GLP-1 promotes angiogenesis in human endothelial cells in a dose-dependent manner, through the Akt, Src and PKC pathways
Open accessAbstract
Introduction Novel anti-diabetic medications that mimic or augment the physiological actions of GLP-1 improve cardiovascular risk factors in diabetics and GLP-1 has been proposed to have a beneficial role in the cardiovascular system. GLP-1 may have a direct cardioprotective role by decreasing infarct size and protecting from ischemia-reperfusion injury while prolonging survival in rodent models. The mechanisms underlying these observations remain largely unknown. In vitro studies suggest that GLP-1 may promote endothelial cell proliferation, but no study to date has evaluated a potential direct effect of GLP-1 on angiogenesis.Specific aim To evaluate whether GLP-1 affects angiogenesis in humans and to elucidate underlying molecular mechanisms.Material and methods We utilized a 3D culture system where spherules of human umbilical vein endothelial cells (HUVECs) embedded in a collagen scaffold were treated with escalating doses of human recombinant GLP-1 (50-2000 nmol/L) and the formation of new vessels was observed and quantified. Signaling inhibitors were utilized to identify molecular pathways through which GLP-1 promotes angiogenesis.Results We demonstrate that GLP-1 promotes angiogenesis in a dose-dependent manner. The maximum effect on angiogenesis was observed at a GLP-1 dose of 500 nmol/L, while increased angiogenesis occurred in response to doses ranging from 200 nmol/L to 1000 nmol/L. Pre-treatment of the system with Akt inhibitor IV, Bisindolylmaleimide (PKC inhibitor) and src inhibitor I resulted in a significant decrease of the GLP-1 induced angiogenesis.Conclusions This is the first study to demonstrate that GLP-1 promotes angiogenesis in a HUVEC three dimensional in vitro model. This effect requires pharmacological doses and is mediated through the Akt, PKC and src pathways.
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?
GLP-1RA-induced angiogenesis appears to be mediated through the PI3K/Akt, PKA, and Src pathways.
“GLP-1RA-induced angiogenesis appears to be mediated through the PI3K/Akt, PKA, and Src pathways [68].”
From Protection against stroke with glucagon-like peptide-1 receptor agonists: a comprehensive review of potential mechanisms (2022) · cites this paper as [68]
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
Role of angiogenesis in tumor growth and metastasis
Folkman, J. (2002) · Seminars in Oncology · doi:10.1016/s0093-7754(02)70065-1 · Cited by 2,862 · see citing works
Role of angiogenesis in tumor growth and metastasis
Folkman, J. (2002) · Seminars in Oncology · doi:10.1053/sonc.2002.37263 · Cited by 2,424 · 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
Ban, K., Noyan-Ashraf, M. H., Hoefer, J., Bolz, S.-S., Drucker, D. J., & Husain, M. (2008) · Circulation · doi:10.1161/circulationaha.107.739938 · Cited by 1,057 · 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
Nikolaidis, L. A., Mankad, S., Sokos, G. G., Miske, G., Shah, A., Elahi, D., & Shannon, R. P. (2004) · Circulation · doi:10.1161/01.cir.0000120505.91348.58 · Cited by 901 · see citing works
Selective Requirement for Src Kinases during VEGF-Induced Angiogenesis and Vascular Permeability
Eliceiri, B. P., Paul, R., Schwartzberg, P. L., Hood, J. D., Leng, J., & Cheresh, D. A. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80221-x · Cited by 814 · see citing works
Klonoff, D. C., Buse, J. B., Nielsen, L. L., Guan, X., Bowlus, C. L., Holcombe, J. H., Wintle, M. E., & Maggs, D. G. (2008) · Current Medical Research and Opinion · doi:10.1185/030079908x253870 · Cited by 699 · see citing works
Nyström, T., Gutniak, M. K., Zhang, Q., Zhang, F., Holst, J. J., Ahrén, B., & Sjöholm, Å. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00237.2004 · Cited by 680 · see citing works
Sokos, G. G., Nikolaidis, L. A., Mankad, S. V., Elahi, D., & Shannon, R. P. (2006) · Journal of Cardiac Failure · doi:10.1016/j.cardfail.2006.08.211 · Cited by 654 · see citing works
Glucagon-like peptide 1 can directly protect the heart against ischemia/reperfusion injury.
