AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress
Open accessAbstract
AMP-activated protein kinase (AMPK) is a stress-activated protein kinase that is regulated by hypoxia and other cellular stresses that result in diminished cellular ATP levels. Here, we investigated whether AMPK signaling in endothelial cells has a role in regulating angiogenesis. Hypoxia induced the activating phosphorylation of AMPK in human umbilical vein endothelial cells (HUVECs), and AMPK activation was required for the maintenance of pro-angiogenic Akt signaling under these conditions. Suppression of AMPK signaling inhibited both HUVEC migration to VEGF and in vitro differentiation into tube-like structures in hypoxic, but not normoxic cultures. Dominant-negative AMPK also inhibited in vivo angiogenesis in Matrigel plugs that were implanted subcutaneously in mice. These data identify AMPK signaling as a new regulator of angiogenesis that is specifically required for endothelial cell migration and differentiation under conditions of hypoxia. As such, endothelial AMPK signaling may be a critical determinant of blood vessel recruitment to tissues that are subjected to ischemic stress.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
AMPK lies upstream of the phosphatidylinositol-3-kinase-protein kinase B pathway, which also leads to eNOS activation and NO production.
“Further evidence also shows that AMPK lies upstream of the phosphatidylinositol-3-kinase-protein kinase B pathway, which also leads to eNOS activation and NO production [162,164,165].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [165]
AMPK is essential for ischemic angiogenesis.
“AMPK has been proven to be essential for ischemic angiogenesis; however, the mechanism by which AMPK promotes angiogenesis is poorly elucidated [165].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [165]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Mechanisms of angiogenesis and arteriogenesis
Carmeliet, P. (2000) · Nature Medicine · doi:10.1038/74651 · Cited by 4,146 · see citing works
Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation
Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R., & Zeiher, A. M. (1999) · Nature · doi:10.1038/21224 · Cited by 3,591 · see citing works
Mechanism of activation of protein kinase B by insulin and IGF‐1.
Alessi, D. R., Andjelković, M., Caudwell, B., Cron, P. D., MORRICE, N. A., Cohen, P., & Hemmings, B. A. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb01045.x · Cited by 2,985 · see citing works
Regulation of endothelium-derived nitric oxide production by the protein kinase Akt
Fulton, D. J., Gratton, J., McCabe, T. J. D., Fontana, J. T., Fujio, Y., Walsh, K., Franke, T. F., Papapetropoulos, A., & Sessa, W. C. (1999) · Nature · doi:10.1038/21218 · Cited by 2,612 · see citing works
Gerber, H. P., McMurtrey, A. E., Kowalski, J., Yan, M., Keyt, B. A., Dixit, V. M., & Ferrara, N. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.46.30336 · Cited by 1,976 · see citing works
Kureishi, Y., Luo, Z., Shiojima, I., Bialik, A., Fulton, D. J., Lefer, D. J., Sessa, W. C., & Walsh, K. X. (2000) · Nature Medicine · doi:10.1038/79510 · Cited by 1,438 · see citing works
Hawley, S. A., Davison, M., Woods, A., Davies, S. P., Beri, R. K., Carling, D., & Hardie, D. G. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.44.27879 · Cited by 1,264 · see citing works
Nitric oxide synthase modulates angiogenesis in response to tissue ischemia.
Murohara, T., Asahara, T., Silver, M., Bauters, C., Masuda, H., Kalka, C., Kearney, M., Chen, D., Symes, J. F., Fishman, M. C., et al. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1560 · Cited by 1,201 · see citing works
Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, C., Buerk, D. G., Huang, P. L., & Jain, R. K. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.041359198 · Cited by 1,020 · see citing works
Role of Akt Signaling in Vascular Homeostasis and Angiogenesis
Shiojima, I., & Walsh, K. (2002) · Circulation Research · doi:10.1161/01.res.0000022200.71892.9f · Cited by 1,011 · see citing works
Oosthuyse, B., Moons, L., Storkebaum, E., Beck, H., Nuyens, D., Brusselmans, K., Dorpe, J. V., Hellings, P., Gorselink, M., Heymans, S., et al. (2001) · Nature Genetics · doi:10.1038/88842 · Cited by 1,007 · see citing works
Clinical applications of angiogenic growth factors and their inhibitors
Ferrara, N., & Alitalo, K. (1999) · Nature Medicine · doi:10.1038/70928 · Cited by 1,004 · see citing works
Mu, J., Brozinick, J. T., Valladares, O., Bucan, M., & Birnbaum, M. J. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00251-9 · Cited by 924 · see citing works
