Evidence for Rapid Oxidative Phosphorylation and Lactate Fermentation in Motile Human Sperm by Hyperpolarized 13C Magnetic Resonance Spectroscopy

Reynolds, Steven; Ismail, Nurul Fadhlina; Calvert, S J; Pacey, Allan; Paley, Martyn N.J.

doi:10.1038/s41598-017-04146-1

Cited by 20 publications

(14 citation statements)

References 46 publications

(50 reference statements)

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“…Lactate was previously reported as the main metabolite produced by human spermatozoa [39]. In addition, human spermatozoa are able to further metabolize lactate into pyruvate and acetate [39,40], which is corroborated by our results that show spermatozoa acetate production after glucose treatment. We were also able to identify and quantify malate in the media.…”

Section: Discussionsupporting

confidence: 90%

Mitochondrial Activation and Reactive Oxygen-Species Overproduction during Sperm Capacitation are Independent of Glucose Stimuli

et al. 2020

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Spermatozoa capacitation is a complex process that requires specific ionic and energetic conditions to support biochemical alterations leading to motility hyperactivation. However, human sperm capacitation is still poorly understood. Herein, we studied the effects of glucose on human sperm capacitation. Healthy men seminal samples (n = 55) were submitted to a density gradient centrifugation and incubated in capacitating conditions in the absence or presence of increasing glucose concentrations (0, 5.5, 11, and 22 mM). Viability and total motility were accessed. Phosphotyrosine levels were measured. Mitochondrial activity and endogenous ROS production were evaluated. Oxidative stress-induced damage was analyzed. Culture media was collected and analyzed by 1H-NMR. Our results show that glucose is essential for human sperm capacitation and motility. Notably, we observed that mitochondrial activity increased even in the absence of glucose. This increased mitochondrial activity was followed by a ROS overproduction, although no oxidative stress-induced damage was detected. Our results show that glucose is essential for capacitation but mitochondrial activation is independent from its stimuli. ROS overproduction may take part on a finely regulated signaling pathway that modulates or even activates capacitation. Taken together, our results constitute a paradigm shift on human sperm capacitation physiology.

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Section: Discussionsupporting

confidence: 90%

Mitochondrial Activation and Reactive Oxygen-Species Overproduction during Sperm Capacitation are Independent of Glucose Stimuli

et al. 2020

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“…Organic acids are produced by the breakdown of amino acids and fatty acids, and the degradation of such metabolites generates energy substrates for tricarboxylic acid (TCA) cycle and respiratory chain [38]. The presence of organic acid suggests that bull spermatozoa have active energy metabolism [8, 39, 40]. In addition, organic acids play crucial roles during anabolism by providing C-atom backbones [38].…”

Section: Discussionmentioning

confidence: 99%

Uncovering sperm metabolome to discover biomarkers for bull fertility

et al. 2019

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Background Subfertility decreases the efficiency of the cattle industry because artificial insemination employs spermatozoa from a single bull to inseminate thousands of cows. Variation in bull fertility has been demonstrated even among those animals exhibiting normal sperm numbers, motility, and morphology. Despite advances in research, molecular and cellular mechanisms underlying the causes of low fertility in some bulls have not been fully elucidated. In this study, we investigated the metabolic profile of bull spermatozoa using non-targeted metabolomics. Statistical analysis and bioinformatic tools were employed to evaluate the metabolic profiles high and low fertility groups. Metabolic pathways associated with the sperm metabolome were also reported. Results A total of 22 distinct metabolites were detected in spermatozoa from bulls with high fertility (HF) or low fertility (LF) phenotype. The major metabolite classes of bovine sperm were organic acids/derivatives and fatty acids/conjugates. We demonstrated that the abundance ratios of five sperm metabolites were statistically different between HF and LF groups including gamma-aminobutyric acid (GABA), carbamate, benzoic acid, lactic acid, and palmitic acid. Metabolites with different abundances in HF and LF bulls had also VIP scores of greater than 1.5 and AUC- ROC curves of more than 80%. In addition, four metabolic pathways associated with differential metabolites namely alanine, aspartate and glutamate metabolism, β-alanine metabolism, glycolysis or gluconeogenesis, and pyruvate metabolism were also explored. Conclusions This is the first study aimed at ascertaining the metabolome of spermatozoa from bulls with different fertility phenotype using gas chromatography-mass spectrometry. We identified five metabolites in the two groups of sires and such molecules can be used, in the future, as key indicators of bull fertility.

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“…The concept of spermatogenic lactate shuttles was introduced by L. Bruce Gladden in his classic review paper (Gladden, 2004). Gladden's review unified extant data in the literature and anticipated subsequent results in the field of fertility so important for human reproduction, veterinary medicine, and animal husbandry agriculture (Boussouar and Benahmed, 2004;Reynolds et al, 2017). Gladden's treatment of the subject has stood the test of time even as the technologies, including magnetic resonance spectroscopy (MRS), have become more sophisticated (Reynolds et al, 2017).…”

Section: Spermatogenic and Sertoli-germ Cell Lactate Shuttlesmentioning

confidence: 99%

The Science and Translation of Lactate Shuttle Theory

2018

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Once thought to be a waste product of anaerobic metabolism, lactate is now known to form continuously under aerobic conditions. Shuttling between producer and consumer cells fulfills at least three purposes for lactate: (1) a major energy source, (2) the major gluconeogenic precursor, and (3) a signaling molecule. "Lactate shuttle" (LS) concepts describe the roles of lactate in delivery of oxidative and gluconeogenic substrates as well as in cell signaling. In medicine, it has long been recognized that the elevation of blood lactate correlates with illness or injury severity. However, with lactate shuttle theory in mind, some clinicians are now appreciating lactatemia as a "strain" and not a "stress" biomarker. In fact, clinical studies are utilizing lactate to treat pro-inflammatory conditions and to deliver optimal fuel for working muscles in sports medicine. The above, as well as historic and recent studies of lactate metabolism and shuttling, are discussed in the following review.

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Evidence for Rapid Oxidative Phosphorylation and Lactate Fermentation in Motile Human Sperm by Hyperpolarized 13C Magnetic Resonance Spectroscopy

Cited by 20 publications

References 46 publications

Mitochondrial Activation and Reactive Oxygen-Species Overproduction during Sperm Capacitation are Independent of Glucose Stimuli

Mitochondrial Activation and Reactive Oxygen-Species Overproduction during Sperm Capacitation are Independent of Glucose Stimuli

Uncovering sperm metabolome to discover biomarkers for bull fertility

The Science and Translation of Lactate Shuttle Theory

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