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Fiber type and metabolic characteristics of lion (Panthera leo), caracal (Caracal caracal) and human skeletal muscle

Profile image of Timothy NoakesTimothy NoakesProfile image of Marthinus HartmanMarthinus Hartman

2011, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology

https://doi.org/10.1016/J.CBPA.2011.02.006
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Abstract

Lion (Panthera leo) and caracal (Caracal caracal) skeletal muscle samples from Vastus lateralis, Longissimus dorsi and Gluteus medius were analyzed for fiber type and citrate synthase (CS; EC 2.3.3.1), 3-hydroxyacyl Co A dehydrogenase (3HAD; EC 1.1.1.35), phosphofructokinase-1 (PFK; EC 2.7.1.11), creatine kinase (CK; EC 2.7.3.2), phosphorylase (PHOS; EC 2.4.1.1) and lactate dehydrogenase (LDH; EC 1.1.1.27) activities and compared to human runners, the latter also serving as validation of methodology. Both felids had predominantly type IIx fibers (range 50-80%), whereas human muscle had more types I and IIa. Oxidative capacity of both felids (CS: 5-9 μmol/min/g ww and 3HAD: 1.4-2.6 μmol/min/g ww) was lower than humans, whereas the glycolytic capacity was elevated. LDH activity of caracal (346 ± 81) was higher than lion (227 ± 62 μmol/min/g ww), with human being the lowest (55 ± 17). CK and PHOS activities were also higher in caracal and lion compared to human, but PFK was lower in both felid species. The current data and past research are illustrated graphically showing a strong relationship between type II fibers and sprinting ability in various species. These data on caracal and lion muscles confirm their sprinting behavior.

Key takeaways
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  1. Lion and caracal muscles predominantly express type IIx fibers, correlating with their sprinting capabilities.
  2. Citrate synthase (CS) and 3-hydroxyacyl CoA dehydrogenase (3HAD) activities are 3.5x and 2.5x lower than humans.
  3. Caracal exhibits higher lactate dehydrogenase (LDH) activity (346 ± 81) than lion (227 ± 62).
  4. Phosphofructokinase (PFK) activities are lower in both felids compared to humans, contradicting expectations.
  5. The study aims to investigate and compare skeletal muscle fiber types and metabolic characteristics in felids and humans.
Figures (6)
Fig. 1. Enzyme activities (Lumol/min/g ww) in Vastus lateralis (VL), Gluteus medius (GM) and Longissimus dorsi (LD) muscles of caracal and lion (circles). The bars represent the mean + SD of human VL for comparative purposes. A. Citrate synthase. B. 3-Hydroxyacetyl Co A dehydrogenase. C. Phosphofructokinase. D.Lactate dehydrogenase. E. Creatine kinase. F. Phosphorylase.
Fig. 1. Enzyme activities (Lumol/min/g ww) in Vastus lateralis (VL), Gluteus medius (GM) and Longissimus dorsi (LD) muscles of caracal and lion (circles). The bars represent the mean + SD of human VL for comparative purposes. A. Citrate synthase. B. 3-Hydroxyacetyl Co A dehydrogenase. C. Phosphofructokinase. D.Lactate dehydrogenase. E. Creatine kinase. F. Phosphorylase.
* Different from human (P<0.05). ** Different from human and caracal. *** Different from caracal (P<0.05).  Enzyme activities and MHC isoform composition of caracal and lion muscles grouped Human muscle composed only of data obtained from the Vastus lateralis. CSA were only determined in the Vastus lateralis muscles of the three species. Values are means + SD
* Different from human (P<0.05). ** Different from human and caracal. *** Different from caracal (P<0.05). Enzyme activities and MHC isoform composition of caracal and lion muscles grouped Human muscle composed only of data obtained from the Vastus lateralis. CSA were only determined in the Vastus lateralis muscles of the three species. Values are means + SD
MHC isoform composition (%) of the three caracal and lion skeletal muscle groups. Human values are expressed as mean + SD.
MHC isoform composition (%) of the three caracal and lion skeletal muscle groups. Human values are expressed as mean + SD.
Fig. 3. Myosin heavy chain (MHC) isoform separation and Western blots of human, caracal and lion skeletal muscles. A rat sample was included in 3E as a positive control for MHC IIb. A. Silver stain (arrow indicates band that was not recognizable by any of the primary antibodies used). B. MHC Ila (antibody 2F7). C. MHC IIx (antibody 6H1). D. MHC I and MHC IIx (antibodies BA-D5 and 6H1). E. MHC IIb (antibody BF-F3).
Fig. 3. Myosin heavy chain (MHC) isoform separation and Western blots of human, caracal and lion skeletal muscles. A rat sample was included in 3E as a positive control for MHC IIb. A. Silver stain (arrow indicates band that was not recognizable by any of the primary antibodies used). B. MHC Ila (antibody 2F7). C. MHC IIx (antibody 6H1). D. MHC I and MHC IIx (antibodies BA-D5 and 6H1). E. MHC IIb (antibody BF-F3).
Fig. 4. Relationships between muscle fiber type and maximal sprinting speeds of different mammalian species. Data were obtained from various literature sources (see text for references). Open circles represent species data from the present study. A. Type I fibers (r= — 0.73, P<0.01). B. Type Ila fibers (r= — 0.83, P<0.01). C. Type IIx fibers (r=0.85, P<0.001).
Fig. 4. Relationships between muscle fiber type and maximal sprinting speeds of different mammalian species. Data were obtained from various literature sources (see text for references). Open circles represent species data from the present study. A. Type I fibers (r= — 0.73, P<0.01). B. Type Ila fibers (r= — 0.83, P<0.01). C. Type IIx fibers (r=0.85, P<0.001).