Bose, A. K., Mocanu, M., Carr, R. D., Brand, C. L., & Yellon, D. (2005) · Diabetes · doi:10.2337/diabetes.54.1.146 · Cited by 642 · see citing works
Herrmann, C., Göke, R., Richter, G., Fehmann, H.-C., Arnold, R., & Göke, B. (2009) · Digestion · doi:10.1159/000201231 · Cited by 597 · see citing works
Noyan-Ashraf, M. H., Momen, M. A., Ban, K., Sadi, A.-M., Zhou, Y.-Q., Riazi, A. M., Baggio, L. L., Henkelman, R. M., Husain, M., & Drucker, D. J. (2009) · Diabetes · doi:10.2337/db08-1193 · Cited by 575 · see citing works
Vilsbøll, T., Agersø, H., Krarup, T., & Holst, J. J. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021053 · Cited by 444 · see citing works
Understanding the biology of angiogenesis: Review of the most important molecular mechanisms
Otrock, Z. K., Mahfouz, R. A., Makarem, J. A., & Shamseddine, A. I. (2007) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2007.04.001 · Cited by 390 · see citing works
Mechanisms of Recovery From Type 2 Diabetes After Malabsorptive Bariatric Surgery
Guidone, C., Manco, M., Valera-Mora, E., Iaconelli, A., Gniuli, D., Mari, A., Nanni, G., Castagneto, M., Calvani, M., & Mingrone, G. (2006) · Diabetes · doi:10.2337/db06-0068 · Cited by 367 · see citing works
Diabetic Retinopathy and Angiogenesis
Crawford, T., Alfaro, D. V., Kerrison, J. B., & Jablon, E. P. (2009) · Current Diabetes Reviews · doi:10.2174/157339909787314149 · Cited by 351 · see citing works
New Roles for Src Kinases in Control of Cell Survival and Angiogenesis
Schlessinger, J. (2000) · Cell · doi:10.1016/s0092-8674(00)80664-9 · Cited by 302 · see citing works
Strader, A. D., Vahl, T. P., Jandacek, R. J., Woods, S. C., D’Alessio, D. A., & Seeley, R. J. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00153.2004 · Cited by 290 · see citing works
Akt Takes Center Stage in Angiogenesis Signaling
Dimmeler, S., & Zeiher, A. M. (2000) · Circulation Research · doi:10.1161/01.res.86.1.4 · Cited by 258 · see citing works
Best, J. H., Hoogwerf, B. J., Herman, W. H., Pelletier, E. M., Smith, D. B., Wenten, M., & Hussein, M. A. (2010) · Diabetes Care · doi:10.2337/dc10-1393 · Cited by 251 · see citing works
Insulinotropic actions of exendin-4 and glucagon-like peptide-1 in vivo and in vitro
Parkes, D. G., Pittner, R. A., Jodka, C. M., Smith, P., & Young, A. J. (2001) · Metabolism · doi:10.1053/meta.2001.22519 · Cited by 241 · see citing works
Hendarto, H., Inoguchi, T., Maeda, Y., Ikeda, N., Zheng, J., Takei, R., Yokomizo, H., Hirata, E., Sonoda, N., & Takayanagi, R. (2012) · Metabolism · doi:10.1016/j.metabol.2012.03.002 · Cited by 232 · see citing works
Erdogdu, Ö., Nathanson, D., Sjöholm, Å., Nyström, T., & Zhang, Q. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.04.022 · Cited by 229 · see citing works
Microvascular Modifications in Diabetic Retinopathy
Durham, J. T., & Herman, I. M. (2011) · Current Diabetes Reports · doi:10.1007/s11892-011-0204-0 · Cited by 198 · see citing works
Gastrointestinal hormones and gastric emptying 20 years after jejunoileal bypass for massive obesity
Näslund, E. B., Grybäck, P., Hellström, P. M., Jacobsson, H., Holst, J. J., Theodorsson, E., & Bäckman, L. (1997) · International Journal of Obesity · doi:10.1038/sj.ijo.0800418 · Cited by 190 · see citing works
Phillips, L. K., & Prins, J. B. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06491.x · Cited by 120 · see citing works
Role of c-Src in regulation of endothelial nitric oxide synthase expression during exercise training
Davis, M. E., Cai, H. “., McCann, L. A., Fukai, T., & Harrison, D. G. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00918.2002 · Cited by 119 · see citing works
Xu, H., Czerwinski, P., Hortmann, M., Sohn, H.-Y., Förstermann, U., & Li, H. (2007) · Cardiovascular Research · doi:10.1093/cvr/cvm085 · Cited by 109 · see citing works
Emerging role of PKA/eNOS pathway in therapeutic angiogenesis for ischaemic tissue diseases
Bir, S. C., Xiong, Y., Kevil, C. G., & Luo, J. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs143 · Cited by 107 · see citing works
Mechanisms responsible for excess weight loss after bariatric surgery
Ionut, V., & Bergman, R. N. (2011) · Journal of Diabetes Science and Technology · doi:10.1177/193229681100500536 · Cited by 105 · see citing works
