Reduced skeletal muscle AMPK and mitochondrial markers do not promote age-induced insulin resistance

Journal article


Bujak, Adam, Blumer, Regje, Marcinko, Katarina, Fullerton, Morgan, Kemp, Bruce and Steinberg, Gregory. (2014) Reduced skeletal muscle AMPK and mitochondrial markers do not promote age-induced insulin resistance. Journal of Applied Physiology. 117(2), pp. 171 - 179. https://doi.org/10.1152/japplphysiol.01101.2013
AuthorsBujak, Adam, Blumer, Regje, Marcinko, Katarina, Fullerton, Morgan, Kemp, Bruce and Steinberg, Gregory
Abstract

In both rodents and humans, aging-associated reductions in skeletal muscle AMP-activated protein kinase (AMPK) activity and mitochondrial function have been linked to the development of skeletal muscle insulin resistance. However, whether reductions in skeletal muscle AMPK and mitochondrial capacity actually precipitate the development of aging-induced insulin resistance is not known. Mice lacking both isoforms of the AMPK β-subunit in skeletal muscle (AMPK-MKO) have no detectable AMPK activity and are characterized by large reductions in exercise capacity, mitochondrial content, and contraction-stimulated glucose uptake making them an ideal model to determine whether reductions in AMPK and mitochondrial content promote the development of aging-induced insulin resistance. In the current study we find that a lack of skeletal muscle AMPK results in a life-long reduction in mitochondrial activity but does not affect body mass, body composition, glucose tolerance, or insulin sensitivity as measured by hyperinsulinemic-euglycemic clamp in mice of old age (18 mo). These data demonstrate that reductions in skeletal muscle AMPK and mitochondrial activity do not cause the development of age-induced insulin resistance.

