Synaptic vesicle cycling at type‐identified diaphragm neuromuscular junctions

Mantilla, Carlos B.; Rowley, Katharine L.; Fahim, Mohamed A.; Zhan, Wen Zhi; Sieck, Gary C.

doi:10.1002/mus.20173

Cited by 31 publications

(71 citation statements)

References 44 publications

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“…Methods for imaging presynaptic terminals at type-identified diaphragm muscle fibers have been described previously (Mantilla et al 2004). Briefly, the diaphragm muscle was excised together with the phrenic nerve and placed in oxygenated Rees-Simpson solution [containing (in mM) 135 Na ϩ , 5 K ϩ , 2 Ca 2ϩ , 1 Mg 2ϩ , 120 Cl Ϫ , and 25 HCO 3 Ϫ ) bubbled with 95% O 2 -5% CO 2 at room temperature.…”

Section: Morphology Of the Presynaptic Terminalmentioning

confidence: 99%

“…From the projection image, presynaptic terminals were manually circumscribed making sure that the entire terminal was included. Presynaptic terminals innervating type I or IIa fibers (expressing MHC isoforms MHC Slow or MHC 2A , respectively) were distinguished from those innervating type IIx and/or IIb fibers (expressing MHC 2X or MHC 2B , respectively) based on NMJ morphology as previously described (Mantilla et al 2004;Prakash et al 1996). The planar area of individual presynaptic terminals was determined from the circumscribed region of interest.…”

Section: Morphology Of the Presynaptic Terminalmentioning

confidence: 99%

“…The methods for electron microscopy of presynaptic terminals at type-identified diaphragm muscle fibers were described previously (Mantilla et al 2004). Briefly, animals were transcardially perfused with 4% paraformaldehyde in phosphate-buffered saline (PBS; pH 7.6).…”

Section: Morphology Of the Presynaptic Terminalmentioning

confidence: 99%

“…Although much is known about synaptic vesicle pools at mammalian NMJs (Ellisman et al 1976;Mantilla et al 2004;Pieribone et al 1995;Reid et al 1999;Wilson 1979), their distribution and size and the mechanisms regulating vesicle release during repeated activation are incompletely understood.…”

Section: Introductionmentioning

confidence: 99%

“…Based on myosin heavy chain (MHC) composition, diaphragm motor units differ in activation history and susceptibility to fatigue (Johnson and Sieck 1993;Sieck and Fournier 1989). Presynaptic terminals at type I or IIa diaphragm fibers have smaller cycling pool size despite greater average synaptic vesicle density at active zones compared with those at type IIx and/or IIb fibers (Mantilla et al 2004). We hypothesize that the more frequently recruited terminals (at type I or IIa fibers) have smaller QC compared with terminals at type IIx and/or IIb fibers and that the mechanisms involved in QC decline vary across fiber types in accordance with known differences in activation history.…”

Section: Introductionmentioning

confidence: 99%

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Synaptic Vesicle Distribution and Release at Rat Diaphragm Neuromuscular Junctions

Rowley

Mantilla²,

Ermilov

et al. 2007

Journal of Neurophysiology

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Rowley KL, Mantilla CB, Ermilov LG, Sieck GC. Synaptic vesicle distribution and release at rat diaphragm neuromuscular junctions. J Neurophysiol 98: 478 -487, 2007. First published May 9, 2007 doi:10.1152/jn.00251.2006. Synaptic vesicle release at the neuromuscular junction (NMJ) is highly reliable and is vital to the success of synaptic transmission. We examined synaptic vesicle number, distribution, and release at individual type-identified rat diaphragm NMJ. Three-dimensional reconstructions of electron microscopy images were used to obtain novel measurements of active zone distribution and the number of docked synaptic vesicles. Diaphragm musclephrenic nerve preparations were used to perform electrophysiological measurements of the decline in quantal content (QC) during repetitive phrenic nerve stimulation. The number of synaptic vesicles available for release vastly exceeds those released with a single stimulus, thus reflecting a relatively low probability of release for individual docked vesicles and at each active zone. There are two components that describe the decline in QC resulting from repetitive stimulation: a rapid phase (Ͻ0.5 s) and a delayed phase (Ͻ2.5 s). Differences in the initial rapid decline in QC were evident across type-identified presynaptic terminals (fiber type classification based on myosin heavy chain composition). At terminals innervating type IIx and/or IIb fibers, the initial decline in QC during repetitive stimulation matched the predicted depletion of docked synaptic vesicles. In contrast, at terminals innervating type I or IIa fibers, a faster than predicted decline in QC with repetitive stimulation suggests that a decrease in the probability of release at these terminals plays a role in addition to depletion of docked vesicles. Differences in QC decline likely reflect fiber-type specific differences in activation history and correspond with welldescribed differences in neuromuscular transmission across muscle fiber types.