Kakizawa, H., Itoh, M., Itoh, Y., Imamura, S., Ishiwata, Y., Matsumoto, T., Yamamoto, K., Kato, T., Ono, Y., Nagata, M., et al. (2004) · Metabolism · doi:10.1016/j.metabol.2003.12.002 · Cited by 94 · see citing works
Ishibashi, Y., Nishino, Y., Matsui, T., Takeuchi, M., & Yamagishi, S. (2011) · Metabolism · doi:10.1016/j.metabol.2011.01.010 · Cited by 92 · see citing works
Focal adhesion kinase inhibitors are potent anti‐angiogenic agents
Cabrita, M. A., Jones, L., Quizi, J. L., Sabourin, L. A., McKay, B. C., & Addison, C. (2011) · Molecular Oncology · doi:10.1016/j.molonc.2011.10.004 · Cited by 86 · see citing works
Marfella, R., Sasso, F. C., Rizzo, M. R., Paolisso, P., Barbieri, M., Sorrentino, V. P., Carbonara, O., Gualdiero, P., Petronella, P., Ferraraccio, F., et al. (2012) · Experimental Diabetes Research · doi:10.1155/2012/892706 · Cited by 85 · see citing works
Schisano, B., Harte, A. L., Lois, K. B., Saravanan, P., Al‐Daghri, N. M., Al-Attas, O. S., Knudsen, L. B., McTernan, P. G., Ceriello, A., & Tripathi, G. (2011) · Regulatory Peptides · doi:10.1016/j.regpep.2011.11.008 · Cited by 85 · see citing works
Huang, C., Shih, C., Tsao, N., Lin, Y., Huang, P., Wu, S., Lee, A., Kao, Y., Chang, N., Hironori Nakagami, A., et al. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.02102.x · Cited by 81 · see citing works
Forst, T., Michelson, G., Ratter, F., Weber, M. M., Anders, S., Mitry, M., Wilhelm, B., & Pfützner, A. (2012) · Diabetic Medicine · doi:10.1111/j.1464-5491.2012.03589.x · Cited by 75 · see citing works
Irace, C., Luca, S. D., Shehaj, E., Carallo, C., Loprete, A., Scavelli, F. B., & Gnasso, A. (2012) · Diabetes and Vascular Disease Research · doi:10.1177/1479164112449562 · Cited by 72 · see citing works
Terasaki, M., Nagashima, M., Watanabe, T., Nohtomi, K., Mori, Y., Miyazaki, A., & Hirano, T. (2012) · Metabolism · doi:10.1016/j.metabol.2011.11.011 · Cited by 62 · see citing works
Cuthbertson, J., Patterson, S., O'Harte, F. P. M., & Bell, P. M. (2010) · Metabolism · doi:10.1016/j.metabol.2010.01.001 · Cited by 54 · see citing works
寺﨑, 道. (2012) · Medical Entomology and Zoology · Cited by 54 · see citing works
VEGF and angiopoietins in diabetic glomerulopathy: How far for a new treatment?
Dei, A., & Gnudi, L. (2012) · Metabolism · doi:10.1016/j.metabol.2012.04.004 · Cited by 52 · see citing works
Seligman, B. G. S., Polanczyk, C. A., Santos, A. S. B., Foppa, M., Junges, M., Bonzanini, L., Nicolaidis, G., Camey, S. A., Lopes, A. L., Sehl, P. L., et al. (2011) · Metabolism · doi:10.1016/j.metabol.2011.05.006 · Cited by 52 · see citing works
Herzlinger, S., & Horton, E. S. (2013) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2012.11.009 · Cited by 41 · see citing works
Glucagon-like peptide–1 and candesartan additively improve glucolipotoxicity in pancreatic β-cells
Wang, H.-W., Mizuta, M., Saitoh, Y., Noma, K., Ueno, H., & Nakazato, M. (2011) · Metabolism · doi:10.1016/j.metabol.2010.11.004 · Cited by 39 · see citing works
pp60c-src Modulates Microvascular Endothelial Phenotype and in Vitro Angiogenesis
Marx, M., Warren, S. L., & Madri, J. A. (2001) · Experimental and Molecular Pathology · doi:10.1006/exmp.2001.2358 · Cited by 18 · see citing works
Exendin-4 regulates GLUT2 expression via the CaMKK/CaMKIV pathway in a pancreatic β-cell line
Chen, K., Yu, X., Murao, K., Imachi, H., Li, J., Muraoka, T., Masugata, H., Zhang, G.-X., Kobayashi, R., Ishida, T., et al. (2010) · Metabolism · doi:10.1016/j.metabol.2010.06.002 · Cited by 17 · see citing works
Pacini, G., Thomaseth, K., & Åhrén, B. (2010) · Metabolism · doi:10.1016/j.metabol.2009.10.021 · Cited by 16 · see citing works
Hamilton, S. J., Chew, G. T., Davis, T. M. E., & Watts, G. F. (2011) · Metabolism · doi:10.1016/j.metabol.2011.07.010 · Cited by 4 · see citing works
Flagged first, then by citations
1 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Nauck, M. A., Meier, J. J., Cavender, M. A., Abd El Aziz, M., & Drucker, D. J. (2017) · Circulation · doi:10.1161/circulationaha.117.028136 · Cited by 582 · see citing works
Nauck, M. A., Quast, D. R., Wefers, J., & Pfeiffer, A. F. H. (2021) · Diabetes, Obesity and Metabolism · doi:10.1111/dom.14496 · Cited by 388 · see citing works
