Proteomics-Based Detection of Immune Dysfunction in an Elite Adventure Athlete Trekking Across the Antarctica

Abstract

Proteomics monitoring of an elite adventure athlete (age 33 years) was conducted over a 28-week period that culminated in the successful, solo, unassisted, and unsupported two month trek across the Antarctica (1500 km). Training distress was monitored weekly using a 19-item, validated training distress scale (TDS). Weekly dried blood spot (DBS) specimens were collected via fingerprick blood drops onto standard blood spot cards. DBS proteins were measured with nano-electrospray ionization liquid chromatography tandem mass spectrometry (nanoLC-MS/MS) in data-independent acquisition (DIA) mode, and 712 proteins were identified and quantified. The 28-week period was divided into time segments based on TDS scores, and a contrast analysis between weeks five and eight (low TDS) and between weeks 20 and 23 (high TDS, last month of Antarctica trek) showed that 31 proteins (n = 20 immune related) were upregulated and 35 (n = 17 immune related) were downregulated. Protein–protein interaction (PPI) networks supported a dichotomous immune response. Gene ontology (GO) biological process terms for the upregulated immune proteins showed an increase in regulation of the immune system process, especially inflammation, complement activation, and leukocyte mediated immunity. At the same time, GO terms for the downregulated immune-related proteins indicated a decrease in several aspects of the overall immune system process including neutrophil degranulation and the antimicrobial humoral response. These proteomics data support a dysfunctional immune response in an elite adventure athlete during a sustained period of mental and physical distress while trekking solo across the Antarctica.

Towards a biochemical approach to occupational stress management

“…The disadvantage of requiring trained personnel on site and interrupting work to take many, regular samples can be partially overcome by blood-spot sampling [ 102 , 103 ]. This technique can be performed by the subject with minimal equipment and training to take a small thumb-prick sample [ 104 ]. It is relatively painless, although most people would prefer not to collect too many samples from themselves in a day.…”

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“…Indeed, nontargeted proteome analysis conducted using data-dependent acquisition (DDA) was able to detect 120 [45] and 253 [36] proteins in separate studies; even when DDA is combined with field asymmetric ion mobility spectrometry, only 350 proteins were detected at maximum [46]. In contrast, Nieman et al [47] applied data-independent acquisition (DIA) to DBS proteomics and identified 712 proteins. In addition, van den Broek et al [28.] utilized VAMS instead of DBS to overcome the effects of haematocrit and sample heterogeneity and noted that 423 proteins were reproducible (average 15.7%CV (n = 3) in peptide abundance) by DIA.…”

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“…Vigorous acute exercise bouts increase body metabolic demands 6 to 20 times above resting levels, and have profound, transitory effects on gene expression and blood/tissue levels of numerous metabolites, lipid mediators, and proteins (49)(50)(51)(52)(53)(54)(55)(56)(57)(58)(59). These exercise-induced molecular changes are complex and incompletely understood.…”

“…Multiomics profiling in exercise science has expanded rapidly due to the development of new technologies that provide simultaneous measurement of hundreds and thousands of molecules from small amounts of body fluids, cells, and tissues. Recent studies have linked acute vigorous exercise to changes in about 6,000 transcripts (from RNA sequencing), more than 300 proteins, and 300 to 700 metabolites (49)(50)(51)(52)(53)(54)(55)(56). Integrated molecular profiling during recovery from vigorous exercise indicates that multiple biological processes are affected including energy metabolism, oxidative stress, immune function and inflammation, tissue repair and remodeling, signaling pathways, cell growth and mobility, cardiovascular signaling and angiogenesis, and apoptosis (49)(50)(51)(52).…”

“…Integrated molecular profiling during recovery from vigorous exercise indicates that multiple biological processes are affected including energy metabolism, oxidative stress, immune function and inflammation, tissue repair and remodeling, signaling pathways, cell growth and mobility, cardiovascular signaling and angiogenesis, and apoptosis (49)(50)(51)(52). Exercise proteomics has shown that hundreds of proteins are secreted by the muscle and other tissues discretely or within extracellular vesicles to regulate physiological processes throughout the body (54,55,60). Exercise metabolomics has established that following intensive bouts lasting more than two hours, large-fold changes in numerous and diverse lipid-related metabolites occur reaching their nadir within a few hours with abatement after one day of recovery (53,58).…”