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Adiponectin, an Adipocyte-Derived Protein, Predicts Future Insulin Resistance: Two-Year Follow-Up Study in Japanese Population

Department of Internal Medicine (Y.Y., H.H., I.S., K.N., T.S.) and Health Center (H.H., I.S.), Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan

Address all correspondence and requests for reprints to: Yukihiro Yamamoto, M.D., Department of Internal Medicine, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. E-mail: yukihiro{at}hh.iij4u.or.jp.

	Abstract

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It has been reported that the serum adiponectin level was negatively correlated with body mass index (BMI), insulin resistance index, and triglycerides and was positively correlated with high-density lipoprotein cholesterol in several cross-sectional studies. However, the causal relationship has not been elucidated. We investigated whether the baseline adiponectin level could predict subsequent changes in insulin resistance, lipid profile, or body weight in a 2-yr longitudinal study. This study included 590 male Japanese subjects, aged 30–65 yr, who received annual health checkups in both 2000 and 2002. Blood pressure, heart rate, and anthropometric and metabolic parameters, including serum insulin and adiponectin levels, were determined. The insulin resistance index was calculated based on homeostasis model assessment. Baseline adiponectin level was not correlated with the subsequent change in lipid profile or BMI in 2 yr after adjustment for each baseline value. However, the baseline adiponectin level was negatively correlated with subsequent changes in insulin and insulin resistance index based on homeostasis model assessment, even after adjustment for change in BMI (r = -0.162 and r = -0.140, respectively). These findings suggest that the serum adiponectin concentration predicts subsequent changes in insulin resistance, but not in lipid profile or body weight.

	Introduction

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ADIPOSE TISSUE IS not only an energy storage organ, but also plays an important role in the development of insulin resistance, type 2 diabetes, hyperlipidemia, and their complications through the secretion of various hormone-like substances (1). Adiponectin is a plasma protein secreted specifically by adipose tissue (2). Increasing evidence suggests that adiponectin may be one of the insulin-sensitizing cytokines secreted by adipose tissue. Adiponectin administration reverses insulin resistance in various mouse models of obesity and diabetes (3, 4). Furthermore, adiponectin-knockout mice exhibited insulin resistance that was reversed by adiponectin administration (5, 6). In rhesus monkeys, plasma adiponectin decreases in parallel with the progression of insulin resistance (7).

In humans, we (8) and others (9, 10, 11) have reported that the serum adiponectin concentration was negatively correlated with insulin resistance and body weight/body mass index (BMI) in cross-sectional studies. As for lipid profile, we (8) reported that the serum adiponectin level was negatively correlated with triglycerides and low-density lipoprotein (LDL) cholesterol and was positively correlated with high-density lipoprotein (HDL) cholesterol even after adjustment for age, sex, and BMI.

However, the causal relationship of serum adiponectin concentration with insulin resistance, lipid profile, and/or body weight in humans is not clear from these cross-sectional studies. To our knowledge, there is only one longitudinal study concerning the effects of adiponectin on insulin sensitivity (positive results) (9) and body weight (no effects) (12) in adult humans. There could be, however, ethnic differences, and these two studies (9, 12) were of Pima Indians. Furthermore, there are no longitudinal studies concerning adiponectin and the lipid profile. To clarify the relationship of the baseline adiponectin level to subsequent changes in insulin resistance, body weight, and lipid profile, we performed this longitudinal study.

	Subjects and Methods

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Subjects

This study included 590 male teachers and employees at Keio University, aged 30–65 yr (46.4 ± 9.3 in 2000), who received annual health checkups in both 2000 and 2002. Subjects with endocrine disease, significant renal or hepatic disease, coronary artery disease, or cerebrovascular disease and those receiving medication for diabetes mellitus or hyperlipidemia were excluded from the analyses.

