Myofibrillar protein isoform expression is correlated with synaptic efficacy in slow fibres of the claw and leg opener muscles of crayfish and lobster
1 Department of Biology, Cell and Molecular Biology Program, Program in Molecular, Cellular and Integrative Neurosciences, Colorado State University, Fort Collins, CO 80523, USA,
2 School of Natural Sciences, Edith Cowan University, Joondalup Drive, Joondalup, WA 6027, Australia and
3 Thomas Hunt Morgan School of Biological Sciences, University of Kentucky, Lexington, KY 40506, USA
*e-mail: don{at}lamar.colostate.edu
Accepted 3 December 2001
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Summary |
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Key words: muscle, troponin, troponin-I, troponin-T, myofibrillar protein, isoform, innervation, neuromuscular junction, synapse, crayfish, lobster, Crustacea, Arthropoda, Homarus americanus, Procambarus clarkii.
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Introduction |
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A facilitation index (FI) is commonly used to quantify differences in STF; this is based on the use of ratios of the amplitudes of the postsynaptic potentials within the train of responses. In the intact animal, the slow muscles involved in limb movements are recruited into action by bursts of activity from the motor neurons. This type of activity results in summation and facilitation of the postsynaptic graded responses to elicit muscle contraction, which can be reproduced with isolated preparations to investigate the mechanisms of synaptic function and muscle properties (Crider and Cooper, 2000).
Differences in the terminal structure and synaptic strength of the excitatory motor neuron that innervates the various regions on the opener muscle in crayfish are well established (Günzel et al., 1993; Govind et al., 1994
; Cooper et al., 1995a
,b
,c
, 1996a
), but how the differences arise is unknown. Local retrograde influences from intrinsic differences among the muscle fibres may alter terminal synaptic structure or synaptic properties early in development may influence the muscle fibres differentially, which then feed back on maintaining the nerve terminal structure and function (for a review, see Atwood, 1973
). Using improved methods for identification of fibre phenotypes in crustaceans (for a review, see Mykles, 1997
), we have investigated whether the opener muscle is homogeneous or heterogeneous in muscle fibre phenotype with respect to the differences in nerve terminal function.
The pinnate arrangement of fibres in the opener muscle of the blue crab (Callinectes sapidus) leg generates differential forces and selective recruitment of tension receptors that monitor muscle force (Tryba and Hartman, 1997). These regional differences, together with the differences in terminal structure and function described in the crayfish, suggest that there are phenotypic differences in the opener muscle fibre type. Three types of fibre have been biochemically characterized in muscles from a variety of crustacean species: fast-twitch, slow-twitch (S1) and slow-tonic (S2) (for a review, see Mykles, 1997
). These fibres differ in their assemblages of myofibrillar protein isoforms, which confer unique contractile properties consistent with their physiological functions.
Fibre-type-specific isoforms of myosin heavy and light chains, tropomyosin, paramyosin and troponin-I, -T and -C are expressed in lobster and crayfish muscles (Mykles, 1985a,b
; Kobayashi et al., 1989
; Li and Mykles, 1990
; Miyazaki et al., 1990
, 1992
, 1993
; Nishita and Ojima, 1990
; Garone et al., 1991
; Miegel et al., 1992
; Cotton and Mykles, 1993
; Neil et al., 1993
; Galler and Neil, 1994
; Sakurai et al., 1996
; Ishimoda-Takagi et al., 1997
; Cooper et al., 1998
; Mykles et al., 1998
; Holmes et al., 1999
; LaFramboise et al., 1999
; Sohn et al., 2000
). However, for an isoform to serve as a suitable diagnostic marker, it must (i) be exclusively expressed in a specific fibre type in various decapod crustacean species and (ii) be easily distinguished in SDSpolyacrylamide gels. Only two proteins meet these criteria: P75 for fast-twitch and troponin-T1 (TnT1) for slow-tonic (S2); neither P75 nor TnT1 is expressed in slow-twitch (S1) fibres (for a review, see Mykles, 1997
). TnT2 is expressed only in fast fibres, but it is not easily distinguished from TnT3, which is expressed in S1 and S2 fibres (Mykles, 1985b
; Sohn et al., 2000
). The presence or absence of the TnT and troponon-I (TnI) isoforms was used in the present study to distinguish the two slow fibre phenotypes in the regions of the opener muscles of crayfish and lobsters.
