Cited by 332Angiogenesis and VEGF in CancerMetabolism, Diabetes, and CancerCancer, Hypoxia, and Metabolism

The DOI matches its Crossref record; 58 of the 58 references it cites were found in a registry or an index.

AMP-activated Protein Kinase (AMPK) Signaling in Endothelial Cells Is Essential for Angiogenesis in Response to Hypoxic Stress

Open access

Nagata, Daisuke, Mogi, Masaki, Walsh, Kenneth·2003·Journal of Biological Chemistry

Open this paper in CoChat — free account Open PDF

Abstract

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

Crossref · 10.1074/jbc.m300643200

Cites

58 of 58 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Mechanisms of angiogenesis and arteriogenesis
Carmeliet, P. (2000) · Nature Medicine · doi:10.1038/74651 · Cited by 4,235
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
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 3,014
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. X., Franke, T. F., Papapetropoulos, A., & Sessa, W. C. (1999) · Nature · doi:10.1038/21218 · Cited by 2,616
Vascular Endothelial Growth Factor Regulates Endothelial Cell Survival through the Phosphatidylinositol 3′-Kinase/Akt Signal Transduction Pathway
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 2,007
The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals.
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
Characterization of the AMP-activated Protein Kinase Kinase from Rat Liver and Identification of Threonine 172 as the Major Site at Which It Phosphorylates AMP-activated Protein Kinase
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
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 1,186
Role of Akt Signaling in Vascular Homeostasis and Angiogenesis
Shiojima, I., & Walsh, K. X. (2002) · Circulation Research · doi:10.1161/01.res.0000022200.71892.9f · Cited by 1,028
Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability
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 1,027

Flagged first, then by citations

Show all 58 references

Research works printed but not linked: 5

Winder, 1996, Am. J. Physiol., 270, E299
Hutber, 1997, Am. J. Physiol., 272, E262
Hayashi, 1998, Diabetes, 47, 1369
Ruderman, 1999, Am. J. Physiol., 276, E1
Fleming, 2001, Circ. Res., 88, E68

