Cited by 736Adipokines, Inflammation, and Metabolic DiseasesAngiogenesis and VEGF in CancerAdipose Tissue and Metabolism

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Angiogenesis modulates adipogenesis and obesity

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Cao, Yihai·2007·Journal of Clinical Investigation

DOI 10.1172/jci32239PMC PMC1963348

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Abstract

Substantial evidence shows that neoplastic and nonneoplastic tissue growth is dependent on angiogenesis. Neovascularization and adipogenesis are temporally and spatially coupled processes during prenatal life and they continue to reciprocally interact via paracrine signaling systems throughout adult life. Activated adipocytes produce multiple angiogenic factors including leptin, angiopoietins, HGF, GM-CSF, VEGF, FGF-2, and TGF-beta, which either alone or collectively stimulate neovascularization during fat mass expansion. Thus antiangiogenic agents provide a novel therapeutic option for prevention and treatment of human obesity and its related disorders.

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“Much less information is 440 available on the interaction of adipocytes and vessels during formation of the adipose 441 tissue (Cao, 2007).”
Background
Association between Mesenchymal Stem Cells and COVID‐19 Therapy: Systematic Review and Current Trends
Javed, A., Karki, S., Sami, Z., Khan, Z., Shree, A., Sah, B. K., Ghosh, S., & Saxena, S. (2022) · BioMed Research International · doi:10.1155/2022/9346939 · Cited by 10
“Also, it is known that the degree of tissue growth and regeneration is based on the level of formation of new blood vessels known as neoangiogenesis [79].”
Unraveling the complex roles of macrophages in obese adipose tissue: an overview
Peng, C. S., Chen, J., Wu, R., Jiang, H., & Li, J. X. (2024) · Frontiers of Medicine · doi:10.1007/s11684-023-1033-7 · Cited by 9
DHL-HisZn, a novel antioxidant, enhances adipogenic differentiation and antioxidative response in adipose-derived stem cells
Chen, C.-C., Hsu, L., Nakano, T., Huang, K., Chen, K., Lai, C.-Y., Goto, S., & Chen, C. (2016) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2016.10.066 · Cited by 10
Genetic Contributions to Childhood Obesity: Association of Candidate Gene Polymorphisms and Overweight/Obesity in Korean Preschool Children
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“Several studies have shown an increase in serum VEGF in obese patients and have proposed that adipocytes produce angiogenic factors that play central roles in allowing for the expansion of adipose tissue (11,17).”
BackgroundInfluential
Systemic inhibition of Janus kinase induces browning of white adipose tissue and ameliorates obesity-related metabolic disorders
Qurania, K. R., Ikeda, K., Wardhana, D. A., Barinda, A. J., Nugroho, D. B., Kuribayashi, Y., Rahardini, E. P., Rinastiti, P., Ryanto, G. R. T., Yagi, K., et al. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.05.131 · Cited by 10
Inhibitory effects of Porphyra dentata extract on 3T3-L1 adipocyte differentiation
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“Hence, it is also closely linked to metabolic diseases such as type 2 diabetes (T2D), liver disease, cardiovascular disease (CVD), cancers, hypertension and other disorders which increased these disease occurrence [5,6].”
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Hepatocyte RXR alpha deletion in mice leads to inhibition of angiogenesis
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“Angiogenesis, the process of the new blood vessels formation, is a combined result of tissue growth and tissue remodeling, which also includes adipose tissue [2, 9].”
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Short-term post-implantation dynamics of in vitro engineered human microvascularized adipose tissues
Proulx, M., Mayrand, D., Vincent, C., Boisvert, A., Aubin, K., Trottier, V., & Fradette, J. (2018) · Biomedical Materials · doi:10.1088/1748-605x/aadff7 · Cited by 10
Functional Outcome Analysis of Autologous Stromal Vascular Fraction (SVF) (Sahaj Therapy®) Using Direct Sonication in Osteonecrosis of the Femoral Head (ONFH): A 6-Year Follow-Up Study
Tantuway, V., Jeyaraman, M., Nallakumarasamy, A., Prikh, M. B., Sharma, A. K., & Sharma, R. L. (2023) · Indian Journal of Orthopaedics · doi:10.1007/s43465-023-01041-y · Cited by 9
