A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias
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The AMP-activated protein kinase (AMPK) is an alphabetagamma heterotrimer that is activated by low cellular energy status and affects a switch away from energy-requiring processes and toward catabolism. While it is primarily regulated by AMP and ATP, high muscle glycogen has also been shown to repress its activation. Mutations in the gamma2 and gamma3 subunit isoforms lead to arrhythmias associated with abnormal glycogen storage in human heart and elevated glycogen in pig muscle, respectively. A putative glycogen binding domain (GBD) has now been identified in the beta subunits. Coexpression of truncated beta subunits lacking the GBD with alpha and gamma subunits yielded complexes that were active and normally regulated. However, coexpression of alpha and gamma with full-length beta caused accumulation of AMPK in large cytoplasmic inclusions that could be counterstained with anti-glycogen or anti-glycogen synthase antibodies. These inclusions were not affected by mutations that increased or abolished the kinase activity and were not observed by using truncated beta subunits lacking the GBD. Our results suggest that the GBD binds glycogen and can lead to abnormal glycogen-containing inclusions when the kinase is overexpressed. These may be related to the abnormal glycogen storage bodies seen in heart disease patients with gamma2 mutations.
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The β-subunit includes a carbohydrate-binding module that grants AMPK the ability to bind glycogen.
“The β-subunit includes a carbohydrate-binding module that grants AMPK to bind to glycogen [25].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [25]
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Cross-talk between Two Essential Nutrient-sensitive Enzymes
Bullen, J. W., Balsbaugh, J. L., Chanda, D., Shabanowitz, J., Hunt, D. F., Neumann, D., & Hart, G. W. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.523068 · Cited by 216 · see citing works
AMPK and autophagy in glucose/glycogen metabolism
Ha, J., Guan, K., & Kim, J. (2015) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2015.08.002 · Cited by 211 · see citing works
AMP-activated protein kinase: balancing the scales
Carling, D. (2004) · Biochimie · doi:10.1016/j.biochi.2004.10.017 · Cited by 201 · see citing works
Miller, V. J., Villamena, F. A., & Volek, J. S. (2018) · Journal of Nutrition and Metabolism · doi:10.1155/2018/5157645 · Cited by 200 · see citing works
AMP-activated protein kinase: Also regulated by ADP?
Hardie, D. G., Carling, D., & Gamblin, S. J. (2011) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2011.06.004 · Cited by 187 · see citing works
Self-citationStructural Basis for Glycogen Recognition by AMP-Activated Protein Kinase
Polekhina, G., Gupta, A., van Denderen, B. J. W., Feil, S. C., Kemp, B. E., Stapleton, D., & Parker, M. W. (2005) · Structure · doi:10.1016/j.str.2005.07.008 · Cited by 187 · see citing works
Salt, I. P., & Hardie, D. G. (2017) · Circulation Research · doi:10.1161/circresaha.117.309633 · Cited by 186 · see citing works
Self-citationHardie, D. G. (2011) · Biochemical Society Transactions · doi:10.1042/bst0390001 · Cited by 177 · see citing works
Self-citationRegulation of AMP-activated protein kinase by natural and synthetic activators
Hardie, D. G. (2015) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2015.06.002 · Cited by 176 · see citing works
Self-citationPhysiological role of AMP-activated protein kinase in the heart: graded activation during exercise
Coven, D. L., Hu, X., Cong, L., Bergeron, R., Shulman, G. I., Hardie, D. G., & Young, L. H. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00171.2003 · Cited by 174 · see citing works
Self-citationDifferential regulation by AMP and ADP of AMPK complexes containing different γ subunit isoforms
Ross, F. A., Jensen, T. E., & Hardie, D. G. (2016) · Biochemical Journal · doi:10.1042/bj20150910 · Cited by 172 · see citing works
Self-citationAMP-activated protein kinase: a key system mediating metabolic responses to exercise
HARDIE, D. G. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000106171.38299.64 · Cited by 165 · see citing works
Self-citationCrystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1
Amodeo, G. A., Rudolph, M. J., & Tong, L. (2007) · Nature · doi:10.1038/nature06127 · Cited by 164 · see citing works
AMP‐activated protein kinase and cancer
Wang, W., & Guan, K. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.01980.x · Cited by 163 · see citing works
Wu, S., Wu, Y., Wu, T.-P., & Wei, Y. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.10.034 · Cited by 159 · see citing works
Role of the energy sensor AMP-activated protein kinase in renal physiology and disease