HIF-1 and human disease: one highly involved factor
Semenza, G. L. (2000) · Genes & Development · doi:10.1101/gad.14.16.1983 · Cited by 909 · see citing works
AMP‐activated protein kinase phosphorylation of endothelial NO synthase
Chen, Z.-P., Mitchelhill, K. I., Michell, B. J., Stapleton, D., Rodríguez‐Crespo, I., Witters, L. A., Power, D. A., de Montellano, P. R. O., & Kemp, B. E. (1999) · FEBS Letters · doi:10.1016/s0014-5793(98)01705-0 · Cited by 835 · see citing works
Hayashi, T., Hirshman, M. F., Kurth, E. J., Winder, W. W., & Goodyear, L. J. (1998) · Diabetes · doi:10.2337/diab.47.8.1369 · Cited by 774 · see citing works
Fleming, I., Fisslthaler, B., Dimmeler, S., Kemp, B. E., & Busse, R. (2001) · Circulation Research · doi:10.1161/hh1101.092677 · Cited by 770 · see citing works
Kudo, N., Barr, A., Barr, R. L., Desai, S. S., & Lopaschuk, G. D. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.29.17513 · Cited by 565 · see citing works
Michell, B. J., Chen, Z., Tiganis, T., Stapleton, D., Katsis, F., Power, D. A., Sim, A. T. R., & Kemp, B. E. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100122200 · Cited by 560 · see citing works
Fujio, Y., & Walsh, K. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.23.16349 · Cited by 552 · see citing works
Jiang, B., Zheng, J. Z., Aoki, M., & Vogt, P. K. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.040560897 · Cited by 524 · see citing works
Akt/Protein Kinase B Is Regulated by Autophosphorylation at the Hypothetical PDK-2 Site
Toker, A., & Newton, A. C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.12.8271 · Cited by 522 · see citing works
Purification and characterization of the AMP‐activated protein kinase
Carling, D., Clarke, P. R., Zammit, V. A., & Hardie, D. G. (1989) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1989.tb15186.x · Cited by 418 · see citing works
Morales‐Ruiz, M., Fulton, D. J., Sowa, G., Languino, L. R., Fujio, Y., Walsh, K., & Sessa, W. C. (2000) · Circulation Research · doi:10.1161/01.res.86.8.892 · Cited by 418 · see citing works
Muoio, D. M., Seefeld, K. J., Witters, L. A., & Coleman, R. (1999) · Biochemical Journal · doi:10.1042/bj3380783 · Cited by 409 · see citing works
Park, H., Kaushik, V. K., Constant, S., Prentki, M., Przybytkowski, E., Ruderman, N. B., & Saha, A. K. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m201692200 · Cited by 384 · see citing works
Dimmeler, S., Dernbach, E., & Zeiher, A. M. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01657-4 · Cited by 363 · see citing works
Mitchelhill, K. I., Stapleton, D., Gao, G., House, C. M., Michell, B. J., Katsis, F., Witters, L. A., & Kemp, B. E. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)41951-x · Cited by 338 · see citing works
Hyperglycemia-Induced Apoptosis in Human Umbilical Vein Endothelial Cells
Ido, Y., Carling, D., & Ruderman, N. B. (2002) · Diabetes · doi:10.2337/diabetes.51.1.159 · Cited by 323 · see citing works
Clarke, P. R., & Hardie, D. G. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07420.x · Cited by 322 · see citing works
Tian, R., Musi, N., D’Agostino, J., Hirshman, M. F., & Goodyear, L. J. (2001) · Circulation · doi:10.1161/hc4001.097183 · Cited by 308 · see citing works
Carling, D., & Grahame Hardie, D. (1989) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(89)90014-1 · Cited by 296 · see citing works
DAVIES, S. P., SIM, A. T. R., & HARDIE, D. G. (1990) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1990.tb15293.x · Cited by 274 · see citing works
Carling, D., Aguan, K., Woods, A., Verhoeven, A., Beri, R. K., Brennan, C. H., Sidebottom, C., Davison, M. D., & Scott, J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)78143-5 · Cited by 253 · see citing works
Kudo, N., Gillespie, J. G., Kung, L., Witters, L. A., Schulz, R., Clanachan, A. S., & Lopaschuk, G. D. (1996) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(96)00013-6 · Cited by 246 · see citing works
MOORE, F., WEEKES, J., & HARDIE, D. G. (1991) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1991.tb16172.x · Cited by 223 · see citing works
Radisavljevic, Z., Avraham, H. K., & Avraham, S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002448200 · Cited by 221 · see citing works
Cell Cycle Withdrawal Promotes Myogenic Induction of Akt, a Positive Modulator of Myocyte Survival
Fujio, Y., Guo, K. Y., Mano, T., Mitsuuchi, Y., Testa, J. R., & Walsh, K. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.7.5073 · Cited by 213 · see citing works