Anti-diabetic actions of glucagon-like peptide-1 on pancreatic beta-cells
Lee, Y.-S., & Jun, H.-S. (2014) · Metabolism · doi:10.1016/j.metabol.2013.09.010 · Cited by 315 · see citing works
DPP4 in Cardiometabolic Disease
Zhong, J., Maiseyeu, A., Davis, S. N., & Rajagopalan, S. (2015) · Circulation Research · doi:10.1161/circresaha.116.305665 · Cited by 190 · see citing works
Host-directed therapy targeting the Mycobacterium tuberculosis granuloma: a review
Kiran, D., Podell, B. K., Chambers, M. A., & Basaraba, R. J. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-015-0537-x · Cited by 129 · see citing works
GLP-1 receptor agonists and atherosclerosis protection: the vascular endothelium takes center stage
Park, B., Bakbak, E., Teoh, H., Krishnaraj, A., Dennis, F., Quan, A., Rotstein, O. D., Butler, J., Hess, D. A., & Verma, S. (2024) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00574.2023 · Cited by 114 · see citing works
Goldney, J., Sargeant, J. A., & Davies, M. J. (2023) · Diabetologia · doi:10.1007/s00125-023-05988-3 · Cited by 100 · see citing works
Gaborit, B., Julla, J.-B., Besbes, S., Proust, M., Vincentelli, C., Alos, B., Ancel, P., Alzaid, F., Garcia, R., Mailly, P., et al. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgz069 · Cited by 95 · see citing works
Contributions of 3D Cell Cultures for Cancer Research
Ravi, M., Ramesh, A., & Pattabhi, A. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25664 · Cited by 88 · see citing works
GLP-1R as a Target for the Treatment of Diabetic Retinopathy: Friend or Foe?
Simó, R., & Hernández, C. (2017) · Diabetes · doi:10.2337/db16-1364 · Cited by 86 · see citing works
Posadino, A. M., Giordo, R., Cossu, A., Nasrallah, G. K., Shaito, A. A., Abou-Saleh, H., Eid, A. H., & Pintus, G. (2019) · Biomolecules · doi:10.3390/biom9060209 · Cited by 82 · see citing works
Vergès, B., Aboyans, V., Angoulvant, D., Boutouyrie, P., Cariou, B., Hyafil, F., Mohammedi, K., & Amarenco, P. (2022) · Cardiovascular Diabetology · doi:10.1186/s12933-022-01686-3 · Cited by 72 · see citing works
Molecular Regulation of Sprouting Angiogenesis
Duran, C. L., Howell, D. W., Dave, J. M., Smith, R. L., Torrie, M. E., Essner, J. J., & Bayless, K. J. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160048 · Cited by 76 · see citing works
Sáez, T., Salsoso, R., Leiva, A., Toledo, F., de Vos, P., Faas, M. M., & Sobrevía, L. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.11.010 · Cited by 66 · see citing works
Vascular Biology of Glucagon Receptor Superfamily Peptides: Mechanistic and Clinical Relevance
Pujadas, G., & Drucker, D. J. (2016) · Endocrine Reviews · doi:10.1210/er.2016-1078 · Cited by 63 · see citing works
Ishii, M., Shibata, R., Kondo, K., Kambara, T., Shimizu, Y., Tanigawa, T., Bando, Y., Nishimura, M., Ouchi, N., & Murohara, T. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.557835 · Cited by 61 · see citing works
Association of Perioperative Glucagon-like Peptide-1 Receptor Agonist Use and Postoperative Outcomes
Aschen, S. Z., Zhang, A., O’Connell, G. M., Salingaros, S., Andy, C., Rohde, C. H., & Spector, J. A. (2024) · Annals of Surgery · doi:10.1097/sla.0000000000006614 · Cited by 59 · see citing works
Marrano, N., Biondi, G., Borrelli, A., Cignarelli, A., Perrini, S., Laviola, L., Giorgino, F., & Natalicchio, A. (2021) · Biomolecules · doi:10.3390/biom11020286 · Cited by 56 · see citing works
Chai, W., Fu, Z., Aylor, K. W., Barrett, E. J., & Liu, Z. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00205.2016 · Cited by 51 · see citing works
Chade, A. (2017) · Hypertension · doi:10.1161/hypertensionaha.116.08319 · Cited by 46 · see citing works
He, X., Wen, S., Tang, X., Wen, Z., Zhang, R. H., Li, S., Gao, R. B., Wang, J., Zhu, Y., Fang, D., et al. (2024) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2024.03.011 · Cited by 44 · see citing works
Exendin-4 induces myocardial protection through MKK3 and Akt-1 in infarcted hearts
Du, J., Zhang, L., Wang, Z., Yano, N., Zhao, Y., Lei, W., Dubielecka, P. M., Liu, P. Y., Zhuang, S., Qin, G., et al. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00194.2015 · Cited by 43 · see citing works