This paper compares the physiological properties of innervation efficacy by a single tonic motor neuron with muscle fibre phenotype in the claw and leg opener muscles of crayfish and lobster. Regional differences in slow fibre phenotype were correlated with the strength of innervation from the motor neuron, suggesting a relationship between synaptic efficacy and expression of troponin isoforms.
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Materials and methods |
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Electrophysiology
The excitatory axon was selectively stimulated by placing a branch of the leg nerve (from the merus segment) into a suction electrode connected to a Grass stimulator (Dudel and Kuffler, 1961). Intracellular recordings were performed with microelectrodes filled with 3 mol l1 KCl. The resistance of the electrode in the bath was 3060 M
. Responses were recorded with an Axoclamp 2A intracellular electrode amplifier (Axon Instrument). Signals were simultaneously recorded using a Vetter PCM VHS tape recorder and digitized using MacLab/s v3.5. The crayfish and lobster salines used were the same as described by Sohn et al. (2000
).
Short-term facilitation was induced by giving a train of 10 or 20 pulses every 10 s. Each pulse consisted of stimulation at either 30 or 50 Hz. To determine FI, 1 was subtracted from the ratio of the amplitude of a preceding pulse (first, third, fifth, tenth or fifteenth) to the amplitude of the last pulse (either tenth or twentieth); FI was zero if no facilitation occurred (Crider and Cooper, 1999; Sohn et al., 2000
). The amplitudes of the EPSPs were measured using the MacLab/s v3.5 programs Scope or Chart. The signals recorded on the computer were calibrated to the raw traces observed on the oscilloscope.
Analysis of myofibrillar proteins
Muscle fibres were glycerinated and analyzed by SDSPAGE and western blotting as described previously (Mykles, 1985b; Sohn et al., 2000
). Briefly, fibres were incubated in glycerination buffer (20 mmol l1 Tris-HCl, pH 7.4, 0.1 mol l1 KCl, 1 mmol l1 EDTA, 0.1 % Triton X-100 and 50 % glycerol) and solubilized overnight in 25100 µl of SDS sample buffer (62.5 mmol l1 Tris-HCl, pH 6.8, 12.5 % glycerol and 1.25 % SDS). Myofibrillar proteins (46 µg) were separated in 10 % SDSpolyacrylamide gels (Laemmli, 1970
). Proteins in gels were either fixed in 10 % glutaraldehyde and stained with silver (Wray et al., 1981
; Mykles, 1985a
,b
) or transferred to PVDF membrane for western blotting (Towbin et al., 1979
). After blocking with 5 % non-fat milk in Tris-buffered saline (TBS; 20 mmol l1 Tris-HCl, pH 7.5, 0.5 mol l1 NaCl), blots were incubated for 1 h with polyclonal antibodies to P75 (7.3 µg IgG ml1), troponin-I3 (1:5000 dilution of antiserum) or troponin-T (0.8 µg IgG ml1) in 0.05 % Tween-20 in TBS (TTBS) containing 3 % non-fat milk. After washing in TTBS, blots were incubated with biotinylated anti-rabbit IgG (1:10 000 dilution in TTBS) for 1 h followed by avidin/biotinylated horseradish peroxidase complex (Vectastain ABC reagent, 1:1000 dilution in TTBS) and chemiluminescent detection (Covi et al., 1999
).
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Results |
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Since the results of the analysis of opener muscles in lobster leg and crayfish claw and leg were similar to those obtained on the lobster claw opener muscle, only the blots probed with the anti-TnT antibody are shown in Fig. 6. In all three muscles, the proximal region consisted of S2 fibres (Fig. 6A, lanes d, e; Fig. 6B, lanes d, e; Fig. 6C, lanes d, e), while the central region consisted of S1 fibres (Fig. 6A, lanes f, g; Fig. 6B, lanes f, g; Fig. 6C, lane f). The distal region of crayfish leg (Fig. 6B, lanes h, i) and claw (Fig. 6C, lane g) openers contained S2 fibres, whereas TnT1 was not detected in the distal fibres of lobster leg opener (Fig. 6A, lane h). As observed in lobster claw opener (Fig. 5), the distal S2 fibres in the crayfish opener muscles expressed lower levels of TnT1 than the most proximal fibres.
