(Circulation. 1999;100:2473.)
© 1999 American Heart Association, Inc.
Brief Rapid Communication |
Novel Modulator for Endothelial Adhesion Molecules
Adipocyte-Derived Plasma Protein Adiponectin
From the Department of Internal Medicine and Molecular Science, Graduate School of Medicine, Osaka University, Osaka, Japan. Drs Ouchi and Kihara contributed equally to the work.
Correspondence to Noriyuki Ouchi, MD, Department of Internal Medicine and Molecular Science, Graduate School of Medicine, Osaka University, 2-2, Yamada-oka, Suita, Osaka, 565-0871, Japan. E-mail ouchi{at}imed2.med.osaka-u.ac.jp
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Abstract |
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Background—Among the many adipocyte-derived endocrine factors, we recently found an adipocyte-specific secretory protein, adiponectin, which was decreased in obesity. Although obesity is associated with increased cardiovascular mortality and morbidity, the molecular basis for the link between obesity and vascular disease has not been fully clarified. The present study investigated whether adiponectin could modulate endothelial function and relate to coronary disease.
Methods and Results—For the in vitro study, human aortic
endothelial cells (HAECs) were preincubated for 18
hours with the indicated amount of adiponectin, then exposed to tumor
necrosis factor-
(TNF-) (10 U/mL) or vehicle for the times
indicated. The adhesion of human monocytic cell line THP-1 cells to
HAECs was determined by adhesion assay. The surface expression of
vascular cell adhesion molecule-1 (VCAM-1),
endothelial-leukocyte adhesion molecule-1 (E-selectin),
and intracellular adhesion molecule-1 (ICAM-1) was measured by cell
ELISA. Physiological concentrations of adiponectin
dose-dependently inhibited TNF-–induced THP-1 adhesion and
expression of VCAM-1, E-selectin, and ICAM-1 on HAECs. For the in vivo
study, the concentrations of adiponectin in human plasma were
determined by a sandwich ELISA system that we recently developed.
Plasma adiponectin concentrations were significantly lower in patients
with coronary artery disease than those in age- and body mass
index–adjusted control subjects.
Conclusions—These observations suggest that adiponectin modulates endothelial inflammatory response and that the measurement of plasma adiponectin levels may be helpful in assessment of CAD risk.
Key Words: endothelium • cell adhesion molecules • coronary disease • adiponectin
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Obesity, the most common nutritional disorder in the industrial countries, is associated with increased cardiovascular mortality and morbidity.1 2 3 Adipose tissue expresses various secretory proteins, including leptin, tumor necrosis factor-
(TNF-), and
plasminogen activator inhibitor
type 1, which may contribute to the development of
cardiovascular diseases.4 5 6 7 TNF-
overproduction in adipose tissue is a possible cause not only
of the development of insulin resistance8 but also of the
development of atherosclerosis through an inflammatory
process in obese subjects. However, the molecular basis for the link
between obesity and vascular disease has not been fully clarified. From
an extensive search of the human adipose tissue cDNA library, we
isolated an adipocyte-specific cDNA, apM1.4 9 The cDNA
encoded a 244-amino-acid protein homologous to collagen VIII and X and
complement factor C1q. Adiponectin, the gene product of apM1, was
found to be a secretory protein abundant in human
plasma.10 Plasma adiponectin level was decreased in
obesity,10 suggesting that dysregulation of adiponectin
may be relevant to obesity-linked disorders. Although adiponectin is
the most abundant gene product in adipose tissue9 and
accounts for 0.01% of total plasma protein,10 its
physiological functions have not been
elucidated.
At the early stages of atherosclerosis,
endothelial cell activation by various inflammatory
stimuli, including TNF-, results in the synthesis of adhesion
molecules and increases the adherence of monocytes.11 This
monocyte adhesion to the arterial
endothelium is considered crucial for the development
of vascular diseases.11 We hypothesized that circulating
adiponectin might modulate vascular wall functions like other
adipocyte-derived secretory proteins.
In this study, we investigated the propositions that
physiological concentrations of adiponectin
suppressed TNF-–mediated expression of adhesion molecules in human
aortic endothelial cells (HAECs) and that plasma
adiponectin levels were markedly low in patients with coronary
artery disease (CAD).
