PKD1 inhibits AMPKα2 through phosphorylation of serine 491 and impairs insulin signaling in skeletal muscle cells

Journal of Biological Chemistry

Volumn 291, Issue 11, 2016, Pages 5664-5675

  Coughlan, Kimberly A ^a   Valentine, Rudy J ^b   Sudit, Bella S ^a   Allen, Katherine ^a   Dagon, Yossi ^c   Kahn, Barbara B ^c   Ruderman, Neil B ^a   Saha, Asish K ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELLS; CYTOLOGY; ENZYME ACTIVITY; GLUCOSE; INSULIN; MUSCLE; PHOSPHORYLATION; SIGNALING;

AMP-ACTIVATED PROTEIN KINASE; CELL-FREE CONDITIONS; INSULIN RESISTANCE; INSULIN SIGNALING; PHORBOL 12 MYRISTATE 13 ACETATES; SERINE PHOSPHORYLATION; SIGNALING MOLECULES; SKELETAL MUSCLE CELLS;

CELL SIGNALING;

2 [1 (3 DIMETHYLAMINOPROPYL) 5 METHOXY 1H INDOL 3 YL] 3 (1H INDOL 3 YL)MALEIMIDE; CRT 0066101; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA1; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN KINASE D; PROTEIN KINASE D1; PROTEIN KINASE INHIBITOR; S6 KINASE; SERINE; UNCLASSIFIED DRUG; AMPK ALPHA2 SUBUNIT, MOUSE;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; GENE SILENCING; IN VITRO STUDY; INTRACELLULAR SIGNALING; MYOTUBE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE CELL; ANIMAL; CELL LINE; CYTOLOGY; METABOLISM; MOUSE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL LINE; INSULIN; MICE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTEIN KINASE C; SERINE; SIGNAL TRANSDUCTION;

EID: 84973389963     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.696849     Document Type: Article

References (29)

