The geometry of the disposition of these myofilaments is illustrated in diagrammatic form in Fig. i c. x Fig. 13. The disposition of myofilaments at the A/H junction in Caraiisius visceral muscle. In the A band (.4) thick and thin filaments occur together, while in the H band (H) only the former are present. There is some evidence that fine strands traverse the H band (arrows). Note the small mitochondrion (m) and transverse profiles of intrafibrillar microtubules (mi), x
23 Journal of Cell Science, Vol. i, No. i 13 D. S. SMITH, 13. L. GUPTA AND U. SMITH
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25 Insect visceral muscles 57 HANSON, J. & LOWY, J. (i960). Structure and function of the contractile apparatus in the muscles of invertebrate animals. In The Structure and Function of Muscle (ed. G. H. Bourne), 1, New York and London: Academic Press. HASSELBACH, W. (1964). Relaxing factor and the relaxation of muscle. Prog. Biophys. molec. Biol. 14, HASWELL, W. (1889). A comparative study of striated muscle. Q. jfl microsc. Sci. 30, HUXLEY, A. F. (1957). Muscle structure and theories of contraction. Prog. Biophys. biophys. Chem. 7, HUXLEY, A. F. (1959). Local activation of muscle. Ann. N.Y. Acad. Sci. 81, HUXLEY, A. F. (1964). The links between excitation and contraction. Proc. R. Soc. B 160, HUXLEY, A. F. & PEACHEY, L. D. (1964). Local activation of crab muscle. J. Cell Biol. 23, 107 A. HUXLEY, H. E. (i960). Muscle cells. In The Celled. J. Brachet and A. E. Mirsky), 4, New York and London: Academic Press. HUXLEY, H. E. (1964). Evidence for continuity between the central elements of the triads and extracellular space in frog sartorius muscle. Nature, Lond. 202, HUXLEY, H. E. & HANSON, J. (1957). Preliminary observations on the structure of insect flight muscle. In Electron Microscopy {Proc. Stockholm Conference, 1956), pp Stockholm: Almqvist and Wiksell. HUXLEY, H. E. & HANSON, J. (i960). The molecular basis of contraction in cross-striatedmuscles. In The Structure and Function of Muscle (ed. G. H. Bourne), 1, New York and London: Academic Press. LOCKE, M. J. (1965). The structure of septate desmosomes. jf. Cell Biol. 25, PAGE, S. (1964). The organization of the sarcoplasmic reticulum in frog muscle. J. Physiol., Lond. 175, 10-11P. PAGE, S. & HUXLEY, H. E. (1963). Filament lengths in striated muscle. J. Cell Biol. 19, PEACHEY, L. D. (1965). The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J. Cell Biol. 25, PEACHEY, L. D. & PORTER, K. R. (1959). Intracellular impulse conduction in muscle cells. Science, N.Y. 129, PORTER, K. R. (1961). The sarcoplasmic reticulum. J. biophys. biochem. Cytol. 10 (Suppl.), PORTER, K. R. & PALADE, G. E. (1957). Studies on the endoplasmic reticulum. III. Jf. biophys. biochem. Cytol. 3, PRINGLE, J. W. S. (1957). Insect Flight. Cambridge University Press. REVEL, J. P. (1962). The sarcoplasmic reticulum of the bat cricothyroid muscle. J. Cell Biol. 12, REYNOLDS, E. S. (1963). The use of lead citrate at high ph as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, SMITH, D. S. (1961 a). The structure of insect fibrillar flight muscle. J. biophys. biochem. Cytol. 10 (Suppl.), SMITH, D. S. (19616). The organization of the flight muscle in a dragonfly, Aeshna sp. (Odonata). J. biophys. biochem. Cytol. n, SMITH, D. S. (1962). Cytological studies on some insect muscles. Revue can. Biol. 21, TIEGS, O. W. (1955). The flight muscles of insects their anatomy and histology; with some observations on the structure of striated muscle in general. Phil. Trans. R. Soc. B 238, VILLAFRANCA, G. W. DE (1961). The A and I band lengths in stretched or contracted horseshoe crab skeletal muscle. Jf. Ultrastruct. Res. 5, (Received 23 May 1965)
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