Subiabre, M., Silva, L., Villalobos-Labra, R., Toledo, F., Mario Paublo, M., López, M. A., Salsoso, R., Pardo, F., Leiva, A., & Sobrevía, L. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.07.022 · Cited by 43 · see citing works
Garczorz, W., Gallego-Colón, E., Kosowska, A., Kłych‐Ratuszny, A., Woźniak, M., Marcol, W., Niesner, K. J., & Francuz, T. (2017) · Cardiovascular Therapeutics · doi:10.1111/1755-5922.12317 · Cited by 43 · see citing works
Intranasal Delivery of Exendin-4 Confers Neuroprotective Effect Against Cerebral Ischemia in Mice
Zhang, H., Meng, J., Zhou, S., Liu, Y., Qu, D., Wang, L., Li, X., Wang, N., Luo, X., & Ma, X. (2015) · The AAPS Journal · doi:10.1208/s12248-015-9854-1 · Cited by 43 · see citing works
Shao, S., Zhang, X., Xu, Q., Pan, R., & Chen, Y. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108270 · Cited by 42 · see citing works
Lei, Y., Hu, L., Yang, G., Piao, L., Jin, M., & Cheng, X. W. (2017) · Circulation Journal · doi:10.1253/circj.cj-16-1326 · Cited by 42 · see citing works
Xu, M., Liu, L., Wu, M., Jiang, M., Shou, L., Wang, W., Wu, J., Zhang, Y., Gong, F.-R., Chen, K., et al. (2018) · Oncogenesis · doi:10.1038/s41389-018-0102-2 · Cited by 42 · see citing works
Diabetic retinopathy: new therapeutic perspectives based on pathogenic mechanisms
Hernández, C., Simó-Servat, A., Bogdanov, P. M., & Simó, R. (2017) · Journal of Endocrinological Investigation · doi:10.1007/s40618-017-0648-4 · Cited by 41 · see citing works
Rodrigues, T., Borges, P. D. N., Mar, L. A., Marques, D., Albano, M. N., Eickhoff, H., Carrêlo, C., Almeida, B., Pires, S., Abrantes, A. M., et al. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105198 · Cited by 41 · see citing works
Love, K. M., Liu, J., Regensteiner, J. G., Reusch, J. E. B., & Liu, Z. (2020) · Journal of Diabetes · doi:10.1111/1753-0407.13045 · Cited by 40 · see citing works
Li, P., Chen, D., Cui, Y., Zhang, W., Weng, J., Yu, L., Chen, L., Chen, Z., Su, H., Yu, S., et al. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00765 · Cited by 40 · see citing works
Li, N., Zhao, Y., Yue, Y., Chen, L., Yao, Z., & Niu, W. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.07.095 · Cited by 38 · see citing works
GLP-1 Receptor Agonists and Myocardial Perfusion: Bridging Mechanisms to Clinical Outcomes
Karakasis, P., Patoulias, D., Theofilis, P., Pamporis, K., Sagris, Μ., Vlachakis, P. K., Koufakis, T., Antoniadis, A. P., & Fragakis, N. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26073050 · Cited by 36 · see citing works
Yoshino, Y., Ishisaka, M., Tsujii, S., Shimazawa, M., & Hara, H. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.01.098 · Cited by 34 · see citing works
Liao, P., Yang, D., Liu, D., & Zheng, Y.-H. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000485820 · Cited by 33 · see citing works
Tate, M., Chong, A., Robinson, E., Green, B. D., & Grieve, D. J. (2015) · British Journal of Pharmacology · doi:10.1111/bph.12943 · Cited by 33 · see citing works
Yin, W., Jiang, Y., Xu, S., Wang, Z., Peng, L., Fang, Q., Deng, T., Zhao, W., Zhang, W., & Lou, J. (2018) · Journal of Diabetes Investigation · doi:10.1111/jdi.12956 · Cited by 33 · see citing works
Chen, Y., Zhang, X., He, J., Xie, Y., & Yang, Y. (2018) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2017.12.015 · Cited by 32 · see citing works
Lewis, J. E., Omenge, D. K., Patterson, A., Anwaegbu, O. S., Tabukum, N. N., Lewis, J. E., & Lee, W. (2025) · Diabetes and Vascular Disease Research · doi:10.1177/14791641251322909 · Cited by 30 · see citing works
Wang, F., Zhang, X., Zhang, J., Xu, Q., Yu, X., Xu, A., Yi, C., Bian, X., & Shao, S. (2024) · Medicinal Research Reviews · doi:10.1002/med.22020 · Cited by 30 · see citing works
Taniguchi, M., Saito, K., Aida, R., Ochiai, A., Saitoh, E., & Tanaka, T. (2019) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2019.02.002 · Cited by 29 · see citing works
Liraglutide Increases VEGF Expression via CNPY2-PERK Pathway Induced by Hypoxia/Reoxygenation Injury
Chong, L., Liu, Y., He, J. N., Mu, R., Di, Y., Shen, N., Liu, X., Gao, X., Wang, J., Chen, T., et al. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00789 · Cited by 29 · see citing works
Do incretins improve endothelial function?
