Mechanical stimulation of skeletal muscle generates lipid‐related second messengers by phospholipase activation

Vandenburgh, Herman H.; Shansky, Janet; Karlisch, Patricia; Solerssi, Rosa

doi:10.1002/jcp.1041550109

Cited by 70 publications

(41 citation statements)

References 33 publications

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“…Persistence of the responses, however, in low external Ca 2ϩ argues against Ca 2ϩ entry as the initiating factor in the stretch-dependent responses of ICC-IM. Phospholipase A 2 (PLA 2 ), which liberates arachidonic acid, is mechanosensitive in some cells (46,47). Thus, it is possible that mechanotransduction coupling, linked through activation of PLA 2 , could be a previously unrecognized property of ICC-IM.…”

Section: Discussionmentioning

confidence: 99%

Interstitial cells of Cajal mediate mechanosensitive responses in the stomach

Won

Sanders

Ward

2005

Proc. Natl. Acad. Sci. U.S.A.

152

141

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Changes in motor activity are a basic response to filling of smooth muscle organs. Responses to gastric filling, for example, are thought to be regulated by neural reflexes. Here, we demonstrate a previously uncharacterized aspect of stretch-dependent responses in visceral smooth muscles that is mediated by mechanosensitive interstitial cells of Cajal. Length ramps were applied to the murine antral muscles while recording intracellular electrical activity and isometric force. Stretching muscles by an average of 27 ؎ 1% of resting length resulted in 5 mN of force. Increasing length caused membrane depolarization and increased slow-wave frequency. The responses were dependent on the rate of stretch. Stretch-dependent responses were not inhibited by neuronal antagonists or nifedipine. Increases in slow-wave frequency, but not membrane depolarization, were inhibited by reducing external Ca 2؉ (100 M) and by Ni 2؉ (250 M). Responses to stretch were inhibited by indomethacin (1 M) and were absent in cyclooxygenase II-deficient mice, suggesting that cyclooxygenase II-derived eicosanoids may mediate these responses. Dual microelectrode impalements of muscle cells within the corpus and antrum showed that stretch-induced changes in slow-wave frequency uncoupled proximal-to-distal propagation of slow waves. This uncoupling could interfere with gastric peristalsis and impede gastric emptying. Stretch of antral muscles of W͞W V mice, which lack intramuscular interstitial cells of Cajal, did not affect membrane depolarization or slow-wave frequency. These data demonstrate a previously uncharacterized nonneural stretch reflex in gastric muscles and provide physiological evidence demonstrating a mechanosensitive role for interstitial cells of Cajal in smooth muscle tissues.gastric compliance ͉ pacemaker ͉ stretch ͉ slow waves ͉ propagation

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Section: Discussionmentioning

confidence: 99%

Interstitial cells of Cajal mediate mechanosensitive responses in the stomach

Won

Sanders

Ward

2005

Proc. Natl. Acad. Sci. U.S.A.

152

141

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“…PGF2a treatment also leads to increased activity of PI-3K, ERK, and JNK, although the mechanism is less clear. PGF2a accumulates in muscle during stretch (10), is a potent stimulator of growth and differentiation (140,141), and inhibitors of prostaglandin synthesis appear to block stretch induced growth in vitro (10,134), but not necessarily in vivo (142).The phospholipase C family are specific for phosphatidylinositols, and cleave the sugar headgroup from the glycerol backbone, leaving a diacylglycerol (DAG) and a soluble inositol (132,145), apparently through a receptor mediated mechanism (145), and this could be a mechanism to amplify an influx of calcium from the extracellular space.Most phospholipase D nonspecifically cleave phospholipids, leaving the phosphate group attached to the glycerol backbone to generate a phosphatidic acid and generally a free choline (146). PLD activity is increased after stretch, potentially activated by PKC, but also potentially by gangliosides or RhoA (146).…”