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Discussion |
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The synaptic strength or efficacy is correlated with muscle phenotype in various invertebrate and vertebrate species. In crayfish and lobster in particular, phasic motor neurons are associated with a fast muscle phenotype and tonic motor neurons are associated with slow muscles (Atwood, 1976; Günzel et al., 1993
; Atwood and Cooper, 1996b
; LaFramboise et al., 1999
; Griffis et al., 2000
). Since troponin-I and -T expression was correlated with regional variation in synaptic properties, we propose that a presynaptic-induced mechanism leads to the enhanced postsynaptic facilitation, which in turn results in a Ca2+-induced activation of genes encoding slow-tonic fibre isoforms. This does not exclude the possibility of a retrograde factor altering the nerve terminal properties or even the possibility of mutual interactions between the synapse and the muscle fibre phenotype.
Our results are in general agreement with earlier work examining regional differences in the phenotype and physiological properties of the crayfish opener muscle. Günzel et al. (1993) distinguished three fibre types (A, B and C) in three species of crayfish on the basis of the stability of myofibrillar ATPase at basic pH values. Fibres with low and intermediate ATPase activities (A and B fibres, respectively) were most abundant in the proximal region, while fibres with the highest ATPase activity (C fibres) were most abundant in the central region. Since all fibres in the opener muscle have long sarcomeres (Günzel et al., 1993
), the A/B fibres probably corresponded to S2 fibres and the C fibres to S1 fibres. The regional differences in the EPSP amplitudes were the same as we show here, although the absolute amplitudes of the EPSPs of the proximal fibres were significantly smaller.
The opener muscle in crayfish has provided a great deal of insight into the fundamental mechanisms of synaptic transmission (Biedermann, 1887; Wiersma, 1933
; Dudel, 1965
; Atwood, 1967
, 1973
, 1976
, 1982
; Atwood et al., 1994
; Zucker, 1973
, 1974a
,b
; Bittner and Sewell, 1976
; Parnas et al., 1982a
,b
,c
,d
; Dudel et al., 1983
; Vyshedskiy and Lin, 1997a
,b
,c
). The regional differentiation in synaptic strength and facilitation, which arises from the single motor neuron, has led to many hypotheses regarding the underlying presynaptic mechanisms (Iravani, 1965
; Atwood, 1967
; Bittner, 1968a
,b
; Sherman and Atwood, 1972
; Zucker, 1974a
; Parnas et al., 1982a
; Zucker and Haydon, 1988
; Dudel, 1989a
,b
,c
,d
). It is now known that the majority of the differences result from local presynaptic changes in synaptic structure and physiology (Atwood et al., 1994
; Atwood and Cooper, 1995
, 1996a
,b
; Cooper et al., 1995b
, 1996a
,b
). However, the basis for the regional differentiation is not understood.
Frank (1973) proposed that the target muscle determines the release properties of the motor nerve terminals in lobsters. For example, it appears that in the cricket Acheta domesticus a retrograde factor from target neurons can locally alter nerve terminal function (Davis and Murphey, 1993
). Similarly, for a motor neuron in the stomatogastric system of the lobster, a similar observation was made for target influences on a single presynaptic neuron for two different terminals (Katz et al., 1993
). It has also been proposed that motor neurons influence muscle differentiation (for reviews, see Atwood, 1973
; Grinnell, 1995
). The proposed mechanisms have focused primarily on activity patterns and neurotrophic substances of the neurons. In crustacean systems, the timing of innervation during fibre differentiation may determine the final properties of the fibre (for a review, see Atwood, 1973
).
Such local differences in the terminals also occur in the crayfish. The central region of the opener muscle contains nerve terminals arranged in long chains of varicosities (swellings), whereas the nerve terminals are grouped into clusters of varicosities in the proximal region (Atwood and Cooper, 1996b). Ultrastructural analysis has shown that the varicosities contain the majority of the synaptic contacts (Florey and Cahill, 1982
; Cooper et al., 1995b
). It has also been shown that the efficacy of synaptic transmission decreases along the length of a single terminal (Cooper et al., 1996a
). The varicosities on the proximal fibres have high synaptic outputs compared with the relatively low output of varicosities in the central region. High-output varicosities along a terminal contain more active sites per synapse than do low-output varicosities, which contain a high percentage of synapses with only one or no active sites on the synapse (Govind et al., 1994
; Cooper et al., 1996a
). This indicates that there are more silent synapses in the low-output varicosities (Atwood and Wojtowicz, 1999
). The differences in the synaptic structure among the varicosities may in part explain the differences in the Ca2+ influx during stimulation at various frequencies (Cooper et al., 1995b
, 1996b
). This synaptic complexity within the varicosities appears to account for much of the difference in EPSP amplitudes between the proximal and central fibres (Cooper et al., 1996a
).