“Adipose tissue in the body has abundant vascularity and there is a major role in the remodeling process of the persistent vessels in the physiological behavior of the adipose tissue [34].”
Adipose angiotensin II type 1 receptor-associated protein ameliorates metabolic disorders via promoting adipose tissue adipogenesis and browning
Luo, C., Lv, N., Chang, Z., Qu, Q., & Huang, J. (2017) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2017.05.003 · Cited by 9
Pigment Epithelium-Derived Factor: Inhibition of Phosphorylation of Insulin Receptor (IR)/IR Substrate (IRS), Osteogeneration from Adipocytes, and Increased Levels Due to Doxorubicin Exposure
Jones, I. C., Carnagarin, R., Armstrong, J., Lin, D., Baxter-Holland, M., Elahy, M., & Dass, C. R. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15071960 · Cited by 9
“Adipose tissue, particularly BAT, is very highly vascularised and angiogenesis within this tissue has been shown to play a role in the homeostasis of adiposity [28,29].”
Background
Overexpression of Prox‐1 gene in omental adipose tissue and adipocytes compared with subcutaneous adipose tissue and adipocytes in healthy patients
Procino, A. (2014) · Cell Biology International · doi:10.1002/cbin.10273 · Cited by 9
Chronic phosphodiesterase type 5 inhibition has beneficial effects on subcutaneous adipose tissue plasticity in type 2 diabetic mice
Fiore, D., Gianfrilli, D., Cardarelli, S., Naro, F., Lenzi, A., Isidori, A. M., & Venneri, M. A. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.26796 · Cited by 9
“AT‐associated endothelial cells (ECs) are key players for a healthy adipocyte microenvironment (Cao, 2007).”
Background
Adipose tissue regeneration
Mohseni, M., Castro, N. J., Dang, H. P., Nguyen, D., Ho, H. M., Tran, N. M., Nguyen, H. T., & Tran, P. A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813477-1.00013-x · Cited by 9
Implant-induced inflammatory angiogenesis is up-regulated in obese mice
Orellano, L. A. A., de Almeida, S. A., Pereira, L. X., Machado, C. T., Viana, C. T. R., Andrade, S. P., & Campos, P. P. (2020) · Microvascular Research · doi:10.1016/j.mvr.2020.104014 · Cited by 9
The shades of grey in adipose tissue reprogramming
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BackgroundInfluential
Characterization of adipose depot-specific stromal cell populations by single-cell mass cytometry
Lee, J. H., Ealey, K. N., Patel, Y., Verma, N., Thakkar, N., Park, S., Kim, J., & Sung, H. (2022) · iScience · doi:10.1016/j.isci.2022.104166 · Cited by 10
“Dynamic interactions of these cell populations are essential for WAT remodeling and its functional adaptation under diverse metabolic and environmental challenges (Burl et al., 2018; Cao, 2007, 2010, 2013; Shao et al., 2021; Spallanzani et al., 2019).”
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Markers to Predict the Efficacy of Bevacizumab in the Treatment of Metastatic Colorectal Cancer
Varol, U., Yıldız, İ., Salman, T., Karabulut, B., & Uslu, R. (2014) · Tumori Journal · doi:10.1177/1636.17888 · Cited by 9
Thymus fat as an attractive source of angiogenic factors in elderly subjects with myocardial ischemia
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“Moreover, the fact that angiogenic factors showed significant strong positive correlations with adipogenic markers, leads us to believe that the increase of angiogenic properties could be due to the increase of adipose mass throughout life, as it is well-known that angiogenesis is linked to adipogenesis (Cao 2007).”
Promotion of adipogenesis by an EP2 receptor agonist via stimulation of angiogenesis in pulmonary emphysema
Tsuji, T., Yamaguchi, K., Kikuchi, R., Itoh, M., Nakamura, H., Nagai, A., & Aoshiba, K. (2014) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2014.05.003 · Cited by 9
Systemic administration of ghrelin did not restore angiogenesis in hindlimb ischemia in control and diet-induced obese mice
Tahergorabi, Z., Khazaei, M., & Rashidi, B. (2015) · Bratislavské lekárske listy/Bratislava medical journal · doi:10.4149/bll_2015_007 · Cited by 9
“Obesity, a complex metabolic disorder, is created following a prolonged dysbalance of caloric intake and energy expenditure (1) and is associated with the most chronic and severe human diseases including type 2 diabetes, hypertension, cardiovascular diseases, stroke and certain types of cancer such as colorectal, brea…”
EFFECT OF PUNICA GRANATUM (POMEGRANATE) FRUIT EXTRACT ON ANGIOGENESIS
Khan, G. J., Omer, M. O., & Ashraf, M. A. (2013) · Journal of Applied Pharmacy · doi:10.21065/19204159.5.59 · Cited by 9
