Ablating the protein TBC1D1 impairs contraction-induced sarcolemmal glucose transporter 4 redistribution but not insulin-mediated responses in rats

Journal article


Whitfield, Jamie, Paglialunga, Sabina, Smith, Brennan K., Miotto, Paula M., Simnett, Genevieve, Robson, Holly L., Jain, Swati S., Herbst, Eric A. F., Desjardins, Eric M., Dyck, David J., Spriet, Lawrence L., Steinberg, Gregory R. and Holloway, Graham P.. (2017). Ablating the protein TBC1D1 impairs contraction-induced sarcolemmal glucose transporter 4 redistribution but not insulin-mediated responses in rats. Journal of Biological Chemistry. 292(40), pp. 16653 - 16664. https://doi.org/10.1074/jbc.M117.806786
AuthorsWhitfield, Jamie, Paglialunga, Sabina, Smith, Brennan K., Miotto, Paula M., Simnett, Genevieve, Robson, Holly L., Jain, Swati S., Herbst, Eric A. F., Desjardins, Eric M., Dyck, David J., Spriet, Lawrence L., Steinberg, Gregory R. and Holloway, Graham P.
Abstract

TBC1 domain family member 1 (TBC1D1), a Rab GTPase-activating protein and paralogue of Akt substrate of 160 kDa (AS160), has been implicated in both insulin- and 5-aminoimidazole-4-carboxamide ribonucleotide formyltransferase/IMP cyclohydrolase-mediated glucose transporter type 4 (GLUT4) translocation. However, the role of TBC1D1 in contracting muscle remains ambiguous. We therefore explored the metabolic consequence of ablating TBC1D1 in both resting and contracting skeletal muscles, utilizing a rat TBC1D1 KO model. Although insulin administration rapidly increased (p < 0.05) plasma membrane GLUT4 content in both red and white gastrocnemius muscles, the TBC1D1 ablation did not alter this response nor did it affect whole-body insulin tolerance, suggesting that TBC1D1 is not required for insulin-induced GLUT4 trafficking events. Consistent with findings in other models of altered TBC1D1 protein levels, whole-animal and ex vivo skeletal muscle fat oxidation was increased in the TBC1D1 KO rats. Although there was no change in mitochondrial content in the KO rats, maximal ADP-stimulated respiration was higher in permeabilized muscle fibers, which may contribute to the increased reliance on fatty acids in resting KO animals. Despite this increase in mitochondrial oxidative capacity, run time to exhaustion at various intensities was impaired in the KO rats. Moreover, contraction-induced increases in sarcolemmal GLUT4 content and glucose uptake were lower in the white gastrocnemius of the KO animals. Altogether, our results highlight a critical role for TBC1D1 in exercise tolerance and contraction-mediated translocation of GLUT4 to the plasma membrane in skeletal muscle.

Keywordscarbohydrate metabolism; fatty acid metabolism; glucose transporter type 4 (GLUT4); GTPase-activating protein (GAP); skeletal muscle metabolism
Year2017
JournalJournal of Biological Chemistry
Journal citation292 (40), pp. 16653 - 16664
PublisherAmerican Society for Biochemistry and Molecular Biology, Inc.
ISSN1083-351X
Digital Object Identifier (DOI)https://doi.org/10.1074/jbc.M117.806786
Scopus EID2-s2.0-85030755511
Open accessOpen access
Page range16653 - 16664
Research GroupMary MacKillop Institute for Health Research
Publisher's version
License
Place of publicationUnited States of America
Permalink -

https://acuresearchbank.acu.edu.au/item/85223/ablating-the-protein-tbc1d1-impairs-contraction-induced-sarcolemmal-glucose-transporter-4-redistribution-but-not-insulin-mediated-responses-in-rats

Download files

  • 115
    total views
  • 72
    total downloads
  • 3
    views this month
  • 6
    downloads this month
These values are for the period from 19th October 2020, when this repository was created.