Oyama, J., Higashi, Y., & Node, K. (2014) · Cardiovascular Diabetology · doi:10.1186/1475-2840-13-21 · Cited by 28 · see citing works
Alhajahjeh, A. A., Al‐Faouri, R., Bahmad, H. F., Bader, T., Dobbs, R. W., Abdulelah, A., Abou-Kheir, W. G., Davicioni, E., Lee, D. I., & Shahait, M. (2024) · Cancers · doi:10.3390/cancers16081538 · Cited by 27 · see citing works
Ali, R., Khamis, T., Enan, G., El–Didamony, G., Sitohy, B., & Abdel-Fattah, G. (2022) · Molecules · doi:10.3390/molecules27072270 · Cited by 25 · see citing works
Ke, J., Wei, R., Yu, F., Zhang, J., & Hong, T. (2016) · Peptides · doi:10.1016/j.peptides.2016.10.009 · Cited by 24 · see citing works
Hepatitis C virus-mediated angiogenesis: Molecular mechanisms and therapeutic strategies
Hassan, M. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i42.15467 · Cited by 23 · see citing works
Pro-healing impact of liraglutide on skin wounds in normoglycemic mice
Han, Y., Zhang, X., Zhao, Z., Gong, S., & Shao, S. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.114050 · Cited by 19 · see citing works
Nakamura, M., Samii, A., Lang, J. M., Götz, F., Samii, M., & Krauss, J. K. (2015) · Neurosurgery · doi:10.1227/neu.0000000000001025 · Cited by 19 · see citing works
Zhang, Y., Wang, S., Zhou, Q., Hu, Y., Xie, Y., Fang, W., Yang, C., Wang, Z., Ye, S., Wang, X., et al. (2024) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.124.320714 · Cited by 19 · see citing works
Identification of a prolonged action molecular GLP-1R agonist for the treatment of femoral defects
Wang, N., Liu, X., Shi, L., Liu, Y., Guo, S., Liu, W., Li, X., Meng, J., Ma, X., & Guo, Z. (2020) · Biomaterials Science · doi:10.1039/c9bm01426h · Cited by 18 · see citing works
Taniguchi, M., Ochiai, A., Namae, T., Saito, K., Kato, T., Saitoh, E., & Tanaka, T. (2018) · Peptides · doi:10.1016/j.peptides.2018.04.017 · Cited by 18 · see citing works
Liraglutide Accelerates Ischemia‐Induced Angiogenesis in a Murine Diabetic Model
Zhu, Y., Li, Y., Ma, Y., Zhang, X., Du, X., Gao, J., Ding, N., Wang, L., Ni, C., Luo, M., et al. (2023) · Journal of the American Heart Association · doi:10.1161/jaha.122.026586 · Cited by 18 · see citing works
Incretin‐based therapy and the risk of diabetic foot ulcers and related events
Werkman, N. C. C., Driessen, J. H. M., Klungel, O. H., Schaper, N. C., Souverein, P. C., Stehouwer, C. D. A., & Nielen, J. T. H. (2024) · Diabetes Obesity and Metabolism · doi:10.1111/dom.15721 · Cited by 18 · see citing works
Exenatide mitigates inflammation and hypoxia along with improved angiogenesis in obese fat tissue
Xian, Y., Chen, Z., Deng, H., Cai, M., Liang, H., Xu, W., Weng, J., & Xu, F. L. (2019) · Journal of Endocrinology · doi:10.1530/joe-18-0639 · Cited by 17 · see citing works
Potential cardioprotective action of GLP-1: from bench to bedside
Aronis, K. N., Tsoukas, M. A., & Mantzoros, C. S. (2014) · Metabolism · doi:10.1016/j.metabol.2014.05.009 · Cited by 14 · see citing works
Self-citationGo, C. C., Annie, F., Drabish, K. S., & Eslami, M. H. (2025) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2025.05.037 · Cited by 13 · see citing works
Glucagon-like peptide-1 receptor agonists and cardiovascular protection in type 2 diabetes
BAJAJ, H. S., Aljabri, B. A., & Verma, S. (2018) · Current Opinion in Cardiology · doi:10.1097/hco.0000000000000562 · Cited by 13 · see citing works
Chen, Y., Edinburgh, R. M., Hengist, A., Smith, H., Walhin, J., Betts, J. A., Thompson, D., & Gonzalez, J. T. (2018) · Experimental Physiology · doi:10.1113/ep087118 · Cited by 11 · see citing works
Chaudagar, K. K., & Mehta, A. A. (2014) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2013-0391 · Cited by 10 · see citing works
Chaudagar, K. K., & Mehta, A. A. (2014) · Clinical and Experimental Hypertension · doi:10.3109/10641963.2014.881842 · Cited by 10 · see citing works
Nakamura, M., & Krauss, J. K. (2016) · Neurosurgery · doi:10.1227/neu.0000000000001210 · Cited by 10 · see citing works
The COL-4A1 polypeptide destroy endothelial cells through the TGF-β/PI3K/AKT pathway