“Chorioallantoic membrane (CAM) is an extra developing membrane which is generally used in research studies of both processes angiogenesis and anti-angiogenesis [15].”
Background
Obesity, Diabetes and Cancer: A Mechanistic Perspective
Cifarelli, V., & Hursting, S. (2015) · International Journal of Diabetology & Vascular Disease Research · doi:10.19070/2328-353x-si04001 · Cited by 9
“Insulin resistance also drives abornomalities in endothelial and vascular smooth muscle function via alterations in many of the same proangiogenic and vasular altering factors [59].”
BackgroundInfluential
Sarcopenia is related to poor prognosis in patients after trimodality therapy for locally advanced non-small cell lung cancer
Katsui, K., Ogata, T., Watanabe, K., Yoshio, K., Kuroda, M., Yamane, M., Hiraki, T., Kiura, K., Toyooka, S., & Kanazawa, S. (2021) · International Journal of Clinical Oncology · doi:10.1007/s10147-021-01927-7 · Cited by 9
“Adipocytes are known to produce angiogenic factors [37], increase levels of proinflammatory cytokines (adipokines), suppress the activity of natural killer lymphocytes, and contribute to the progression of cancer [38].”
Background
Impact of TNF and IL-1β on capillary networks within engineered human adipose tissues
Proulx, M., Safoine, M., Mayrand, D., Aubin, K., Maux, A., & Fradette, J. (2016) · Journal of Materials Chemistry B · doi:10.1039/c6tb00265j · Cited by 8
The role of progranulin in ischemic heart disease and its related risk factors
Alyahya, A. M. (2022) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2022.106215 · Cited by 9
Generation of mega brown adipose tissue in adults by controlling brown adipocyte differentiation in vivo
Du, Q., Wu, J., Fischer, C., Seki, T., Xu, J., Gao, J., He, X., Hosaka, K., Tong, L., Yasue, A., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203307119 · Cited by 10
“BAT constitutes a myriad of cell types, including mature BAT adipocytes, preadipocytes, vascular cells, stromal fibroblasts, inflammatory cells, and various immune cells (25).”
BackgroundSelf-citation
The miRNA Contribution in Adipocyte Maturation
Giammona, A., Franco, S. D., Dico, A. L., & Stassi, G. (2024) · Non-Coding RNA · doi:10.3390/ncrna10030035 · Cited by 8
“…being the most important among them [9,10]. during obesity and inducing apoptosis in dysfunctional Moreover, this process directly influences pre-adipocyte proliferation and differentiation, thus reducing vascularization during obesity and inducing apoptosis in dysfunctional adipocytes [11–13].”
Background
Expression of leptin and its long form receptor at the porcine maternal-fetal interface: contrasting healthy and arresting conceptus attachment sites during early and mid-pregnancy
Kerr, A., Kridli, R. T., Khalaj, K., Wessels, J. M., Hahnel, A. C., & Tayade, C. (2014) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-12-91 · Cited by 8
“The binding of LEP to OB-Rb within endothelial cells has been linked to the activation of the JAK/ STAT3 molecular pathway which promotes endothelial tube formations and corneal neovascularization in vitro [13,17,18] and has also been associated with the upregulation of VEGF transcription [19].”
Background
Immediate cell-supplemented lipotransfer (iCSL)
Condé‐Green, A., & Lamblet, H. (2011) · European Journal of Plastic Surgery · doi:10.1007/s00238-011-0651-5 · Cited by 8
Review of the Interaction Between Body Composition and Clinical Outcomes in Metastatic Renal Cell Cancer Treated With Targeted Therapies
Yip, S., Heng, D. Y. C., & Tang, P. A. (2016) · Journal of Kidney Cancer and VHL · doi:10.15586/jkcvhl.2016.45 · Cited by 8
“Furthermore, a proangiogenic state is created by the production of factors such as VEGF and leptin by adipose tissue (11).”
Background
Changes of serum angiogenic biomarkers and their correlations with serum leptin concentration
Tahergorabi, Z., & Khazaei, M. (2014) · Bratislavské lekárske listy/Bratislava medical journal · doi:10.4149/bll_2014_065 · Cited by 8
“During embryogenesis, adipose tissue development spatially and temporally is associated with microvessel growth (Cao, 2007).”
Common therapeutic target for both cancer and obesity
Chang, Y. (2017) · World Journal of Biological Chemistry · doi:10.4331/wjbc.v8.i2.102 · Cited by 8
A protocol for prospective studies of 25-hydroxyvitamin D, leptin and body mass index in relation to cutaneous melanoma incidence and survival
Stenehjem, J. S., Grimsrud, T. K., Rees, J. R., Vos, L., Babigumira, R., Veierød, M. B., & Robsahm, T. E. (2017) · BMJ Open · doi:10.1136/bmjopen-2016-014829 · Cited by 8