Sorted by citations

Items 101–200 of 332

Fibroblast Growth Factor-2 Is a Downstream Mediator of Phosphatidylinositol 3-Kinase-Akt Signaling in 14,15-Epoxyeicosatrienoic Acid-induced Angiogenesis*
Zhang, B., Cao, H.-F., & Rao, G. N. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m503945200 · Cited by 79
A novel inverse relationship between metformin-triggered AMPK-SIRT1 signaling and p53 protein abundance in high glucose-exposed HepG2 cells
Nelson, L. E., Valentine, R. J., Cacicedo, J. M., Gauthier, M., Ido, Y., & Ruderman, N. B. (2012) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00296.2011 · Cited by 81
“The recombinant adenoviral vector expressing a dominant negative mutant of AMPK 2 (DN-AMPK) was constructed from AMPK 2 bearing a mutation of lysine 45 to arginine (K45R) as described previously (40, 41, 63).”
Method
Calcitonin gene-related peptide promotes angiogenesis via AMP-activated protein kinase
Zheng, S., Li, W., Xu, M., Bai, X., Zhou, Z., Han, J., Shyy, J. Y.-J., & Wang, X. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00173.2010 · Cited by 79
“AMPK has been shown to promote angiogenesis (22), especially under hypoxic and/or ischemic stresses (27).”
Background
Extracellular Nucleotides and Adenosine Independently Activate AMP-Activated Protein Kinase in Endothelial Cells
da Silva, C. G., Jarzyna, R., Specht, A., & Kaczmarek, E. (2006) · Circulation Research · doi:10.1161/01.res.0000215436.92414.1d · Cited by 78
Endothelial CD146 is required for in vitro tumor-induced angiogenesis: The role of a disulfide bond in signaling and dimerization
Zheng, C., Qiu, Y., Zeng, Q., Zhang, Y., Lü, D., Yang, D., Feng, J., & Yan, X. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.03.014 · Cited by 76
Function of the master energy regulator adenosine monophosphate‐activated protein kinase in stroke
Manwani, B., & McCullough, L. D. (2013) · Journal of Neuroscience Research · doi:10.1002/jnr.23207 · Cited by 76
“In endothelial cells, hypoxia also leads to AMPK activation (Nagata et al., 2003), but, in contrast to what is seen in neurons, AMPK activation is protective in endothelial cells (Zou and Wu, 2008).”
Background
Fluid Shear Stress and NO Decrease the Activity of the Hydroxy-Methylglutaryl Coenzyme A Reductase in Endothelial Cells via the AMP-Activated Protein Kinase and FoxO1
Fißlthaler, B., Fleming, I., Keserü, B., Walsh, K., & Busse, R. (2007) · Circulation Research · doi:10.1161/01.res.0000257747.74358.1c · Cited by 75
Ginsenoside Rb1 reduces H2O2‑induced HUVEC dysfunction by stimulating the sirtuin‑1/AMP‑activated protein kinase pathway
Zheng, Z., Wang, M., Cheng, C., Liu, D., Wu, L., Zhu, J., & Qian, X. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11096 · Cited by 73
“nagata et al (22) demonstrated that endothelial aMPK signaling plays a critical role in blood vessel recruitment to tissues responding to ischemic stress.”
Background
Acute renal ischemia rapidly activates the energy sensor AMPK but does not increase phosphorylation of eNOS-Ser1177
Mount, P. F., Hill, R., Fraser, S. A., Levidiotis, V., Katsis, F., Kemp, B. E., & Power, D. A. (2005) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00458.2004 · Cited by 74
“Since this original observation, activation of AMPK has also been associated with increased phosphorylation of eNOS-Ser(1177) in response to peroxynitrite, adiponectin, the AMP mimetic 5-aminoimidazole 4-carboxamide riboside (AICAR) and during angiogenesis in response to hypoxia (9, 34, 35, 55).”
Background
A lipidomic screen of hyperglycemia-treated HRECs links 12/15-Lipoxygenase to microvascular dysfunction during diabetic retinopathy via NADPH oxidase
Ibrahim, A. S., Elshafey, S., Sellak, H., Hussein, K. A., El‐Sherbiny, M., Abdelsaid, M. A., Rizk, N. M., Beasley, S., Tawfik, A. M., Smith, S. B., et al. (2015) · Journal of Lipid Research · doi:10.1194/jlr.m056069 · Cited by 75
Longevity Factor FOXO3: A Key Regulator in Aging-Related Vascular Diseases
Zhao, Y., & Liu, Y. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.778674 · Cited by 74
“Two more studies demonstrate that AMPK signaling in ECs is required for angiogenesis in response to hypoxic stress and differentiation of endothelial progenitor cells (57, 58).”
Background
RETRACTED: Redox Regulation of the AMP-Activated Protein Kinase
Han, Y., Wang, Q., Song, P., Zhu, Y., & Zou, M.-H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015420 · Cited by 71
“In addition to its roles in energy homeostasis, more recent studies have identified some broader protective roles for AMPK in atherosclerosis [16] and inflammation [17] as well as some beneficial angiogenic effects [18,19].”
Background
Retracted
α1AMP-Activated Protein Kinase Preserves Endothelial Function During Chronic Angiotensin II Treatment by Limiting Nox2 Upregulation
Schuhmacher, S., Foretz, M., Knorr, M., Jansen, T., Hortmann, M., Wenzel, P., Oelze, M. W., Kleschyov, A. L., Daiber, A., Keaney, J. F., et al. (2011) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.219543 · Cited by 72
Interleukin-1β induces fibroblast growth factor 2 expression and subsequently promotes endothelial progenitor cell angiogenesis in chondrocytes
Chien, S.-Y., Huang, C., Tsai, C., Wang, S., Lin, Y., & Tang, C. (2016) · Clinical Science · doi:10.1042/cs20150622 · Cited by 71
