Peripheral impairments of oxidative metabolism after a 10‐day bed rest are upstream of mitochondrial respiration

Zuccarelli, Lucrezia; Baldassarre, Giovanni; Magnesa, Benedetta; Degano, Cristina; Comelli, Marina; Gasparini, Mladen; Manferdelli, Giorgio; Marzorati, Mauro; Mavelli, Irene; Pilotto, Andrea; Porcelli, Simone; Rasica, Letizia; Šimunič, Boštjan; Pišot, Rado; Narici, Marco V.; Grassi, Bruno

doi:10.1113/jp281800

Cited by 25 publications

(23 citation statements)

References 65 publications

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“…After having checked that the TSI signal following VOT returned to baseline values (~ 5 min), skeletal muscle oxidative capacity was evaluated in vivo by measuring post-exercise muscle oxygen consumption ( m V̇O 2 ) recovery kinetics by NIRS and the repeated occlusions method 16 , 17 . The protocol consisted of a 3-min rest followed by a 10-min moderate intensity (~ 50% V̇O 2peak ) constant work rate exercise bout aiming to increase m V̇O 2 and desaturate the muscle to ~ 50% of A TSI (i.e.…”

Section: Methodsmentioning

confidence: 99%

Microvascular and oxidative stress responses to acute high-altitude exposure in prematurely born adults

Manferdelli

Narang

Pialoux

et al. 2023

Sci Rep

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Premature birth is associated with endothelial and mitochondrial dysfunction, and chronic oxidative stress, which might impair the physiological responses to acute altitude exposure. We assessed peripheral and oxidative stress responses to acute high-altitude exposure in preterm adults compared to term born controls. Post-occlusive skeletal muscle microvascular reactivity and oxidative capacity from the muscle oxygen consumption recovery rate constant (k) were determined by Near-Infrared Spectroscopy in the vastus lateralis of seventeen preterm and seventeen term born adults. Measurements were performed at sea-level and within 1 h of arrival at high-altitude (3375 m). Plasma markers of pro/antioxidant balance were assessed in both conditions. Upon acute altitude exposure, compared to sea-level, preterm participants exhibited a lower reperfusion rate (7 ± 31% vs. 30 ± 30%, p = 0.046) at microvascular level, but higher k (6 ± 32% vs. −15 ± 21%, p = 0.039), than their term born peers. The altitude-induced increases in plasma advanced oxidation protein products and catalase were higher (35 ± 61% vs. −13 ± 48% and 67 ± 64% vs. 15 ± 61%, p = 0.034 and p = 0.010, respectively) and in xanthine oxidase were lower (29 ± 82% vs. 159 ± 162%, p = 0.030) in preterm compared to term born adults. In conclusion, the blunted microvascular responsiveness, larger increases in oxidative stress and skeletal muscle oxidative capacity may compromise altitude acclimatization in healthy adults born preterm.

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Section: Methodsmentioning

confidence: 99%

Microvascular and oxidative stress responses to acute high-altitude exposure in prematurely born adults

Manferdelli

Narang

Pialoux

et al. 2023

Sci Rep

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“…In health, skeletal muscle oxidative capacity is strongly correlated with whole body aerobic capacity and exercise performance (Holloszy, 1967;Hood et al, 2011;Hoppeler et al, 1985). Moreover, muscle oxidative capacity and mitochondrial function are impaired in conditions of physical inactivity (Buso et al, 2019;Zuccarelli et al, 2021), aging (Layec et al, 2013) and chronic disease, such as obesity (Lazzer et al, 2013;Menshikova et al, 2005), diabetes (Joseph et al, 2012) myopathy (Grassi et al, 2019(Grassi et al, , 2020, pulmonary obstructive disease (Adami et al, 2017(Adami et al, , 2020 and neuromuscular disease (Breuer et al, 2013). Traditionally, muscle oxidative capacity has been studied using ex vivo approaches involving muscle biopsy samples and measurement of enzyme activity or mitochondrial respiratory capacity in isolated mitochondrial preparations and permeabilized muscle fibres (Brand & Nicholls, 2011;Chance & Williams, 1955;Gnaiger, 2009;Holloszy, 1967;Perry et al, 2013).…”

Section: Nirs and Muscle Oxidative Capacitymentioning

confidence: 99%

Near‐infrared spectroscopy estimation of combined skeletal muscle oxidative capacity and O₂ diffusion capacity in humans