Export as

Related outputs

Metabolic Adaptations to Training
Whitfield, Jamie. (2023). Metabolic Adaptations to Training. In Endurance Training - Science and practice  pp. 185-197 Iñigo Mujika S.L.U..
The Impact of a Short-Term Ketogenic Low-Carbohydrate High-Fat Diet on Biomarkers of Intestinal Epithelial Integrity and Gastrointestinal Symptoms
McKay, Alannah Kelli Anique, Wallett, Alice M., McKune, Andrew, Periard, Julien, Saunders, Philo, Whitfield, Jamie, Tee, Nicolin, Heikura, Ida, Ross, Megan Louise Rhys, Sharma, Avish P., Costa, Ricardo J.S. and Burke, Louise Mary. (2023). The Impact of a Short-Term Ketogenic Low-Carbohydrate High-Fat Diet on Biomarkers of Intestinal Epithelial Integrity and Gastrointestinal Symptoms. International Journal of Sport Nutrition and Exercise Metabolism. 33(6), pp. 305-315. https://doi.org/10.1123/ijsnem.2023-0009
Short severe energy restriction with refueling reduces body mass without altering training-associated performance improvement
Burke, Louise M., Whitfield, Jamie, Ross, Megan L., Tee, Nicolin, Sharma, Avish P., King, Andy K., Heikura, Ida A., Morabito, Aimee and McKay, Alannah K. A.. (2023). Short severe energy restriction with refueling reduces body mass without altering training-associated performance improvement. Medicine and Science in Sports and Exercise. 55(8), pp. 1487-1498. https://doi.org/10.1249/MSS.0000000000003169
The use of continuous glucose monitors in sport : Possible applications and considerations
Bowler, Amy-Lee, Whitfield, Jamie, Marshall, Lachlan, Coffey, Vernon G., Burke, Louise M. and Cox, Gregory R.. (2023). The use of continuous glucose monitors in sport : Possible applications and considerations. International Journal of Sport Nutrition and Exercise Metabolism. 33(2), pp. 121-132. https://doi.org/10.1123/ijsnem.2022-0139
Six days of low carbohydrate, not energy availability, alters the iron and immune response to exercise in elite athletes
McKay, Alannah K. A., Peeling, Peter, Pyne, David B., Tee, Nicolin, Whitfield, Jamie, Sharma, Avish P., Heikura, Ida A. and Burke, Louise M.. (2022). Six days of low carbohydrate, not energy availability, alters the iron and immune response to exercise in elite athletes. Medicine and Science in Sports and Exercise. 54(3), pp. 377-387. https://doi.org/10.1249/MSS.0000000000002819
Disrupting AMPK-glycogen binding in mice increases carbohydrate utilization and reduces exercise capacity
Janzen, Natalie R., Whitfield, Jamie, Murray-Segal, Lisa, Kemp, Bruce E., Hawley, John A. and Hoffman, Nolan J.. (2022). Disrupting AMPK-glycogen binding in mice increases carbohydrate utilization and reduces exercise capacity. Frontiers in Physiology. 13, p. 859246. https://doi.org/10.3389/fphys.2022.859246
Dietary manipulation for optimizing endurance training adaptations and performance : Carbohydrate vs. fat
Whitfield, Jamie and Burke, Louise M.. (2021). Dietary manipulation for optimizing endurance training adaptations and performance : Carbohydrate vs. fat. In In Tiidus, Peter M., MacPherson, Rebecca E. K., LeBlanc, Paul J. and Josse, Andrea R. (Ed.). The Routledge handbook on biochemistry of exercise pp. 292-303 Routledge. https://doi.org/10.4324/9781003123835-19
Mice with whole-body disruption of AMPK-glycogen binding have increased adiposity, reduced fat oxidation and altered tissue glycogen dynamics