Presynaptic structural elements that control the amount of neurotransmitter release may indeed drive muscle phenotype, but then what drives the regional differences of a single motor neuron to display structural differences in terminal length and degree of branching? Perhaps the regional differences in a developmentally regulated muscle phenotype determine and maintain the regional differences of the motor neuron. This suggests that the phenotype is developmentally fixed, either by a fibres location during development or by some property of timing in innervation with development (for a review, see Atwood, 1973).
An alternative hypothesis is that, given the pinnate arrangement of the fibres, some fibres are stretched more than others and thus have a greater amount of force exerted on them per fibre mass, resulting in differential cellular regulation of muscle phenotype. This, in turn, may cause the muscle to induce changes in synaptic structure during development. Alterations in the levels of proteins involved with synaptic vesicle docking and release change the release characteristics of motor neurons in crustaceans (He et al., 1999). A factor secreted from the muscle or localized on the surface could produce regional differences in synaptic properties. For example, it is known that a reduced expression of Fasciclin II in Drosophila melanogaster neuromuscular junctions produces shorter motor nerve terminals but, as a result, the nerve compensates by altering synaptic structure to produce an enhanced synaptic efficacy (Stewart et al., 1996
). In another Drosophila melanogaster mutation, Highwire, lower-output synapses are associated with greatly expanded terminals on the muscle fibres (Wan et al., 2000
). Such evidence in insects and crustaceans suggests a tight regulation in the communication between the nerve and muscle as for classical Hebbian models and homeostatic mechanisms (for a review, see Turrigiano, 1999
).
The strong correlation between synaptic properties and expression of troponin-T and -I isoforms suggests that neurotransmission patterns regulate or maintain gene expression and, thus, determine slow-twitch (S1) and slow-tonic (S2) phenotypes. In mammals, motor neuron activity controls the expression of fibre-type-specific isoforms of myosin heavy and light chains, tropomyosin and troponin-I, -C and -T (for reviews, see Buonanno et al., 1998; Pette, 1998
). Differences in muscle phenotype, identified by biochemical properties, and characteristics in the strength of synaptic transmission correlate well in the abdominal superficial flexor muscle in lobsters (Neil and Fowler, 1990
). However, this particular muscle is innervated by five excitatory neurons and one inhibitory neuron, so numerous mechanisms may give rise to fibre type differentiation. Chronic electrical stimulation of crayfish abdominal muscle induces a shift from fast to slow-tonic myofibrillar protein composition, although the identities of the isoforms have not been established (Cooper et al., 1998
). Fibre transformation during claw differentiation in lobsters and snapping shrimp Alpheus heterochelis requires an intact nerve supply (Govind and Kent, 1982
; Govind et al., 1988
). In mammalian and avian muscles, elevated intracellular [Ca2+], driven by motor neuron activity, stimulates Ca2+-dependent signal-transduction enzymes (e.g. calcineurin, calmodulin kinase and protein kinase C) that regulate slow fibre genes (Antipenko et al., 1999
; Naya et al., 2000
; DiMario, 2001
).
In conclusion, regional differences in synaptic transmission and myofibrillar protein isoform composition were observed in a muscle that is innervated by a single excitatory tonic motor neuron. The high-output terminals on the proximal region of the muscle produced larger EPSPs than the low-output terminals on the central region of the muscle. The distal region behaved electrophysiologically as being intermediate between the central and proximal regions. There were also differences in STF between these regions. The differential responses to facilitation depended on the type of stimulation paradigm used, so a range of stimulation conditions from trains of 10 to 20 stimuli given at frequencies of 3050 Hz was used to characterize regional differences in STF.
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Antipenko, A., Frías, J. A., Parra, J., Cadefau, J. A. and Cussó, R. (1999). Effect of chronic electrostimulation of rabbit skeletal muscle on calmodulin level and protein kinase activity. Int. J. Biochem. Cell Biol. 31, 303310.[Medline]
Atwood, H. L. (1967). Variation in physiological properties of crustacean motor synapses. Nature 215, 5758.[Medline]
Atwood, H. L. (1973). An attempt to account for the diversity of crustacean muscles. Am. Zool. 13, 357378.
Atwood, H. L. (1976). Organization and synaptic physiology of crustacean neuromuscular systems. Prog. Neurobiol. 7, 291391.[Medline]
Atwood, H. L. (1982). Synapses and neurotransmitters. In The Biology of Crustacea, vol. 3 (ed. H. L. Atwood and D. C. Sandeman), pp. 105150. New York: Academic Press, Inc.