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Methods |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Cell Culture
HAECs (Clonetics) were maintained in MCDB131 medium (Clonetics) supplemented with 5% FCS, and cells from passages 4 through 6 were used for experiments. HAECs (confluent in type I collagen–coated plate) were incubated for 18 hours in medium 199 (Gibco) containing 0.5% FCS and 3% BSA with the indicated amount of adiponectin, then exposed to human recombinant TNF-
(R&D systems) at a final
concentration of 10 U/mL or vehicle for the times indicated. Human
recombinant adiponectin was prepared as previously
described.10
Adhesion Assay
The adhesion of the THP-1 human monocytic cell line to HAECs was
determined as previously described.12 FITC-labeled THP-1
cells (5x105 cells/well) were incubated with
HAECs in 24-well plates for 10 minutes at 37°C. The plates were
sealed, inverted, and centrifuged (250g) for 5
minutes to separate nonadherent monocytes. Adherent cells were lysed
with 50 mmol/L Tris (pH 8.4)/0.1% SDS, and the
fluorescence was measured. Statistical significance was
determined by a paired t test.
Cell ELISA
HAECs were incubated at room temperature with anti–human
vascular cell adhesion molecule-1 (VCAM-1),
anti–endothelial-leukocyte adhesion molecule-1
(E-selectin), or anti–intracellular adhesion molecule-1 (ICAM-1)
monoclonal antibody (DAKO) at 1:1000 dilution in medium 199 containing
0.5% BSA for 1 hour and then with horseradish peroxidase–conjugated
goat anti-mouse IgG (Cappel) at 1:1000 dilution in the same
medium. Color formation with
o-phenylenediamine dihydrochloride was
measured at 492 nm.
Northern Blot Analysis
HAECs were pretreated with 50 µg/mL of adiponectin and exposed
to TNF- for 4 hours. Total RNA (20 µg per lane) was extracted,
electrophoresed, and transferred to a nylon membrane. The membranes
were hybridized with human VCAM-1, E-selectin, or ICAM-1 cDNA probes
labeled with [-32P]dCTP.
Measurement of Plasma Adiponectin Concentration
Consecutive CAD patients were recruited from inpatients admitted
to Osaka University Hospital. The criterion for CAD was a 
75%
organic stenosis of 1 segment of a major coronary
artery confirmed by coronary angiogram. The control subjects
were selected from the inpatients of Osaka University Hospital and
matched with the CAD patients for age and body mass index (BMI). They
had no evidence of vascular diseases, including angina pectoris. All
subjects enrolled in this study were Japanese and gave written informed
consent. The Ethics Committee of Osaka University approved this
study.
The concentrations of adiponectin in human plasma were determined as described.10 The significance of the differences between the groups was determined by the Mann-Whitney test. Linear regression analysis was used to evaluate the relationship between the variables.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Adiponectin Inhibits TNF-
–Induced Monocyte Adhesion and
Expression of Adhesion MoleculesWe investigated the effects of adiponectin on monocyte adhesion to HAECs. Adiponectin treatment alone had no significant effect on the adhesion of human monocytic cell line THP-1 cells to HAECs (Figure 1A
). TNF- treatment (10 U/mL for 6
hours) enhanced adhesion of THP-1 cells to HAECs by 2-fold (Figure 1A). When HAECs were preincubated with adiponectin for 18 hours
before a 6-hour coincubation with TNF-, THP-1 cell adhesion was
dose-dependently suppressed by adiponectin treatment (Figure 1A). However, THP-1 cell adhesion to TNF-–stimulated HAECs
was not suppressed when adiponectin was added at the same time as THP-1
cells (data not shown), suggesting that adiponectin does not occupy the
binding sites of THP-1 cells on HAECs.
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TNF- treatment increased the surface expression of VCAM-1,
E-selectin, and ICAM-1 on HAECs by 2- to 5-fold (Figure 1
, B
through D). Dose-dependent suppression of TNF-–induced surface
expression of VCAM-1, E-selectin, and ICAM-1 was observed when HAECs
were pretreated with adiponectin (Figure 1, B through D).
Adiponectin treatment alone did not lead to any significant changes in
the surface expression of these molecules in the absence of TNF-
(Figure 1, B through D). The suppressive effects of adiponectin
on cell-surface expression of these adhesion molecules were accompanied
by changes in steady-state mRNA levels analyzed by Northern
blot (Figure 1, B through D, inset).
Plasma Adiponectin Concentrations in Patients With CAD
Plasma adiponectin levels were significantly lower in patients
with CAD than in age- and BMI-adjusted control subjects both in men
(3.4±1.8 versus 7.4±3.5 µg/mL) (P<0.01) and in women
(4.3±1.5 versus 9.3±6.8 µg/mL) (P<0.05) (Figure 2). Although atherogenic lipid profiles
were observed in the CAD group compared with the control (data not
shown), the decreased plasma adiponectin level may be another
coronary risk factor.