Janzen, Natalie, Whitfield, Jamie, Murray-Segal, Lisa, Kemp, Bruce E., Hawley, John A. and Hoffman, Nolan J.. (2021). Mice with whole-body disruption of AMPK-glycogen binding have increased adiposity, reduced fat oxidation and altered tissue glycogen dynamics. International Journal of Molecular Sciences. 22(17), p. Article: 9616. https://doi.org/10.3390/ijms22179616
Myofibre hypertrophy in the absence of changes to satellite cell content following concurrent exercise training in young healthy men
Shamim, Baubak, Camera, Donny M. and Whitfield, Jamie. (2021). Myofibre hypertrophy in the absence of changes to satellite cell content following concurrent exercise training in young healthy men. Frontiers in Physiology. 12, p. Article 625044. https://doi.org/10.3389/fphys.2021.625044
Neither beetroot juice supplementation nor increased carbohydrate oxidation enhance economy of prolonged exercise in elite race walkers
Burke, Louise M., Hall, Rebecca, Heikura, Ida A., Ross, Megan L., Tee, Nicolin, Kent, Georgina L., Whitfield, Jamie, Forbes, Sara F., Sharma, Avish P., Jones, Andrew M., Peeling, Peter, Blackwell, Jamie R., Mujika, Iñigo, Mackay, Karen, Kozior, Marta, Vallance, Brent and McKay, Alannah K. A.. (2021). Neither beetroot juice supplementation nor increased carbohydrate oxidation enhance economy of prolonged exercise in elite race walkers. Nutrients. 13(8), p. Article 2767. https://doi.org/10.3390/nu13082767
Acute ketogenic diet and ketone ester supplementation impairs race walk performance
Whitfield, Jamie, Burke, Louise M., McKay, Alannah K. A., Heikura, Ida A., Hall, Rebecca, Fensham, Nikita and Sharma, Avish P.. (2021). Acute ketogenic diet and ketone ester supplementation impairs race walk performance. Medicine and Science in Sports and Exercise. 53(4), pp. 776-784. https://doi.org/10.1249/MSS.0000000000002517
Sustained Exposure to High Carbohydrate Availability Does Not Influence Iron-Regulatory Responses in Elite Endurance Athletes
McKay, A., Peeling, P., Pyne, D.B., Tee, N., Welveart, M., Heikura, I., Sharma, A.P., Whitfield, J., Ross, M., van Swelm, R.P.L., Laarakkers, C.M. and Burke, L.. (2021). Sustained Exposure to High Carbohydrate Availability Does Not Influence Iron-Regulatory Responses in Elite Endurance Athletes. International Journal of Sport Nutrition and Exercise Metabolism. 31(2), pp. 101-108. https://doi.org/10.1123/ijsnem.2020-0224
Chronic pantothenic acid supplementation does not affect muscle coenzyme A content or cycling performance
Whitfield, Jamie, Harris, Roger C., Broad, Elizabeth M., Patterson, Alison K., Ross, Megan L. R., Shaw, Gregory, Spriet, Lawrence L. and Burke, Louise M.. (2021). Chronic pantothenic acid supplementation does not affect muscle coenzyme A content or cycling performance. Applied Physiology, Nutrition and Metabolism. 46(3), pp. 280-283. https://doi.org/10.1139/apnm-2020-0692
Adaptation to Low Carbohydrate High Fat diet is rapid but impairs endurance exercise metabolism and performance despite enhanced glycogen availability
Burke, Louise M., Whitfield, Jamie, Heikura, Ida A., Ross, Megan L. R., Tee, Nicolin, Forbes, Sara F., Hall, Rebecca, McKay, Alannah K. A., Wallett, Alice M. and Sharma, Avish P.. (2021). Adaptation to Low Carbohydrate High Fat diet is rapid but impairs endurance exercise metabolism and performance despite enhanced glycogen availability. Journal of Physiology. 599(3), pp. 771-790. https://doi.org/10.1113/JP280221
