Mitochondrial ATP synthase β‐subunit production rate and ATP synthase specific activity are reduced in skeletal muscle of humans with obesity
New Findings What is the central question of this study? Humans with obesity have lower ATP synthesis in muscle along with lower content of the β‐subunit of the ATP synthase (β‐F1‐ATPase), the catalytic component of the ATP synthase. Does lower synthesis rate of β‐F1‐ATPase in muscle contribute to t...
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| Published in | Experimental physiology Vol. 104; no. 1; pp. 126 - 135 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
John Wiley & Sons, Inc
01.01.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | New Findings
What is the central question of this study?
Humans with obesity have lower ATP synthesis in muscle along with lower content of the β‐subunit of the ATP synthase (β‐F1‐ATPase), the catalytic component of the ATP synthase. Does lower synthesis rate of β‐F1‐ATPase in muscle contribute to these responses in humans with obesity?
What is the main finding and its importance?
Humans with obesity have a lower synthesis rate of β‐F1‐ATPase and ATP synthase specific activity in muscle. These findings indicate that reduced production of subunits forming the ATP synthase in muscle may contribute to impaired generation of ATP in obesity.
The content of the β‐subunit of the ATP synthase (β‐F1‐ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese humans, along with a reduced capacity for ATP synthesis. We studied 18 young (37 ± 8 years) subjects of which nine were lean (BMI = 23 ± 2 kg m−2) and nine were obese (BMI = 34 ± 3 kg m−2) to determine the fractional synthesis rate (FSR) and gene expression of β‐F1‐ATPase, as well as the specific activity of the ATP synthase. FSR of β‐F1‐ATPase was determined using a combination of isotope tracer infusion and muscle biopsies. Gene expression of β‐F1‐ATPase and specific activity of the ATP synthase were determined in the muscle biopsies. When compared to lean, obese subjects had lower muscle β‐F1‐ATPase FSR (0.10 ± 0.05 vs. 0.06 ± 0.03% h−1; P < 0.05) and protein expression (P < 0.05), but not mRNA expression (P > 0.05). Across subjects, abundance of β‐F1‐ATPase correlated with the FSR of β‐F1‐ATPase (P < 0.05). The specific activity of muscle ATP synthase was lower in obese compared to lean subjects (0.035 ± 0.004 vs. 0.042 ± 0.007 arbitrary units; P < 0.05), but this difference was not significant after the activity of the ATP synthase was adjusted to the β‐F1‐ATPase content (P > 0.05). Obesity impairs the synthesis of β‐F1‐ATPase in muscle at the translational level, reducing the content of β‐F1‐ATPase in parallel with reduced capacity for ATP generation via the ATP synthase complex. |
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| AbstractList | What is the central question of this study? Humans with obesity have lower ATP synthesis in muscle along with lower content of the β-subunit of the ATP synthase (β-F1-ATPase), the catalytic component of the ATP synthase. Does lower synthesis rate of β-F1-ATPase in muscle contribute to these responses in humans with obesity? What is the main finding and its importance? Humans with obesity have a lower synthesis rate of β-F
-ATPase and ATP synthase specific activity in muscle. These findings indicate that reduced production of subunits forming the ATP synthase in muscle may contribute to impaired generation of ATP in obesity.