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FAQs

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AI

What were the main muscle fiber types identified in lions and caracals?add

The study found that both species primarily expressed type IIx fibers, indicating a sprinting capability.

How do the enzymatic activities of felid muscles compare to human athletes?add

The enzyme activities for CK and PHOS were approximately twice as high in felids compared to humans.

What unique MHC isoform finding was observed in caracal compared to lions?add

Caracals exhibited an additional unidentified band between MHC IIx and MHC I isoforms, suggesting unique characteristics.

How did muscle morphology differ between felids and humans?add

Felid muscle fibers were smaller in cross-sectional area, while type IIx fibers of caracals were larger compared to humans.

What metabolic implications arise from the low PFK activity in felids?add

Despite being anticipated for sprinting, low PFK activity challenges assumptions about glycolytic reliance in these species.

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Lion (Panthera leo) and caracal (Caracal caracal) type IIx single muscle fibre force and power exceed that of trained humans

Journal of Experimental Biology, 2013

This study investigated for the first time maximum force production, shortening velocity (V max ) and power output in permeabilised single muscle fibres at 12°C from lion, Panthera leo (Linnaeus 1758), and caracal, Caracal caracal (Schreber 1776), and compared the values with those from human cyclists. Additionally, the use and validation of previously frozen tissue for contractile experiments is reported. Only type IIx muscle fibres were identified in the caracal sample, whereas type IIx and only two type I fibres were found in the lion sample. Only pure type I and IIa, and hybrid type IIax fibres were identified in the human samplesthere were no pure type IIx fibres. Nevertheless, compared with all the human fibre types, the lion and caracal fibres were smaller (P<0.01) in cross-sectional area (human: 6194±230μm 2 , lion: 3008±151μm 2 , caracal: 2583±221μm 2 ). On average, the felid type IIx fibres produced significantly greater force (191-211kNm −2 ) and ~3 times more power (29.0-30.3kNm −2 fibre lengthss −1 ) than the human IIax fibres (100-150kNm −2 , 4-11kNm −2 fibre lengthss −1 ). V max values of the lion type IIx fibres were also higher than those of human type IIax fibres. The findings suggest that the same fibre type may differ substantially between species and potential explanations are discussed.