Omega-3 polyunsaturated fatty acids mitigate palmitate-induced impairments in skeletal muscle cell viability and differentiation
Tachtsis, Bill, Whitfield, Jamie, Hawley, John A. and Hoffman, Nolan J.. (2020). Omega-3 polyunsaturated fatty acids mitigate palmitate-induced impairments in skeletal muscle cell viability and differentiation. Frontiers in Physiology. 11, pp. 1-13. https://doi.org/10.3389/fphys.2020.00563
Exploring the mechanisms by which nitrate supplementation improves skeletal muscle contractile function: one fibre at a time
Luke C. McIlvenna, David J. Muggeridge and Jamie Whitfield. (2020). Exploring the mechanisms by which nitrate supplementation improves skeletal muscle contractile function: one fibre at a time. The Journal of Physiology. 598(1), pp. 25-27. https://doi.org/10.1113/Jp279118
Genetic loss of AMPK-glycogen binding destabilizes AMPK and disrupts metabolism
Hoffman, Nolan J., Whitfield, Jamie, Janzen, Natalie R., Belhaj, Mehdi R., Galic, Sandra, Murray-Segal, Lisa, Smiles, William J., Ling, Naomi X. Y., Dite, Toby A., Scott, John W., Oakhill, Jonathan S., Brink, Robert, Kemp, Bruce E. and Hawley, John A.. (2020). Genetic loss of AMPK-glycogen binding destabilizes AMPK and disrupts metabolism. Molecular Metabolism. 41, pp. 1-13. https://doi.org/10.1016/j.molmet.2020.101048
Exploring the mechanisms by which nitrate supplementation improves skeletal muscle contractile function: one fibre at a time
McIlvenna, L.C., Muggeridge, D.J. and Whitfield, J.. (2020). Exploring the mechanisms by which nitrate supplementation improves skeletal muscle contractile function: one fibre at a time. The Journal of Physiology. 598(1), pp. 25-27. https://doi.org/10.1113/JP279118
Estimated sweat loss, fluid and CHO intake, and sodium balance of male major junior, AHL, and NHL players during on-ice practices
Gamble, Alexander S. D., Bigg, Jessica L., Vermeulen, Tyler F., Boville, Stephanie M., Eskedjian, Greg S., Jannas-Vela, Sebastian, Whitfield, Jamie, Palmer, Matthew S. and Spriet, Lawrence L.. (2019). Estimated sweat loss, fluid and CHO intake, and sodium balance of male major junior, AHL, and NHL players during on-ice practices. International Journal of Sport Nutrition and Exercise Metabolism. 29(6), pp. 612 - 619. https://doi.org/10.1123/ijsnem.2019-0029
Contemporary nutrition interventions to optimize performance in middle-distance runners
Stellingwerff, Trent, Bovim, Ingvill Måkestad and Whitfield, Jamie. (2019). Contemporary nutrition interventions to optimize performance in middle-distance runners. International Journal of Sport Nutrition and Exercise Metabolism. 29(2), pp. 106 - 116. https://doi.org/10.1123/ijsnem.2018-0241
Interactive roles for AMPK and glycogen from cellular energy sensing to exercise metabolism
Janzen, Natalie, Whitfield, Jamie and Hoffman, Nolan. (2018). Interactive roles for AMPK and glycogen from cellular energy sensing to exercise metabolism. International Journal of Molecular Sciences. 19(11), pp. 1 - 18. https://doi.org/10.3390/ijms19113344
Alpha-Linolenic acid and exercise training independently, and additively, decrease blood pressure and prevent diastolic dysfunction in obese Zucker rats
Barbeau, Pierre-Andre, Holloway, Tanya M., Whitfield, Jamie, Baechler, Brittany L., Quadrilatero, Joe, van Loon, Luc J. C., Chabowski, Adrian and Holloway, Graham P.. (2017). Alpha-Linolenic acid and exercise training independently, and additively, decrease blood pressure and prevent diastolic dysfunction in obese Zucker rats. The Journal of Physiology. 595(13), pp. 4351 - 4364. https://doi.org/10.1113/JP274036