Glutathione Adducts on Sarcoplasmic/Endoplasmic Reticulum Ca2+ ATPase Cys-674 Regulate Endothelial Cell Calcium Stores and Angiogenic Function as Well as Promote Ischemic Blood Flow Recovery
Thompson, M. D., Mei, Y., Weisbrod, R. M., Silver, M., Shukla, P. C., Bolotina, V. M., Cohen, R. A., & Tong, X. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.554451 · Cited by 70
“The Matrigel assay (12, 13) takes advantage of the phenomenon that cultured endothelial cells will spontaneously form network structures when seeded on this complex solubilized extracellular matrix rich in laminin, collagen IV, and heparan sulfate proteoglycans.”
Method
Shear stress-induced activation of the AMP-activated protein kinase regulates FoxO1a and angiopoietin-2 in endothelial cells
Dixit, M., Bess, E. N., Fißlthaler, B., Härtel, F. V., Noll, T., Busse, R., & Fleming, I. (2007) · Cardiovascular Research · doi:10.1093/cvr/cvm017 · Cited by 70
Leptin-Stimulated Endothelial Nitric-Oxide Synthase via an Adenosine 5′-Monophosphate-Activated Protein Kinase/Akt Signaling Pathway Is Attenuated by Interaction with C-Reactive Protein
Procopio, M. C., Andreozzi, F., Laratta, E., Cassese, A., Bèguinot, F., Arturi, F., Hribal, M. L., Perticone, F., & Sesti, G. (2009) · Endocrinology · doi:10.1210/en.2008-0921 · Cited by 73
“The finding that the inhibitory effects of the dominant-negative AMPK on endothelial cell migration and differentiation can be reversed by cotransduction with a constitutively active Akt (30) is consistent with the idea that Akt is a downstream kinase of AMPK in the signaling pathways leading to eNOS activation.”
Background
Endothelial Cell–Specific Liver Kinase B1 Deletion Causes Endothelial Dysfunction and Hypertension in Mice In Vivo
Zhang, W., Wang, Q., Wu, Y., Moriasi, C. M., Liu, Z., Dai, X., Wang, Q., Liu, W., Yuan, Z., & Zou, M. (2014) · Circulation · doi:10.1161/circulationaha.113.004146 · Cited by 69
The AMP-Activated Protein Kinase Plays a Role in Antioxidant Defense and Regulation of Vascular Inflammation
Jansen, T., Kvandová, M., Daiber, A., Stamm, P., Frenis, K., Schulz, E., Münzel, T., & Kröller-Schön, S. (2020) · Antioxidants · doi:10.3390/antiox9060525 · Cited by 68
“A wide range of endogenous physiological stimuli has been found to activate AMPK in the vasculature, including angiotensin II [35], hypoxia [36], shear stress [37], low glucose [38] and oxidative stress [39,40].”
Background
Resveratrol reduces intracellular reactive oxygen species levels by inducing autophagy through the AMPK-mTOR pathway
Song, J., Huang, Y., Zheng, W., Yan, J. Y., Cheng, M., Zhao, R., Chen, L., Hu, C., & Jia, W. (2018) · Frontiers of Medicine · doi:10.1007/s11684-018-0655-7 · Cited by 67
Metformin inhibits inflammatory angiogenesis in a murine sponge model
Xavier, D. O., Amaral, L. S. D. B., Gomes, M. A., Rocha, M. A., Campos, P. R., Cota, B. D. C. V., Tafuri, L., Paiva, A., Silva, J. H., Andrade, S. P., et al. (2009) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2009.08.004 · Cited by 70
Protective effects of AMP‐activated protein kinase in the cardiovascular system
Xu, Q., & Si, L. (2010) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2010.01179.x · Cited by 68
“Journal compilation © 2010 Foundation for Cellular and Molecular Medicine/Blackwell Publishing Ltd under conditions of hypoxia [96].”
Background
Activation of AMPK α- and γ-isoform complexes in the intact ischemic rat heart
Li, J., Coven, D. L., Miller, E. J., Hu, X., Young, M. E., Carling, D., Sinusas, A. J., & Young, L. H. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00251.2006 · Cited by 67
“Endothelial cell AMPK activity is known to be increased during oxidative stress and hypoxia (24, 32).”
Background
Identification of SNF1/AMP Kinase-related Kinase as an NF-κB-regulated Anti-apoptotic Kinase Involved in CD95-induced Motility and Invasiveness
Legembre, P., Schickel, R., Barnhart, B. C., & Peter, M. E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404334200 · Cited by 66
AMP‐dependent protein kinase alpha 2 isoform promotes hypoxia‐induced VEGF expression in human glioblastoma
Neurath, K. M., Keough, M. P., Mikkelsen, T., & Claffey, K. P. (2006) · Glia · doi:10.1002/glia.20326 · Cited by 67
“Investigative studies aimed at determining the role for AMPK in hypoxic responses have incorporated the overexpression of dominant negative AMPKa1 or AMPKa2 isoforms, or chemical inhibitors (Hwang et al., 2004; Lee et al., 2003; Nagata et al., 2003; Yun et al., 2005).”
Background
Adenosine 5′-Monophosphate Kinase-Activated Protein Kinase (PRKA) Activators Delay Meiotic Resumption in Porcine Oocytes1
Mayes, M. A., Laforest, M. F., Guillemette, C., Gilchrist, R. B., & Richard, F. J. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.106.057828 · Cited by 71
“The concentration of AICAR commonly used for other cell types, such as skeletal muscle cells [61, 62], endothelial cells [63], and dermal fibroblasts [64], is 1 mM.”
Background
Akt/FOXO3a signaling modulates the endothelial stress response through regulation of heat shock protein 70 expression
Kim, H.-S., Skurk, C., Maatz, H., Shiojima, I., Ivashchenko, Y., Yoon, S., Park, Y., & Walsh, K. X. (2005) · The FASEB Journal · doi:10.1096/fj.04-2841fje · Cited by 63
“The Akt pathway is also activated by stress to preserve cellular viability (3, 4).”
Background