Luo, Z., Fujio, Y., Kureishi, Y., Rudic, R. D., Daumerie, G., Fulton, D. J., Sessa, W. C., & Walsh, K. (2000) · Journal of Clinical Investigation · doi:10.1172/jci9419 · Cited by 212 · see citing works
Dagher, Z., Ruderman, N. B., Tornheim, K., & Ido, Y. (2001) · Circulation Research · doi:10.1161/hh1201.092998 · Cited by 209 · see citing works
Zou, M., Hou, X., Shi, C., Nagata, D., Walsh, K., & Cohen, R. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204512200 · Cited by 189 · see citing works
Podokinesis in endothelial cell migration: role of nitric oxide
Noiri, E., Lee, E., Testa, J. E., Quigley, J. P., Colflesh, D. E., Keese, C. R., Giæver, I., & Goligorsky, M. S. (1998) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1998.274.1.c236 · Cited by 181 · see citing works
Shizukuda, Y., Tang, S., Yokota, R., & Ware, J. A. (1999) · Circulation Research · doi:10.1161/01.res.85.3.247 · Cited by 174 · see citing works
Myogenic Akt Signaling Regulates Blood Vessel Recruitment during Myofiber Growth
Takahashi, A., Kureishi, Y., Jiang, Y., Luo, Z., Guo, K. Y., Mukhopadhyay, D., Ivashchenko, Y., Branellec, D., & Walsh, K. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.13.4803-4814.2002 · Cited by 159 · see citing works
Mühlhauser, J., Merrill, M. J., Пили, Р., Maeda, H., Bacic, M., Bewig, B., Passaniti, A., Edwards, N. A., Crystal, R. G., & Capogrossi, M. C. (1995) · Circulation Research · doi:10.1161/01.res.77.6.1077 · Cited by 154 · see citing works
Signaling Angiogenesis via p42/p44 MAP Kinase Cascade
Pagès, G., Milanini, J., Richard, D. E., Berra, E., Gothié, E., Viñals, F., & Pouysségur, J. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06313.x · Cited by 135 · see citing works
Expression of the AMP‐activated protein kinase β1 and β2 subunits in skeletal muscle
Chen, Z., Heierhorst, J., Mann, R. J., Mitchelhill, K. I., Michell, B. J., Witters, L. A., Lynch, G. S., Kemp, B. E., & Stapleton, D. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01371-x · Cited by 134 · see citing works
Angiogenesis in Embryos and Ischemic Diseases
Breier, G., Damert, A., Plate, K. H., & Risau, W. (1997) · Thrombosis and Haemostasis · doi:10.1055/s-0038-1657611 · Cited by 130 · see citing works
Regulation of Angiogenesis by Glycogen Synthase Kinase-3β
Kim, H.-S., Skurk, C., Thomas, S. R., Bialik, A., Suhara, T., Kureishi, Y., Birnbaum, M. J., Keaney, J. F., & Walsh, K. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206657200 · Cited by 123 · see citing works
Involvement of Endothelial Nitric Oxide in Sphingosine-1-Phosphate–Induced Angiogenesis
Rikitake, Y., Hirata, K., Kawashima, S., Ozaki, M., Takahashi, T., Ogawa, W., Inoue, N., & Yokoyama, M. (2002) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/hq0102.101843 · Cited by 122 · see citing works
Velasco, G., Geelen, M. J. H., & Guzmán, M. (1997) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1996.9784 · Cited by 115 · see citing works
Decorin-mediated Signal Transduction in Endothelial Cells
Schönherr, E., Levkau, B., Schaefer, L., Kresse, H., & Walsh, K. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105426200 · Cited by 110 · see citing works
Dagher, Z., Ruderman, N. B., Tornheim, K., & Ido, Y. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1635 · Cited by 95 · see citing works
Hypoxia-induced adrenomedullin production in the kidney
Nagata, D., Hirata, Y., Suzuki, E., Kakoki, M., Hayakawa, H., Goto, A., Ishimitsu, T., Minamino, N., Ono, Y., Kangawa, K., et al. (1999) · Kidney International · doi:10.1046/j.1523-1755.1999.00361.x · Cited by 87 · see citing works
WEEKES, J., Hawley, S. A., Corton, J. M., Shugar, D., & Hardie, D. G. (1994) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1994.tb18554.x · Cited by 84 · see citing works
Regulation of smooth muscle cell migration and integrin expression by the Gax transcription factor
Witzenbichler, B., Kureishi, Y., Luo, Z., Roux, A. L., Branellec, D., & Walsh, K. (1999) · Journal of Clinical Investigation · doi:10.1172/jci7251 · Cited by 80 · see citing works
Verbeek, M. M., Nostrand, W. E. V., Otte‐Höller, I., Wesseling, P., & de Waal, R. M. W. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06368.x · Cited by 55 · see citing works
Nagata, D., Suzuki, E., Nishimatsu, H., Yoshizumi, M., Mano, T., Walsh, K. X., Sata, M., Kakoki, M., Goto, A., Omata, M., et al. (2000) · Circulation Research · doi:10.1161/01.res.87.8.699 · Cited by 32 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, C. O., Buerk, D. G., Huang, P. L., and Jain, R. K. (2001) Proc. Natl. Acad. Sci. U. S. A. 98, 2604 -2609
- Jiang, B. H., Zheng, J. Z., Aoki, M., and Vogt, P. K. (2000) Proc. Natl. Acad. Sci.