Hindlimb Muscle Fiber Populations of Five Mammals

Journal of Histochemistry & Cytochemistry, 1973

The fiber type profiles of hindlimb muscles in the Hartley guinea pig, Sprague-Dawley rat, cat, Galago senegalensis (lesser bushbaby) and Nycticebus coucang (slow loris) were estimated histochemically. Fibers were classified as fast oxidative glycolytic, fast glycolytic or slow oxidative according to their myosin adenosine triphosphatase, α-glycerophosphate dehydrogenase and reduced nicotinamide adenine dinucleotide diaphorase activities. It was found that the soleus and vastus intermedius muscles had the highest proportion of slow oxidative fibers in all five species, demonstrating the constancy of muscle fiber profiles dependent upon anatomical position and functional utilization. The tensor fascia latae and white vastus lateralis of the guinea pig were mostly fast glycolytic, while the red vastus lateralis of the guinea pig consisted of predominantly fast oxidative glycolytic fibers. The majority of muscles investigated in these five mammals were heterogeneous, having a wide rang...

Black wildebeest skeletal muscle exhibits high oxidative capacity and a high proportion of type IIx fibres

Journal of Experimental Biology, 2011

The aim of the study was to investigate the skeletal muscle characteristics of black wildebeest (Connochaetes gnou) in terms of fibre type and metabolism. Samples were obtained post mortem from the vastus lateralis and longissimus lumborum muscles and analysed for myosin heavy chain (MHC) content. Citrate synthase (CS), 3-hydroxyacyl co A dehydrogenase (3HAD), phosphofructokinase (PFK), lactate dehydrogenase (LDH) and creatine kinase (CK) activities were measured spectrophotometrically to represent the major metabolic pathways in these muscles. Both muscles had less than 20% MHC I, whereas MHC IIa and MHC IIx were expressed in excess of 50% in the vastus lateralis and longissimus lumborum muscles, respectively. Overall fibre size was 2675±1034m 2 , which is small compared with other species. Oxidative capacity (CS and 3HAD) in both muscles was high and did not differ from one another, but the longissimus lumborum had significantly (P<0.05) higher PFK, LDH and CK activities. No relationships were observed between fibre type and the oxidative and oxygen-independent metabolic capacity as measured by specific enzyme activities. This study confirms the presence of both fast-twitch fibres and high oxidative capacity in black wildebeest, indicating an animal that can run very fast but is also fatigue resistant.

High oxidative capacity and type IIx fibre content in springbok and fallow deer skeletal muscle suggest fast sprinters with a resistance to fatigue

Journal of Experimental Biology, 2012

Some wild antelopes are fast sprinters and more resistant to fatigue than others. This study therefore investigated two wild antelope species to better understand their reported performance capability. Muscle samples collected post mortem from the vastus lateralis and longissimus lumborum of fallow deer (Dama dama) and springbok (Antidorcas marsupialis) were analysed for myosin heavy chain isoform content, citrate synthase, 3-hydroxyacyl CoA dehydrogenase, phosphofructokinase, lactate dehydrogenase and creatine kinase activities. Cross-sectional areas, fibre type and oxidative capacities of each fibre type were determined in the vastus lateralis only. The predominant fibre type in both muscle groups and species were type IIX (>50%), with springbok having more type IIX fibres than fallow deer (P<0.05). Overall cross-sectional area was not different between the two species. The metabolic pathway analyses showed high glycolytic and oxidative capacities for both species, but springbok had significantly higher CS activities than fallow deer. Large variation and overlap in oxidative capacities existed within and between the fibre types. Some type IIX fibres presented with oxidative capacities similar to those from type I and IIA fibres. The data suggest that springbok and fallow deer are able sprint at >90 and 46kmh -1 , respectively, partly from having large type IIX fibre contents and high glycolytic capacities. The high oxidative capacities also suggest that these animals may be able to withstand fatigue for long periods of time.