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Section: Morphology Of the Presynaptic Terminalmentioning

confidence: 99%

Section: Morphology Of the Presynaptic Terminalmentioning

confidence: 99%

Section: Morphology Of the Presynaptic Terminalmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Synaptic Vesicle Distribution and Release at Rat Diaphragm Neuromuscular Junctions

Rowley

Mantilla²,

Ermilov

et al. 2007

Journal of Neurophysiology

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Mechanical Properties of Respiratory Muscles

Sieck

Ferreira

Reid

et al. 2013

Comprehensive Physiology

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Striated respiratory muscles are necessary for lung ventilation and to maintain the patency of the upper airway. The basic structural and functional properties of respiratory muscles are similar to those of other striated muscles (both skeletal and cardiac). The sarcomere is the fundamental organizational unit of striated muscles and sarcomeric proteins underlie the passive and active mechanical properties of muscle fibers. In this respect, the functional categorization of different fiber types provides a conceptual framework to understand the physiological properties of respiratory muscles. Within the sarcomere, the interaction between the thick and thin filaments at the level of cross-bridges provides the elementary unit of force generation and contraction. Key to an understanding of the unique functional differences across muscle fiber types are differences in cross-bridge recruitment and cycling that relate to the expression of different myosin heavy chain isoforms in the thick filament. The active mechanical properties of muscle fibers are characterized by the relationship between myoplasmic Ca2+ and cross-bridge recruitment, force generation and sarcomere length (also cross-bridge recruitment), external load and shortening velocity (cross-bridge cycling rate), and cross-bridge cycling rate and ATP consumption. Passive mechanical properties are also important reflecting viscoelastic elements within sarcomeres as well as the extracellular matrix. Conditions that affect respiratory muscle performance may have a range of underlying pathophysiological causes, but their manifestations will depend on their impact on these basic elemental structures.

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Evolution and Functional Differentiation of the Diaphragm Muscle of Mammals

Fogarty¹,

Sieck²

2019

Comprehensive Physiology

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Symmorphosis is a concept of economy of biological design, whereby structural properties are matched to functional demands. According to symmorphosis, biological structures are never over designed to exceed functional demands. Based on this concept, the evolution of the diaphragm muscle (DIAm) in mammals is a tale of two structures, a membrane that separates and partitions the primitive coelomic cavity into separate abdominal and thoracic cavities and a muscle that serves as a pump to generate intra-abdominal (P ab ) and intra-thoracic (P th ) pressures. The DIAm partition evolved in reptiles from folds of the pleural and peritoneal membranes that was driven by the biological advantage of separating organs in the larger coelomic cavity into separate thoracic and abdominal cavities, especially with the evolution of aspiration breathing. The DIAm pump evolved from the advantage afforded by more effectively generation of both a negative P th for ventilation of the lungs and a positive P ab for venous return of blood to the heart and expulsive behaviors such as airway clearance, defecation, micturition, and child birth. Didactic SynopsisThe DIAm separates abdominal and thoracic cavities; thus, it is a partition, and its evolution reflects that important role in isolating organs into separate thoracic and abdominal cavities. However, the DIAm is also a muscle, and is most often described as the principal pump muscle of inspiration. However, the DIAm also serves as a pump for generating both negative P th and positive P ab in other motor behaviors. Accordingly, the evolution of the DIAm is more complex and should be considered in the context of its dual physiological roles as a partition and muscular pump. In considering DIAm evolution, we adopt the guiding concept of symmorphosis or economy of design, where biological structures are not over designed for their functional roles. Thus, this is a tale of the evolution of two diaphragms, a partition and a muscular pump that separates thoracic and abdominal cavities but also affects generation of P th and P ab .

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Synaptic vesicle cycling at type‐identified diaphragm neuromuscular junctions

Cited by 31 publications

References 44 publications

Synaptic Vesicle Distribution and Release at Rat Diaphragm Neuromuscular Junctions

Synaptic Vesicle Distribution and Release at Rat Diaphragm Neuromuscular Junctions

Mechanical Properties of Respiratory Muscles

Evolution and Functional Differentiation of the Diaphragm Muscle of Mammals

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