Cited by
Sorted by citations
AMP-Activated Protein Kinase in Metabolic Control and Insulin Signaling
Towler, M. C., & Hardie, D. G. (2007) · Circulation Research · doi:10.1161/01.res.0000256090.42690.05 · Cited by 1,248 · see citing works
Shibata, R., Sato, K., Pimentel, D. R., Takemura, Y., Kihara, S., Ohashi, K., Funahashi, T., Ouchi, N., & Walsh, K. (2005) · Nature Medicine · doi:10.1038/nm1295 · Cited by 982 · see citing works
Self-citationUngvari, Z., Tarantini, S., Donato, A. J., Galvan, V., & Csiszar, A. (2018) · Circulation Research · doi:10.1161/circresaha.118.311378 · Cited by 919 · see citing works
Ouchi, N., Kobayashi, H., Kihara, S., Kumada, M., Sato, K., Inoue, T., Funahashi, T., & Walsh, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310389200 · Cited by 759 · see citing works
Mechanisms of Dysfunction in the Aging Vasculature and Role in Age-Related Disease
Donato, A. J., Machin, D. R., & Lesniewski, L. A. (2018) · Circulation Research · doi:10.1161/circresaha.118.312563 · Cited by 699 · see citing works
Adiponectin-mediated modulation of hypertrophic signals in the heart
Shibata, R., Ouchi, N., Ito, M., Kihara, S., Shiojima, I., Pimentel, D. R., Kumada, M., Sato, K., Schiekofer, S., Ohashi, K., et al. (2004) · Nature Medicine · doi:10.1038/nm1137 · Cited by 671 · see citing works
Self-citationSelective Suppression of Endothelial Cell Apoptosis by the High Molecular Weight Form of Adiponectin
Kobayashi, H., Ouchi, N., Kihara, S., Walsh, K., Kumada, M., Abe, Y., Funahashi, T., & Matsuzawa, Y. (2004) · Circulation Research · doi:10.1161/01.res.0000119921.86460.37 · Cited by 658 · see citing works
Curcumin Inhibits Adipogenesis in 3T3-L1 Adipocytes and Angiogenesis and Obesity in C57/BL Mice
Ejaz, A., Wu, D., Kwan, P., & Meydani, M. (2009) · Journal of Nutrition · doi:10.3945/jn.108.100966 · Cited by 585 · see citing works
Cellular and molecular biology of aging endothelial cells
Donato, A. J., Morgan, R. G., Walker, A. E., & Lesniewski, L. A. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.01.021 · Cited by 538 · see citing works
Davis, B. J., Xie, Z., Viollet, B., & Zou, M. (2006) · Diabetes · doi:10.2337/diabetes.55.02.06.db05-1064 · Cited by 467 · see citing works
Zang, M., Zuccollo, A., Hou, X., Nagata, D., Walsh, K. X., Herscovitz, H., Brecher, P. I., Ruderman, N. B., & Cohen, R. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408149200 · Cited by 450 · see citing works
Laderoute, K. R., Amin, K., Calaoagan, J. M., Knapp, M., Le, T., Orduna, J. M., Foretz, M., & Viollet, B. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00166-06 · Cited by 443 · see citing works
Akt Activity Negatively Regulates Phosphorylation of AMP-activated Protein Kinase in the Heart
Kovacic, S., Soltys, C.-L. M., Barr, A., Shiojima, I., Walsh, K., & Dyck, J. R. B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305371200 · Cited by 407 · see citing works
AMPK inhibition in health and disease
Viollet, B., Horman, S., Leclerc, J., Lantier, L., Foretz, M., Billaud, M., Giri, S., & Andreelli, F. (2010) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2010.488215 · Cited by 383 · see citing works
The Link Between Angiogenesis and Endothelial Metabolism
Potente, M., & Carmeliet, P. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105134 · Cited by 353 · see citing works
Horman, S., Vertommen, D., Heath, R. B., Neumann, D., Mouton, V., Woods, A., Schlattner, U., Wallimann, T., Carling, D., Hue, L., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m506850200 · Cited by 345 · see citing works
Shibata, R., Ouchi, N., Kihara, S., Sato, K., Funahashi, T., & Walsh, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402558200 · Cited by 336 · see citing works
Self-citationEmerling, B. M., Weinberg, F., Snyder, C., Burgess, Z., Mutlu, G. M., Viollet, B., Budinger, G. R. S., & Chandel, N. S. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.02.019 · Cited by 330 · see citing works
Adiponectin actions in the cardiovascular system
Hopkins, T. A., Ouchi, N., Shibata, R., & Walsh, K. X. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.10.009 · Cited by 326 · see citing works
Fleming, I., Fißlthaler, B., Dixit, M., & Busse, R. (2005) · Journal of Cell Science · doi:10.1242/jcs.02541 · Cited by 328 · see citing works
Rattan, R., Graham, R. P., Maguire, J. L., Giri, S., & Shridhar, V. (2011) · Neoplasia · doi:10.1593/neo.11148 · Cited by 316 · see citing works