Muscle Fiber Types of Gluteus Medius in the Colombian Creole Horse

Journal of Equine Veterinary Science, 2015

The skeletal muscle has several types of fibers that differ in structure, metabolism, and function. Fiber types determine the ability of horses to perform in various sports or work activities. Gluteus medius muscles of Colombian creole horses (CCHs) were sampled to determine their fiber types. Samples were processed using myosin adenosine triphosphatase (mATPase) and immunohistochemistry for fiber typing, myofibril electrophoresis for myosin heavy chain composition, and nicotinamide adenine dinucleotide diaphorase activity for oxidative capacity. The following fiber proportions were observed by immunohistochemistry (n ¼ 7): 22.5 AE 3.7% type I, 33.6 AE 2.3% type IIA, 43.6 AE 4.4% type IIX, and 0.3 AE 0.2% hybrid I/IIA fibers. The results obtained by mATPase were comparable. Regarding the oxidative capacity, 20.1 AE 4.0% had a high oxidative reaction, 32.7 AE 6.1% an intermediate reaction, and 47.2 AE 7.4% a low oxidative reaction. Of these, the high and low capacity correlated with type I and IIX fibers, respectively. Myosin heavy chain composition experiments (n ¼ 7) showed 22.2 AE 1.6% of type I, 30.4 AE 2.7% of type IIA, and 47.4 AE 2.3% of type IIX. These values are close to those published for Andalusian horses but differ from some reported for other breeds. Considering the high percentage of type IIX fibers and low to intermediate oxidative capacity, we conclude that the CCH is adapted to perform power exercise and moderate-to high-intensity anaerobic work with short to average duration. Therefore, training should be aimed at increasing aerobic capacity and endurance if these animals are required to perform long-length exercise.

Related topics

  • Physiology
  • Zoology
  • Skeletal muscle biology
  • Citrate Synthase
  • Biochemistry and cell biology
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    Group hunting within the Carnivora: physiological, cognitive and environmental influences on strategy and cooperation

    Behavioral Ecology and Sociobiology, 2013

    Cooperative hunting is believed to have important implications for the evolution of sociality and advanced cognitive abilities. Variation in the level of hunt organisation amongst species and how their cognitive, behavioural and athletic adaptations may contribute to observed patterns of cooperative hunting behaviour, however, are poorly understood. We, therefore, reviewed the literature for evidence of different levels of hunt organisation and cooperation in carnivorans and examined their social and physical adaptations for hunting. Descriptions of group hunting were scarce for many species and often of insufficient detail for us to be able to classify the level of hunt organisation involved. However, despite this, reports of behaviour fitting the description of collaboration, the most advanced level of hunt organisation, were found in over half the carnivorans reported to hunt cooperatively. There was no evidence that this behaviour would require advanced cognitive abilities. However, there was some evidence that both social mechanisms reducing aggression between group members and information transfer amongst individuals may aid cooperative hunting. In general, the cooperative strategies used seemed to depend partly on the species' locomotor abilities and habitat. There was some evidence that individuals take on consistent roles during cooperative hunts in some species, but it was not clear if this reflects individuals' physical differences, social factors or life experiences. Better understanding of the social, cognitive and physical mechanisms underlying cooperative hunting, and indeed establishing to what degree it exists in the first instance, will require more data for multiple individuals and species over many hunts.

    McArdle disease does not affect skeletal muscle fibre type profiles in humans

    Biology open, 2014

    Patients suffering from glycogen storage disease V (McArdle disease) were shown to have higher surface electrical activity in their skeletal muscles when exercising at the same intensity as their healthy counterparts, indicating more muscle fibre recruitment. To explain this phenomenon, this study investigated whether muscle fibre type is shifted towards a predominance in type I fibres as a consequence of the disease. Muscle biopsies from the Biceps brachii (BB) (n = 9) or Vastus lateralis (VL) (n = 8) were collected over a 13-year period from male and female patients diagnosed with McArdle disease, analysed for myosin heavy chain (MHC) isoform content using SDS-PAGE, and compared to healthy controls (BB: n = 3; VL: n = 10). All three isoforms were expressed and no difference in isoform expression in VL was found between the McArdle patients and healthy controls (MHC I: 33±19% vs. 43±7%; MHC IIa: 52±9% vs. 40±7%; MHC IIx: 15±18% vs. 17±9%). Similarly, the BB isoform content was also...