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confidence: 99%

Mechanotransduction in skeletal muscle

Burkholder¹

2007

Front Biosci

110

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Mechanical signals are critical to the development and maintenance of skeletal muscle, but the mechanisms that convert these shape changes to biochemical signals is not known. When a deformation is imposed on a muscle, changes in cellular and molecular conformations link the mechanical forces with biochemical signals, and the close integration of mechanical signals with electrical, metabolic, and hormonal signaling may disguise the aspect of the response that is specific to the mechanical forces. The mechanically induced conformational change may directly activate downstream signaling and may trigger messenger systems to activate signaling indirectly. Major effectors of mechanotransduction include the ubiquitous mitogen activated protein kinase (MAP) and phosphatidylinositol-3' kinase (PI-3K), which have well described receptor dependent cascades, but the chain of events leading from mechanical stimulation to biochemical cascade is not clear. This review will discuss the mechanics of biological deformation, loading of cellular and molecular structures, and some of the principal signaling mechanisms associated with mechanotransduction. KeywordsSkeletal muscle; mechanotransduction; stretch INTRODUCTIONThe detection and response to physical forces is essential to all cells, but is particularly relevant to those that play a fundamentally mechanical role. The primordial nature of the cellular interaction with the physical world suggests that its control should be highly regulated and specific, and that the response should integrate many aspects of cellular physiology. Pathways involved in detecting and producing forces in muscle overlap those involved in detecting nutrient availability (1,2), intracellular energy status (3,4), and oxidative status (5,6). The signaling pathways modulated by force, insulin and insulin-like growth factor I (IGF-I)(7), adenosine monophosphate (AMP) dependent kinase (AMPK) (8), reactive oxygen species (ROS) (9), and prostaglandins (PG) (10) seem intractably intertwined.The adaptations of skeletal muscle to mechanical signals have been widely described, and the interested reader is referred to several recent reviews (11)(12)(13)(14). The physiological increase in force generating capacity associated with activity, and the increase in flexibility associated with stretch, were recognized in antiquity, but the mechanisms by which those changes manifest are still unclear. The present intention is to consider the shape changes and forces associated with mechanical signals and juxtapose them with observed changes in biochemical signaling to determine what might contribute to the cellular perception of mechanical signals.Careful consideration of the mechanical environment is the first step to sort out that labyrinth of signaling. When one considers mechanisms by which the mechanical environment can be NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript sensed, it is common to think of "force" and "deformation" separately. Sometimes this distinction is legitimate, bu...

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“…Although little is known of the mechanisms of mechanical signal transduction in muscle, previous investigations have provided evidence that soluble factors released by muscle cells experiencing loads in vitro may contribute to signaling an increase in protein synthesis (12). In addition, stretch-activated ion channels (14) could provide increases in the concentration of specific cytosolic ions that are capable of activating signaling pathways that can influence gene expression.…”

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confidence: 99%

Nitric-oxide Synthase Is a Mechanical Signal Transducer That Modulates Talin and Vinculin Expression

Tidball

Spencer

Wehling

et al. 1999

Journal of Biological Chemistry

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Mechanical stimuli can cause changes in muscle mass and structure which indicate that mechanisms exist for transducing mechanical stimuli into signals that influence gene expression. Myotendinous junctions show adaptations to modified muscle loading which suggest that these are transcriptionally distinct domains in muscle fibers that may experience local regulation of expression of structural proteins that are concentrated at these sites. Vinculin and talin are cytoskeletal proteins that are highly enriched at myotendinous junctions that we hypothesize to be subject to local transcriptional regulation. Our findings show that mechanical stimulation of muscle cells in vivo and in vitro causes an increase in the expression of vinculin and talin that is mediated by nitric oxide. Furthermore, nitric oxidestimulated increases in vinculin and talin expression occur through a protein kinase G-dependent pathway and therefore differ from other mechanisms through which nitric oxide has been shown previously to modulate transcription. Analysis of vinculin mRNA distribution in mechanically stimulated muscle fibers shows that the mRNA is highly concentrated at myotendinous junctions, which supports the hypothesis that myotendinous junctions are distinct domains in which the expression of cytoskeletal proteins is modulated by mechanical stimuli through a nitric oxide and protein kinase G-dependent pathway.

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Mechanical stimulation of skeletal muscle generates lipid‐related second messengers by phospholipase activation

Cited by 70 publications

References 33 publications

Interstitial cells of Cajal mediate mechanosensitive responses in the stomach

Interstitial cells of Cajal mediate mechanosensitive responses in the stomach

Mechanotransduction in skeletal muscle

Nitric-oxide Synthase Is a Mechanical Signal Transducer That Modulates Talin and Vinculin Expression

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