Atwood, H. L. and Cooper, R. L. (1995). Functional and structural parallels in crustaceans and Drosophila neuromuscular systems. Am. Zool. 35, 556565.
Atwood, H. L. and Cooper, R. L. (1996a). Assessing ultrastructure of crustacean and insect neuromuscular junctions. J. Neurosci. Meth. 69, 5158.[Medline]
Atwood, H. L. and Cooper, R. L. (1996b). Synaptic diversity and differentiation: Crustacean neuromuscular junctions. Invertebrate Neurosci. 1, 291307.
Atwood, H. L., Cooper, R. L. and Wojtowicz, J. M. (1994). Non-uniformity and plasticity of quantal release at crustacean motor nerve terminals. In Advances in Second Messenger and Phosphoprotein Research. Molecular and Cellular Mechanisms of Neurotransmitter Release (ed. L. Stjärne, P. Greengard, S. E. Grillner, T. G. M. Hökfelt and D. R. Ottoson), pp. 363382. New York: Raven Press.
Atwood, H. L. and Wojtowicz, J. M. (1986). Short-term plasticity and physiological differentiation of crustacean motor synapses. Int. Rev. Neurobiol. 28, 275362.[Medline]
Atwood, H. L. and Wojtowicz, J. M. (1999). Silent synapses in neural plasticity: Current evidence. Learning Memory 6, 542571.
Biedermann, W. (1887). Beiträge zur allgemeinen Nerven- und Muskelphysiologie. Zwanzigste Mittheilung. Über die Innervation der Krebsschere. Sitz. Berlin D. Akad. Wiss. Wien, Math. Naturwiss. Kl. Abt. III 95, 740.
Bittner, G. D. (1968a). Differentiation of nerve terminals in the crayfish opener muscle and its functional significance. J. Gen. Physiol. 51, 731758.
Bittner, G. D. (1968b). The differentiation of crayfish muscle fibers during development. J. Exp. Zool. 167, 439456.
Bittner, G. D. and Sewell, V. L. (1976). Facilitation at crayfish neuromuscular junctions. J. Comp. Neurol. 109, 287308.
Buonanno, A., Cheng, J., Venepally, P., Weis, J. and Calvo, S. (1998). Activity-dependent regulation of muscle genes: repressive and stimulatory effects of innervation. Acta Physiol. Scand. 163, S17S26.[Medline]
Cooper, R. L., Hampson, D. and Atwood, H. L. (1995a). Synaptotagmin-like expression in the motor nerve terminals of crayfish. Brain Res. 703, 214216.[Medline]
Cooper, R. L., Harrington, C. C., Marin, L. and Atwood, H. L. (1996a). Quantal release at visualized terminals of a crayfish motor axon: Intraterminal and regional differences. J. Comp. Neurol. 375, 583600.[Medline]
Cooper, R. L., Marin, L. and Atwood, H. L. (1995b). Synaptic differentiation of a single motor neuron: Conjoint definition of transmitter release, presynaptic calcium signals and ultrastructure. J. Neurosci. 15, 42094222.[Abstract]
Cooper, R. L., Stewart, B. A., Wojtowicz, J. M., Wang, S. and Atwood, H. L. (1995c). Quantal measurement and analysis methods compared for crayfish and Drosophila neuromuscular junctions and rat hippocampus. J. Neurosci. Meth. 61, 6779.[Medline]
Cooper, R. L., Warren, W. M. and Ashby, H. E. (1998). Activity of phasic motor neurons partially transforms the neuronal and muscle phenotype to a tonic-like state. Muscle Nerve 21, 921931.[Medline]
Cooper, R. L., Winslow, J., Govind, C. K. and Atwood, H. L. (1996b). Synaptic structural complexity as a factor enhancing probability of calcium-mediated transmitter release. J. Neurophysiol. 75, 24512466.
Cotton, J. L. S. and Mykles, D. L. (1993). Cloning of a crustacean myosin heavy chain isoform: exclusive expression in fast muscle. J. Exp. Zool. 267, 578586.[Medline]
Covi, J. A., Belote, J. M. and Mykles, D. L. (1999). Subunit compositions and catalytic properties of proteasomes from developmental temperature-sensitive mutants of Drosophila melanogaster. Arch. Biochem. Biophys. 368, 8597.[Medline]
Crider, M. E. and Cooper, R. L. (1999). The importance of the stimulation paradigm in determining facilitation and effects of neuromodulation. Brain Res. 842, 324331.[Medline]
Crider, M. E. and Cooper, R. L. (2000). Differentially facilitation of high- and low-output nerve terminals from a single motor neuron. J. Appl. Physiol. 88, 987996.