15(S)-Hydroxyeicosatetraenoic Acid Induces Angiogenesis via Activation of PI3K-Akt-mTOR-S6K1 Signaling
Zhang, B., Cao, H., & Rao, G. N. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0633 · Cited by 62
Activation of AMP-Activated Protein Kinase by 5-Aminoimidazole-4-Carboxamide-1-β- d -Ribofuranoside in the Muscle Microcirculation Increases Nitric Oxide Synthesis and Microvascular Perfusion
Bradley, E. A., Eringa, E. C., Stehouwer, C. D. A., Korstjens, I. J. M., Amerongen, G. P. V. N., Musters, R. J. P., Sipkema, P., Clark, M. G., & Rattigan, S. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.204404 · Cited by 62
AMPK activation inhibits the expression of HIF-1α induced by insulin and IGF-1
Treins, C., Murdaca, J., OBBERGHEN, E. V., & Giorgetti‐Peraldi, S. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.02.088 · Cited by 60
Inhibition of APE1/Ref-1 redox activity with APX3330 blocks retinal angiogenesis in vitro and in vivo
Jiang, A., Gao, H., Kelley, M. R., & Qiao, X. (2010) · Vision Research · doi:10.1016/j.visres.2010.10.008 · Cited by 59
eNOS activation and NO function: Differential control of steroidogenesis by nitric oxide and its adaptation with hypoxia
Ducsay, C. A., & Myers, D. A. (2011) · Journal of Endocrinology · doi:10.1530/joe-11-0034 · Cited by 58
“In addition, however, direct eNOS phosphorylation by AMPK was suggested to become appreciable under conditions of prolonged hypoxia (Nagata et al. 2003).”
Background
AMP-activated protein kinase rescues the angiogenic functions of endothelial progenitor cells via manganese superoxide dismutase induction in type 1 diabetes
Wang, X., Zhang, M., Chen, D.-D., Zhang, Y., & Chen, A. F. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00001.2011 · Cited by 59
Reduced scar maturation and contractility lead to exaggerated left ventricular dilation after myocardial infarction in mice lacking AMPKα1
Noppe, G., Dufeys, C., Buchlin, P., Marquet, N., Castanares‐Zapatero, D., Balteau, M., Hermida, N., Bouzin, C., Esfahani, H., Viollet, B., et al. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.04.018 · Cited by 59
AMP-activated protein kinase promotes epithelial-mesenchymal transition in cancer cells through Twist1 upregulation
Saxena, M. T., Balaji, S. A., Deshpande, N., Ranganathan, S., Pillai, D. M., Hindupur, S. K., & Rangarajan, A. (2018) · Journal of Cell Science · doi:10.1242/jcs.208314 · Cited by 61
“For instance, AMPK activation was shown to be important for migration of human umbilical vein endothelial cells (HUVECs) (Nagata et al., 2003) and transendothelial lymphocyte migration (Martinelli et al., 2009).”
Mitochondria and Angiogenesis
Marcu, R., Zheng, Y. Y., & Hawkins, B. J. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-55330-6_21 · Cited by 60
VEGF Triggers Transient Induction of Autophagy in Endothelial Cells via AMPKα1
Spengler, K., Kryeziu, N., Größe, S., Mosig, A. S., & Heller, R. (2020) · Cells · doi:10.3390/cells9030687 · Cited by 60
High Mobility Group Box 1 Inhibits Human Pulmonary Artery Endothelial Cell Migration via a Toll-like Receptor 4- and Interferon Response Factor 3-dependent Mechanism(s)
Bauer, E. M., Shapiro, R. A., Billiar, T. R., & Bauer, P. M. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.434142 · Cited by 58
“Similarly, HMGB1 stimulated iNOS, but not IFN or ISG20 in HUVECs (Fig.”
BackgroundInfluential
AMP-Activated Protein Kinase α2 in Neutrophils Regulates Vascular Repair via Hypoxia-Inducible Factor-1α and a Network of Proteins Affecting Metabolism and Apoptosis
Malik, R. A., Zippel, N., Frömel, T., Heidler, J., Zukunft, S., Walzog, B., Ansari, N., Pampaloni, F., Wingert, S., Rieger, M. A., et al. (2016) · Circulation Research · doi:10.1161/circresaha.116.309937 · Cited by 57
Brain cytokines and neuropsychiatric disorders
Theoharides, T. C., Weinkauf, C., & Conti, P. (2004) · Journal of Clinical Psychopharmacology · doi:10.1097/01.jcp.0000148026.86483.4f · Cited by 56
T-cadherin suppresses angiogenesis in vivo by inhibiting migration of endothelial cells
Rubina, K. A., Kalinina, N., Potekhina, A. V., Efimenko, A. Y., Semina, E. V., Poliakov, A., Wilkinson, D. G., Parfyonova, Y. V., & Va, T. (2007) · Angiogenesis · doi:10.1007/s10456-007-9072-2 · Cited by 58
“The formation of vascular-like structures by HUVECs on growth factor-reduced Matrigel (BD Biosciences) was performed as previously described [21] according to the manufacturer’s instructions.”
Method
AMP kinase activation improves angiogenesis in pulmonary artery endothelial cells with in utero pulmonary hypertension
Teng, R., Du, J., Afolayan, A. J., Eis, A., Shi, Y., & Konduri, G. G. (2012) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00200.2012 · Cited by 54
“AMPK signaling in endothelial cells is essential for angiogenesis under hypoxic stress (35), which is Address for reprint requests and other correspondence: Ru-Jeng Teng, Div.”
Background
Neuron-derived Neurotrophic Factor Functions as a Novel Modulator That Enhances Endothelial Cell Function and Revascularization Processes
Ohashi, K., Enomoto, T., Joki, Y., Shibata, R., Ogura, Y., Kataoka, Y., Shimizu, Y., Kambara, T., Uemura, Y., Yuasa, D., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.555789 · Cited by 53
“NDNF Stimulates the Phosphorylation of Akt and eNOS—Because Akt is a key regulator of endothelial cell function and survival (26, 27, 30, 31), we tested whether NDNF affects Akt signaling in endothelial cells.”
