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Repetitive Bouts of Exhaustive Exercise Induces a Systemic Inflammatory Response and Multi-Organ Damage in Rats.

ABSTRACT: Multiple organ dysfunction syndrome can follow severe infection or injury, but its relationship to exercise is not well understood. Previous studies have observed that prolonged strenuous exercise can lead to transiently increased level and/or activity of markers for systemic inflammatory response and multiple organ damage. However, few studies have analyzed the pathogenesis of the inflammatory response and subsequent multi-organ injury in exhaustive exercise conditions. In this study, we established a rat model of repetitive bouts of exhaustive running (RBER) and investigated its effects on multiple organ damage. Rats were subjected to RBER in either uphill or downhill running modes daily for a period of 7 days. Morphologically, RBER causes tissue structural destruction and infiltration of inflammatory cells in the skeletal muscles and many visceral organs. RBER also causes sustained quantitative changes in leukocytes, erythrocytes, and platelets, and changes in the concentration of blood inflammatory factors. These inflammatory alterations are accompanied by increases in serum enzyme levels/activities which serve as functional markers of organ damage. In general, RBER in the downhill mode seemed to cause more damage evaluated by the above-mentioned measures than that produced in the uphill mode. A period of rest could recover some degree of damage, especially for organs such as the heart and kidneys with strong compensatory capacities. Together, our data suggest that, as a result of multi-organ interactions, RBER could cause a sustained inflammatory response for at least 24 h, resulting in tissue lesion and ultimately multiple organ dysfunction.

SUBMITTER: Liao P

PROVIDER: S-EPMC7324715 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Repetitive Bouts of Exhaustive Exercise Induces a Systemic Inflammatory Response and Multi-Organ Damage in Rats.

Liao Peng P He Qinghua Q Zhou Xuan X Ma Kai K Wen Jie J Chen Hang H Li Qingwen Q Qin Di D Wang Hui H

Frontiers in physiology 20200623

Multiple organ dysfunction syndrome can follow severe infection or injury, but its relationship to exercise is not well understood. Previous studies have observed that prolonged strenuous exercise can lead to transiently increased level and/or activity of markers for systemic inflammatory response and multiple organ damage. However, few studies have analyzed the pathogenesis of the inflammatory response and subsequent multi-organ injury in exhaustive exercise conditions. In this study, we establ ...[more]

PMID: 32655413

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Project description:Circulating microRNAs have proven to be reliable biomarkers, due to their high stability, both in vivo in the circulation, and ex vivo during sample preparation and storage. Small nucleolar RNAs (snoRNAs) are a different type of small non-coding RNAs that can also be reliably measured in plasma, but have only been studied sporadically. In this study, we aimed to identify RNA-biomarkers that can distinguish between different exercise regimes and that entail clues about muscle repair and recovery after prolonged exhaustive endurance exercise. We compared plasma microRNA profiles between two cohorts of elite cyclists, subjected to two different types of exercise regimes, as well as a cohort of patients with peripheral artery disease (PAD) that were scheduled to undergo lower limb amputation, due to critical limb ischemia. In elite athletes, muscle tissue recovers quickly even after exhaustive exercise, whereas in PAD patients, recovery is completely impaired. Furthermore, we measured levels of a specific group of snoRNAs in the plasma of both elite cyclists and PAD patients. Using a multiplex qPCR screening, we detected a total of 179 microRNAs overall, of which, on average, 161 microRNAs were detected per sample. However, only 30 microRNAs were consistently expressed in all samples. Of these, two microRNAs, miR-29a-3p and miR193a-5p, that responded differently two different types of exercise, namely exhaustive exercise and non-exhaustive endurance exercise. Using individual rt/qPCR, we also identified a snoRNA, SNORD114.1, which was significantly upregulated in plasma in response to endurance exercise. Furthermore, two microRNAs, miR-29a-3p and miR-495-3p, were significantly differentially expressed in athletes compared to PAD patients, but only following exercise. We suggest that these two microRNAs could function as markers of impaired muscle repair and recovery. In conclusion, microRNAs miR-29a-3p and miR-193a-5p may help us distinguish between repeated exhaustive and non-exhaustive endurance exercise. MicroRNA miR-29a-3p, as well as miR-495-3p, may further mark impaired muscle recovery in patients with severe critical limb ischemia. Furthermore, we showed for the first time that a circulating snoRNA, SNORD114.1, is regulated in response to exercise and may be used as biomarker.