Li, T., Ling, Z., Xie, K., Wang, Y., Miao, Z., Ji, X., Li, J., Hou, W., Tang, Q., Yuan, X., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-94801-5 · Cited by 9 · see citing works
Machida, A., Suzuki, K., Nakayama, T., Miyagi, S., Maekawa, Y., Murakami, R., Uematsu, M., Kitaoka, T., & Oishi, A. (2025) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.66.5.15 · Cited by 8 · see citing works
Incretin-based therapy for diabetic ulcers: from bench to bedside
Ku, H.-C., & Liang, Y. (2018) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2018.1548607 · Cited by 8 · see citing works
The role of glucagon-like peptide-1/GLP-1R and autophagy in diabetic cardiovascular disease
Guo, Z. (2024) · Pharmacological Reports · doi:10.1007/s43440-024-00609-1 · Cited by 6 · see citing works
Muralikrishnan, A. S., Biasin, V., Zabini, D., & Osto, E. (2025) · Acta Physiologica · doi:10.1111/apha.70091 · Cited by 5 · see citing works
Lee, C. C., Newland, M., Yau, A., Chroneos, R., & Johnson, T. S. (2025) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000012703 · Cited by 5 · see citing works
Li, J., Zhang, Y., Sun, X., Guan, H., Wang, J., Zhao, S., Tian, C., Han, M., Ma, K., & Li, M. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1742296 · Cited by 6 · see citing works
Obesity Alters the Vascular Morphology and VEGF‐A Signaling in Adipose Tissue
Lee, Y., Tukei, K. L., Fang, Y., Kuila, S., Liu, X., & Imoukhuede, P. I. (2025) · FASEB BioAdvances · doi:10.1096/fba.2025-00027 · Cited by 5 · see citing works
Novel glucose-lowering agents that benefit diabetic foot: icing on the cake
Li, Q., Yu, S., Rui, S., Lin, X., Yuan, Y. C., Armstrong, D. G., Xu, Y., & Deng, W. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1581403 · Cited by 5 · see citing works
Granulomatous Response to Mycobacterium tuberculosis Infection
Kolloli, A., Singh, P., & Subbian, S. (2018) · Springer eBooks · doi:10.1007/978-3-319-97367-8_3 · Cited by 5 · see citing works
Introductory Chapter: Microcirculation in Health and Disease
Lenasi, H. (2016) · InTech eBooks · doi:10.5772/64680 · Cited by 5 · see citing works
Drewa, J., Lazar-Juszczak, K., Adamowicz, J., & Juszczak, K. (2025) · Cancers · doi:10.3390/cancers17091576 · Cited by 4 · see citing works
Samanidou, V., Tsamis, K., Ceasovschih, A., Koufakis, T., Patoulias, D., Rizos, E. C., Rizzo, M., Milionis, H. J., & Barkas, F. (2026) · Journal of Central Nervous System Disease · doi:10.1177/11795735261444425 · Cited by 4 · see citing works
GLP‐1: A Prospective Guardian for Comprehensive Myocardial Perfusion
Li, Z., Yu, Y., Li, J., Jiang, X., Chen, J., Ye, N., Wu, B., Sun, Y., & Sun, G. (2024) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.70004 · Cited by 4 · see citing works
Molecular Regulation of Sprouting Angiogenesis
Duran, C. L., Howell, D. W., Dave, J. M., Smith, R. L., Torrie, M. E., Essner, J. J., & Bayless, K. J. (2018) · Comprehensive physiology · doi:10.1002/j.2040-4603.2018.tb00003.x · Cited by 4 · see citing works
Muir, K. C., Stone, C. R., Harris, D. D., Kanuparthy, M., Broadwin, M., Hamze, J., Feng, J., & Sellke, F. W. (2026) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00828.2025 · Cited by 4 · see citing works
Kim, M. T., Lee, S., Goh, G. S.-H., & Riew, K. D. (2026) · Global Spine Journal · doi:10.1177/21925682261419753 · Cited by 3 · see citing works
Vascular failure and recent anti-diabetic drugs
Oyama, J., & Node, K. (2017) · Vascular Failure · doi:10.30548/vascfail.1.1_2 · Cited by 3 · see citing works
Effects of IFN-γ on the proliferation of 32D cells expressing Akt after IRF-1 gene silencing
Lin, Y. H., Zhang, R., Jiang, S., Lü, W., Lin, Z., & Liu, H. (2021) · Translational Cancer Research · doi:10.21037/tcr-20-1866 · Cited by 2 · see citing works
Salingaros, S., Zhang, A., Rohde, C. H., & Spector, J. A. (2026) · Annals of Plastic Surgery · doi:10.1097/sap.0000000000004657 · Cited by 3 · see citing works
GLP-1 Receptor Agonist Use Is Associated with Venous Ulcer Healing and Fewer Wound Infections
Go, C. C., Annie, F., Drabish, K. S., & Eslami, M. H. (2026) · Annals of Vascular Surgery · doi:10.1016/j.avsg.2026.03.023 · Cited by 2 · see citing works