    Myosin Isoform Expression in the Prehensile Tails of Didelphid Marsupials: Functional Differences Between Arboreal and Terrestrial Opossums

    The Anatomical Record, 2014

    Prehensile tails are defined as having the ability to grasp objects and are commonly used as a fifth appendage during arboreal locomotion. Despite the independent evolution of tail prehensility in numerous mammalian genera, data relating muscle structure, physiology, and function of prehensile tails are largely incomplete. Didelphid marsupials make an excellent model to relate myosin heavy chain (MHC) isoform fiber type with structure/function of caudal muscles, as all opossums have a prehensile tail and tail use varies between arboreal and terrestrial forms. Expanding on our previous work in the Virginia opossum, this study tests the hypothesis that arboreal and terrestrial opossums differentially express faster versus slower MHC isoforms, respectively. MHC isoform expression and percent fiber type distribution were determined in the flexor caudae longus (FCL) muscle of Caluromys derbianus (arboreal) and Monodelphis domestica (terrestrial), using a combination of gel electrophoresis and immunohistochemistry analyses. C. derbianus expresses three MHC isoforms (1, 2A, 2X) that are distributed (mean percentage) as 8.2% MHC-1, 2.6% 1/2A, and 89.2% 2A/X hybrid fibers. M. domestica also expresses MHC-1, 2A, and 2X, in addition to the 2B isoform, distributed as 17.0% MHC-1, 1.3% 1/2A, 9.0% 2A, 75.2% 2A/X, and 0.3% 2X/B hybrid fibers. The distribution of similar isoform fiber types differed significantly between species (P < 0.001). Although not statistically significant, C. derbianus was observed to have larger cross-sectional area (CSA) for each corresponding fiber type along with a greater amount of extra-cellular matrix. An overall faster fiber type composition (and larger fibers) in the tail of an arboreal specialist supports our hypothesis, and correlates with higher muscle force required for tail hanging and arboreal maneuvering on terminal substrates. Conversely, a broader distribution of highly oxidative fibers in the caudal musculature is well suited for tail nest building/remodeling behaviors of terrestrial opossums. Anat Rec, 00:000-000,

    Cheap Labor: Myosin fiber type expression and enzyme activity in the forelimb musculature of sloths (Pilosa: Xenarthra)

    Journal of applied physiology (Bethesda, Md. : 1985), 2018

    Sloths are canopy-dwelling inhabitants of American neotropical rainforests that exhibit suspensory behaviors. These abilities require both strength and muscular endurance to hang for extended periods of time; however, the skeletal muscle mass of sloths is reduced, thus requiring modifications to muscle architecture and leverage for large joint torque. We hypothesize that intrinsic muscle properties also are modified for fatigue resistance and predict a heterogeneous expression of slow/fast myosin heavy chain (MHC) fibers that utilize oxidative metabolic pathways for economic force production. MHC fiber type distribution and energy metabolism in the forelimb muscles of three-toed ( Bradypus variegatus, N=5) and two-toed ( Choloepus hoffmanni, N=4) sloths were evaluated using SDS-PAGE, immunohistochemistry, and enzyme activity assays. The results partially support our hypothesis by a primary expression of the slow MHC-1 isoform as well as moderate expression of fast MHC-2A fibers, whi...

    Recurrent erosion of COA1/MITRAC15 demonstrates gene dispensability in oxidative phosphorylation

    2021

    Skeletal muscle fibers rely upon either oxidative phosphorylation or glycolytic pathway to achieve muscular contractions that power mechanical movements. Species with energy-intensive adaptive traits that require sudden bursts of energy have a greater dependency on fibers that use the glycolytic pathway. Glycolytic fibers have decreased reliance on OXPHOS and lower mitochondrial content compared to oxidative fibers. Hence, we hypothesized that adaptive gene loss might have occurred within the OXPHOS pathway in lineages that largely depend on glycolytic fibers. The protein encoded by the COA1/MITRAC15 gene with conserved orthologs found in budding yeast to humans promotes mitochondrial translation. We show that gene disrupting mutations have accumulated within the COA1/MITRAC15 gene in the cheetah, several species of galliforms, and rodents. The genomic region containing COA1/MITRAC15 is a well-established evolutionary breakpoint region in mammals. Careful inspection of genome assemb...