Activation and Signaling by the AMP-Activated Protein Kinase in Endothelial Cells
Fisslthaler, B., & Fleming, I. (2009) · Circulation Research · doi:10.1161/circresaha.109.201590 · Cited by 295 · see citing works
AMPK, Mitochondrial Function, and Cardiovascular Disease
Wu, S., & Zou, M.-H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144987 · Cited by 286 · see citing works
Storozhuk, Y., Hopmans, S., Sanli, T., Barron, C. C., Tsiani, E., Cutz, J.-C., Pond, G. R., Wright, J. R., Singh, G., & Tsakiridis, T. K. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.187 · Cited by 272 · see citing works
Adenovirus-mediated chronic “hyper-resistinemia” leads to in vivo insulin resistance in normal rats
Satoh, H., Nguyen, M. T., Miles, P. D. G., Imamura, T., Usui, I., & Olefsky, J. M. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20785 · Cited by 266 · see citing works
Ong, K. W., Hsu, A., & Tan, B. K. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032718 · Cited by 270 · see citing works
Tanaka, T., Kojima, I., Ohse, T., Ingelfinger, J. R., Adler, S., Fujita, T., & Nangaku, M. (2005) · Laboratory Investigation · doi:10.1038/labinvest.3700328 · Cited by 238 · see citing works
Ouchi, N., Shibata, R., & Walsh, K. (2005) · Circulation Research · doi:10.1161/01.res.0000163633.10240.3b · Cited by 238 · see citing works
Li, X., Song, J., Zhang, L., LeMaire, S. A., Hou, X., Zhang, C., Coselli, J. S., Chen, L., Wang, X. L., Zhang, Y., et al. (2009) · Diabetes · doi:10.2337/db08-1512 · Cited by 237 · see citing works
Park, G.-H., Zhang, Y., Georgescu, S. P., Johnson, K. L., Kong, D., & Galper, J. (2006) · Stem Cell Reviews and Reports · doi:10.1007/s12015-006-0015-x · Cited by 223 · see citing works
Stahmann, N., Woods, A., Carling, D., & Heller, R. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00383-06 · Cited by 214 · see citing works
Zhang, Y., Lee, T.-S., Kolb, E. M., Sun, K., Lu, X., Sladek, F. M., Kassab, G. S., Garland, T., & Shyy, J. Y.-J. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000221230.08596.98 · Cited by 212 · see citing works
Adipokine resistin promotes in vitro angiogenesis of human endothelial cells
Mu, H. H., OHASHI, R., YAN, S., Chai, H., Yang, H., LIN, P., YAO, Q., & CHEN, C. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.01.015 · Cited by 209 · see citing works
CD146 is a coreceptor for VEGFR-2 in tumor angiogenesis
Jiang, T.-X., Zhuang, J., Duan, H., Luo, Y., Zeng, Q., Fan, K., Yan, H., Lü, D., Ye, Z., Hao, J., et al. (2012) · Blood · doi:10.1182/blood-2012-01-406108 · Cited by 209 · see citing works
Agonist-modulated Regulation of AMP-activated Protein Kinase (AMPK) in Endothelial Cells
Levine, Y. C., Li, G. K., & Michel, T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702182200 · Cited by 207 · see citing works
Nagata, D., Takeda, R., Sata, M., Satonaka, H., Suzuki, E., Nagano, T., & Hirata, Y. (2004) · Circulation · doi:10.1161/01.cir.0000136025.96811.76 · Cited by 198 · see citing works
Gray, D., Jubb, A. M., Hogue, D. A., Dowd, P., Kljavin, N. M., Yi, S., Bai, W., Frantz, G. D., Zhang, Z., Koeppen, H., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4531 · Cited by 190 · see citing works
Yu, J., Deng, Y., Han, X., Ren, G., Cai, J., & Jiang, G. (2016) · Cardiovascular Diabetology · doi:10.1186/s12933-016-0408-3 · Cited by 188 · see citing works
Salt, I. P., & Hardie, D. G. (2017) · Circulation Research · doi:10.1161/circresaha.117.309633 · Cited by 186 · see citing works
AMPK, metabolism, and vascular function
Rodríguez, C., Muñoz, M., Contreras, C., & Prieto, D. (2021) · FEBS Journal · doi:10.1111/febs.15863 · Cited by 178 · see citing works
Phoenix, K. N., Vumbaca, F., & Claffey, K. P. (2008) · Breast Cancer Research and Treatment · doi:10.1007/s10549-008-9916-5 · Cited by 173 · see citing works
Activation of AMPK stimulates heme oxygenase-1 gene expression and human endothelial cell survival
Liu, X., Peyton, K. J., Shebib, A. R., Wang, H., Korthuis, R. J., & Durante, W. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00749.2010 · Cited by 171 · see citing works
Effects of AMP-Activated Protein Kinase in Cerebral Ischemia
Li, J., & McCullough, L. D. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.255 · Cited by 163 · see citing works
AICAr, a Widely Used AMPK Activator with Important AMPK-Independent Effects: A Systematic Review