New research developments and insights from Metabolism
Farr, O. M., Camp, M., & Mantzoros, C. S. (2014) · Metabolism · doi:10.1016/j.metabol.2014.12.002 · Cited by 2 · see citing works
Self-citationShadboorestan, A., Eftekhari, S., Mottaghi-Dastjerdi, N., Shahparvari, R., Tarighi, P., Jahandar, H., Faghihi, H., & Montazeri, H. (2022) · PubMed Central · doi:10.22038/ijbms.2022.64117.14117 · Cited by 2 · see citing works
Semaglutide, a GLP-1 Agonist Like 'Ozempic' and its Potential Role as a Preventive Anti-Cancer Agent
Akl, M. M., & Ahmed, A. (2024) · Cell & Cellular Life Sciences Journal · doi:10.23880/cclsj-16000195 · Cited by 2 · see citing works
Gupta, N., Uwawah, T. D., Singh, K., Madan, H., Kumar, S., Midha, B., Soni, K., Singh, A., Bhogal, A., & Jain, A. (2024) · Cureus · doi:10.7759/cureus.64668 · Cited by 2 · see citing works
Kotb, S. M., Farid, M. M., Al-Karmalawy, A. A., Zahran, M. A. H., Mohamed, B. S., Gadallah, A.-N. A.-A., & El‐Aarag, B. (2025) · Fitoterapia · doi:10.1016/j.fitote.2025.106939 · Cited by 2 · see citing works
Hsu, J., Ho, B., Sayed, R., Patel, N. T. P., & Dardik, A. (2026) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2026.02.003 · Cited by 1 · see citing works
Lin, M.-P., Xue, B.-J., & Bai, X. (2026) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-026-10759-7 · Cited by 1 · see citing works
Mylavarapu, M., Obi, O. S., Abarca, Y. A., Fatima, H., Roshni, P., Huda, N. U., Lysak, Y., Gandapur, A., Vazquez, S. A. C., Siddiqui, M. A., et al. (2026) · World Journal of Cardiology · doi:10.4330/wjc.v18.i3.112189 · Cited by 1 · see citing works
Muir, K. C., Harris, D. D., Stone, C. R., Kanuparthy, M., Hamze, J., Feng, J., & Sellke, F. W. (2026) · Microvascular Research · doi:10.1016/j.mvr.2026.104956 · Cited by 1 · see citing works
Zeraatian, S., Aghdam, R. M., & Hossein, A. S. (2015) · Cardiovascular Pharmacology Open Access · doi:10.4172/2329-6607.1000159 · Cited by 1 · see citing works
The Skeletal Muscle Microvasculature and Its Effects on Metabolism
Kolka, C. (2016) · InTech eBooks · doi:10.5772/63535 · Cited by 5 · see citing works
Wu, J., Guo, P., He, T., & Cai, F. (2017) · Turkish Journal of Biochemistry · doi:10.1515/tjb-2017-0013
Kiaei, N., & Aghdam, R. M. (2020) · Research Square · doi:10.21203/rs.3.rs-102352/v1
Glucagon Like Peptide-1: More than Glucose Control and Weight ReductionPreprint
Chen, Y., Shao, S., Zhang, X., Xu, Q., & Pan, R. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4161722
Dao, M. Q., Kim, A. Y., Wang, S., Won, P., Laspro, M., Gillenwater, T. J., Yenikomshian, H. A., & Johnson, M. B. (2025) · Burns · doi:10.1016/j.burns.2025.107848
- Authors
- Aronis, K. N., Chamberland, J. P., & Mantzoros, C. S.
- Affiliations
- Boston University (US)
- Beth Israel Deaconess Medical Center (US)
- Corresponding author
- Aronis, Konstantinos N.
- Venue
- Metabolism
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 62
- Issue
- 9
- Pages
- 1279-1286
- ISSN
- 0026-0495 (ISSN-L)
- PMC
- PMC3755020
- OpenAlex
- W1989453119
- Cited by
- 104
- References
- 51
- Citations by year
- 2026: 13 · 2025: 13 · 2024: 11 · 2023: 2 · 2022: 5 · 2021: 4 · 2020: 4 · 2019: 5 · 2018: 10 · 2017: 13 · 2016: 9 · 2015: 6 · 2014: 8 · 2013: 1
- FWCI
- 3.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 CX000422)
- National Institute on Aging (R01AG032030, AG032030.)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK079929, DK-081913, R01DK058785, R56DK058785, DK079929, DK058785, K24DK081913)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Keywords
- glucagon-like peptide-1, angiogenesis, human umbilical vein endothelial cells, Akt signaling, Src kinase, protein kinase C, dose-dependent effects, endothelial cell proliferation, cardioprotection, diabetes mellitus
- MeSH terms
- Cells, Cultured, Humans, Protein Kinase C, Neovascularization, Physiologic, src-Family Kinases, Endothelial Cells, Proto-Oncogene Proteins c-akt, Glucagon-Like Peptide 1, Human Umbilical Vein Endothelial Cells
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