“Another hypothesis suggests that adipocytes produce high levels of vascular endothelial growth factor, associated with visceral fat, which contributes to angiogenesis and tumour growth.(36) The metabolic hormone leptin may be a risk factor for both CM and CM progression.”
Background
Overexpressing STAMP 2 attenuates adipose tissue angiogenesis and insulin resistance in diabetic ApoE−/−/ LDLR −/− mouse via a PPAR γ/ CD 36 pathway
Wang, F., Han, L., Qin, R., Zhang, Y.-Y., Wang, D., Wang, Z., Tang, M., Zhang, Y., Zhong, M., & Zhang, W. (2017) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13233 · Cited by 8
“In the metabolically active BAT, angiogenesis can increase energy consumption and improve IR [11].”
Background
Adipose-derived stem cells and their microenvironment (Niche) in type 2 diabetes mellitus
Karina, K., Pawitan, J. A., & Rosadi, I. (2020) · Stem Cell Investigation · doi:10.21037/sci.2019.12.02 · Cited by 8
“However, adipose tissue not only has angiogenesis activators but also inhibitors (16).”
Background
Adipocinas y síndrome metabólico: múltiples facetas de un proceso fisiopatológico complejo
N., J. C. S., Z., D. F. L., D., Ó. A. P., & Arias, J. C. (2010) · Revista Colombiana de Cardiología · doi:10.1016/s0120-5633(10)70236-9 · Cited by 8
Resistin: TWEAKing angiogenesis
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The effect of growth hormone on ovarian function recovery in a mouse model of ovarian insufficiency
Kim, S. M., Yoo, J. Y., Hong, Y. H., Lee, J., Kim, J. H., & Lee, J. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1184977 · Cited by 7
“Capillary endothelial cells engage in crosstalk with adipocytes and extracellular components via both paracrine pathways and direct cell-to-cell interactions (39).”
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The Role of Angiogenesis in Obesity
Yoon, M. (2014) · Journal of Life Science · doi:10.5352/jls.2014.24.5.573 · Cited by 7
“Similarly, the growth and development of adipose tissue require the formation of new blood vessels to provide oxygen and nutrients to adipocytes [13, 63].”
BackgroundInfluential
Obesity-Related Genes and Oral Cancer: A Bioinformatics Approach and Systematic Review
Santos, E. M. S., & Santos, H. O. (2016) · Journal of Applied Bioinformatics & Computational Biology · doi:10.4172/2329-9533.1000124 · Cited by 7
“One possible reason for the association with tumor development, proliferation and invasion may be the stimulation of vascular endothelial growth factor expression, resulting in enhanced angiogenesis [41,42].”
Background
Clinical application of AD-MSCs – A review
Semenova, E., Chrościńska–Krawczyk, M., Grudniak, M., Ołdak, T., & Machaj, E. K. (2018) · Journal of Pre-Clinical and Clinical Research · doi:10.26444/jpccr/94910 · Cited by 7
“Supported by earlier studies, the identification of AD-MSCs as a part of the vasculature niche claims that adipocytes develop in close contact with blood vessels [62].”
Result
Inhibitory Effects ofCorni FructusExtract on Angiogenesis and Adipogenesis
Hwang, J., & Kim, J. (2011) · Korean Journal of Physiology and Pharmacology · doi:10.4196/kjpp.2011.15.1.43 · Cited by 7

Authors: Cao, Y.
Affiliations: Karolinska Institutet (SE)
Corresponding author: Cao, Yihai
ORCID: Cao, Yihai
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2007-09-04
Volume: 117
Issue: 9
Pages: 2362-2368
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci32239
PMC: PMC1963348
OpenAlex: W2027442301
Cited by: 736
References: 120
Citations by year: 2026: 18 · 2025: 18 · 2024: 24 · 2023: 32 · 2022: 32 · 2021: 25 · 2020: 43 · 2019: 47 · 2018: 59 · 2017: 48 · 2016: 40 · 2015: 42 · 2014: 66 · 2013: 67 · 2012: 43
FWCI: 21.41
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Swedish Cancer Foundation
European Commission
Hjärt-Lungfonden
Karolinska Institutet
Vetenskapsrådet
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: angiogenesis, adipogenesis, obesity, neovascularization, adipocytes, angiogenic factors, leptin, vascular endothelial growth factor, angiopoietins, paracrine signaling, anti-angiogenic therapy
MeSH terms: Animals, Cell Communication, Humans, Neovascularization, Pathologic, Obesity, Adipocytes, Endothelial Cells, Angiogenesis Inducing Agents, Adipogenesis

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Angiogenesis modulates adipogenesis and obesity

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