The present study was conducted according to the principles expressed in the Declaration of Helsinki. Informed consent was obtained from each subject after full explanation of the purpose, nature, and risk of all procedures used. The protocol was approved by the ethical review committees of the Health Center and the Department of Internal Medicine, Keio University School of Medicine (Tokyo, Japan).

Measurements

Height, weight, fasting plasma glucose, serum insulin, adiponectin, total cholesterol, triglycerides, HDL cholesterol, and LDL cholesterol levels were measured in the morning after an overnight fast. Plasma glucose and lipids were assayed by routine automated laboratory methods. The serum insulin concentration was measured by an enzyme immunoassay, using a commercially available kit (Tosoh, Tokyo, Japan) with intra- and interassay coefficients ranging from 2.9–4.6% and 4.5–7.0%, respectively. The insulin resistance index was calculated based on homeostasis model assessment (HOMA-IR) (13, 14). The serum adiponectin level was measured by ELISA without a denaturing step, with intra- and inter-assay coefficients ranging from 4.8–4.9% and 3.3–6.8%, respectively, as described previously (8, 15).

Statistical analysis

All statistical analyses were performed using the StatView program for Windows (version 5.0-J, SAS Institute, Inc., Cary, NC). Relationships between parameters in 2000 and those in 2002 were analyzed by the Wilcoxon signed-rank test. Relationships between adiponectin at baseline and changes in other parameters in 2 yr were analyzed by simple correlation and by multiple regression. Because serum insulin, triglycerides, and adiponectin levels and HOMA-IR were normally distributed after log transformation, the logarithms of these parameters were used for the analyses. All data are expressed as the mean ± SD, and P < 0.05 was considered statistically significant.

	Results

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The clinical and laboratory characteristics of the subjects are summarized in Table 1. Body weight, BMI, systolic blood pressure, diastolic blood pressure, fasting plasma glucose, insulin, HOMA-IR, total cholesterol, and HDL cholesterol were significantly increased, and serum adiponectin was significantly decreased after 2 yr.

View this table: [in this window] [in a new window]   TABLE 2. Simple regression and multiple regression analyses between log [serum adiponectin at baseline] and changes in several parameters () in 590 Japanese men, aged 30–65 yr

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

We previously reported that the serum adiponectin level was negatively correlated with HOMA-IR, triglycerides, and LDL cholesterol and was positively correlated with HDL cholesterol independently of age, sex, and BMI (8). Because the study was cross-sectional, the causal relationship has not been elucidated. Stefan et al. (9) reported that the plasma adiponectin concentration at baseline was positively correlated with insulin-stimulated glucose disposal at follow-up after adjustment for insulin-stimulated glucose disposal at baseline, sex, age at follow-up, time of follow-up, and change in percent body fat in adult Pima Indians, who have the highest prevalence of obesity and diabetes in the world. In Pima Indian children, the plasma adiponectin concentration at 5 yr of age was not predictive of the change in plasma insulin concentration (16). However, there has been no longitudinal study of the relationship between serum adiponectin level and insulin sensitivity except for these Pima Indian studies. In rhesus monkeys, the plasma adiponectin level decreased in parallel with the progression of insulin resistance (7). In the present study the serum adiponectin level at baseline was negatively correlated with subsequent change in HOMA-IR, independently of change in BMI. That is, when the adiponectin level is high, insulin sensitivity improves in the subsequent 2 yr in the Japanese population.

Our findings coincide with animal studies demonstrating that replenishment of adiponectin increases insulin sensitivity in both lipoatrophic diabetic mice and murine models of obesity and type 2 diabetes (3) and with studies demonstrating reduced insulin sensitivity in adiponectin-knockout mice (5, 6). As for the mechanism, adiponectin activates 5'-AMP-activated protein kinase (AMPK), which then mediates phosphorylation of acetyl-coenzyme A carboxylase and fatty acid oxidation in myocytes and hepatocytes, and thereby directly regulates glucose metabolism and insulin sensitivity (17). Further studies are needed to clarify whether the same mechanism applies to improving insulin sensitivity in humans.