Glucagon receptor knockout mice are protected against acute olanzapine-induced hyperglycemia
Castellani, Laura N., Peppler, Willem T., Sutton, Charles D., Whitfield, Jamie, Charron, Maureen J. and Wright, David C.. (2017). Glucagon receptor knockout mice are protected against acute olanzapine-induced hyperglycemia. Psychoneuroendocrinology. 82, pp. 38 - 45. https://doi.org/10.1016/j.psyneuen.2017.05.005
Beetroot juice increases human muscle force without changing Ca2+-handling proteins
Whitfield, Jamie, Gamu, Daniel, Heigenhauser, George J. F., van Loon, Luc J. C., Spriet, Lawrence L., Tupling, A. Russell and Holloway, Graham P.. (2017). Beetroot juice increases human muscle force without changing Ca2+-handling proteins. Medicine and Science in Sports and Exercise. 49(10), pp. 2016 - 2024. https://doi.org/10.1249/MSS.0000000000001321
Beetroot juice supplementation reduces whole body oxygen consumption but does not improve indices of mitochondrial efficiency in human skeletal muscle
Whitfield, J., Ludzki, A., Heigenhauser, G. J. F., Senden, Joan M. G., Verdijk, Lex B., van Loon, Luc J. C., Spriet, L. L. and Holloway, Graham P.. (2016). Beetroot juice supplementation reduces whole body oxygen consumption but does not improve indices of mitochondrial efficiency in human skeletal muscle. Journal of Physiology. 594(2), pp. 421 - 435. https://doi.org/10.1113/JP270844
Taurine and skeletal muscle function
Spriet, Lawrence L. and Whitfield, Jamie. (2015). Taurine and skeletal muscle function. Current Opinion in Clinical Nutrition and Metabolic Care. 18(1), pp. 96 - 101. https://doi.org/10.1097/MCO.0000000000000135
Activation of AMPK alpha2 is not required for mitochondrial FAT/CD36 accumulation during exercise
Monaco, Cynthia, Whitfield, Jamie, Jain, Swati S., Spriet, Lawrence L., Bonen, Arend and Holloway, Graham P.. (2015). Activation of AMPK alpha2 is not required for mitochondrial FAT/CD36 accumulation during exercise. PLoS ONE. 10(5), pp. 1 - 15. https://doi.org/10.1371/journal.pone.0126122
Variable effects of 12 weeks of omega-3 supplementation on resting skeletal muscle metabolism
Gerling, Christopher J., Whitfield, Jamie, Mukai, Kazutaka and Spriet, Lawrence L.. (2014). Variable effects of 12 weeks of omega-3 supplementation on resting skeletal muscle metabolism. Applied Physiology, Nutrition and Metabolism. 39(9), pp. 1083 - 1091. https://doi.org/10.1139/apnm-2014-0049
Omega-3 supplementation alters mitochondrial membrane composition and respiration kinetics in human skeletal muscle
Herbst, E. A. F., Paglialunga, S., Gerling, C., Whitfield, Jamie, Mukai, K., Chabowski, Adrian, Heigenhauser, G. J. F., Spriet, L. L. and Holloway, Graham P.. (2014). Omega-3 supplementation alters mitochondrial membrane composition and respiration kinetics in human skeletal muscle. The Journal of Physiology. 592(6), pp. 1341 - 1352. https://doi.org/10.1113/jphysiol.2013.267336
Beetroot juice supplementation does not improve performance of elite 1500-m runners
Boorsma, Robert K., Whitfield, Jamie and Spriet, Lawrence L.. (2014). Beetroot juice supplementation does not improve performance of elite 1500-m runners. Medicine and Science in Sports and Exercise. 46(12), pp. 2326 - 2334. https://doi.org/10.1249/MSS.0000000000000364