Hallows, K. R., Mount, P. F., Pastor‐Soler, N. M., & Power, D. A. (2010) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00005.2010 · Cited by 156 · see citing works
More than a store: regulatory roles for glycogen in skeletal muscle adaptation to exercise
Philp, A., Hargreaves, M., & Baar, K. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00004.2012 · Cited by 155 · see citing works
AMPK: a cellular energy sensor primarily regulated by AMP
Gowans, G. J., & Hardie, D. G. (2014) · Biochemical Society Transactions · doi:10.1042/bst20130244 · Cited by 149 · see citing works
Self-citationStarch-binding domains as CBM families–history, occurrence, structure, function and evolution
Janeĉek, Ŝ., Mareček, F., MacGregor, E. A., & Svensson, B. (2019) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.107451 · Cited by 151 · see citing works
Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism
Hardie, D. G. (2011) · Proceedings of the Nutrition Society · doi:10.1017/s0029665110003915 · Cited by 146 · see citing works
Self-citationExercise-induced AMPK activity in skeletal muscle: Role in glucose uptake and insulin sensitivity
Friedrichsen, M., Mortensen, B., Pehmøller, C., Birk, J. B., & Wojtaszewski, J. F. P. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.06.013 · Cited by 143 · see citing works
Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance
Wredenberg, A., Freyer, C., Sandström, M. E., Katz, A., Wibom, R., Westerblad, H., & Larsson, N.-G. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.09.029 · Cited by 141 · see citing works
AMPK: A cellular metabolic and redox sensor. A minireview
Shirwany, N. A. (2014) · Frontiers in bioscience · doi:10.2741/4218 · Cited by 142 · see citing works
McConell, G. K., Lee, R. S., Chen, Z., Stepto, N. K., Huynh, N., Stephens, T. J., Canny, B. J., & Kemp, B. E. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.089839 · Cited by 138 · see citing works
The strange case of AMPK and cancer: Dr Jekyll or Mr Hyde?
Vara‐Ciruelos, D., Russell, F. M., & Hardie, D. G. (2019) · Open Biology · doi:10.1098/rsob.190099 · Cited by 136 · see citing works
Self-citationMarino, A., Hausenloy, D. J., Andreadou, I., Horman, S., Bertrand, L., & Beauloye, C. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.02.047 · Cited by 134 · see citing works
Iseli, T. J., Walter, M., van Denderen, B. J. W., Katsis, F., Witters, L. A., Kemp, B. E., Michell, B. J., & Stapleton, D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412993200 · Cited by 134 · see citing works
Janeĉek, Ŝ., Svensson, B., & MacGregor, E. A. (2011) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2011.07.002 · Cited by 134 · see citing works
AMP-activated protein kinase phosphorylates and inactivates liver glycogen synthase
Bultot, L., Guigas, B., Von Wilamowitz-Moellendorff, A., Maisin, L., Vertommen, D., Hussain, N., Beullens, M., Guinovart, J. J., Foretz, M., Viollet, B., et al. (2012) · Biochemical Journal · doi:10.1042/bj20112026 · Cited by 131 · see citing works
Role of AMP-activated protein kinase in healthy and diseased hearts
Dolinsky, V. W., & Dyck, J. R. B. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00329.2006 · Cited by 130 · see citing works
- Authors
- Hudson, E. R., Pan, D. A., James, J., Lucocq, J. M., Hawley, S. A., Green, K. A., Baba, O., Terashima, T., & Hardie, D. G.
- Affiliations
- University of Dundee (GB)
- Tokyo Medical and Dental University (JP)
- Corresponding author
- Hardie, D.Grahame
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2003-05
- Volume
- 13
- Issue
- 10
- Pages
- 861-866
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2154405414
- Cited by
- 332
- References
- 28
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 6 · 2023: 4 · 2022: 10 · 2021: 11 · 2020: 8 · 2019: 10 · 2018: 13 · 2017: 10 · 2016: 12 · 2015: 17 · 2014: 16 · 2013: 16 · 2012: 20
- FWCI
- 7.75
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 3730 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion)
- Funders
- Tenovus
- European Commission
- Wellcome Trust (QLG1-CT-2001-01488)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Rheumatology › Glycogen Storage Diseases and Myoclonus
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Keywords
- AMPK, glycogen synthase, protein inclusions, energy homeostasis, kinase overexpression
- MeSH terms
- Arrhythmias, Cardiac, Inclusion Bodies, Glycogen, Glycogen Synthase, Humans, Multienzyme Complexes, Precipitin Tests, Recombinant Fusion Proteins, Protein Serine-Threonine Kinases, Sequence Deletion, Protein Structure, Tertiary, Protein Subunits, Cell Line, Tumor, AMP-Activated Protein Kinases
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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