Davis, G. W. and Murphey, R. K. (1993). A role for postsynaptic neurons in determining presynaptic release properties in the cricket CNS: Evidence for retrograde control of facilitation. J. Neurosci. 13, 38273838.[Abstract]
DiMario, J. X. (2001). Protein kinase C signaling controls skeletal muscle fiber types. Exp. Cell Res. 263, 2332.[Medline]
Dudel, J. (1965). Potential changes in the crayfish motor nerve terminal during repetitive stimulation. Pflügers Arch. 282, 323337.
Dudel, J. (1989a). Calcium dependence of quantal release triggered by graded depolarization pulses to nerve terminals on crayfish and frog muscle. Pflügers Arch. 415, 289298.[Medline]
Dudel, J. (1989b). Shifts in the voltage dependence of synaptic release due to changes in the extracellular calcium concentration at nerve terminals on muscle of crayfish and frogs. Pflügers Arch. 415, 299303.[Medline]
Dudel, J. (1989c). Calcium and depolarization dependence of twin-pulse facilitation of synaptic release at nerve terminal of crayfish and frog muscle. Pflügers Arch. 415, 304309.[Medline]
Dudel, J. (1989d). Twin pulse facilitation in dependence on pulse duration and calcium concentration at motor nerve terminals of crayfish and frog. Pflügers Arch. 415, 310315.[Medline]
Dudel, J. and Kuffler, S. W. (1961). The quantal nature of transmission and spontaneous miniature potentials at the crayfish neuromuscular junction. J. Physiol., Lond. 155, 514529.[Medline]
Dudel, J., Parnas, I. and Parnas, H. (1983). Neurotransmitter release and its facilitation in crayfish muscle. VI. Release determined by both intracellular calcium concentration and depolarization of the nerve terminal. Pflügers Arch. 399, 110.[Medline]
Florey, E. and Cahill, M. A. (1982). The innervation pattern of crustacean skeletal muscle. Cell Tissue Res. 224, 527541.[Medline]
Frank, E. (1973). Matching of facilitation at the neuro-muscular junction of the lobster: a possible case for influence of muscle on nerve. J. Physiol., Lond. 233, 635658.[Medline]
Galler, S. and Neil, D. M. (1994). Calcium-activated and stretch-induced force responses in two biochemically defined muscle fibre types of the Norway lobster. J. Muscle Res. Cell Motil. 15, 390399.[Medline]
Garone, L., Theibert, J. L., Miegel, A., Maeda, Y., Murphy, C. and Collins, J. H. (1991). Lobster troponin C: Amino acid sequences of three isoforms. Arch. Biochem. Biophys. 291, 8991.[Medline]
Govind, C. K. and Kent, K. S. (1982). Transformation of fast fibres to slow prevented by lack of activity in developing lobster muscle. Nature 298, 755757.[Medline]
Govind, C. K., Pearce, J., Wojtowicz, J. M. and Atwood, H. L. (1994). Strong and weak synaptic differentiation in the crayfish opener muscle: structural correlates. Synapse 16, 4558.[Medline]
Govind, C. K., Wong, A. and Pearce, J. (1988). Experimental induction of claw transformation in snapping shrimps. J. Exp. Zool. 248, 371375.
Griffis, B., Bonner, P. and Cooper, R. L. (2000). Sensitivity of transformed (phasic to tonic) motor neurons to the neuromodulator 5-HT. Comp. Biochem. Physiol. 127A, 495504.
Grinnell, A. (1995). Dynamics of nervemuscle interaction in developing and mature neuromuscular junctions. Physiol. Rev. 75, 789834.
Günzel, D., Galler, S. and Rathamayer, W. (1993). Fibre heterogeneity in the closer and opener muscles of the crayfish walking legs. J. Exp. Biol. 175, 267281.
He, P., Southard, R. C., Whiteheart, S. W. and Cooper, R. L. (1999). Role of -SNAP in promoting efficient neurotransmission at the crayfish neuromuscular junction. J. Neurophysiol. 82, 34063416.
Holmes, J. M., Hilber, K., Galler, S. and Neil, D. M. (1999). Shortening properties of two biochemically defined muscle fibre types of the Norway lobster Nephrops norvegicus L. J. Muscle Res. Cell Motil. 20, 265278.[Medline]
Iravani, J. (1965). Membrandepolarisation der Muskelfasern des Öffnermuskels des Flusskrebses auf Nervenreiz und Kaliumapplikation. Experientia 21, 609610.[Medline]
Ishimoda-Takagi, T., Itoh, M. and Koyama, H. (1997). Distribution of tropomyosin isoforms in spiny lobster muscles. J. Exp. Zool. 277, 8798.
