Protein ingestion after endurance exercise: the ‘evolving’ needs of the mitochondria?

Humans have evolved with incredible biological capacity to adapt to their environment, with nutrients and exercise being two of the most robust stimuli. Considerable progress has been made in elucidating the relevant transcriptional and molecular networks and their subsequent phenotypic endpoints responsible for driving these adaptations. However, we are only beginning to understand the importance of nutrition in optimizing these exercise adaptations. The importance of carbohydrates and fats for optimal aerobic exercise recovery has received the bulk of research attention. Conversely, we arguably know relatively little insofar as the role dietary protein plays in enhancing the recovery from and/or adaptation to endurance exercise. Therefore, it was with great interest that we read the recent paper published in The Journal of Physiology by Breen and colleagues (Breen et al. 2011) who investigated the impact that dietary protein ingestion has on fraction-specific muscle protein synthesis after endurance exercise. In their paper, trained subjects acutely performed 90 min of exercise at ∼77%, which is an exercise stimulus that chronically would be associated with training-induced adaptations such as mitochondrial biogenesis and enhanced aerobic capacity. In a cross-over design, subjects ingested carbohydrate beverages immediately and 30 min after exercise with one trial including a total of 20 g of whey protein, which is a dose that maximally stimulates muscle protein synthesis post-resistance exercise in average ∼80 kg young men. Myofibrillar and mitochondrial protein synthesis were then measured by a primed, constant infusion of ring-[13C6]phenylalanine. The authors demonstrated that the co-ingestion of protein with carbohydrate enhanced the synthesis of the myofibrillar, but not the mitochondrial, protein fraction up to 4 h after exercise. In addition, alteration in the phosphorylation status, and presumably activity, of some intracellular signalling molecules involved in mRNA translation (i.e. mTOR, p70S6K and eEF2) previously linked to muscle growth pathways generally supported the observed changes in myofibrillar protein synthesis. Although basal protein synthetic rates were not measured and hence exercise effects could not be fully delineated, the authors speculated that the lack of enhanced mitochondrial protein synthesis with protein ingestion may have been related to the endurance-trained nature of the subjects and/or the relatively abbreviated 4 h post-exercise recovery time period over which the study was performed (Breen et al. 2011). Nevertheless, these results are consistent with another recent report demonstrating a similar myofibrillar-only fraction-specific synthetic response with dietary protein ingestion after high-intensity sprint exercise (Coffey et al. 2011). However, these post-exercise results are in apparent contrast to observations at rest, whereby exogenous amino acids have been shown to robustly stimulate the synthesis both of myofibrillar and mitochondrial protein fractions (Bohe et al. 2003). This discrepancy begs the question as to why there is an apparent difference in nutrient sensitivity between rested and exercised skeletal muscles. Given the vital requirement for ATP for all cellular processes, it is of paramount importance that energy production, and hence mitochondrial function, is prioritized to maintain cell viability. Aerobic exercise represents a stimulus that results in a marked disturbance to cellular energy homeostasis and would elicit adaptations, such as mitochondrial biogenesis, aimed to lessen future disturbances by optimizing ATP production. In this manner, it is tempting to speculate that skeletal muscle may have evolved mechanisms that would somehow target and channel intracellular amino acids towards this essential physiological process of mitochondrial protein synthesis to enhance the remodelling of this vital organelle. Thus, the availability of intracellular amino acids may be prioritized towards mitochondrial protein synthesis in the acute recovery period to maintain maximal synthetic rates even in the fasted state (Breen et al. 2011; Coffey et al. 2011). In contrast, it is generally accepted that myofibrillar protein is the major labile pool and, in addition to its role in converting chemical energy into mechanical work, acts as the sole storage reservoir for body amino acids. As such, this protein fraction is essentially at the disposal of the nutrient environment as it is catabolised during periods of reduced amino acid supply (i.e. fasted state) and resynthesized during periods of abundance (i.e. with protein feeding). Therefore, despite its synthesis being stimulated after aerobic exercise, myofibrillar protein synthesis (and probably net balance of this protein fraction) is not maximized until a source of exogenous amino acids is provided regardless of prior contractile activity (Bohe et al. 2003; Breen et al. 2011; Coffey et al. 2011). Given that protein ingestion did not further augment mitochondrial protein synthesis over a protein-free control (Breen et al. 2011; Coffey et al. 2011), it begs the question of whether there is any role for post-exercise protein in enhancing recovery from and/or adaptation to endurance exercise. At the outset, the enhanced myofibrillar protein synthesis with moderate