The content of the β-subunit of the ATP synthase (β-F
-ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese humans, along with a reduced capacity for ATP synthesis. We studied 18 young (37 ± 8 years) subjects of which nine were lean (BMI = 23 ± 2 kg m
) and nine were obese (BMI = 34 ± 3 kg m
) to determine the fractional synthesis rate (FSR) and gene expression of β-F
-ATPase, as well as the specific activity of the ATP synthase. FSR of β-F
-ATPase was determined using a combination of isotope tracer infusion and muscle biopsies. Gene expression of β-F
-ATPase and specific activity of the ATP synthase were determined in the muscle biopsies. When compared to lean, obese subjects had lower muscle β-F
-ATPase FSR (0.10 ± 0.05 vs. 0.06 ± 0.03% h
; P < 0.05) and protein expression (P < 0.05), but not mRNA expression (P > 0.05). Across subjects, abundance of β-F
-ATPase correlated with the FSR of β-F
-ATPase (P < 0.05). The specific activity of muscle ATP synthase was lower in obese compared to lean subjects (0.035 ± 0.004 vs. 0.042 ± 0.007 arbitrary units; P < 0.05), but this difference was not significant after the activity of the ATP synthase was adjusted to the β-F
-ATPase content (P > 0.05). Obesity impairs the synthesis of β-F
-ATPase in muscle at the translational level, reducing the content of β-F
-ATPase in parallel with reduced capacity for ATP generation via the ATP synthase complex. The content of the β‐subunit of the ATP synthase (β‐F1‐ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese humans, along with a reduced capacity for ATP synthesis. We studied 18 young (37 ± 8 years) subjects of which nine were lean (BMI = 23 ± 2 kg m−2) and nine were obese (BMI = 34 ± 3 kg m−2) to determine the fractional synthesis rate (FSR) and gene expression of β‐F1‐ATPase, as well as the specific activity of the ATP synthase. FSR of β‐F1‐ATPase was determined using a combination of isotope tracer infusion and muscle biopsies. Gene expression of β‐F1‐ATPase and specific activity of the ATP synthase were determined in the muscle biopsies. When compared to lean, obese subjects had lower muscle β‐F1‐ATPase FSR (0.10 ± 0.05 vs. 0.06 ± 0.03% h−1; P < 0.05) and protein expression (P < 0.05), but not mRNA expression (P > 0.05). Across subjects, abundance of β‐F1‐ATPase correlated with the FSR of β‐F1‐ATPase (P < 0.05). The specific activity of muscle ATP synthase was lower in obese compared to lean subjects (0.035 ± 0.004 vs. 0.042 ± 0.007 arbitrary units; P < 0.05), but this difference was not significant after the activity of the ATP synthase was adjusted to the β‐F1‐ATPase content (P > 0.05). Obesity impairs the synthesis of β‐F1‐ATPase in muscle at the translational level, reducing the content of β‐F1‐ATPase in parallel with reduced capacity for ATP generation via the ATP synthase complex. The content of the beta subunit of the ATP synthase (β-F1-ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese humans, along with reduced capacity for ATP synthesis. We studied 18 young (37 ± 8 years old) subjects of which nine were lean (BMI = 23 ± 2 kg/m 2 ) and nine were obese (BMI = 34 ± 3 kg/m 2 ) to determine the fractional synthesis rate (FSR) and gene expression of β-F1-ATPase, as well as the specific activity of the ATP synthase. FSR of β-F1-ATPase was determined using a combination of isotope tracer infusion and muscle biopsies. Gene expression of β-F1-ATPase and specific activity of the ATP synthase were determined in the muscle biopsies. When compared to lean, obese subjects had lower muscle β-F1-ATPase FSR (0.10 ± 0.05 vs 0.06 ± 0.03 %/hr; P < 0.05) and protein expression ( P < 0.05), but not mRNA expression ( P > 0.05). Across subjects, abundance of β-F1-ATPase correlated with the FSR of β-F1-ATPase ( P < 0.05). The specific activity of muscle ATP synthase was lower in the obese when compared to lean subjects (0.035 ± 0.004 vs 0.042 ± 0.007 arbitrary units; P < 0.05), but this difference was not significant after the activity of the ATP synthase was adjusted to the β-F1-ATPase content ( P > 0.05). Obesity impairs the synthesis of β-F1-ATPase in muscle at the translational level, reducing the content of β-F1-ATPase in parallel with reduced capacity for ATP generation via the ATP synthase complex. New Findings What is the central question of this study? Humans with obesity have lower ATP synthesis in muscle along with lower content of the β‐subunit of the ATP synthase (β‐F1‐ATPase), the catalytic component of the ATP synthase. Does lower synthesis rate of β‐F1‐ATPase in muscle contribute to these responses in humans with obesity? What is the main finding and its importance? Humans with obesity have a lower synthesis rate of β‐F1‐ATPase and ATP synthase specific activity