Estrogen Activates AMP-Activated Protein Kinase in Human Endothelial Cells via ERβ/Ca2+/Calmodulin-Dependent Protein Kinase Kinase β Pathway

Cell Biochemistry and Biophysics

Volumn 72, Issue 3, 2015, Pages 701-707

  Yang, Songbai ^a   Wang, Jing ^b  

^a CHINA JAPAN UNION HOSPITAL OF JILIN UNIVERSITY   (China)

^b JILIN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Acetyl coenzyme A carboxylase (ACC); AMP activated protein kinase (AMPK); Calmodulin dependent protein kinase kinase (CaMKK ); Endothelial nitric oxide synthase (eNOS); Estradiol (E2); Estrogen receptor (ER )

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; BENZIMIDAZOLE DERIVATIVE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR BETA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NAPHTHALIMIDE DERIVATIVE; PROTEIN KINASE INHIBITOR; STO 609;

ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; ENDOTHELIUM CELL; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

ACETYL-COA CARBOXYLASE; AMP-ACTIVATED PROTEIN KINASES; BENZIMIDAZOLES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 1; CELLS, CULTURED; ENDOTHELIAL CELLS; ESTRADIOL; ESTROGEN RECEPTOR BETA; ESTROGENS; HUMANS; NAPHTHALIMIDES; NITRIC OXIDE SYNTHASE TYPE III; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION;

EID: 84933679222     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-015-0521-z     Document Type: Article

References (32)