Year2014
JournalJournal of Applied Physiology
Journal citation117 (2), pp. 171 - 179
ISSN8750-7587
Digital Object Identifier (DOI)https://doi.org/10.1152/japplphysiol.01101.2013
Page range171 - 179
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Zordoky, Beshay N.M., Nagendran, Jeevan, Pulinilkunnil, Thomas, Kienesberger, Petra C., Masson, Grant, Waller, Terri J., Kemp, Bruce E., Steinberg, Gregory R. and Dyck, Jason R. B.. (2012) AMPK-dependent inhibitory phosphorylation of ACC is not essential for maintaining myocardial fatty acid oxidation. Circulation Research. 115(5), pp. 518 - 524. https://doi.org/10.1161/CIRCRESAHA.115.304538
The ancient drug salicylate directly activates AMP-activated protein kinase
Hawley, Simon, Fullerton, Morgan, Ross, Fiona, Schertzer, Jonathan, Chevtzoff, Cyrille, Walker, Katherine, Peggie, Mark, Zibrova, Darya, Green, Kevin, Mustard, Kirsty, Kemp, Bruce, Sakamoto, Kei, Steinberg, Gregory and Hardie, D. Grahame. (2012) The ancient drug salicylate directly activates AMP-activated protein kinase. Science. 336(6083), pp. 918 - 922. https://doi.org/10.1126/science.1215327
Pro-GRP-derived peptides are expressed in colorectal cancer cells and tumors and are biologically active in vivo
Patel, Oneel, Clyde, Daniel, Chang, Mike, Nordlund, Marianne, Steel, Rohan, Kemp, Bruce, Pritchard, D. Mark, Shulkes, Arthur and Baldwin, Graham. (2012) Pro-GRP-derived peptides are expressed in colorectal cancer cells and tumors and are biologically active in vivo. Endocrinology. 153(3), pp. 1082 - 1092. https://doi.org/10.1210/en.2011-1875
The outcome of renal ischemia-reperfusion injury is unchanged in AMPK-ß1 deficient mice
Mount, Peter, Gleich, Kurt, Tam, Shanna, Fraser, Scott, Choy, Suet-Wan, Dwyer, Karen, Lu, Bo, Van Denderen, Bryce, Fingerle-Rowson, Gunter, Bucala, Richard, Kemp, Bruce and Power, David. (2012) The outcome of renal ischemia-reperfusion injury is unchanged in AMPK-ß1 deficient mice. PLoS One (online). 7(1), pp. 1 - 10. https://doi.org/10.1371/journal.pone.0029887
Inhibition of the heterotetrameric K+ channel KCNQ1/KCNE1 by the AMP-activated protein kinase
Alesultan, Ioana, Foller, Michael, Sopjani, Mentor, Dermaku-Sopjani, Miribane, Zelenak, Christine, Frohlich, Henning, Velic, Ana, Fraser, Scott, Kemp, Bruce, Seebohm, Guiscard, Volkl, Harald and Lang, Florian. (2011) Inhibition of the heterotetrameric K+ channel KCNQ1/KCNE1 by the AMP-activated protein kinase. Molecular Membrane Biology. 28(2), pp. 79 - 89. https://doi.org/10.3109/09687688.2010.520037
AMP-activated protein kinase (AMPK) ß1ß2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise
O'Neill, Hayley M., Maarbjerg, Stine J., Crane, Justin D., Jeppesen, Jacob, Jorgensen, Sebastian B., Schertzer, Jonathan D., Shyroka, Olga, Kiens, Bente, Van Denderen, Bryce J., Tarnopolsky, Mark A., Kemp, Bruce Ernest, Richter, Erik A. and Steinberg, Gregory R.. (2011) AMP-activated protein kinase (AMPK) ß1ß2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proceedings of the National Academy of Sciences of USA. 108(38), pp. 16092 - 16097. https://doi.org/10.1073/pnas.1105062108
Ca 2+/calmodulin-dependent protein kinase kinase beta is regulated by multisite phosphorylation
Green, Michelle, Scott, John, Steel, Rohan, Oakhill, Jonathan, Kemp, Bruce and Means, Anthony. (2011) Ca 2+/calmodulin-dependent protein kinase kinase beta is regulated by multisite phosphorylation. Journal of Biological Chemistry. 286(32), pp. 28066 - 28079. https://doi.org/10.1074/jbc.M111.251504
Hematopoietic AMPK beta1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity
Galic, Sandra, Fullerton, Morgan, Schertzer, Jonathan, Sikkema, Sarah, Marcinko, Katarina, Walkley, Carl, Izon, David, Honeyman, Jane, Chen, Zhi-Ping, Van Denderen, Bryce, Kemp, Bruce and Steinberg, Gregory. (2011) Hematopoietic AMPK beta1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity. Journal of Clinical Investigation. 121(12), pp. 4903 - 4915. https://doi.org/10.1172/JCI58577
Hematopoietic AMPK Beta ß1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity
Galic, Sandra, Fullerton, Morgan D., Schertzer, Jonathan D., Sikkema, Sarah, Marcinko, Katarina, Walkley, Carl R., Izon, David, Honeyman, Jane, Chen, Zhi-Ping, van Denderen, Bryce J., Kemp, Bruce Ernest and Steinberg, Gregory R.. (2011) Hematopoietic AMPK Beta ß1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity. Journal of Clinical Investigation. 121(12), pp. 4903 - 4915. https://doi.org/10.1172/JCI58577
Inhibition of Kir2.1 (KCNJ2) by the AMP-activated protein kinase
Alesutan, Ioana, Munoz, Carlos, Sopjani, Mentor, Dermaku-Sopjani, Miribane, Michael, Diana, Fraser, Scott, Kemp, Bruce, Seebohm, Guiscard, Foller, Michael and Lang, Florian. (2011) Inhibition of Kir2.1 (KCNJ2) by the AMP-activated protein kinase. Biochemical and Biophysical Research Communications. 408(4), pp. 505 - 510. https://doi.org/10.1016/j.bbrc.2011.04.015
Inhibition of Connexin 26 by the AMP-activated protein kinase
Alesutan, Ioana, Sopjani, Mentor, Munoz, Carlos, Fraser, Scott, Kemp, Bruce, Foller, Michael and Lang, Florian. (2011) Inhibition of Connexin 26 by the AMP-activated protein kinase. Journal of Membrane Biology: an international journal for studies on the structure, function and genesis of biomembranes. 240(3), pp. 151 - 158. https://doi.org/10.1007/s00232-011-9353-y
AMPK is a direct adenylate charge-regulated protein kinase
Oakhill, Jonathan S., Steel, Rohan, Chen, Zhi-Ping, Scott, John W., Ling, Naomi, Tam, Shanna and Kemp, Bruce Ernest. (2011) AMPK is a direct adenylate charge-regulated protein kinase. Science. 332(6036), pp. 1433 - 1435. https://doi.org/10.1126/science.1200094
AMPK couples plasma renin to cellular metabolism by phosphorylation of ACC1
Fraser, Scott A., Choy, Suet-Wan, Pastor-Soler, Núria M., Li, Hui, Davies, Matthew R. P., Cook, Natasha, Katerelos, Marina, Mount, Peter F., Gleich, Kurt, McRae, Jennifer L., Dwyer, Karen M., van Denderen, Bryce J. W., Hallows, Kenneth R., Kemp, Bruce E. and Power, David A.. (2010) AMPK couples plasma renin to cellular metabolism by phosphorylation of ACC1. American Journal of Physiology - Renal Physiology. 305(5), pp. F679 - F690. https://doi.org/10.1152/ajprenal.00407.2012
Impaired skeletal muscle beta-adrenergic activation and lipolysis are associated with whole-body insulin resistance in rats bred for low intrinsic exercise capacity
Lessard, Sarah J., Rivas, Donato A., Chen, Zhu-Ping, van Denderen, Bryce J., Watt, Matthew J., Koch, Lauren G., Britton, Steven L., Kemp, Bruce Ernest and Hawley, John Alan. (2009) Impaired skeletal muscle beta-adrenergic activation and lipolysis are associated with whole-body insulin resistance in rats bred for low intrinsic exercise capacity. Endocrinology. 150(11), pp. 4883 - 4891. https://doi.org/10.1210/en.2009-0158
Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans
Yeo, Wee Kian, Lessard, Sarah J., Chen, Zhi-Ping, Garnham, Andrew P., Burke, Louise, Rivas, Donato A., Kemp, Bruce Ernest and Hawley, John Alan. (2008) Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans. Journal of Applied Physiology. 105(5), pp. 1519 - 1526. https://doi.org/10.1152/japplphysiol.90540.2008
Activation of AMPK reduces the co-transporter activity of NKCC1
Fraser, Scott A., Davies, Matthew, Katerelos, Marina, Gleich, Kurt, Choy, Suet-Wan, Steel, Rohan, Galic, Sandra, Mount, Peter F., Kemp, Bruce E. and Power, David A.. (1999) Activation of AMPK reduces the co-transporter activity of NKCC1. Molecular Membrane Biology. 31(2-3), pp. 95 - 102. https://doi.org/10.3109/09687688.2014.902128
Myosin light chain kinases
Kemp, Bruce E. and Stull, James T.. (1990) Myosin light chain kinases. In In B. E. Kemp (Ed.). Peptides and Protein Phosphorylation pp. 115 - 133 CRC Press. https://doi.org/10.1201/9781351075442