Background
Imbalanced Production of Reactive Oxygen Species and Mitochondrial Antioxidant SOD2 in Fabry Disease-Specific Human Induced Pluripotent Stem Cell-Differentiated Vascular Endothelial Cells
Tseng, W.-L., Chou, S., Chiang, H.-C., Wang, M., Chien, C., Chen, K.-H., Leu, H., Wang, C., Chang, Y.-L., Liu, Y.-Y., et al. (2017) · Cell Transplantation · doi:10.3727/096368916x694265 · Cited by 54
Caffeine Enhances Endothelial Repair by an AMPK-Dependent Mechanism
Spyridopoulos, I., Fichtlscherer, S., Popp, R., Toennes, S. W., Fißlthaler, B., Trepels, T., Zernecke, A., Liehn, E. A., Weber, C., Zeiher, A. M., et al. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.174060 · Cited by 53
Protein kinase LKB1 promotes RAB7-mediated neuropilin-1 degradation to inhibit angiogenesis
Okon, I. S., Coughlan, K. A., Zhang, C., Moriasi, C., Ding, Y., Song, P., Zhang, W., Li, G., & Zou, M.-H. (2014) · Journal of Clinical Investigation · doi:10.1172/jci75371 · Cited by 52
Association between Risk Factors for Vascular Dementia and Adiponectin
Song, J., Lee, W. T., Park, K. A., & Lee, J. E. (2014) · BioMed Research International · doi:10.1155/2014/261672 · Cited by 58
“Then, the activation of VEGF by the activated AMPK signaling promotes angiogenesis in cerebral ischemic brain [212, 213].”
Background
Metabolic Regulation of Angiogenesis in Diabetes and Aging
Sawada, N., & Arany, Z. P. (2017) · Physiology · doi:10.1152/physiol.00039.2016 · Cited by 55
“AMPK, fatty acid-binding proteins, and transporters.”
BackgroundInfluential
Bradykinin stimulates endothelial cell fatty acid oxidation by CaMKK-dependent activation of AMPK
Mount, P. F., Lane, N., Venkatesan, S., Steinberg, G. R., Fraser, S. A., Kemp, B. E., & Power, D. A. (2008) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2007.12.003 · Cited by 52
“[6] Nagata D, Mogi M, Walsh K.”
Background
Biguanides drugs: Past success stories and promising future for drug discovery
Grytsai, O., Myrgorodska, I., Rocchi, S., Ronco, C., & Benhida, R. (2021) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2021.113726 · Cited by 51
Apelin-13 stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in myocardial microvascular endothelial cells
Yang, X., Zhu, W. P., ZHANG, P., Chen, K., Zhao, L., LI, J., WEI, M., & Liu, M. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.1984 · Cited by 51
Activation of AMP-Activated Protein Kinase Inhibits the Proliferation of Human Endothelial Cells
Peyton, K. J., Liu, X., Yu, Y., Yates, B., & Durante, W. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.194712 · Cited by 54
“In contrast, our finding that AMPK activation by AICAR augments endothelial cell tube formation is in agreement with earlier studies and underscores the critical role of AMPK in promoting endothelial cell differentiation (Nagata et al., 2003; Li et al., 2008; Stahmann et al., 2010; Su et al., 2012).”
Result
Endothelial SIRT1 prevents adverse arterial remodeling by facilitating HERC2-mediated degradation of acetylated LKB1
Bai, B., Man, A. W. C., Yang, K., Guo, Y., Xu, C., Tse, H., Han, W., Bloksgaard, M., Mey, J. G. R. D., Vanhoutte, P. M., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.9687 · Cited by 51
Metformin stimulates ischemia-induced revascularization through an eNOS dependent pathway in the ischemic hindlimb mice model
Takahashi, N. K., Shibata, R., Ouchi, N., Sugimoto, M., Murohara, T., & Komori, K. (2014) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2013.09.061 · Cited by 51
TAK1 signaling is a potential therapeutic target for pathological angiogenesis
Zhu, L., Lama, S., Tu, L., Dusting, G. J., Wang, J.-H., & Liu, G. (2021) · Angiogenesis · doi:10.1007/s10456-021-09787-5 · Cited by 48
“Nagata et al. found that inhibition of AMPK signaling can inhibit endothelial cell migration and tube formation under hypoxic conditions and suppress the growth of blood vessels in mice subcutaneously implanted with Matrigel [57].”
Background
The dipeptidyl peptidase-IV inhibitor inhibits the expression of vascular adhesion molecules and inflammatory cytokines in HUVECs via Akt- and AMPK-dependent mechanisms
Hwang, H., Chung, H. S., Jung, T. W., Ryu, J. Y., Hong, H. C., Seo, J. A., Kim, S. G., Kim, N. H., Choi, K. M., Choi, D. S., et al. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.01.025 · Cited by 48
Hypoglycemic pharmacological treatment of type 2 diabetes: Targeting the endothelium
Nathanson, D., & Nyström, T. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.11.016 · Cited by 48
Prostaglandin E2 Promotes Endothelial Differentiation from Bone Marrow-Derived Cells through AMPK Activation
Zhu, Z., Fu, C., Li, X., Song, Y., Li, C., Zou, M., Guan, Y., & Zhu, Y. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023554 · Cited by 48
“We previously reported that activation of AMPK by VEGF and statins promoted the differentiation of human cord-blood–derived EPCs into mature ECs via an NO-dependent mechanism [13].”
Background
Cinobufagin suppresses colorectal cancer angiogenesis by disrupting the endothelial mammalian target of rapamycin/hypoxia‐inducible factor 1α axis
Li, X., Chen, C., Dai, Y., Huang, C., Han, Q., Jing, L., Ma, Y., Xu, Y., Liu, Y., Zhao, L., et al. (2019) · Cancer Science · doi:10.1111/cas.13988 · Cited by 48