1. Carling, D. (2004). The AMP-activated protein kinase cascade–A unifying system for energy control. Trends in Biochemical Sciences,29, 18–24.
2. Hardie, D. G. (2004). AMP-activated protein kinase: A master switch in glucose and lipid metabolism. Reviews in Endocrine & Metabolic Disorders,5, 119–125.
3. Kahn, B. B., Alquier, T., Carling, D., & Hardie, D. G. (2005). AMP-activated protein kinase: Ancient energy gauge provides clues to modern understanding of metabolism. Cell Metabolism,1, 15–25.
4. Hardie, D. G., Salt, I. P., Hawley, S. A., & Davies, S. P. (1999). AMP-activated protein kinase: An ultrasensitive system for monitoring cellular energy charge. The Biochemical Journal,338(Pt 3), 717–722.
5. Hawley, S. A., Boudeau, J., Reid, J. L., Mustard, K. J., Udd, L., Makela, T. P., et al. (2003). Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. Journal of Biology,2, 28.
6. Hong, S. P., Leiper, F. C., Woods, A., Carling, D., & Carlson, M. (2003). Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proceedings of the National Academy of Sciences of the United States of America,100, 8839–8843.
7. Shaw, R. J., Kosmatka, M., Bardeesy, N., Hurley, R. L., Witters, L. A., DePinho, R. A., et al. (2004). The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proceedings of the National Academy of Sciences of the United States of America,101, 3329–3335.
8. Woods, A., Johnstone, S. R., Dickerson, K., Leiper, F. C., Fryer, L. G., Neumann, D., et al. (2003). LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Current Biology: CB,13, 2004–2008.
9. Hawley, S. A., Pan, D. A., Mustard, K. J., Ross, L., Bain, J., Edelman, A. M., et al. (2005). Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metabolism,2, 9–19.
10. Hurley, R. L., Anderson, K. A., Franzone, J. M., Kemp, B. E., Means, A. R., & Witters, L. A. (2005). The Ca2 +/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. The Journal of Biological Chemistry,280, 29060–29066.
11. Woods, A., Dickerson, K., Heath, R., Hong, S. P., Momcilovic, M., Johnstone, S. R., et al. (2005). Ca2 +/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metabolism,2, 21–33.
12. Fryer, L. G., Parbu-Patel, A., & Carling, D. (2002). The Anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. The Journal of Biological Chemistry,277, 25226–25232.
13. Mendelsohn, M. E., & Karas, R. H. (1999). The protective effects of estrogen on the cardiovascular system. The New England Journal of Medicine,340, 1801–1811.
14. Shi, Y., Feletou, M., Ku, D. D., Man, R. Y., & Vanhoutte, P. M. (2007). The calcium ionophore A23187 induces endothelium-dependent contractions in femoral arteries from rats with streptozotocin-induced diabetes. British Journal of Pharmacology,150, 624–632.
15. Przygodzki, T., Sokal, A., & Bryszewska, M. (2005). Calcium ionophore A23187 action on cardiac myocytes is accompanied by enhanced production of reactive oxygen species. Biochimica et Biophysica Acta,1740, 481–488.
16. Rubio-Gayosso, I., Sierra-Ramirez, A., Garcia-Vazquez, A., Martinez-Martinez, A., Munoz-Garcia, O., Morato, T., et al. (2000). 17Beta-estradiol increases intracellular calcium concentration through a short-term and nongenomic mechanism in rat vascular endothelium in culture. Journal of Cardiovascular Pharmacology,36, 196–202.
17. Tokumitsu, H., Inuzuka, H., Ishikawa, Y., Ikeda, M., Saji, I., & Kobayashi, R. (2002). STO-609, a specific inhibitor of the Ca(2 +)/calmodulin-dependent protein kinase kinase. The Journal of Biological Chemistry,277, 15813–15818.
18. Zou, M. H., Hou, X. Y., Shi, C. M., Kirkpatick, S., Liu, F., Goldman, M. H., et al. (2003). Activation of 5′-AMP-activated kinase is mediated through c-Src and phosphoinositide 3-kinase activity during hypoxia-reoxygenation of bovine aortic endothelial cells. Role of peroxynitrite. The Journal of Biological Chemistry,278, 34003–34010.
19. Zou, M. H., Hou, X. Y., Shi, C. M., Nagata, D., Walsh, K., & Cohen, R. A. (2002). Modulation by peroxynitrite of Akt- and AMP-activated kinase-dependent Ser1179 phosphorylation of endothelial nitric oxide synthase. The Journal of Biological Chemistry,277, 32552–32557.
20. Nagata, D., Mogi, M., & Walsh, K. (2003). AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. The Journal of Biological Chemistry,278, 31000–31006.
21. Chen, H., Montagnani, M., Funahashi, T., Shimomura, I., & Quon, M. J. (2003). Adiponectin stimulates production of nitric oxide in vascular endothelial cells. The Journal of Biological Chemistry,278, 45021–45026.
22. Ouchi, N., Kobayashi, H., Kihara, S., Kumada, M., Sato, K., Inoue, T., et al. (2004). Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. The Journal of Biological Chemistry,279, 1304–1309.
23. Zou, M. H., Kirkpatrick, S. S., Davis, B. J., Nelson, J. S., Wiles, W. G. T., Schlattner, U., et al. (2004). Activation of the AMP-activated protein kinase by the anti-diabetic drug metformin in vivo. Role of mitochondrial reactive nitrogen species. The Journal of Biological Chemistry,279, 43940–43951.
24. Schulz, E., Anter, E., Zou, M. H., & Keaney, J. F, Jr. (2005). Estradiol-mediated endothelial nitric oxide synthase association with heat shock protein 90 requires adenosine monophosphate-dependent protein kinase. Circulation,111, 3473–3480.
25. Mount, P. F., Hill, R. E., Fraser, S. A., Levidiotis, V., Katsis, F., Kemp, B. E., et al. (2005). Acute renal ischemia rapidly activates the energy sensor AMPK but does not increase phosphorylation of eNOS-Ser1177. American Journal of Physiology Renal Physiology,289, F1103–F1115.
26. Thors, B., Halldorsson, H., & Thorgeirsson, G. (2004). Thrombin and histamine stimulate endothelial nitric-oxide synthase phosphorylation at Ser1177 via an AMPK mediated pathway independent of PI3 K-Akt. FEBS Letters,573, 175–180.
27. Dagher, Z., Ruderman, N., Tornheim, K., & Ido, Y. (1999). The effect of AMP-activated protein kinase and its activator AICAR on the metabolism of human umbilical vein endothelial cells. Biochemical and Biophysical Research Communications,265, 112–115.
28. Ido, Y., Carling, D., & Ruderman, N. (2002). Hyperglycemia-induced apoptosis in human umbilical vein endothelial cells: Inhibition by the AMP-activated protein kinase activation. Diabetes,51, 159–167.
29. Morrow, V. A., Foufelle, F., Connell, J. M., Petrie, J. R., Gould, G. W., & Salt, I. P. (2003). Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. The Journal of Biological Chemistry,278, 31629–31639.
30. Chen, Z. P., Mitchelhill, K. I., Michell, B. J., Stapleton, D., Rodriguez-Crespo, I., Witters, L. A., et al. (1999). AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Letters,443, 285–289.
31. Fleming, I., & Busse, R. (2003). Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology,284, R1–R12.
32. Hardie, D. G., & Pan, D. A. (2002). Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochemical Society Transactions,30, 1064–1070.