Višnjić, D., Lalić, H., Dembitz, V., Tomić, B., & Smoljo, T. (2021) · Cells · doi:10.3390/cells10051095 · Cited by 164 · see citing works
Skurk, C., Maatz, H., Rocnik, E. F., Bialik, A., Force, T. L., & Walsh, K. (2005) · Circulation Research · doi:10.1161/01.res.0000156273.30274.f7 · 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
AMP kinase acts as a negative regulator of RANKL in the differentiation of osteoclasts
Lee, Y., Kim, Y.-S., Lee, S.-Y., Kim, G.-H., Kim, B., Lee, S., Lee, K., Kim, G.-S., Kim, S., & Koh, J. (2010) · Bone · doi:10.1016/j.bone.2010.08.001 · Cited by 152 · see citing works
Paradoxic effects of metformin on endothelial cells and angiogenesis
Dallaglio, K., Bruno, A., Cantelmo, A. R., Esposito, A. I., Ruggiero, L., Orecchioni, S., Calleri, A., Bertolini, F., Pfeffer, U., Noonan, D. M., et al. (2014) · Carcinogenesis · doi:10.1093/carcin/bgu001 · Cited by 146 · see citing works
Frigo, D. E., Howe, M. K., Wittmann, B. M., Brunner, A. M., Cushman, I., Wang, Q., Brown, M. A., Means, A. R., & McDonnell, D. P. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-2581 · Cited by 140 · 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
The Warburg Effect in Endothelial Cells and its Potential as an Anti-angiogenic Target in Cancer
Fitzgerald, G., Soro-Arnáiz, I., & Bock, K. D. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00100 · Cited by 135 · see citing works
Marino, 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
Chronic metformin treatment improves post‐stroke angiogenesis and recovery after experimental stroke
Venna, V. R., Li, J., Hammond, M. D., Mancini, N. S., & McCullough, L. D. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12556 · Cited by 134 · see citing works
Dasgupta, B., & Milbrandt, J. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.01.005 · Cited by 133 · see citing works
Young, A., Wu, W., Sun, W., Larman, H. B., Wang, N., Li, Y.-S. J., Shyy, J. Y., Chien, S., & García‐Cardeña, G. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.193540 · Cited by 132 · see citing works
An essential role for SRC-activated STAT-3 in 14,15-EET–induced VEGF expression and angiogenesis
Cheranov, S. Y., Karpurapu, M., Wang, D., Zhang, B., Venema, R. C., & Rao, G. N. (2008) · Blood · doi:10.1182/blood-2007-11-126680 · Cited by 127 · see citing works
Mishra, R., Cool, B. L., Laderoute, K. R., Foretz, M., Viollet, B., & Simonson, M. S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800902200 · Cited by 128 · see citing works
PGC-1α mediates exercise-induced skeletal muscle VEGF expression in mice
Leick, L., Hellsten, Y., Fentz, J., Lyngby, S. S., Wojtaszewski, J. F. P., Hidalgo, J., & Pilegaard, H. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00076.2009 · Cited by 124 · see citing works
AMPK in cardiovascular health and disease
Shirwany, N. A., & Zou, M. (2010) · Acta Pharmacologica Sinica · doi:10.1038/aps.2010.139 · Cited by 121 · see citing works
Activation of AMP kinase α1 subunit induces aortic vasorelaxation in mice
Goirand, F., Solar, M., Athea, Y., Viollet, B., Mateo, P., Fortin, D., Leclerc, J., Hoerter, J., Ventura‐Clapier, R., & Garnier, A. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.132589 · Cited by 121 · see citing works
ESFAHANIAN, N., SHAKIBA, Y., NIKBIN, B., SORAYA, H., MALEKI-DIZAJI, N., GHAZI-KHANSARI, M., & GARJANI, A. (2012) · Molecular Medicine Reports · doi:10.3892/mmr.2012.753 · Cited by 120 · see citing works
Modulation of endothelium function by fatty acids
Mallick, R., & Duttaroy, A. K. (2021) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-021-04260-9 · Cited by 122 · see citing works
Regulation of NAD(P)H oxidases by AMPK in cardiovascular systems
Song, P., & Zou, M. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.01.025 · Cited by 119 · see citing works
Oxygen and glucose deprivation induces widespread alterations in mRNA translation within 20 minutes
Andreev, D. E., O’Connor, P. B. F., Zhdanov, A. V., Dmitriev, R. I., Shatsky, I. N., Papkovsky, D. B., & Baranov, P. V. (2015) · Genome biology · doi:10.1186/s13059-015-0651-z · Cited by 111 · see citing works
AMP‐ACTIVATED PROTEIN KINASE ACTIVATION AS A STRATEGY FOR PROTECTING VASCULAR ENDOTHELIAL FUNCTION
Zou, M., & Wu, Y. (2007) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2007.04851.x · Cited by 115 · see citing works