dietary protein ingestion is consistent with the repair or remodelling of the contractile protein apparatus, which would undoubtedly be beneficial for recovery. Whether this post-exercise enhancement of myofibrillar protein synthesis could result in training-induced increases in muscle power, which in turn could enhance aerobic performance, is unclear due to the absence of longer-term training studies featuring protein synthetic measures. Nevertheless, some evolutionary biologists have theorized that humans evolved to run as a means to procure meat through ‘persistence hunting’, in which prey are essentially run to (heat) exhaustion prior to the kill. From the perspective of enhancing aerobic capacity per se, proponents of this theory may argue that natural selection may have favoured larger protein intakes that would have occurred after a successful hunt as a means to fully drive aerobic adaptations. In this scenario, an abundant or, in the context of the saturation of protein synthetic capacity, excessive protein intake could have indicated that ample amino acid substrates were available to not only repair all protein fractions (i.e. both mitochondrial and myofibrillar) but also drive further adaptive responses that could have provided a competitive advantage. Potentially in partial support of this theory is the observation in trained athletes that higher protein intakes (∼64 g) during the immediate 2 h acute recovery period after 2.5 h of cycling initiate a transcriptional profile up to 48 h later that favours the expression of genes involved in type I myofibril remodelling and enhanced cellular energy pathways (e.g. peroxisome proliferator-activated receptor gamma family expression) (Rowlands et al. 2011). This effect was observed despite equivalent energy intake and otherwise identical daily diets, suggesting a direct effect of the post-exercise dietary amino acid ingestion. In addition, rodent models have demonstrated a role for the branched chain amino acids, the human equivalent of ∼10 g per day, in enhancing mitochondrial biogenesis through sirtuin-1 expression with the functional significance evident in an enhanced aerobic capacity (D'Antona et al. 2010). Admittedly, the translation of these results to humans with whole foods (e.g. complete proteins) in conjunction with exercise is currently unclear. Nevertheless, outside of a measurable effect on mitochondrial protein synthesis, it is possible that post-endurance exercise protein intake, and perhaps relatively greater amounts than what has been studied previously (Breen et al. 2011; Coffey et al. 2011), may have subtle yet meaningful effects on the facilitation and support of cellular adaptations that could ultimately translate into mitochondrial biogenesis and enhanced aerobic performance. So what could be the next steps? As Breen and colleagues suggest in their paper, it is possible that the synergies between exercise and protein ingestion for mitochondrial protein synthesis lie outside the acute 4 h recovery window (Breen et al. 2011). In this respect, as the aerobic stimulus begins to wane in the hours to days post-exercise a more ‘rested’ mitochondrial turnover rate is observed. Given that exogenous amino acids stimulate resting mitochondrial protein synthesis (Bohe et al. 2003), it is possible that protein ingestion later (i.e. >4 h) in recovery enhances the synthesis of this protein fraction (over and above what would normally occur in unexercised muscle) and helps sustain the elevated post-exercise protein synthesis; this could be akin to what is observed within the myofibrillar protein fraction after resistance exercise (Burd et al. 2011) and, compared to a rested or a fasted exercised muscle, could translate into a greater 24–48 h mitochondrial protein synthesis and net protein accretion. Nevertheless, what is clear is that more studies need to investigate the synthetic response of specific muscle protein sub-fractions both at basal levels and with combined exercise and nutrition interventions given the divergent responses that can occur between protein fractions (Breen et al. 2011; Burd et al. 2011; Coffey et al. 2011), some of which may not be detected with mixed muscle homogenates due to the confounding influences of protein pool size and turnover rate. Moreover, the further development and refinement of methods that quantify proteome synthesis, for example 2D gel electrophoresis with tandem mass spectrometry, should greatly enhance our understanding of the specific and synergistic effects of exercise and nutrition on the turnover of individual muscle proteins. This acute protein fraction-specific information could provide a guiding ‘snapshot’ to help elucidate the potential phenotypic adaptations that might occur with more prolonged interventions. Additionally, marrying up these protein-specific synthetic data with information from other molecular and transcriptomic technologies could provide further insights into the subtle or overt regulation of the acute training phenotype. However, this mechanistic knowledge must ultimately be leveraged into longer-term studies with functional outcomes to validate the predictive ability of these acute models. Ultimately, it is clear that many questions remain in the quest to evolve our knowledge of what the mitochondria really ‘need’ to optimally adapt to aerobic exercise stimuli.

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