Characterization of skeletal muscle mitochondria in endurance athletes and acute effects of carbohydrate and energy manipulation on muscle glycogen and performance during shortterm maximal exercise

Camilla Tvede Schytz

Research output: ThesisPh.D. thesis

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Abstract

Skeletal muscle mitochondrial and glycogen content are important for performance. Mitochondria aerobically convert nutrients to energy in the skeletal muscle cell in a process known as oxidative phosphorylation. Thus, an elevated mitochondrial volume per muscle volume (mitochondrial volume density) enablesprovision of ATP at greater rates, hence augmenting the capacity of an individualto use oxidative metabolism and improve resistance to fatigue. Also, subcellularstores of glycogen particles are important for performance by serving as readilyavailable energy stores, which is degraded anaerobically, and where the product,pyruvate, can be metabolized in the mitochondria. Both of these cellular components are investigated in the present thesis, which is presented in three paperswith the following findings:

In Paper I skeletal muscle mitochondrial respiration was analyzed in relation to mitochondrial volume and cristae density, across different training statuses and sex. Data were combined from skeletal muscle biopsies originating from independent studies conducted previously, but where mitochondrial cristae density had not yet been assessed. Participants included both females (n=12) and males (n=41) across a broad range of training statuses from untrained (UT, n=8), recreationally active (RA, n=9), active-to-elite runners (RUN, n=27) and cross-country skiers (XC, n=9). The results showed that: 1) The XC and RUN groups demonstrated higher mitochondrial volume density than the RA and UT groups, while all active groups (RA, RUN, and XC) displayed higher mass-specific capacity of oxidative phosphorylation (OXPHOS) and mitochondrial cristae density than UT. Differences in OXPHOS were smaller between active groups and UT when normalizing to mitochondrial volume density, and not evident when normalizing to
muscle cristae surface area density. 2) No differences were found between active females (n=6-9) and males (n=15-18) within the RUN-group in mitochondrial volume and cristae density as well as mass-specific OXPHOS, or when normalizing to mitochondrial volume density and muscle cristae surface area density. Thus, the results suggest that differences in OXPHOS between active and untrained individuals may be explained by higher mitochondrial cristae density in active individuals, and not by difference in intrinsic mitochondrial respiratory capacity. The results also suggest that active females and males do not differ in mitochondrial volume and cristae density as well as mass-specific OXPHOS.

In Paper II it was investigated how lowering dietary carbohydrates (CHO) andenergy content affect skeletal muscle glycogen content, body mass, and performance in maximal exercises of short duration (1-min and 15-min). The applied cross-over design was randomized and counterbalanced where participantsperformed two maximal cycle tests lasting either 1 minute (n=10) or 15 minutes(n=12). These were conducted after consumption of two different diets: one withhigh (H-CHO) and the other with lowered carbohydrate and energy content (MCHO). The manipulation of dietary carbohydrates and energy was started threedays prior following a glycogen-depleting exercise protocol involving both the upper and lower body. Muscle biopsies from m. vastus lateralis were obtained before and after the exercises, and participants were weighed at a standardizedtime-point prior to the exercises. The results showed that: 1) The M-CHO condition induced a 159 mmol·kg DW-1lower skeletal muscle glycogen level and a 0.7kg lowered body mass prior the exercises than the H-CHO condition. 2) Initiatingexercise with a glycogen level of 367 mmol·kg DW-1(M-CHO) rather than 525mmol·kg DW-1 (H-CHO) did not affect performance (W·kg-1) during the 1- or 15-min maximal exercises. Thus, the results suggest that an acute lowering of dietary CHO and energy content induce a lower pre-exercise skeletal muscle glycogen level and body mass, while performance in non-weight-bearing maximal exercises of short duration was not affected. 

In Paper III, it was investigated how exercise at different intensities (1- and 15-min maximal exercise) with known differences in the glycogenolytic rate and inthe relative contribution of anaerobic metabolism affects the utilization of the distinct subcellular pools of glycogen. Also, it was investigated how lowered carbohydrate and energy intake affected the storage of glycogen particles (localization,size, and number) and the subsequent utilization during the exercises. The biopsyspecimens prepared for transmission electron microscopy originate from thesame biopsy material as described in Paper II, although with a lower sample size(n=10 in both exercises). The results showed that: 1) Intermyofibrillar glycogenwas predominantly utilized during the 1-min exercise, whereas intramyofibrillarglycogen was preferentially utilized during the 15-min exercise. 2) The loweredcarbohydrate and energy intake reduced the particle size across all subcellularpools and reduced the numerical density in the intramyofibrillar and subsarcolemmal pools, with no effects on the utilization of glycogen during the subsequentexercise. Thus, the results suggest that distinct subcellular glycogen pools aredifferentially utilized during 1-min and 15-min maximal exercise, and lowered carbohydrate and energy consumption reduces particle size and numerical density,depending on subcellular localization.
Translated title of the contributionKarakterisering af udholdenhedsatleters skeletmusklers mitokondrier og akutte effekter af manipulation af kulhydrat og energi på muskelglykogen og præstation under kortvarigt maksimalt arbejde
Original languageEnglish
Awarding Institution
  • University of Southern Denmark
Supervisors/Advisors
  • Nielsen, Joachim, Principal supervisor
  • Gejl, Kasper Degn, Co-supervisor
  • Ørtenblad, Niels, Co-supervisor
Date of defence7. Dec 2023
Publisher
DOIs
Publication statusPublished - 19. Oct 2023

Note re. dissertation

Print copy of the full thesis is restricted to reference use in the library.

Keywords

  • Skeletal muscle
  • Mitochondria
  • Mitochondrial cristae density
  • Diet manipulation
  • Weight management
  • Maximal exercise
  • Glycogen
  • Transmission electron microscopy

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