in muscle. These findings indicate that reduced production of subunits forming the ATP synthase in muscle may contribute to impaired generation of ATP in obesity. The content of the β‐subunit of the ATP synthase (β‐F1‐ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese humans, along with a reduced capacity for ATP synthesis. We studied 18 young (37 ± 8 years) subjects of which nine were lean (BMI = 23 ± 2 kg m−2) and nine were obese (BMI = 34 ± 3 kg m−2) to determine the fractional synthesis rate (FSR) and gene expression of β‐F1‐ATPase, as well as the specific activity of the ATP synthase. FSR of β‐F1‐ATPase was determined using a combination of isotope tracer infusion and muscle biopsies. Gene expression of β‐F1‐ATPase and specific activity of the ATP synthase were determined in the muscle biopsies. When compared to lean, obese subjects had lower muscle β‐F1‐ATPase FSR (0.10 ± 0.05 vs. 0.06 ± 0.03% h−1; P < 0.05) and protein expression (P < 0.05), but not mRNA expression (P > 0.05). Across subjects, abundance of β‐F1‐ATPase correlated with the FSR of β‐F1‐ATPase (P < 0.05). The specific activity of muscle ATP synthase was lower in obese compared to lean subjects (0.035 ± 0.004 vs. 0.042 ± 0.007 arbitrary units; P < 0.05), but this difference was not significant after the activity of the ATP synthase was adjusted to the β‐F1‐ATPase content (P > 0.05). Obesity impairs the synthesis of β‐F1‐ATPase in muscle at the translational level, reducing the content of β‐F1‐ATPase in parallel with reduced capacity for ATP generation via the ATP synthase complex. What is the central question of this study? Humans with obesity have lower ATP synthesis in muscle along with lower content of the β-subunit of the ATP synthase (β-F1-ATPase), the catalytic component of the ATP synthase. Does lower synthesis rate of β-F1-ATPase in muscle contribute to these responses in humans with obesity? What is the main finding and its importance? Humans with obesity have a lower synthesis rate of β-F1 -ATPase and ATP synthase specific activity in muscle. These findings indicate that reduced production of subunits forming the ATP synthase in muscle may contribute to impaired generation of ATP in obesity.NEW FINDINGSWhat is the central question of this study? Humans with obesity have lower ATP synthesis in muscle along with lower content of the β-subunit of the ATP synthase (β-F1-ATPase), the catalytic component of the ATP synthase. Does lower synthesis rate of β-F1-ATPase in muscle contribute to these responses in humans with obesity? What is the main finding and its importance? Humans with obesity have a lower synthesis rate of β-F1 -ATPase and ATP synthase specific activity in muscle. These findings indicate that reduced production of subunits forming the ATP synthase in muscle may contribute to impaired generation of ATP in obesity.The content of the β-subunit of the ATP synthase (β-F1 -ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese humans, along with a reduced capacity for ATP synthesis. We studied 18 young (37 ± 8 years) subjects of which nine were lean (BMI = 23 ± 2 kg m-2 ) and nine were obese (BMI = 34 ± 3 kg m-2 ) to determine the fractional synthesis rate (FSR) and gene expression of β-F1 -ATPase, as well as the specific activity of the ATP synthase. FSR of β-F1 -ATPase was determined using a combination of isotope tracer infusion and muscle biopsies. Gene expression of β-F1 -ATPase and specific activity of the ATP synthase were determined in the muscle biopsies. When compared to lean, obese subjects had lower muscle β-F1 -ATPase FSR (0.10 ± 0.05 vs. 0.06 ± 0.03% h-1 ; P < 0.05) and protein expression (P < 0.05), but not mRNA expression (P > 0.05). Across subjects, abundance of β-F1 -ATPase correlated with the FSR of β-F1 -ATPase (P < 0.05). The specific activity of muscle ATP synthase was lower in obese compared to lean subjects (0.035 ± 0.004 vs. 0.042 ± 0.007 arbitrary units; P < 0.05), but this difference was not significant after the activity of the ATP synthase was adjusted to the β-F1 -ATPase content (P > 0.05). Obesity impairs the synthesis of β-F1 -ATPase in muscle at the translational level, reducing the content of β-F1 -ATPase in parallel with reduced capacity for ATP generation via the ATP synthase complex.ABSTRACTThe content of the β-subunit of the ATP synthase (β-F1 -ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese humans, along with a reduced capacity for ATP synthesis. We studied 18 young (37 ± 8 years) subjects of which nine were lean (BMI = 23 ± 2 kg m-2 ) and nine were obese (BMI = 34 ± 3 kg m-2 ) to determine the fractional synthesis rate (FSR) and gene expression of β-F1 -ATPase, as well as the specific activity of the ATP synthase. FSR of β-F1 -ATPase was determined using a combination of isotope tracer infusion and muscle biopsies. Gene expression of β-F1 -ATPase and specific activity of the ATP synthase were determined in the muscle biopsies. When compared to lean, obese subjects had lower muscle β-F1 -ATPase FSR (0.10 ± 0.05 vs. 0.06 ± 0.03% h-1 ; P < 0.05) and protein expression (P < 0.05), but not mRNA expression (P > 0.05). Across subjects, abundance of β-F1 -ATPase correlated with the FSR of β-F1 -ATPase (P < 0.05). The specific activity of muscle ATP synthase was lower in obese compared to lean subjects (0.035 ± 0.004 vs. 0.042 ± 0.007 arbitrary units; P < 0.05), but this difference was not significant after the activity of the ATP synthase was adjusted to the β-F1 -ATPase content (P > 0.05). Obesity impairs the synthesis of β-F1 -ATPase in muscle at the translational level, reducing the content of β-F1 -ATPase in parallel with reduced capacity for ATP generation via the ATP synthase complex. |
| Author | Langlais, Paul R. Roust, Lori Hoffman, Nyssa Tran, Lee Katsanos, Christos S. |
| AuthorAffiliation | 1 Center for Metabolic and Vascular Biology, Arizona State University, Tempe, AZ 85297 2 College of Medicine, Mayo Clinic in Arizona, Scottsdale, AZ 85259 |
| AuthorAffiliation_xml | – name: 2 College of Medicine, Mayo Clinic in Arizona, Scottsdale, AZ 85259 – name: 1 Center for Metabolic and Vascular Biology, Arizona State University, Tempe, AZ 85297 |
| Author_xml | – sequence: 1 givenname: Lee surname: Tran fullname: Tran, Lee organization: Arizona State University – sequence: 2 givenname: Paul R. surname: Langlais fullname: Langlais, Paul R. organization: Mayo Clinic in Arizona – sequence: 3 givenname: Nyssa surname: Hoffman fullname: Hoffman, Nyssa organization: Arizona State University – sequence: 4 givenname: Lori surname: Roust fullname: Roust, Lori organization: Mayo Clinic in Arizona – sequence: 5 givenname: Christos S. orcidid: 0000-0003-3025-5752 surname: Katsanos fullname: Katsanos, Christos S. email: christos.katsanos@asu.edu organization: Mayo Clinic in Arizona |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30362197$$D View this record in MEDLINE/PubMed |
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| Keywords | protein synthesis adiposity insulin resistance mitochondria |
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| Notes | Funding information This study was supported by National Institutes of Health (NIH)/National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) grant R01DK094062 (C.S.K.) and the Mayo Clinic Metabolomics Resource Core through grant U24DK100469 from the NIH/NIDDK. Edited by: Philip Atherton ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 L.T. and C.S.K were involved in the conception of the work. All authors were involved in the acquisition, analysis and interpretation of the data and in drafting and revising the manuscript for important intellectual content. All authors approved the final version of the manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All persons designated as authors qualify for authorship, and all those who qualify for authorship are listed. Author contributions |
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| Snippet | New Findings
What is the central question of this study?
Humans with obesity have lower ATP synthesis in muscle along with lower content of the β‐subunit of... What is the central question of this study? Humans with obesity have lower ATP synthesis in muscle along with lower content of the β-subunit of the ATP... The content of the β‐subunit of the ATP synthase (β‐F1‐ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese... The content of the beta subunit of the ATP synthase (β-F1-ATPase), which forms the catalytic site of the enzyme ATP synthase, is reduced in muscle of obese... |
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| StartPage | 126 |
| SubjectTerms | Adenosine triphosphatase Adenosine Triphosphate - metabolism adiposity Adult ATP synthase Biopsy Gene expression Gene Expression - physiology Humans insulin resistance Middle Aged Mitochondria Mitochondria - metabolism Mitochondrial Proton-Translocating ATPases - metabolism Muscle, Skeletal - metabolism Obesity Obesity - metabolism protein synthesis Skeletal muscle |
| Title | Mitochondrial ATP synthase β‐subunit production rate and ATP synthase specific activity are reduced in skeletal muscle of humans with obesity |
| URI | https://onlinelibrary.wiley.com/doi/abs/10.1113%2FEP087278 https://www.ncbi.nlm.nih.gov/pubmed/30362197 https://www.proquest.com/docview/2161769851 https://www.proquest.com/docview/2126901079 https://pubmed.ncbi.nlm.nih.gov/PMC6312454 |
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