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): 58 men and 20 women, matched for age and BMI. Concentrations of
adiponectin were determined by ELISA. |
Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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In the present study, we demonstrated that physiological concentrations of adiponectin (5 to 25 µg/mL) had significant inhibitory effects on TNF-
–induced monocyte adhesion and adhesion molecule expression in
a dose-dependent manner in vitro. Atherosclerosis has
been regarded as an inflammatory disease. The initial atherosclerotic
lesion consists of monocytes/macrophages and T
lymphocytes.11 At this stage, adhesion molecules on
arterial endothelial cells are responsible
for the accumulation of these hemocytes. VCAM-1, E-selectin, and ICAM-1
have been detected in human atherosclerotic lesions.13 The
expression of adhesion molecule plays an important role in the
regulation of inflammatory reactions in various types of
cells.14 15 If the excess inflammatory response could be
neutralized by adiponectin, it might be possible to prevent the process
of atherogenesis. Our findings indicate that adiponectin acts as an
endogenous modulator of endothelial cell
function, although further investigation is needed to elucidate the
intracellular signals by which adiponectin suppresses adhesion
molecules. Recently, we developed an ELISA system to quantify the plasma adiponectin concentration.10 Paradoxically, the plasma adiponectin levels in obese subjects were significantly lower than those in nonobese subjects,10 although adiponectin is secreted only from adipose tissue. Because obesity is frequently accompanied by vascular diseases, we postulated that the dysregulation of adiponectin may be associated with vascular disease in obese subjects. In this study, plasma adiponectin levels were significantly lower in patients with CAD than in age- and BMI-adjusted control subjects. This finding suggests that the decreased plasma adiponectin level may relate to the development of CAD.
Adiponectin is an adipocyte-specific plasma protein, which acts as an endogenous regulator of endothelial cells in response to inflammatory stimuli. Our observations raise the possibility that the measurement of plasma adiponectin levels may be helpful in assessment of CAD risk.
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Acknowledgments |
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This work was supported by grants from the Japanese Ministry of Education and the Japan Society for Promotion of Science Research for the Future Program. We thank N. Kume for providing a human VCAM-1 cDNA probe.
Received July 29, 1999; revision received October 5, 1999; accepted October 11, 1999.
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C. Zoccali Endothelial dysfunction in CKD: a new player in town? Nephrol. Dial. Transplant., March 1, 2008; 23(3): 783 - 785. [Full Text] [PDF]
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R. Schnabel, C. M. Messow, E. Lubos, C. Espinola-Klein, H. J. Rupprecht, C. Bickel, C. Sinning, S. Tzikas, T. Keller, S. Genth-Zotz, et al. Association of adiponectin with adverse outcome in coronary artery disease patients: results from the AtheroGene study Eur. Heart J., March 1, 2008; 29(5): 649 - 657. [Abstract] [Full Text] [PDF]
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Y. Tabara, H. Osawa, R. Kawamoto, R. Tachibana-Iimori, M. Yamamoto, J. Nakura, T. Miki, H. Makino, and K. Kohara Reduced High-Molecular-Weight Adiponectin and Elevated High-Sensitivity C-Reactive Protein Are Synergistic Risk Factors for Metabolic Syndrome in a Large-Scale Middle-Aged to Elderly Population: the Shimanami Health Promoting Program Study J. Clin. Endocrinol. Metab., March 1, 2008; 93(3): 715 - 722. [Abstract] [Full Text] [PDF]
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X. Wu, K. Mahadev, L. Fuchsel, R. Ouedraogo, S.-q. Xu, and B. J. Goldstein Adiponectin suppresses I{kappa}B kinase activation induced by tumor necrosis factor-{alpha} or high glucose in endothelial cells: role of cAMP and AMP kinase signaling Am J Physiol Endocrinol Metab, December 1, 2007; 293(6): E1836 - E1844. [Abstract] [Full Text] [PDF]