As for the lipid profile, it was reported that the serum adiponectin level was negatively correlated with triglycerides and was positively correlated with HDL cholesterol in Japanese (8, 18, 19) and Caucasians (11) in cross-sectional studies. The causal relationship has not been elucidated, because no animal study or longitudinal human study focusing on the relationship between adiponectin and the lipid profile has been reported. In the present longitudinal study the serum adiponectin level at baseline was not correlated with subsequent change in lipid profile. Taking this result into consideration, adiponectin may not directly affect lipid metabolism. However, because in cross-sectional studies the serum adiponectin level was positively correlated with HDL cholesterol, even after adjustment for insulin sensitivity (8, 11), a direct effect of adiponectin on lipid metabolism cannot be ruled out.

As mentioned above, adiponectin activates AMPK (17). 5-Aminoimidazole-4-carboxamide ribonucleoside (AICAR) is often used in experiments as an AMPK activator (20). Infusion of AICAR in an animal model of diabetes activates AMPK and then improves glucose tolerance (21, 22). The effect of AICAR on lipid metabolism is controversial. One study reported that treatment with AICAR in diabetic animals decreased plasma triglycerides (21), but others reported that the treatment increased plasma triglycerides (22). The effect of adiponectin on lipid metabolism through activation of AMPK and/or another as yet unknown mechanism needs to be validated.

The serum adiponectin level was negatively correlated with body weight and BMI in cross-sectional human studies (8, 9, 10, 11, 12, 18, 23, 24). Weight reduction significantly elevated the serum adiponectin level after 2 months of a calorie-restricted diet (18) and in obese patients who received gastric partition surgery (25). In the present study the baseline adiponectin level did not affect subsequent change in body weight or BMI. This result is consistent with that reported by Vozarova et al. in Pima Indians (12). In humans no other studies have been reported. In mice the administration of adiponectin caused weight reduction without affecting food intake, through its ability to stimulate lipid oxidation (26). In humans, however, the serum adiponectin level was not associated with fat oxidation (27). This discrepancy may be due to differences in adiponectin concentration (pharmacological or physiological), diet (high fat/high sucrose diet or not), and/or adiposity. At least in humans, weight reduction affects the serum adiponectin level, but the serum adiponectin level does not seem to affect weight reduction.

To summarize, the findings of this study suggest that the serum adiponectin concentration predicts the subsequent change in insulin resistance, but not changes in lipid profile or body weight. With a longer study period, it is possible that these factors might also be affected. In conclusion, it is suggested that in humans adiponectin plays an important role in insulin sensitivity. However, further studies are needed to clarify the effects of adiponectin on lipid metabolism and body weight in humans.

	Acknowledgments

 
We thank Chugai Diagnostics Science, Inc. (Tokyo, Japan), and Fujirebio Inc. (Tokyo, Japan), for technical assistance with the ELISA system of nondenatured adiponectin, and Hitoshi Sekiguchi, Shuji Oguchi, and Eiko Takeshita (Department of Laboratory Medicine, Keio University Hospital, Tokyo, Japan) for their technical assistance with the insulin assay.

	Footnotes

 
This work was supported in part by research grants (to Y.Y. and H.H.) from Keio University (Tokyo, Japan).

Abbreviations: AICAR, 5-Aminoimidazole-4-carboxamide ribonucleoside; AMPK, 5'-AMP-activated protein kinase; BMI, body mass index; HDL, high-density lipoprotein; HOMA-IR, insulin resistance index based on homeostasis model assessment; LDL, low-density lipoprotein.

Received July 8, 2003.

Accepted September 15, 2003.

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This Article Abstract Full Text (PDF) Submit a related Letter to the Editor Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Copyright Permission Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Yamamoto, Y. Articles by Saruta, T. Search for Related Content PubMed PubMed Citation Articles by Yamamoto, Y. Articles by Saruta, T.