Project description:ObjectiveAcute single strenuous exercise increases circulating cell free DNA (cf DNA). We tested whether three repeated bouts of exhaustive exercise induced the cf DNA response without development of tolerance in healthy men.MethodsEleven average-trained men (age 34.0±5.2 years, body mass index 26.2±3.1 kg/m2, maximal oxygen consumption-VO2max 49.6±4.5 ml/kg*min) performed three treadmill exercise tests to exhaustion at speed corresponding to 70% VO2max separated by 72 hours of resting. Blood was collected before and after each bout of exercise for determination of cell free nuclear and mitochondrial DNA (cf n-DNA, cf mt-DNA) by real-time PCR, selected markers of muscle damage, and blood cell count.ResultsEach bout induced the increase (p<0.05) in plasma cf n-DNA: from 3.4±1.4 to 38.5±27.5, from 4.1±3.3 to 48.5±26.2, and 3.1±1.6 to 53.8±39.9 ng/mL after the first, second, and third exercise, respectively. In a congruent way, cf mt-DNA rose significantly after the second (from 229±216 to 450±228*103 GE/mL) and third bout of exercise (from 173±120 to 462±314*103 GE/mL). Pre-exercise cf mt-DNA decreased (p<0.05) by 2-times (from 355±219 before the first bout to 173±120*103 GE/mL before the third bout) over the study period and were accompanied by significant increase in white blood cells, platelets, creatine kinase, creatinine and lactate after each bout. However, the exercise induced percentage increment of cf n-DNA was always many times higher than corresponding increments of the afore-mentioned markers at any occasion.ConclusionsRepeated bouts of exhaustive exercise induced remarkable increase in circulating cf n-DNA without signs of tolerance development. Baseline cf mt-DNA decreased in response to series of strenuous exercise. Since percentage increments of cf n-DNA in response to exercise were many times higher than those observed for other markers, measurement of circulating cf n-DNA could be a sensitive tool for monitoring acute exercise effects in human body.

Project description:Exhaustive exercise has emerged as an important health issue nowadays. This study was designed to assess the metabolite abnormalities of rats after exhaustive exercise and the holistic efficacy of Chinese medicine Sanqi oral solution (SQ). Through exhaustive swimming, the exhaustive exercise model in rats was established. Thirty male Sprague-Dawley rats were randomly divided into control, model, and treatment groups. SQ (12 mL·kg-1·d-1) or 0.9% saline solution was administrated orally by gastric gavage. After 4 weeks, serum samples were collected for biochemical measurements and ultra performance liquid chromatography (UPLC)/quadrupole time-of-flight mass spectrometry (Q-TOF-MS)-based metabonomic study. It was found that rats with SQ intervention showed longer exhaustive swimming time (P < 0.05) than model rats, with an average of 1,160.36 ± 123.89 s in SQ group and 906.57 ± 172.11 s in model group. Among the biochemical indices, the levels of creatine kinase isoenzyme, lactate dehydrogenase, and glucose of exhaustive exercise rats increased, whereas levels of creatine kinase, urea, triglyceride, and total cholesterol decreased. These biochemical indices came normal after SQ administration, except for triglyceride. Twenty-seven potential biomarkers belonging to sphingolipids, phospholipids, fatty acids, amino acid, and other classes were identified in serum. This study indicated that SQ exerted protective effects on exhaustive exercise by significantly prolonging the swimming endurance time. The metabonomic-based findings of the metabolic state and analysis of potential biomarkers in serum well correlated with biochemical assessment, confirming that SQ had a definite efficacy. Moreover, the shifts in lipid-related metabolites and glycolytic pathway suggested that SQ may serve as a potential supplementation in sports nutrition for its pharmacological effect of regulating energy metabolism as well as improving signal transduction and muscle-cell physiological functions.

Dataset Information

Repetitive Bouts of Exhaustive Exercise Induces a Systemic Inflammatory Response and Multi-Organ Damage in Rats.

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Repetitive Bouts of Exhaustive Exercise Induces a Systemic Inflammatory Response and Multi-Organ Damage in Rats.

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