Katz, B. and Miledi, R. (1968). The role of calcium in neuromuscular facilitation. J. Physiol., Lond. 195, 481492.[Medline]
Katz, P. S., Kirk, M. D. and Govind, C. K. (1993). Facilitation and depression at different branches of the same motor axon: evidence for presynaptic differences in release. J. Neurosci. 13, 30753089.[Abstract]
Kobayashi, T., Takagi, T., Konishi, K. and Wnuk, W. (1989). Amino acid sequence of the two major isoforms of troponin C from crayfish. J. Biol. Chem. 264, 1824718259.
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680685.[Medline]
LaFramboise, W., Griffis, B., Bonner, P., Warren, W., Scalise, D., Guthrie, R. D. and Cooper, R. L. (1999). Muscle type-specific myosin isoforms in crustacean muscles. J. Exp. Zool. 286, 3648.
Li, Y. and Mykles, D. L. (1990). Analysis of myosins from lobster muscles: Fast and slow isozymes differ in heavy-chain composition. J. Exp. Zool. 255, 163170.
Linder, T. M. (1974). The accumulative properties of facilitation at crayfish neuromuscular synapses. J. Physiol., Lond. 238, 223234.[Medline]
Miegel, A., Kobayashi, T. and Maéda, Y. (1992). Isolation, purification and partial characterization of tropomyosin and troponin subunits from the lobster tail muscle. J. Muscle Res. Cell Motil. 13, 608618.[Medline]
Miyazaki, J.-I., Hosoya, M., Ishimoda-Takagi, T. and Hirabayashi, T. (1990). Tissue specificity of tropomyosin from the crayfish, Cambarus clarki. J. Biochem. 108, 5965.[Abstract]
Miyazaki, J.-I., Makioka, T., Fujiwara, Y. and Hirabayashi, T. (1992). Tissue specificity of crustacean tropomyosin. J. Exp. Zool. 263, 235244.
Miyazaki, J.-I., Yahata, K., Makioka, T. and Hirabayashi, T. (1993). Tissue specificity of arthropod tropomyosin. J. Exp. Zool. 267, 501509.
Mykles, D. L. (1985a). Multiple variants of myofibrillar proteins in single fibers of lobster claw muscles: evidence for two types of slow fibers in the cutter closer muscle. Biol. Bull. 169, 476483.
Mykles, D. L. (1985b). Heterogeneity of myofibrillar proteins in lobster fast and slow muscles: variants of troponin, paramyosin and myosin light chains comprise four distinct protein assemblages. J. Exp. Zool. 234, 2332.[Medline]
Mykles, D. L. (1988). Histochemical and biochemical characterization of two slow fiber types in decapod crustacean muscles. J. Exp. Zool. 245, 232243.[Medline]
Mykles, D. L. (1997). Crustacean muscle plasticity: Molecular mechanisms determining mass and contractile properties. Comp. Biochem. Physiol. 117B, 367378.
Mykles, D. L., Cotton, J. L. S., Taniguchi, H., Sano, K. I. and Maeda, Y. (1998). Cloning of tropomyosins from lobster (Homarus americanus) striated muscles: fast and slow isoforms may be generated from the same transcript. J. Muscle Res. Cell Motil. 19, 105115.[Medline]
Naya, F. J., Mercer, B., Shelton, J., Richardson, J. A., Williams, R. S. and Olson, E. N. (2000). Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J. Biol. Chem. 275, 45454548.
Neil, D. M. and Fowler, W. S. (1990). Histochemical and biochemical heterogeneity in crustacean postural muscle. In Frontiers in Crustacean Neurobiology. Advances in Life Sciences (ed. K. Wiese, W.-D. Krenz, J. Tautz, H. Reichert and B. Mulloney), pp. 359367. Basel: Birkhäuser Verlag.
Neil, D. M., Fowler, W. S. and Tobasnick, G. (1993). Myofibrillar protein composition correlates with histochemistry in fibres of the abdominal flexor muscles of the Norway lobster Nephrops norvegicus. J. Exp. Biol. 183, 185201.