    Recurrent erosion of COA1/MITRAC15 exemplifies conditional gene dispensability in oxidative phosphorylation

    Scientific Reports, 2021

    Skeletal muscle fibers rely upon either oxidative phosphorylation or the glycolytic pathway with much less reliance on oxidative phosphorylation to achieve muscular contractions that power mechanical movements. Species with energy-intensive adaptive traits that require sudden bursts of energy have a greater dependency on glycolytic fibers. Glycolytic fibers have decreased reliance on OXPHOS and lower mitochondrial content compared to oxidative fibers. Hence, we hypothesized that gene loss might have occurred within the OXPHOS pathway in lineages that largely depend on glycolytic fibers. The protein encoded by the COA1/MITRAC15 gene with conserved orthologs found in budding yeast to humans promotes mitochondrial translation. We show that gene disrupting mutations have accumulated within the COA1 gene in the cheetah, several species of galliform birds, and rodents. The genomic region containing COA1 is a well-established evolutionary breakpoint region in mammals. Careful inspection of genome assemblies of closely related species of rodents and marsupials suggests two independent COA1 gene loss events co-occurring with chromosomal rearrangements. Besides recurrent gene loss events, we document changes in COA1 exon structure in primates and felids. The detailed evolutionary history presented in this study reveals the intricate link between skeletal muscle fiber composition and the occasional dispensability of the chaperone-like role of the COA1 gene. Skeletal muscles control numerous locomotor functions in vertebrates 1 . The hundreds of different muscles in the body consist of highly organized heterogeneous bundles of fibers. These fibers are classified based on the contractile properties, power source, and myosin component into type-1, 2A, 2B, and 2X 2 . Muscles with aerobic type-1 and 2A fibers rely on the oxidative phosphorylation (OXPHOS) pathway for sustained locomotion 3 . Locomotion that requires sudden energy bursts depends on the predominantly anaerobic 2B and 2X fibers 4 . OXPHOS is the energy-releasing electron transport chain (ETC) coupled with the energy-requiring chemiosmosis . A chain of mitochondrial inner membrane-embedded proteins encoded by mitochondrial and nuclear genes forms four large complexes that transport electrons through redox reactions. The energy released results in a proton gradient, which uses a fifth membrane-embedded complex to generate ATP through chemiosmosis. The individual complexes are known to assemble into supercomplexes 7 . Optimization of the OXPHOS pathway leads to improved locomotor performance 8 . However, degeneration of locomotor abilities leads to a relaxed selective constraint on the OXPHOS pathway 9,10 . The special locomotory needs of galliform birds, rodents, marsupials, and felids lead to a greater reliance on anaerobic fast fibers for sudden bursts of energy . The ability to fly is a distinctive feature of birds except for lineages that have become entirely flightless or retain only a limited flying capacity . The large amount of energy required for flight has necessitated a high metabolic rate in birds 18 . Increased ATP generation fulfills these energy demands through metabolic adaptations in the OXPHOS pathway . Avian flight is possible through a combination of flight muscles that consist of anaerobic white (fast glycolytic), intermediate/red-pink (fast oxidative), and aerobic red (slow oxidative) fibers . Birds with strong flight abilities, such as long-distance migrants and small passerines, contain fast oxidative fibers 23 . However, galliform species have mostly glycolytic fibers to allow short bursts of activity 24 . Hence, the OXPHOS pathway is under stronger selective constraint in non-galliform bird species than galliform birds due to the functional specialization of mitochondria to different muscle fibers 25 .

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