Insulin-like growth factor binding protein-4 (IGFBP-4) is a novel anti-angiogenic and anti-tumorigenic mediator secreted by dibutyryl cyclic AMP (dB-cAMP)-differentiated glioblastoma cells
Moreno, M., Ball, M., Andrade, M. F., McDermid, A., & Stanimirovic, D. B. (2006) · Glia · doi:10.1002/glia.20345 · Cited by 48
“This method is widely used to assess angiogenic transformation of peripheral endothelial cells (Nagata et al., 2003) and has been adapted by us (Semov et al.”
Method
Potentiation of insulin-stimulated glucose transport by the AMP-activated protein kinase
Ju, J.-S., Gitcho, M. A., Casmaer, C. A., Patil, P. B., Han, D.-G., Spencer, S. A., & Fisher, J. S. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00269.2006 · Cited by 47
A role for AMPK in increased insulin action after serum starvation
Ching, J. K., Rajguru, P., Marupudi, N., Banerjee, S., & Fisher, J. S. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00514.2009 · Cited by 50
“The myc-tagged AMPK-DN adenoviral vector (constructed by Morris Birnbaum, University of Pennsylvania, Philadelphia, PA) was constructed from AMPK 2 bearing a mutation of Lys-45 to arginine (K45R), as described previously (25, 26, 41).”
Method
The role of AMP-activated protein kinase in the functional effects of vascular endothelial growth factor-A and -B in human aortic endothelial cells
Reihill, J. A., Ewart, M., & Salt, I. P. (2011) · Vascular Cell · doi:10.1186/2045-824x-3-9 · Cited by 47
“Such findings are consistent with previous observations demonstrating AMPK-mediated angiogenesis in response to both adiponectin [22] and hypoxia [15].”
Both hydrogen peroxide and transforming growth factor beta 1 contribute to endothelial Nox4 mediated angiogenesis in endothelial Nox4 transgenic mouse lines
Chen, L., Hou, X., Xiao, J. M., Kuroda, J., Ago, T., Sadoshima, J., Cohen, R. A., & Tong, X. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.10.007 · Cited by 46
NADPH oxidase 4 mediates reactive oxygen species induction of CD146 dimerization in VEGF signal transduction
Zhuang, J., Jiang, T.-X., Lü, D., Luo, Y., Zheng, C., Feng, J., Yang, D., Chen, C., & Yan, X. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.04.007 · Cited by 46
Divergent Roles for Adiponectin Receptor 1 (AdipoR1) and AdipoR2 in Mediating Revascularization and Metabolic Dysfunction in Vivo
Parker, J., Nakamura, K., Silver, M., Zuriaga, M. A., MacLauchlan, S., Aprahamian, T. R., & Walsh, K. X. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.548115 · Cited by 46
Inorganic polyphosphate induces accelerated tube formation of HUVEC endothelial cells
Müller, W. E. G., Ackermann, M., Wang, S., Neufurth, M., Muñoz‐Espí, R., Feng, Q., Schröder, H. C., & Wang, X. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2601-2 · Cited by 46
A Review of Molecular Responses of Catfish to Bacterial Diseases and Abiotic Stresses
Zhou, T., Yuan, Z., Tan, S., Jin, Y., Yang, Y., Shi, H., Wang, W., Niu, D., Gao, L., Jiang, W., et al. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01113 · Cited by 46
“Vaccines for ESC have been researched for over three decades (Saeed and Plumb, 1986; Newman, 1993; Thune et al., 1994).”
Background
eNOS activation mediated by AMPK after stimulation of endothelial cells with histamine or thrombin is dependent on LKB1
Thors, B., Halldórsson, H., & Þorgeirsson, G. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.12.001 · Cited by 45
“after treatment with AICAR [6], metformin [7], PPAR agonists [8], adiponectin [9], VEGF [10] or ICAM1 [11] and under hypoxic conditions [12].”
BackgroundMethod
p-Hydroxybenzyl alcohol-containing biodegradable nanoparticle improves functional blood flow through angiogenesis in a mouse model of hindlimb ischemia
Cho, B. R., Ryu, D. R., Lee, K.-S., Lee, D.-K., Bae, S., Kang, D. G., Ke, Q., Singh, S., Ha, K., Kwon, Y., et al. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.02.107 · Cited by 45
LKB1 in endothelial cells is required for angiogenesis and TGFβ-mediated vascular smooth muscle cell recruitment
Londesborough, A., Vaahtomeri, K., Tiainen, M., Katajisto, P., Ekman, N., Vallenius, T., & Mäkelä, T. P. (2008) · Development · doi:10.1242/dev.017038 · Cited by 44
“Of these, AMPK has been shown to regulate endothelial migration and tube formation in culture under hypoxic conditions (Nagata et al., 2003), whereas no specific role in vascular development has been reported for the other LKB1 substrate kinases.”
Background
Mechanisms of action of metformin and its regulatory effect on microRNAs related to angiogenesis
Wang, G., Lin, F., Wan, Q., Wu, J., & Luo, M. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105390 · Cited by 45
15(S)-HETE Production in Human Retinal Microvascular Endothelial Cells by Hypoxia: Novel Role for MEK1 in 15(S)-HETE–Induced Angiogenesis
Bajpai, A. K., Blaskova, E., Pakala, S. B., Zhao, T., Glasgow, W. C., Penn, J. S., Johnson, D. A., & Rao, G. N. (2007) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-0617 · Cited by 44
“Cell migration was performed using a modified Boyden chamber method, as described by Nagata et al.35 Cell culture inserts containing membranes with 10-mm diameter and 8- m pore size (Nalgene Nunc International, Rochester, NY) were placed in a 24-well tissue culture Downloaded From: http://iovs.arvojournals.org/pdfacce…”
MethodInfluential
