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Adiponectin Stimulates Angiogenesis in Response to Tissue Ischemia through Stimulation of AMP-activated Protein Kinase Signaling
Open accessAbstract
Obesity is a risk factor for the development of cardiovascular diseases that are associated with impaired angiogenesis. Adiponectin is an adipocyte-specific adipocytokine with anti-atherogenic and anti-diabetic properties, and its plasma levels are reduced in association with obesity-linked diseases. Here, we investigated whether adiponectin regulates angiogenesis in response to tissue ischemia using adiponectin knock-out (KO) mice. Angiogenic repair of ischemic hind limbs was impaired in adiponectin-KO mice compared with wild-type (WT) mice as evaluated by laser Doppler flow method and capillary density analyses. Adenovirus-mediated supplement of adiponectin accelerated angiogenic repair in both adiponectin-KO and WT mice. Intramuscular injection of an adenovirus encoding dominant-negative AMP-activated kinase diminished the improvement in limb perfusion seen in WT mice and abolished the adiponectin-induced enhancement of perfusion. These data indicate that adiponectin can function to stimulate angiogenesis in response to ischemic stress by promoting AMP-activated kinase signaling. Therefore, adiponectin may be useful in the treatment for obesity-related vascular deficiency diseases.
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“In addition to authentic angiogenic factors, AT secretes several important adipokines and endogenous angiogenesis inhibitors to modulate the balance of new blood vessel formation, including adiponectin (36,37), leptin (34), resistin (38), visfatin/thrombospondin 1 (39), and plasminogen activator inhibitor (40).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [37]
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“…receptor (Sasaki et al., 2002), endothelial-derived nitric oxide synthase (eNOS; Murohara et al., 1998), matrix metalloproteinase-9 (Johnson et al., 2004), caveolin-1 (Sonveaux et al., 2004), adiponectin (Shibata et al., 2004), PlGF (Carmeliet et al., 2001), and IL-10 (Silvestre et al., 2000).”
Wang, Y., Gao, E., Tao, L., Lau, W. B., Yuan, Y., Goldstein, B. J., Lopez, B. L., Christopher, T. A., Tian, R., Koch, W. J., et al. (2009) · Circulation · doi:10.1161/circulationaha.108.815043 · Cited by 136
Adiponectin and adipocyte fatty acid binding protein in the pathogenesis of cardiovascular disease
Xu, A., & Vanhoutte, P. M. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00765.2011 · Cited by 130
“Adiponectin-null mice are more susceptible to pressure overload-induced cardiac hypertrophy and ischemia/reperfusion injury-induced myocardial infarction compared with wild-type mice (89, 90, 99).”
Ohashi, K., Ouchi, N., & Matsuzawa, Y. (2011) · American Journal of Hypertension · doi:10.1038/ajh.2010.216 · Cited by 127
Self-citationDifferential Effects of Leptin and Adiponectin in Endothelial Angiogenesis
Adya, R., Tan, B. K., & Randeva, H. S. (2015) · Journal of Diabetes Research · doi:10.1155/2015/648239 · Cited by 130
“This is contributed by vascular cells and inflamed hypertrophied adipocytes as a result of endoplasmic reticulum (ER) stress”
BackgroundResultde la Torre, N. G., Rubio, M. Á., Bordiú, E., Cabrerizo, L., Aparicio, E., Hernández, C., Sánchez-Pernaute, A., Díez-Valladares, L. I., Torres, A. J., Puente, M., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1370 · Cited by 126
“Some studies showed that adiponectin can stimulate new blood vessel formation in ischemic tissue (15), and stimulate the differentiation of humanendothelialcellsintocapillarylikestructuresinvitroand blood vessel growth in vivo in a rabbit corneal assay ( 16 ).”