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J. Golledge, P. Clancy, K. Jamrozik, and P. E. Norman Obesity, Adipokines, and Abdominal Aortic Aneurysm: Health in Men Study Circulation, November 13, 2007; 116(20): 2275 - 2279. [Abstract] [Full Text] [PDF]
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K. Ohashi, H. Iwatani, S. Kihara, Y. Nakagawa, N. Komura, K. Fujita, N. Maeda, M. Nishida, F. Katsube, I. Shimomura, et al. Exacerbation of Albuminuria and Renal Fibrosis in Subtotal Renal Ablation Model of Adiponectin-Knockout Mice Arterioscler Thromb Vasc Biol, September 1, 2007; 27(9): 1910 - 1917. [Abstract] [Full Text] [PDF]
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S.-K. Kim, K.-Y. Hur, H.-J. Kim, W.-S. Shim, C.-W. Ahn, S.-W. Park, Y.-W. Cho, S.-K. Lim, H.-C. Lee, and B.-S. Cha The increase in abdominal subcutaneous fat depot is an independent factor to determine the glycemic control after rosiglitazone treatment Eur. J. Endocrinol., August 1, 2007; 157(2): 167 - 174. [Abstract] [Full Text] [PDF]
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M. Cesari, K. Narkiewicz, R. De Toni, E. Aldighieri, C. J. Williams, and G. P. Rossi Heritability of Plasma Adiponectin Levels and Body Mass Index in Twins J. Clin. Endocrinol. Metab., August 1, 2007; 92(8): 3082 - 3088. [Abstract] [Full Text] [PDF]
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R. Shibata, K. Sato, M. Kumada, Y. Izumiya, M. Sonoda, S. Kihara, N. Ouchi, and K. Walsh Adiponectin accumulates in myocardial tissue that has been damaged by ischemia-reperfusion injury via leakage from the vascular compartment Cardiovasc Res, June 1, 2007; 74(3): 471 - 479. [Abstract] [Full Text] [PDF]
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R. Jaumdally, C. Varma, R. J. Macfadyen, and G. Y.H. Lip Coronary sinus blood sampling: an insight into local cardiac pathophysiology and treatment? Eur. Heart J., April 2, 2007; 28(8): 929 - 940. [Abstract] [Full Text] [PDF]
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C.-J. Li, H.-W. Sun, F.-L. Zhu, L. Chen, Y.-Y. Rong, Y. Zhang, and M. Zhang Local adiponectin treatment reduces atherosclerotic plaque size in rabbits J. Endocrinol., April 1, 2007; 193(1): 137 - 145. [Abstract] [Full Text] [PDF]
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P. E. Szmitko, H. Teoh, D. J. Stewart, and S. Verma Adiponectin and cardiovascular disease: state of the art? Am J Physiol Heart Circ Physiol, April 1, 2007; 292(4): H1655 - H1663. [Abstract] [Full Text] [PDF]
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T. A. Hopkins, N. Ouchi, R. Shibata, and K. Walsh Adiponectin actions in the cardiovascular system Cardiovasc Res, April 1, 2007; 74(1): 11 - 18. [Abstract] [Full Text] [PDF]
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D. Teta, M. Maillard, A. Tedjani, J. Passlick-Deetjen, and M. Burnier The effect of pH-neutral peritoneal dialysis fluids on adipokine secretion from cultured adipocytes Nephrol. Dial. Transplant., November 28, 2006; (2006) gfl698v1. [Abstract] [Full Text] [PDF]
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T. J. Orchard, T. Costacou, A. Kretowski, and R. W. Nesto Type 1 diabetes and coronary artery disease. Diabetes Care, November 1, 2006; 29(11): 2528 - 2538. [Full Text] [PDF]
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K. Ikeda, H. Maegawa, S. Ugi, Y. Tao, Y. Nishio, S. Tsukada, S. Maeda, and A. Kashiwagi Transcription Factor Activating Enhancer-binding Protein-2beta: A NEGATIVE REGULATOR OF ADIPONECTIN GENE EXPRESSION J. Biol. Chem., October 20, 2006; 281(42): 31245 - 31253. [Abstract] [Full Text] [PDF]
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E. Cavusoglu, C. Ruwende, V. Chopra, S. Yanamadala, C. Eng, L. T. Clark, D. J. Pinsky, and J. D. Marmur Adiponectin is an independent predictor of all-cause mortality, cardiac mortality, and myocardial infarction in patients presenting with chest pain Eur. Heart J., October 1, 2006; 27(19): 2300 - 2309. [Abstract] [Full Text] [PDF]