Nishita, K. and Ojima, T. (1990). American lobster troponin. J. Biochem. 108, 677683.[Abstract]
Parnas, H., Dudel, J. and Parnas, I. (1982a). Neurotransmitter release and its facilitation in crayfish. I. Saturation kinetics of release and of entry and removal of calcium. Pflügers Arch. 393, 114.[Medline]
Parnas, I., Parnas, H. and Dudel, J. (1982b). Neurotransmitter release and its facilitation in crayfish muscle. II. Duration of facilitation and removal processes of calcium from the terminal. Pflügers Arch. 393, 323236.
Parnas, H., Dudel, J. and Parnas, I. (1982c). Neurotransmitter release and its facilitation in crayfish. IV. The effect of Mg2+ ions on the duration of facilitation. Pflügers Arch. 395, 15.[Medline]
Parnas, I., Parnas, H. and Dudel, J. (1982d). Neurotransmitter release and its facilitation in crayfish muscle. V. Basis for synapse differentiation of the fast and slow type in one axon. Pflügers Arch. 395, 261270.[Medline]
Pette, D. (1998). Training effects on the contractile apparatus. Acta Physiol. Scand. 162, 367376.[Medline]
Sakurai, Y., Kanzawa, N. and Maruyama, K. (1996). Characterization of myosin and paramyosin from crayfish fast and slow muscles. Comp. Biochem. Physiol. 113B, 105111.
Sherman, R. G. and Atwood, H. L. (1972). Correlated electrophysiological and ultrastructural studies of a crustacean motor unit. J. Gen. Physiol. 59, 586615.
Sohn, J., Mykles, D. L. and Cooper, R. L. (2000). The anatomical, physiological and biochemical characterization of muscles associated with the articulating membrane in the dorsal surface of the crayfish abdomen. J. Exp. Zool. 287, 353377.[Medline]
Stewart, B. A., Schuster, C. M., Goodman, C. S. and Atwood, H. L. (1996). Homeostasis of synaptic transmission in Drosophila with genetically altered nerve terminal morphology. J. Neurosci. 5, 38773886.
Towbin, H., Stahelin, T. and Gordon, J. (1979). Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 43504354.[Abstract]
Tryba, A. K. and Hartman, H. B. (1997). Dynamic responses of series force receptors innervating the opener muscle apodeme in the blue crab, Callinectes sapidus. J. Comp. Physiol. A 180, 215221.[Medline]
Turrigiano, G. G. (1999). Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci. 22, 221227.[Medline]
Velez, S. J., Bittner, G. D., Atwood, H. L. and Govind, C. K. (1981). Trophic interactions of crayfish muscle fibers and neuromuscular synapses after denervation, tenotomy and immobilization. Exp. Neurol. 71, 307325.[Medline]
Vyshedskiy, A. and Lin, J.-W. (1997a). Study of the inhibitor of the crayfish neuromuscular junction by presynaptic voltage control. J. Neurophysiol. 77, 103115.
Vyshedskiy, A. and Lin, J.-W. (1997b). Activation and detection of facilitation as studied by presynaptic voltage control at the inhibitor of the crayfish opener muscle. J. Neurophysiol. 77, 23002315.
Vyshedskiy, A. and Lin, J.-W. (1997c). Change of transmitter release kinetics during facilitation revealed by prolong test pulses at the inhibitor of the crayfish opener muscle. J. Neurophysiol. 78, 17911799.
Wan, H. I., DiAntonin, A., Fetter, R. D., Bergstrom, K., Strauss, R. and Goodman, C. S. (2000). Highwire regulates synaptic growth in Drosophila. Neuron 26, 313329.[Medline]
Wiersma, C. A. G. (1933). Vergleichende Untersuchungen über das periphere NerveMuskel-System von Crustaceen. Z. Vergl. Physiol. 19, 349385.
Wray, W., Boulikas, T., Wray, V. P. and Hancock, R. (1981). Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118, 197203.[Medline]
Zucker, R. S. (1973). Changes in the statistics of transmitter release during facilitation. J. Physiol., Lond. 229, 787810.[Medline]
Zucker, R. S. (1974a). Crayfish neuromuscular facilitation activated by constant presynaptic action potentials and depolarizing pules. J. Physiol., Lond. 241, 6989.[Medline]
Zucker, R. S. (1974b). Characteristics of crayfish neuromuscular facilitation and their calcium dependence. J. Physiol., Lond. 241, 91110.[Medline]
Zucker, R. S. and Haydon, P. G. (1988). Membrane potential has no direct role in evoking neurotransmitter release. Nature 335, 360362.[Medline]