Epoxyeicosatrienoic acids are part of the VEGF-activated signaling cascade leading to angiogenesis
Webler, A. C., Michaelis, U. R., Popp, R., Barbosa‐Sicard, E., Murugan, A., Falck, J. R., Fißlthaler, B., & Fleming, I. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00230.2008 · Cited by 114 · see citing works
AMPK-Dependent Metabolic Regulation by PPAR Agonists
Lee, W. H., & Kim, S. G. (2010) · PPAR Research · doi:10.1155/2010/549101 · Cited by 114 · see citing works
Schulz, E., Anter, E., Zou, M., & Keaney, J. F. (2005) · Circulation · doi:10.1161/circulationaha.105.546812 · Cited by 114 · see citing works
Luo, B., Soesanto, Y., & McClain, D. A. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.107.159533 · Cited by 112 · see citing works
Omura, J., Satoh, K., Kikuchi, N., Satoh, T., Kurosawa, R., Nogi, M., Otsuki, T., Kozu, K., Numano, K., Suzuki, K., et al. (2016) · Circulation Research · doi:10.1161/circresaha.115.308178 · Cited by 111 · see citing works
Ewart, M., & Kennedy, S. (2010) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2010.11.002 · Cited by 110 · see citing works
Lee, S., Youn, S., Cho, H., Li, L., Kim, T.-Y., Yook, H.-S., Chung, J.-W., Hur, J., Yoon, C., Park, K. W., et al. (2006) · Circulation · doi:10.1161/circulationaha.105.595918 · Cited by 108 · see citing works
Altered Metabolism and Persistent Starvation Behaviors Caused by Reduced AMPK Function in Drosophila
Johnson, E. C., Kazgan, N., Bretz, C. A., Forsberg, L. J., Hector, C. E., Worthen, R. J., Onyenwoke, R. U., & Brenman, J. E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012799 · Cited by 105 · see citing works
Skeletal Muscle Capillarity during Hypoxia: VEGF and Its Activation
Breen, E. C., Tang, K., Olfert, M., Knapp, A. E., & Wagner, P. D. (2008) · High Altitude Medicine & Biology · doi:10.1089/ham.2008.1010 · Cited by 103 · see citing works
Abaci, H. E., Truitt, R., Luong, E., Drazer, G., & Gerecht, S. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00484.2009 · Cited by 101 · see citing works
Xing, S.-S., Yang, X.-Y., Zheng, T., Li, W.-J., Wu, D., Chi, J.-Y., Bian, F., Bai, X.-L., Wu, G.-J., Zhang, Y.-Z., et al. (2015) · Vascular Pharmacology · doi:10.1016/j.vph.2015.07.004 · Cited by 99 · see citing works
Xie, Z., Dong, Y., Zhang, J., Scholz, R., Neumann, D., & Zou, M. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01417-08 · Cited by 98 · see citing works
Stahmann, N., Woods, A., Spengler, K., Heslegrave, A., Bauer, R., Krause, S., Viollet, B., Carling, D., & Heller, R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.108688 · Cited by 98 · see citing works
Ushio‐Fukai, M., Ash, D., Nagarkoti, S., de Chantemèle, E. J. B., Fulton, D. J., & Fukai, T. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2020.8161 · Cited by 96 · see citing works
Cardiovascular and metabolic effects of Berberine
Affuso, F. (2010) · World Journal of Cardiology · doi:10.4330/wjc.v2.i4.71 · Cited by 94 · see citing works
The prokineticin receptor‐1 (GPR73) promotes cardiomyocyte survival and angiogenesis
Urayama, K., Guilini, C., Messaddeq, N., Hu, K., Steenman, M., Kurose, H., Ert, G., & Nebigil, C. G. (2007) · The FASEB Journal · doi:10.1096/fj.07-8116com · Cited by 94 · see citing works
Anti-Angiogenic Properties of Ginsenoside Rg3
Nakhjavani, M., Smith, E., Townsend, A. R., Price, T. J., & Hardingham, J. E. (2020) · Molecules · doi:10.3390/molecules25214905 · Cited by 93 · see citing works
AMP-activated protein kinase mediates VEGF-stimulated endothelial NO production
Reihill, J. A., Ewart, M., Hardie, D. G., & Salt, I. P. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.01.110 · Cited by 91 · see citing works
AMP-activated Protein Kinase in the Control of Cardiac Metabolism and Remodeling
Horman, S., Beauloye, C., Vanoverschelde, J., & Bertrand, L. (2012) · Current Heart Failure Reports · doi:10.1007/s11897-012-0102-z · Cited by 90 · see citing works
Patel, S., Leal, A. D., & Gorski, D. H. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3431 · Cited by 93 · see citing works
Liu, H., Yu, S., Zhang, H., & Xu, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046720 · Cited by 93 · see citing works
RetractedEvidence of cancer‐promoting roles for AMPK and related kinases
Monteverde, T., Muthalagu, N., Port, J., & Murphy, D. J. (2015) · FEBS Journal · doi:10.1111/febs.13534 · Cited by 88 · see citing works