Pilotto

Adami

Mazzolari

et al. 2022

The Journal of Physiology

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The final steps of the O2 cascade during exercise depend on the product of the microvascular‐to‐intramyocyte PO2${P}_{{{\rm{O}}}_{\rm{2}}}$ difference and muscle O2 diffusing capacity (DmnormalO2$D{{\rm{m}}}_{{{\rm{O}}}_2}$). Non‐invasive methods to determine DmnormalO2$D{{\rm{m}}}_{{{\rm{O}}}_2}$ in humans are currently unavailable. Muscle oxygen uptake (mtrueV̇O2${\dot{V}}_{{{\rm{O}}}_{\rm{2}}}$) recovery rate constant (k), measured by near‐infrared spectroscopy (NIRS) using intermittent arterial occlusions, is associated with muscle oxidative capacity in vivo. We reasoned that k would be limited by DmnormalO2$D{{\rm{m}}}_{{{\rm{O}}}_2}$ when muscle oxygenation is low (kLOW), and hypothesized that: (i) k in well oxygenated muscle (kHIGH) is associated with maximal O2 flux in fibre bundles; and (ii) ∆k (kHIGH – kLOW) is associated with capillary density (CD). Vastus lateralis k was measured in 12 participants using NIRS after moderate exercise. The timing and duration of arterial occlusions were manipulated to maintain tissue saturation index within a 10% range either below (LOW) or above (HIGH) half‐maximal desaturation, assessed during sustained arterial occlusion. Maximal O2 flux in phosphorylating state was 37.7 ± 10.6 pmol s−1 mg−1 (∼5.8 ml min−1 100 g−1). CD ranged 348 to 586 mm–2. kHIGH was greater than kLOW (3.15 ± 0.45 vs. 1.56 ± 0.79 min–1, P < 0.001). Maximal O2 flux was correlated with kHIGH (r = 0.80, P = 0.002) but not kLOW (r = –0.10, P = 0.755). Δk ranged –0.26 to –2.55 min–1, and correlated with CD (r = –0.68, P = 0.015). mtrueV̇O2${\dot{V}}_{{{\rm{O}}}_{\rm{2}}}$ k reflects muscle oxidative capacity only in well oxygenated muscle. ∆k, the difference in k between well and poorly oxygenated muscle, was associated with CD, a mediator of DmnormalO2$D{{\rm{m}}}_{{{\rm{O}}}_2}$. Assessment of muscle k and ∆k using NIRS provides a non‐invasive window on muscle oxidative and O2 diffusing capacity. Key points We determined post‐exercise recovery kinetics of quadriceps muscle oxygen uptake (mtrueV̇O2${\dot{V}}_{{{\rm{O}}}_{\rm{2}}}$) measured by near‐infrared spectroscopy (NIRS) in humans under conditions of both non‐limiting (HIGH) and limiting (LOW) O2 availability, for comparison with biopsy variables. The mtrueV̇O2${\dot{V}}_{{{\rm{O}}}_{\rm{2}}}$ recovery rate constant in HIGH O2 availability was hypothesized to reflect muscle oxidative capacity (kHIGH) and the difference in k between HIGH and LOW O2 availability (∆k) was hypothesized to reflect muscle O2 diffusing capacity. kHIGH was correlated with phosphorylating oxidative capacity of permeabilized muscle fibre bundles (r = 0.80). ∆k was negatively correlated with capillary density (r = −0.68) of biopsy samples. NIRS provides non‐invasive means of assessing both muscle oxidative and oxygen diffusing capacity in vivo.

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“…Female were excluded from the study to avoid confounding physiological conditions related to the menstrual cycle. Participants’ body mass and body mass index estimated in pre and post bed rest conditions in a parallel study revealed a slight but significant decrease ( Zuccarelli et al, 2021 ).…”

Section: Methodsmentioning

confidence: 99%

Early Biomarkers of Altered Renal Function and Orthostatic Intolerance During 10-day Bedrest

et al. 2022

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Exposure to actual or simulated microgravity results in alterations of renal function, fluid redistribution, and bone loss, which is coupled to a rise of urinary calcium excretion. We provided evidence that high calcium delivery to the collecting duct reduces local Aquaporin 2 (AQP2)-mediated water reabsorption under vasopressin action, thus limiting the maximal urinary concentration to reduce calcium saturation. To investigate early renal adaptation into simulated microgravity, we investigated the effects of 10 days of strict bedrest in 10 healthy volunteers. We report here that 10 days of inactivity are associated with a transient, significant decrease (day 5) in vasopressin (copeptin) paralleled by a decrease in AQP2 excretion, consistent with an increased central volume to the heart, resulting in reduced water reabsorption. Moreover, bedrest caused a significant increase in calciuria secondary to bone demineralization paralleled by a decrease in PTH. Urinary osteopontin, a glycoprotein exerting a protective effect on stone formation, was significantly reduced during bedrest. Moreover, a significant increase in adrenomedullin (day 5), a peptide with vasodepressor properties, was observed at day 5, which may contribute to the known reduced orthostatic capacity post-bedrest. We conclude that renal function is altered in simulated microgravity and is associated with an early increase in the risk of stone formation and reduced orthostatic capacity post-bedrest within a few days of inactivity.

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Peripheral impairments of oxidative metabolism after a 10‐day bed rest are upstream of mitochondrial respiration

Abstract: The peer review history is available in the supporting information section of this article (https://doi.org/10.1113/JP281800#support-information-section).

Cited by 25 publications

References 65 publications

Microvascular and oxidative stress responses to acute high-altitude exposure in prematurely born adults

Microvascular and oxidative stress responses to acute high-altitude exposure in prematurely born adults

Near‐infrared spectroscopy estimation of combined skeletal muscle oxidative capacity and O₂ diffusion capacity in humans

Early Biomarkers of Altered Renal Function and Orthostatic Intolerance During 10-day Bedrest

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Peripheral impairments of oxidative metabolism after a 10‐day bed rest are upstream of mitochondrial respiration

Abstract: The peer review history is available in the supporting information section of this article (https://doi.org/10.1113/JP281800#support-information-section).

Cited by 25 publications

References 65 publications

Microvascular and oxidative stress responses to acute high-altitude exposure in prematurely born adults

Microvascular and oxidative stress responses to acute high-altitude exposure in prematurely born adults

Near‐infrared spectroscopy estimation of combined skeletal muscle oxidative capacity and O2 diffusion capacity in humans

Early Biomarkers of Altered Renal Function and Orthostatic Intolerance During 10-day Bedrest

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Product

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Near‐infrared spectroscopy estimation of combined skeletal muscle oxidative capacity and O₂ diffusion capacity in humans