BackgroundPGC-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 126
Wang, Y., Zhang, X., Shao, J., Liu, H., Liu, X., & Luo, E. (2017) · Scientific Reports · doi:10.1038/s41598-017-03899-z · Cited by 125
Kondo, M., Shibata, R., Miura, R., Shimano, M., Kondo, K., Li, P., Ohashi, T., Kihara, S., Maeda, N., Walsh, K., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805301200 · Cited by 124
Self-citationAdiponectin in Cardiovascular Inflammation and Obesity
Aprahamian, T. R., & Sam, F. (2011) · International Journal of Inflammation · doi:10.4061/2011/376909 · Cited by 124
“Furthermore, adiponectindeficient mice have a poor angiogenic response to ischemic hind-limb surgery; however, the systemic administration of adiponectin restores the angiogenic response to that seen in wild-type controls [20].”
BackgroundMethodSchiekofer, S., Galasso, G., Sato, K., Kraus, B. J., & Walsh, K. X. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000171994.89106.ca · Cited by 120
Self-citationAMP-activated protein kinase promotes the differentiation of endothelial progenitor cells
Li, X., Han, Y., Pang, W., Li, C., Xie, X., Shyy, J. Y.-J., & Zhu, Y. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.172452 · Cited by 113
Shimano, M., Ouchi, N., Shibata, R., Ohashi, K., Pimentel, D. R., Murohara, T., & Walsh, K. X. (2010) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2010.02.021 · Cited by 111
“We have previously reported that adiponectin promotes ischemia-induced revascularization in skeletal muscle which is partly dependent on its ability to activate AMPK signaling [26,27,37].”
BackgroundSelf-citationDuda, M. K., O’Shea, K. M., & Stanley, W. C. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp169 · Cited by 105
AMP-Activated Protein Kinase and Metabolic Control
Viollet, B., & Andréelli, F. (2011) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-17214-4_13 · Cited by 113
Adiponectin: a biomarker of obesity-induced insulin resistance in adipose tissue and beyond
Lu, J., Huang, K., Chang, L., Huang, Y.-S., Chi, Y., Su, T.-C., Chen, C., & Yang, W. (2008) · Journal of Biomedical Science · doi:10.1007/s11373-008-9261-z · Cited by 104
“This function was found to be impaired in the adiponectin KO mice compared with the WT [46].”
ResultHadjadj, S., Aubert, R., Fumeron, F., Péan, F., Tichet, J., Roussel, R., Marre, M., & groups, S. A. D. S. (2005) · Diabetologia · doi:10.1007/s00125-005-1747-x · Cited by 102
“Interestingly, adiponectin can stimulate angiogenesis both in vitro and in vivo [26, 27].”
BackgroundRoy, S., Khanna, S., Rink, C. L., Biswas, S., & Sen, C. K. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.00045.2008 · Cited by 102
“Adiponectin stimulates angiogenesis in response to ischemic stress, as known to occur in wounds, by promoting AMP-activated kinase signaling (72).”
BackgroundAprahamian, T. R., Bonegio, R. G. B., Richez, C., Yasuda, K., Chiang, L.-K., Sato, K., Walsh, K. X., & Rifkin, I. R. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.1.340 · Cited by 101
Self-citationPrinciples and Therapeutic Implications of Angiogenesis, Vasculogenesis and Arteriogenesis
Fischer, C., Schneider, M., & Carmeliet, P. (2006) · Springer eBooks · doi:10.1007/3-540-36028-x_6 · Cited by 105
Human Adipose Tissue Extract Induces Angiogenesis and Adipogenesis In Vitro
Sarkanen, J., Kaila, V., Mannerström, B., Räty, S., Kuokkanen, H., Miettinen, S., & Ylikomi, T. J. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0712 · Cited by 96
“30,51 Adiponectin, a major adipogenic hormone reported to have a dual role as an inhibitor 52 and stimulator 53,54 of angiogenesis, as well as leptin, one of the major adipogenic and angiogenic hormone, is secreted by mature adipocytes.”
