Effects of Plantar Mechanical Stimulation on Anabolic and Catabolic Signaling in Rat Postural Muscle Under Short-Term Simulated Gravitational Unloading

Tyganov, Sergey A.; Mochalova, Ekaterina P.; Belova, Svetlana P.; Sharlo, Kristina A.; Rozhkov, Sergey V.; Vilchinskaya, Natalia A.; Paramonova, Inna I.; Mirzoev, Timur M.; Шенкман, Борис

doi:10.3389/fphys.2019.01252

Cited by 22 publications

(33 citation statements)

References 93 publications

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“…At the same time, literature analysis indicates that the molecular mechanisms underlying the maintenance of the structural and contractile characteristics of postural muscles during the PMS under unloading conditions have not been thoroughly studied. In our laboratory, it was previously shown that PMS can prevent a decrease in the rate of global protein synthesis and changes in 4E-BP1, GSK-3β, AMPK phosphorylation in rat soleus muscle under short-term hindlimb suspension 31 . It was also demonstrated that the application of PMS during short-term unloading (1–3 days) can prevent or attenuate an increase in MuRF-1 mRNA expression 31 , a decrease in MyHC Iβ expression via calcineurin-NFATc1 signaling pathway 32 as well as the loss of neuronal NO-synthase 33 .…”

Section: Introductionmentioning

confidence: 97%

Plantar mechanical stimulation attenuates protein synthesis decline in disused skeletal muscle via modulation of nitric oxide level

Tyganov

Mochalova

Belova

et al. 2021

Sci Rep

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Both research conducted under microgravity conditions and ground-based space analog studies have shown that air pump-based plantar mechanical stimulation (PMS) of cutaneous mechanoreceptors of the sole of the foot is able to increase neuromuscular activity in the musculature of the lower limbs. This type of stimulation is able to attenuate unloading-induced skeletal muscle atrophy and impaired muscle function. The aim of the present study was to evaluate the effects of PMS on anabolic signaling pathways in rat soleus muscle following 7-day hindlimb suspension (HS) and to elucidate if the effects of PMS on anabolic processes would be NO-dependent. The soles of the feet were stimulated with a frequency of 1-s inflation/1-s deflation with a total of 20 min followed by 10 min rest. This cycle was repeated for 4 h each day. We observed a decrease in the soleus muscle mass after 7-day HS, which was not prevented by PMS. We also observed a decrease in slow-type fiber cross-sectional area (CSA) by 56%, which significantly exceeded a decrease (–22%) in fast-type fiber CSA. PMS prevented a reduction in slow-twitch fiber CSA, but had no effect on fast-twitch fiber CSA. PMS prevented a 63% decrease in protein synthesis after 7-day HS as well as changes in several key anabolic signaling regulators, such as p70S6k, 4E-BP1, GSK3β, eEF-2, p90RSK. PMS also prevented a decrease in the markers of translational capacity (18S and 28S rRNA, c-myc, 45S pre-rRNA). Some effects of PMS on anabolic signaling were altered due to NO-synthase inhibitor (L-NAME) administration. Thus, PMS is able to partially prevent atrophic processes in rat soleus muscle during 7-day HS, affecting slow-type muscle fibers. This effect is mediated by alterations in anabolic signaling pathways and may depend on NO-synthase activity.

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Section: Introductionmentioning

confidence: 97%

Plantar mechanical stimulation attenuates protein synthesis decline in disused skeletal muscle via modulation of nitric oxide level

Tyganov

Mochalova

Belova

et al. 2021

Sci Rep

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“…At the same time, Suzuki and colleagues minced the soleus muscle tissue and measured NO content at room temperature [ 31 ] so these differences in the experimental procedures could lead to discordant results. A number of evidences concerning the states of NO-dependent signaling pathways, such as Akt-independent GSK-3beta activation during the early stage of hindlimb unloading [ 26 , 44 ], indirectly support the suggestion that NO content in soleus muscle tissue is more likely to decrease than increase under unloading conditions. However, neuronal NOS does not significantly contribute to prevention of atrophy during soleus muscle stretching upon rat hindlimb suspension, but is involved in the maintenance of expression of some muscle proteins, in particular in the regulation of MHC I mRNA expression upon muscle stretching [ 45 ].…”

Section: Discussionmentioning

confidence: 99%

Plantar Mechanical Stimulation Maintains Slow Myosin Expression in Disused Rat Soleus Muscle via NO-Dependent Signaling