1. Amati, F. (2012) Revisiting the diacylglycerol-induced insulin resistance hypothesis. Obes Rev. 13, 40-50
2. IDF. (2014) International Diabetes Federation Diabetes Atlas, 6th Edn. update (Federation, I. D., ed), Brussels, Belgium
3. Kahn, B. B., Alquier, T., Carling, D., and Hardie, D. G. (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1, 15-25
4. Valentine, R. J., Coughlan, K. A., Ruderman, N. B., and Saha, A. K. (2014) Insulin inhibits AMPK activity and phosphorylates AMPK Ser through Akt in hepatocytes, myotubes and incubated rat skeletal muscle. Arch. Biochem. Biophys. 562, 62-69
5. Dagon, Y., Hur, E., Zheng, B., Wellenstein, K., Cantley, L. C., and Kahn, B. B. (2012) p70S6 kinase phosphorylates AMPK on serine 491 to mediate leptin's effect on food intake. Cell Metab. 16, 104-112
6. Hawley, S. A., Ross, F. A., Gowans, G. J., Tibarewal, P., Leslie, N. R., and Hardie, D. G. (2014) Phosphorylation by Akt within the ST loop of AMPK-alpha1 down-regulates its activation in tumour cells. Biochem. J. 459, 275-287
7. Horman, S., Vertommen, D., Heath, R., Neumann, D., Mouton, V., Woods, A., Schlattner, U., Wallimann, T., Carling, D., Hue, L., and Rider, M. H. (2006) Insulin antagonizes ischemia-induced Thr172 phosphorylation of AMP-activated protein kinase α-subunits in heart via hierarchical phosphorylation of Ser485/491. J. Biol. Chem. 281, 5335-5340
8. Coughlan, K. A., Balon, T. W., Valentine, R. J., Petrocelli, R., Schultz, V., Brandon, A., Cooney, G. J., Kraegen, E. W., Ruderman, N. B., and Saha, A. K. (2015) Nutrient excess and AMPK downregulation in incubated skeletal muscle and muscle of glucose infused rats. PloS one 10, e0127388
9. Garcia-Haro, L., Garcia-Gimeno, M. A., Neumann, D., Beullens, M., Bollen, M., and Sanz, P. (2012) Glucose-dependent regulation of AMP-activated protein kinase in MIN6 beta cells is not affected by the protein kinase A pathway. FEBS Letts. 586, 4241-4247
10. Ning, J., Xi, G., and Clemmons, D. R. (2011) Suppression of AMPK activation via S485 phosphorylation by IGF-I during hyperglycemia is mediated by AKT activation in vascular smooth muscle cells. Endocrinology 152, 3143-3154
11. Berggreen, C., Gormand, A., Omar, B., Degerman, E., and Göransson, O. (2009) Protein kinase B activity is required for the effects of insulin on lipid metabolism in adipocytes. Am. J. Physiol. Endocrinol. Metab. 296, E635-E646
12. Park, D. W., Jiang, S., Liu, Y., Siegal, G. P., Inoki, K., Abraham, E., and Zmijewski, J. W. (2014) GSK3β-dependent inhibition of AMPK potentiates activation of neutrophils and macrophages and enhances severity of acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 307, L735-L745
13. López-Cotarelo, P., Escribano-Diaz, C., González-Bethencourt, I. L., Gómez-Moreira, C., Deguiz, M. L., Torres-Bacete, J., Gómez-Cabanas, L., Fernández-Barrera, J., Delgado-Martín, C., Mellado, M., Regueiro, J. R., Miranda-Carús, M. E., and Rodríguez-Fernández, J. L. (2015) A Novel MEK-ERK-AMPK signaling axis controls chemokine receptor CCR7-dependent Survival in human mature dendritic cells. J. Biol. Chem. 290, 827-840
14. Hurley, R. L., Barré, L. K., Wood, S. D., Anderson, K. A., Kemp, B. E., Means, A. R., and Witters, L. A. (2006) Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J. Biol. Chem. 281, 36662-36672
15. Rhim, J. H., Jang, I. S., Song, K. Y., Ha, M. K., Cho, S. C., Yeo, E. J., and Park, S. C. (2008) Lysophosphatidic acid and adenylyl cyclase inhibitor increase proliferation of senescent human diploid fibroblasts by inhibiting adenosine monophosphate-activated protein kinase. Rejuvenation Res. 11, 781-792
16. Bollag, G. E., Roth, R. A., Beaudoin, J., Mochly-Rosen, D., and Koshland, D. E., Jr. (1986) Protein kinase C directly phosphorylates the insulin receptor in vitro and reduces its protein-tyrosine kinase activity. Proc. Natl. Acad. Sci. U.S.A. 83, 5822-5824
17. Avkiran, M., Rowland, A. J., Cuello, F., and Haworth, R. S. (2008) Protein kinase D in the cardiovascular system: emerging roles in health and disease. Circ. Res. 102, 157-163
18. Johannes, F. J., Prestle, J., Eis, S., Oberhagemann, P., and Pfizenmaier, K. (1994) PKCu is a novel, atypical member of the protein kinase C family. J. Biol. Chem. 269, 6140-6148
19. LaValle, C. R., George, K. M., Sharlow, E. R., Lazo, J. S., Wipf, P., and Wang, Q. J. (2010) Protein kinase D as a potential new target for cancer therapy. Biochim. Biophys. Acta 1806, 183-192
20. Bossuyt, J., Helmstadter, K., Wu, X., Clements-Jewery, H., Haworth, R. S., Avkiran, M., Martin, J. L., Pogwizd, S. M., and Bers, D. M. (2008) Ca2+/Calmodulin-dependent protein kinase IIδ and protein kinase D overexpression reinforce the histone deacetylase 5 redistribution in heart failure. Circ. Res. 102, 695-702
21. Harrison, B. C., Kim, M. S., van Rooij, E., Plato, C. F., Papst, P. J., Vega, R. B., McAnally, J. A., Richardson, J. A., Bassel-Duby, R., Olson, E. N., and McKinsey, T. A. (2006) Regulation of cardiac stress signaling by protein kinase d1. Mol. Cell. Biol. 26, 3875-3888
22. Tsuchiya, Y., Denison, F. C., Heath, R. B., Carling, D., and Saggerson, D. (2012) 5′-AMP-activated protein kinase is inactivated by adrenergic signalling in adult cardiac myocytes.Biosci. Rep. 32, 197-213
23. Park, H., Kaushik, V. K., Constant, S., Prentki, M., Przybytkowski, E., Ruderman, N. B., and Saha, A. K. (2002) Coordinate regulation of malonyl-CoA decarboxylase, sn-glycerol-3-phosphate acyltransferase, and acetyl-CoA carboxylase by AMP-activated protein kinase in rat tissues in response to exercise. J. Biol. Chem. 277, 32571-32577
24. Saha, A. K., Xu, X. J., Lawson, E., Deoliveira, R., Brandon, A. E., Kraegen, E. W., and Ruderman, N. B. (2010) Downregulation of AMPK accompanies leucine- and glucose-induced increases in protein synthesis and insulin resistance in rat skeletal muscle. Diabetes 59, 2426-2434
25. McGee, S. L., Swinton, C., Morrison, S., Gaur, V., Campbell, D. E., Jorgensen, S. B., Kemp, B. E., Baar, K., Steinberg, G. R., and Hargreaves, M. (2014) Compensatory regulation of HDAC5 in muscle maintains metabolic adaptive responses and metabolism in response to energetic stress. Faseb. J. 28, 3384-3395
26. Kim, M. S., Fielitz, J., McAnally, J., Shelton, J. M., Lemon, D. D., McKinsey, T. A., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2008)Protein kinase D1 stimulates MEF2 activity in skeletal muscle and enhances muscle performance. Mol. Cell. Biol. 28, 3600-3609
27. Ellwanger, K., Kienzle, C., Lutz, S., Jin, Z. G., Wiekowski, M. T., Pfizenmaier, K., and Hausser, A. (2011) Protein kinase D controls voluntaryrunning-induced skeletal muscle remodelling. Biochem. J. 440, 327-335
28. Richter, E. A., and Ruderman, N. B. (2009) AMPK and the biochemistry of exercise: implications for human health and disease. Biochem. J. 418, 261-275
29. O'Neill, H. M., Maarbjerg, S. J., Crane, J. D., Jeppesen, J., Jørgensen, S. B., Schertzer, J. D., Shyroka, O., Kiens, B., van Denderen, B. J., Tarnopolsky, M. A., Kemp, B. E., Richter, E. A., and Steinberg, G. R. (2011)AMP-activated protein kinase (AMPK) β1β2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proc. Natl. Acad. Sci. U.S.A. 108, 16092-16097