Plasma adiponectin concentrations in non-pregnant, normal and overweight pregnant women
Nien, J. K., Mazaki‐Tovi, S., Romero, R. J., Erez, O., Kusanovic, J. P., Gotsch, F., Pineles, B. L., Gómez, R., Edwin, S. S., Mazor, M., et al. (2007) · Journal of Perinatal Medicine · doi:10.1515/jpm.2007.123 · Cited by 93
The role of adipokines in cardiovascular disease
Shibata, R., Ouchi, N., Ohashi, K., & Murohara, T. (2017) · Journal of Cardiology · doi:10.1016/j.jjcc.2017.02.006 · Cited by 97
Self-citationShibata, R., Sato, K., Kumada, M., Izumiya, Y., Sonoda, M., Kihara, S., Ouchi, N., & Walsh, K. X. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2007.02.010 · Cited by 93
“The adenoviral vectors expressing β-galactosidase (Ad-βgal) or murine adiponectin (Ad-APN) have been described previously [21].”
BackgroundResultSelf-citationMultifaceted roles of Adiponectin in cancer
Hebbard, L., & Ranscht, B. (2013) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2013.11.005 · Cited by 94
Tamura, T., Furukawa, Y., Taniguchi, R., Sato, Y., Ono, K., Horiuchi, H., Nakagawa, Y., Kita, T., & Kimura, T. (2007) · Circulation Journal · doi:10.1253/circj.71.623 · Cited by 91
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Self-citationCritical function of Bmx/Etk in ischemia-mediated arteriogenesis and angiogenesis
He, Y. (2006) · Journal of Clinical Investigation · doi:10.1172/jci28123 · Cited by 88
Adiponectin promotes endothelial progenitor cell number and function
Shibata, R., Skurk, C., Ouchi, N., Galasso, G., Kondo, K., Ohashi, T., Shimano, M., Kihara, S., Murohara, T., & Walsh, K. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.04.006 · Cited by 87
“The entire left femoral artery and vein were excised surgically in this model [9].”
BackgroundMethodSelf-citationAdiponectin Ameliorates Doxorubicin-induced Cardiotoxicity through Akt Protein-dependent Mechanism
Maruyama, S., Shibata, R., Ohashi, K., Ohashi, T., Daida, H., Walsh, K. X., Murohara, T., & Ouchi, N. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.245985 · Cited by 85
Self-citationDescription of a local cardiac adiponectin system and its deregulation in dilated cardiomyopathy
Skurk, C., Wittchen, F., Suckau, L., Witt, H., Noutsias, M., Fechner, H., Schultheiss, H.-P., & Poller, W. C. (2008) · European Heart Journal · doi:10.1093/eurheartj/ehn136 · Cited by 86
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
“Hind limb blood flow was measured using a laser Doppler blood flow (LDBF) analyzer (Moor LDI; Moor Instruments) (40, 46).”
BackgroundInfluentialSelf-citation
Metadata
- Authors
- Shibata, R., Ouchi, N., Kihara, S., Sato, K., Funahashi, T., & Walsh, K.
- Affiliations
- Boston University (US)
- The University of Osaka (JP)
- Corresponding author
- Walsh, Kenneth
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2004-07
- Volume
- 279
- Issue
- 27
- Pages
- 28670-28674
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W1990840335
- Cited by
- 336
- References
- 35
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 10 · 2023: 10 · 2022: 7 · 2021: 7 · 2020: 13 · 2019: 7 · 2018: 6 · 2017: 16 · 2016: 5 · 2015: 13 · 2014: 21 · 2013: 19 · 2012: 23
- FWCI
- 13.89
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (HD23681, AG15052)
- U.S. Public Health Service (HE 23641)
- National Institute on Aging (AG17241, AG15052, R01AG017241)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR-40197, R01AR040197)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Keywords
- adiponectin, angiogenesis, tissue ischemia, AMPK, AMPK signaling, hindlimb ischemia, limb perfusion, adiponectin knockout mice, adenoviral gene transfer, obesity, adipokines
- MeSH terms
- Adenoviridae, Animals, Antibodies, Monoclonal, Capillaries, Genes, Dominant, Ischemia, Mice, Inbred C57BL, Multienzyme Complexes, Neovascularization, Pathologic, Obesity, Proteins, Time Factors, Blotting, Western, Signal Transduction, Protein Serine-Threonine Kinases, Adipocytes, Gene Transfer Techniques, Mice, Knockout, Platelet Endothelial Cell Adhesion Molecule-1, Intercellular Signaling Peptides and Proteins, Mice, Adiponectin, AMP-Activated Protein Kinases
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