Sharlo

Paramonova

Lvova

et al. 2021

IJMS

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It was observed that gravitational unloading during space missions and simulated microgravity in ground-based studies leads to both transformation of slow-twitch muscle fibers into fast-twitch fibers and to the elimination of support afferentation, leading to the “switching-off” of postural muscle motor units electrical activity. In recent years, plantar mechanical stimulation (PMS) has been found to maintain the neuromuscular activity of the hindlimb muscles. Nitric oxide (NO) was shown to be one of the mediators of muscle fiber activity, which can also promote slow-type myosin expression. We hypothesized that applying PMS during rat hindlimb unloading would lead to NO production upregulation and prevention of the unloading-induced slow-to-fast fiber-type shift in rat soleus muscles. To test this hypothesis, Wistar rats were hindlimb suspended and subjected to daily PMS, and one group of PMS-subjected animals was also treated with nitric oxide synthase inhibitor (L-NAME). We discovered that PMS led to sustained NO level in soleus muscles of the suspended animals, and NOS inhibitor administration blocked this effect, as well as the positive effects of PMS on myosin I and IIa mRNA transcription and slow-to-fast fiber-type ratio during rat hindlimb unloading. The results of the study indicate that NOS activity is necessary for the PMS-mediated prevention of slow-to-fast fiber-type shift and myosin I and IIa mRNA transcription decreases during rat hindlimb unloading.

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“…However, recently Chibalin et al, 2018 showed an increase in PKA activity in rat soleus muscle after 6 and 12 h of HS [ 34 ], so it is unlikely that this protein kinase is responsible for a decrease in inhibitory GSK3β Ser9 phosphorylation at this stage. In addition, a decrease in AKT Ser473 phosphorylation in rat soleus after 24 h of unloading was not prevented by foot mechanostimulation, while a decrease in GSK3β Ser9 phosphorylation was successfully prevented by mechanostimulation [ 14 ]. It was found that GSK3β can be phosphorylated on Ser9 by one of the cGMP-dependent protein kinases (most likely by protein kinase G) [ 115 , 116 ].…”

Section: Nitric Oxide: Friend or Foe In Signaling Remodeling? Locamentioning

confidence: 99%

“…GSK3β is also able to reduce the intensity of rRNA synthesis through ubiquitylation of proto-oncogene c-Myc, a key regulator of the expression of ribosomal genes [ 120 ]. We first found a significant decrease in the rate of protein synthesis and 18S and 28S rRNA content in rat soleus muscle after 24 h of HS, accompanied by a decrease in the content of GSK3β Ser9 phosphorylation indicating an increase in the GSK3β enzymatic activity [ 14 ]. GSK3β can also have a negative impact on mitochondrial dynamics.…”

Section: Nitric Oxide: Friend or Foe In Signaling Remodeling? Locamentioning

confidence: 99%

“…One-day mechanical unloading results in a significant increase in mRNA expression of muscle-specific E3-ubiquitin ligases MuRF-1 and MAFbx/atrogin-1 as well as MuRF-1 protein content in rat soleus muscle [ 13 ]. At the same time, a decrease in protein synthesis by more than 40% and more than a twofold decrease in the content of 18S and 28S ribosomal RNAs are demonstrated in rat soleus following 24-h unloading [ 14 ]. These events are accompanied by a significant reduction in the expression of myh7 gene encoding slow isoform of myosin heavy chains (MyHC I (β)) [ 15 , 16 ].…”

Section: Introduction When the Support Is Withdrawn Emg Dropmentioning

confidence: 99%

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How Postural Muscle Senses Disuse? Early Signs and Signals

Шенкман

2020

IJMS

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A mammalian soleus muscle along with other “axial” muscles ensures the stability of the body under the Earth’s gravity. In rat experiments with hindlimb suspension, zero-gravity parabolic flights as well as in human dry immersion studies, a dramatic decrease in the electromyographic (EMG) activity of the soleus muscle has been repeatedly shown. Most of the motor units of the soleus muscle convert from a state of activity to a state of rest which is longer than under natural conditions. And the state of rest gradually converts to the state of disuse. This review addresses a number of metabolic events that characterize the earliest stage of the cessation of the soleus muscle contractile activity. One to three days of mechanical unloading are accompanied by energy-dependent dephosphorylation of AMPK, accumulation of the reactive oxygen species, as well as accumulation of resting myoplasmic calcium. In this transition period, a rapid rearrangement of the various signaling pathways occurs, which, primarily, results in a decrease in the rate of protein synthesis (primarily via inhibition of ribosomal biogenesis and activation of endogenous inhibitors of mRNA translation, such as GSK3β) and an increase in proteolysis (via upregulation of muscle-specific E3-ubiquitin ligases).

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Effects of Plantar Mechanical Stimulation on Anabolic and Catabolic Signaling in Rat Postural Muscle Under Short-Term Simulated Gravitational Unloading

Cited by 22 publications

References 93 publications

Plantar mechanical stimulation attenuates protein synthesis decline in disused skeletal muscle via modulation of nitric oxide level

Plantar mechanical stimulation attenuates protein synthesis decline in disused skeletal muscle via modulation of nitric oxide level

Plantar Mechanical Stimulation Maintains Slow Myosin Expression in Disused Rat Soleus Muscle via NO-Dependent Signaling

How Postural Muscle Senses Disuse? Early Signs and Signals

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