Antiangiogenic effects of N6‐isopentenyladenosine, an endogenous isoprenoid end product, mediated by AMPK activation
Pisanti, S., Picardi, P., Ciaglia, E., Margarucci, L., Ronca, R., Giacomini, A., Malfitano, A. M., Casapullo, A., Laezza, C., Gazzerro, P., et al. (2013) · The FASEB Journal · doi:10.1096/fj.13-238238 · Cited by 42
“It is known that AMPK exerts a protective effect on endothelial cells under conditions such as metabolic, oxidative, or inflammatory stress, mainly through the activation of eNOS (38).”
Background
Overexpression of Adiponectin Improves Neurobehavioral Outcomes After Focal Cerebral Ischemia in Aged Mice
Miao, J., Shen, L., Tang, Y., Wang, Y., Tao, M., Jin, K., Zhao, Y., & Yang, G. (2013) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12198 · Cited by 42
“Ischemic stress activates AMPK signaling pathway in the HUVEC culture and in the mouse ischemic hind limb model [53,54].”
Method
Transforming Growth Factor-β–Activated Kinase 1 Regulates Angiogenesis via AMP-Activated Protein Kinase-α1 and Redox Balance in Endothelial Cells
Zippel, N., Malik, R. A., Frömel, T., Popp, R., Bess, E., Strilić, B., Wettschureck, N., Fleming, I., & Fißlthaler, B. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.113.301848 · Cited by 44
Tumor growth inhibitory effect of ADAMTS 1 is accompanied by the inhibition of tumor angiogenesis
Obika, M., Ogawa, H., Takahashi, K., Li, J., Hatipoğlu, Ö. F., Cilek, M. Z., Miyoshi, T., Inagaki, J., Ohtsuki, T., Kusachi, S., et al. (2012) · Cancer Science · doi:10.1111/j.1349-7006.2012.02381.x · Cited by 46
Endothelial nitric oxide synthase negatively regulates hydrogen peroxide-stimulated AMP-activated protein kinase in endothelial cells
Jin, B. Y., Sartoretto, J. L., Gladyshev, V. N., & Michel, T. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907409106 · Cited by 42
“AMPK is one of several kinases that stimulate eNOS phosphorylation (17, 20, 37).”
Background
Estrogen Activates AMP-Activated Protein Kinase in Human Endothelial Cells via ERβ/Ca2+/Calmodulin-Dependent Protein Kinase Kinase β Pathway
Yang, S., & Wang, J. (2015) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-015-0521-z · Cited by 41
“Lately, a connection between AMPK and eNOS activation has garnered extensive interest, and NO generation has been believed to be involved in anti-inflammatory and angiogenic effects of AMPK [18–24, 26, 29].”
BackgroundInfluential
Metformin Suppresses Pancreatic Tumor Growth With Inhibition of NFκB/STAT3 Inflammatory Signaling
Tan, X., Bhattacharyya, K. K., Dutta, S. K., Bamlet, W. R., Rabe, K. G., Wang, E., Smyrk, T. C., Oberg, A. L., Petersen, G. M., & Mukhopadhyay, D. (2015) · Pancreas · doi:10.1097/mpa.0000000000000308 · Cited by 41
“It has previously been demonstrated that AMPK activation can contribute to increased vascular endothelial growth factor (VEGF) expression(42,43) and angiogenesis.(44,45) Vascular endothelial growth factor is a well-established stimulator of vascular permeability and angiogenesis, whereas TSP-1, originally isolated fro…”
Background
LKB1 Deficiency in Tie2-Cre-expressing Cells Impairs Ischemia-induced Angiogenesis
Ohashi, K., Ouchi, N., Higuchi, A., Shaw, R. J., & Walsh, K. X. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.123794 · Cited by 43
Radio-sensitivities and angiogenic signaling pathways of irradiated normal endothelial cells derived from diverse human organs
Park, M.-T., Oh, E., Song, M. J., Lee, H., & Park, H. J. (2012) · Journal of Radiation Research · doi:10.1093/jrr/rrs011 · Cited by 40
“Furthermore, AMPK activation is reported to be involved in the angiogenic process [36].”
Background
Epicardium-derived cells organize through tight junctions to replenish cardiac muscle in salamanders
Eroglu, E., Yen, C. Y. T., Tsoi, Y. L., Witman, N., Elewa, A., Joven, A., Wang, H., Szattler, T., Umeano, C. H., Sohlmér, J., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00902-2 · Cited by 43
15(S)-Hydroxyeicosatetraenoic Acid–Induced Angiogenesis Requires STAT3-Dependent Expression of VEGF
Srivastava, K., Kundumani‐Sridharan, V., Zhang, B., Bajpai, A. K., & Rao, G. N. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3594 · Cited by 40
“Tube formation assay was done as described by Nagata et al. ( 33 ).”
Method
Impaired Expression of Uncoupling Protein 2 Causes Defective Postischemic Angiogenesis in Mice Deficient in AMP-Activated Protein Kinase α Subunits
Xu, M.-J., Song, P., Shirwany, N., Liang, B., Xing, J., Viollet, B., Wang, X., Zhu, Y., & Zou, M.-H. (2011) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.227991 · Cited by 39
Apelinergic system in endothelial cells and its role in angiogenesis in myocardial ischemia
Novakova, V., Sandhu, G. S., Dragomir‐Daescu, D., & Klabusay, M. (2015) · Vascular Pharmacology · doi:10.1016/j.vph.2015.08.005 · Cited by 39
Pravastatin accelerates ischemia-induced angiogenesis through AMP-activated protein kinase
Izumi, Y., Shiota, M., Kusakabe, H., Hikita, Y., Nakao, T., Nakamura, Y., Muro, T., Miura, K., Yoshiyama, M., & Iwao, H. (2009) · Hypertension Research · doi:10.1038/hr.2009.77 · Cited by 39
MiRNA-27b Regulates Angiogenesis by Targeting AMPK in Mouse Ischemic Stroke Model
Yuan, Y., Zhang, Z., Wang, Z., & Liu, J. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.11.041 · Cited by 37
Kinetic Mechanism of AKT/PKB Enzyme Family