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T. Soccio, Y.-Y. Zhang, S. Bacci, W. Mlynarski, G. Placha, G. Raggio, R. Di Paola, A. Marucci, M. T. Johnstone, E. V. Gervino, et al. Common Haplotypes at the Adiponectin Receptor 1 (ADIPOR1) Locus Are Associated With Increased Risk of Coronary Artery Disease in Type 2 Diabetes. Diabetes, October 1, 2006; 55(10): 2763 - 2770. [Abstract] [Full Text] [PDF]
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F. Otsuka, S. Sugiyama, S. Kojima, H. Maruyoshi, T. Funahashi, K. Matsui, T. Sakamoto, M. Yoshimura, K. Kimura, S. Umemura, et al. Plasma Adiponectin Levels Are Associated With Coronary Lesion Complexity in Men With Coronary Artery Disease J. Am. Coll. Cardiol., September 19, 2006; 48(6): 1155 - 1162. [Abstract] [Full Text] [PDF]
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M. J. Yoon, G. Y. Lee, J.-J. Chung, Y. H. Ahn, S. H. Hong, and J. B. Kim Adiponectin Increases Fatty Acid Oxidation in Skeletal Muscle Cells by Sequential Activation of AMP-Activated Protein Kinase, p38 Mitogen-Activated Protein Kinase, and Peroxisome Proliferator-Activated Receptor {alpha} Diabetes, September 1, 2006; 55(9): 2562 - 2570. [Abstract] [Full Text] [PDF]
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N. Sattar, G. Wannamethee, N. Sarwar, J. Tchernova, L. Cherry, A. M. Wallace, J. Danesh, and P. H. Whincup Adiponectin and Coronary Heart Disease: A Prospective Study and Meta-Analysis Circulation, August 15, 2006; 114(7): 623 - 629. [Abstract] [Full Text] [PDF]
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Y. Nakano, S. Tajima, A. Yoshimi, H. Akiyama, M. Tsushima, T. Tanioka, T. Negoro, M. Tomita, and T. Tobe A novel enzyme-linked immunosorbent assay specific for high-molecular-weight adiponectin J. Lipid Res., July 1, 2006; 47(7): 1572 - 1582. [Abstract] [Full Text] [PDF]
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C. Herder, H. Hauner, B. Haastert, K. Rohrig, W. Koenig, H. Kolb, S. Muller-Scholze, B. Thorand, R. Holle, and W. Rathmann Hypoadiponectinemia and Proinflammatory State: Two Sides of the Same Coin?: Results From the Cooperative Health Research in the Region of Augsburg Survey 4 (KORA S4) Diabetes Care, July 1, 2006; 29(7): 1626 - 1631. [Abstract] [Full Text] [PDF]
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M. Nishimura, T. Hashimoto, H. Kobayashi, S. Yamazaki, K. Okino, H. Fujita, N. Inoue, H. Takahashi, and T. Ono Association of the circulating adiponectin concentration with coronary in-stent restenosis in haemodialysis patients Nephrol. Dial. Transplant., June 1, 2006; 21(6): 1640 - 1647. [Abstract] [Full Text] [PDF]
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R. Ouedraogo, X. Wu, S.-Q. Xu, L. Fuchsel, H. Motoshima, K. Mahadev, K. Hough, R. Scalia, and B. J. Goldstein Adiponectin Suppression of High-Glucose-Induced Reactive Oxygen Species in Vascular Endothelial Cells: Evidence for Involvement of a cAMP Signaling Pathway Diabetes, June 1, 2006; 55(6): 1840 - 1846. [Abstract] [Full Text] [PDF]
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L. Qi, A. Doria, J. E. Manson, J. B. Meigs, D. Hunter, C. S. Mantzoros, and F. B. Hu Adiponectin genetic variability, plasma adiponectin, and cardiovascular risk in patients with type 2 diabetes. Diabetes, May 1, 2006; 55(5): 1512 - 1516. [Abstract] [Full Text] [PDF]
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J. M. Bruun, J. W. Helge, B. Richelsen, and B. Stallknecht Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects Am J Physiol Endocrinol Metab, May 1, 2006; 290(5): E961 - E967. [Abstract] [Full Text] [PDF]
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H. Ekmekci and O. B. Ekmekci The Role of Adiponectin in Atherosclerosis and Thrombosis Clinical and Applied Thrombosis/Hemostasis, April 1, 2006; 12(2): 163 - 168. [Abstract] [PDF]
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K. Matsushita, H. Yatsuya, K. Tamakoshi, K. Wada, R. Otsuka, S. Takefuji, K. Sugiura, T. Kondo, T. Murohara, and H. Toyoshima Comparison of Circulating Adiponectin and Proinflammatory Markers Regarding Their Association With Metabolic Syndrome in Japanese Men Arterioscler Thromb Vasc Biol, April 1, 2006; 26(4): 871 - 876. [Abstract] [Full Text] [PDF]
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