Metabolic activation of AMP kinase in vascular smooth muscle
Rubin, L. J., Magliola, L., Feng, X., JONES, A. W., & Hale, C. C. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00075.2004 · Cited by 88 · see citing works
Son, J. S., Liu, X., Tian, Q., Zhao, L., Chen, Y., Hu, Y., Chae, S. A., de Avila, J. M., Zhu, M. J., & Du, . (2019) · The Journal of Physiology · doi:10.1113/jp277698 · Cited by 86 · see citing works
García‐Prieto, C. F., Hernández-Nuño, F., Rio, D. D., Ruiz‐Hurtado, G., Aránguez, I., Ruiz‐Gayo, M., Somoza, B., & Fernández‐Alfonso, M. S. (2014) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400539 · Cited by 86 · see citing works
Muscle-derived follistatin-like 1 functions to reduce neointimal formation after vascular injury
Miyabe, M., Ohashi, K., Shibata, R., Uemura, Y., Ogura, Y., Yuasa, D., Kambara, T., Kataoka, Y., Yamamoto, T., Matsuo, K., et al. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu105 · Cited by 86 · see citing works
Ohashi, K., Ouchi, N., Sato, K., Higuchi, A., Ishikawa, T., Herschman, H. R., Kihara, S., & Walsh, K. X. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00126-09 · Cited by 83 · see citing works
Han, B., Zhang, H., Tian, R., Liu, H., Wang, Z., Wang, Z., Tian, J., Cui, Y., Ren, S., Zuo, X., et al. (2022) · Theranostics · doi:10.7150/thno.72404 · Cited by 84 · see citing works
Lopez‐Lopez, C., Dietrich, M. O., Metzger, F., Loetscher, H., & Torres‐Alemán, I. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4345-06.2007 · Cited by 83 · see citing works
AMP-activated protein kinase conducts the ischemic stress response orchestra
Young, L. H. (2008) · Circulation · doi:10.1161/circulationaha.107.713115 · Cited by 82 · see citing works
Kaneko, K., Yagui, K., Tanaka, A., Yoshihara, K., Ishikawa, K., Takahashi, K., Bujo, H., Sakurai, K., & Saitō, Y. (2008) · Microvascular Research · doi:10.1016/j.mvr.2007.12.003 · Cited by 82 · see citing works
Martinelli, R., Gegg, M. E., Longbottom, R. E., Adamson, P., Turowski, P., & Greenwood, J. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-06-0636 · Cited by 82 · see citing works
Giannantonio, M. D., Frydas, S., Kempuraj, D., Karagouni, E., Hatzistilianou, M. N., Conti, C. M., Boucher, W. S., Papadopoulou, N., Donelan, J., Cao, J., et al. (2005) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463200501800101 · Cited by 82 · see citing works
Kimura, T., Tomura, H., Sato, K., Ito, M., Matsuoka, I., Im, D., Kuwabara, A., Mogi, C., Itoh, H., Kurose, H., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.043869 · Cited by 81 · see citing works
The role of AMP-activated protein kinase in the cardiovascular system
Nagata, D., & Hirata, Y. (2009) · Hypertension Research · doi:10.1038/hr.2009.187 · Cited by 81 · see citing works
- Authors
- Nagata, D., Mogi, M., & Walsh, K.
- Affiliations
- Boston University (US)
- Corresponding author
- Walsh, Kenneth
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2003-08
- Volume
- 278
- Issue
- 33
- Pages
- 31000-31006
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2070475419
- Cited by
- 331
- References
- 58
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 7 · 2023: 6 · 2022: 9 · 2021: 14 · 2020: 18 · 2019: 12 · 2018: 14 · 2017: 11 · 2016: 8 · 2015: 20 · 2014: 24 · 2013: 14 · 2012: 22
- FWCI
- 5.53
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Japan Heart Foundation
- National Institutes of Health (AG17241, AR40197, AG15052)
- National Institute on Aging (AG17241, AG15052, R01AG017241)
- National Heart, Lung, and Blood Institute (HL-66957, P01HL066957)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR-40197, R01AR040197)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- AMPK, AMPK signaling, angiogenesis, hypoxia, endothelial cells, human umbilical vein endothelial cells, Akt signaling, endothelial cell migration, tube formation, vascular endothelial growth factor, ischemia
- MeSH terms
- Hypoxia, Biocompatible Materials, Capillaries, Cell Movement, Cells, Cultured, Collagen, Drug Combinations, Endothelium, Vascular, Humans, Laminin, Multienzyme Complexes, Proteoglycans, Proto-Oncogene Proteins, Stress, Physiological, Umbilical Veins, Signal Transduction, Protein Serine-Threonine Kinases, Neovascularization, Physiologic, Proto-Oncogene Proteins c-akt, AMP-Activated Protein Kinases
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review