Zhang, X., Zhang, S., Yamane, H. K., Wahl, R. C., Ali, A., Lofgren, J. A., & Kendall, R. L. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601384200 · Cited by 39
P2Y1 Gene Deficiency Protects from Renal Disease Progression and Capillary Rarefaction during Passive Crescentic Glomerulonephritis
Hohenstein, B., Renk, S., Lang, K., Daniel, C., Freund, M., Léon, C., Amann, K., Gachet, C., & Hugo, C. (2007) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006050439 · Cited by 39
“A recently published work also demonstrated a possible link between the activation of AMP-activated protein kinases via P2Y1 receptors (45) and hypoxic conditions that might influence the regulation of hypoxia-induced factor-1 and thereby the induction of genes such as vascular endothelial growth factor (46).”
Background
α1AMP-activated protein kinase mediates vascular protective effects of exercise
Kröller-Schön, S., Jansen, T., Hauptmann, F., Schüler, A., Heeren, T., Hausding, M., Oelze, M., Viollet, B., Keaney, J. F., Wenzel, P., et al. (2012) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.243980 · Cited by 38
“Emerging data suggest that AMPK has also distinct functions in the vasculature because it activates and phosphorylates endothelial NO synthase (eNOS),(1) protects endothelial cells against oxidative stress,(2) prevents vascular smooth muscle proliferation,(3) and mediates angiogenesis.(4) All these effects suggest a p…”
Background
Novel Tetrazole-Containing Analogues of Itraconazole as Potent Antiangiogenic Agents with Reduced Cytochrome P450 3A4 Inhibition
Li, Y., Pasunooti, K. K., Li, R.-J., Liu, W., Head, S. A., Shi, W. Q., & Liu, J. O. (2018) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.8b01252 · Cited by 43
MicroRNA-9 regulates osteoblast differentiation and angiogenesis via the AMPK signaling pathway
Qu, J., Lu, D., Guo, H., Miao, W., Wu, G., & Zhou, M. (2015) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2565-1 · Cited by 38
Mitochondrial damage-induced impairment of angiogenesis in the aging rat kidney
Satoh, M., Fujimoto, S., Horike, H., Ozeki, M., Nagasu, H., Tomita, N., Sasaki, T., & Kashihara, N. (2010) · Laboratory Investigation · doi:10.1038/labinvest.2010.175 · Cited by 37
“AMPK and p38 MAPK are stress-activated protein kinases, and their signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress”
Background
Uncoupling Protein 2 Impacts Endothelial Phenotype via p53-Mediated Control of Mitochondrial Dynamics
Shimasaki, Y., Pan, N., Messina, L. M., Li, C., Chen, K., Liu, L., Cooper, M. P., Vita, J. A., & Keaney, J. F. (2013) · Circulation Research · doi:10.1161/circresaha.113.301319 · Cited by 39
Liraglutide Inhibits Endothelial-to-Mesenchymal Transition and Attenuates Neointima Formation after Endovascular Injury in Streptozotocin-Induced Diabetic Mice
Tsai, T.-H., Lee, C.-H., Cheng, C.-I., Fang, Y.-N., Chung, S.-Y., Chen, S.-M., Lin, C.-J., Wu, C.-J., Hang, C.-L., & Chen, W.-Y. (2019) · Cells · doi:10.3390/cells8060589 · Cited by 37
“In addition, AMPK signaling is essential for angiogenesis in response to hypoxic stress [58], which contributes to re-endothelisation [55].”
Background
Hop derived flavonoid xanthohumol inhibits endothelial cell functionsviaAMPK activation
Gallo, C., Dallaglio, K., Bassani, B., Rossi, T., Rossello, A., Noonan, D. M., D’Uva, G., Bruno, A., & Albini, A. (2016) · Oncotarget · doi:10.18632/oncotarget.10990 · Cited by 39
“It is able to activate several signaling pathways in order to protect from hypoxia, shear and oxidative stress [37].”
BackgroundResult
Loss of VLDL Receptor Activates Retinal Vascular Endothelial Cells and Promotes Angiogenesis
Jiang, A., Hu, W., Meng, H., Gao, H., & Qiao, X. (2009) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.08-2447 · Cited by 37
“The formation of capillary-like structures by RVECs in growth factorreduced basement membrane matrix (Matrigel; BD Biosciences) was performed as previously described with modifications.(26) Wild-type and vldlr / RVECs at the same level of confluence were starved in BM for 24 hours before seeded at a density of 2 10(5)…”
Method
AMPK protects proximal tubular cells from stress-induced apoptosis by an ATP-independent mechanism: potential role of Akt activation
Lieberthal, W., Zhang, L., Patel, V. A., & Levine, J. S. (2011) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00034.2011 · Cited by 37
“Finally, Akt-mediated increases in angiogenesis, induced by both hypoxic stress (50) and adiponectin (52), have been shown to depend upon activation of AMPK.”
Background
Metformin inhibits ALK1-mediated angiogenesis via activation of AMPK
Ying, Y., Ueta, T., Jiang, S., Lin, H., Wang, Y., Vavvas, D. G., Wen, R., Chen, Y., & Luo, Z. (2017) · Oncotarget · doi:10.18632/oncotarget.15825 · Cited by 36

Authors: Nagata, D., Mogi, M., & Walsh, K.
Affiliations: Boston University (US)
Corresponding author: Walsh, Kenneth
ORCID: Nagata, Daisuke
Mogi, Masaki
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)
DOI: 10.1074/jbc.m300643200
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: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 6270 d)
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

AMP-activated Protein Kinase (AMPK) Signaling in Endothelial Cells Is Essential for Angiogenesis in Response to Hypoxic Stress

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks