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Gastric Inhibitory Polypeptide (GIP) Is Selectively Decreased in the Roux-Limb of Dietary Obese Mice after RYGB Surgery

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      Abstract

      Gastric inhibitory polypeptide (GIP, glucose-dependent insulinotropic polypeptide) is expressed by intestinal K cells to regulate glucose-induced insulin secretion. The impact of Roux-en Y bypass (RYGB) surgery on blood GIP is highly contraversial. This study was conducted to address the mechanism of controversy. GIP mRNA was examined in the intestine, and serum GIP was determined using Luminex and ELISA in diet-induced obese (DIO) mice. The assays were conducted in RYGB mice in fasting and fed conditions. Food preference, weight loss and insulin sensitivity were monitored in RYGB mice. In DIO mice, GIP mRNA was increased by 80% in all sections of the small intestine over the lean control. The increase was observed in both fasting and fed conditions. After RYGB surgery, the food-induced GIP expression was selectively reduced in the Roux-limb, but not in the biliopancreatic and common limbs of intestine in fed condition. Lack of stimulation by glucose or cholesterol contributed to the reduction. Jejunal mucosa of Roux-limb exhibited hypertrophy, but villous surface was decreased by the undigested food. Serum GIP (total) was significantly higher in the fasting condition, but not in the fed condition due to attenuated GIP response to food intake in RYGB mice. The GIP alteration was associated with chow diet preference, sustained weight loss and insulin sensitization in RYGB mice. RYGB increased serum GIP in the fasting, but not in the fed conditions. The loss of food-induced GIP response in Roux-limb of intestine likely contributes to the attenuated serum GIP response to feeding.

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      Bariatric surgery: a systematic review and meta-analysis.

      About 5% of the US population is morbidly obese. This disease remains largely refractory to diet and drug therapy, but generally responds well to bariatric surgery. To determine the impact of bariatric surgery on weight loss, operative mortality outcome, and 4 obesity comorbidities (diabetes, hyperlipidemia, hypertension, and obstructive sleep apnea). Electronic literature search of MEDLINE, Current Contents, and the Cochrane Library databases plus manual reference checks of all articles on bariatric surgery published in the English language between 1990 and 2003. Two levels of screening were used on 2738 citations. A total of 136 fully extracted studies, which included 91 overlapping patient populations (kin studies), were included for a total of 22,094 patients. Nineteen percent of the patients were men and 72.6% were women, with a mean age of 39 years (range, 16-64 years). Sex was not reported for 1537 patients (8%). The baseline mean body mass index for 16 944 patients was 46.9 (range, 32.3-68.8). A random effects model was used in the meta-analysis. The mean (95% confidence interval) percentage of excess weight loss was 61.2% (58.1%-64.4%) for all patients; 47.5% (40.7%-54.2%) for patients who underwent gastric banding; 61.6% (56.7%-66.5%), gastric bypass; 68.2% (61.5%-74.8%), gastroplasty; and 70.1% (66.3%-73.9%), biliopancreatic diversion or duodenal switch. Operative mortality (< or =30 days) in the extracted studies was 0.1% for the purely restrictive procedures, 0.5% for gastric bypass, and 1.1% for biliopancreatic diversion or duodenal switch. Diabetes was completely resolved in 76.8% of patients and resolved or improved in 86.0%. Hyperlipidemia improved in 70% or more of patients. Hypertension was resolved in 61.7% of patients and resolved or improved in 78.5%. Obstructive sleep apnea was resolved in 85.7% of patients and was resolved or improved in 83.6% of patients. Effective weight loss was achieved in morbidly obese patients after undergoing bariatric surgery. A substantial majority of patients with diabetes, hyperlipidemia, hypertension, and obstructive sleep apnea experienced complete resolution or improvement.
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        Inhibition of gastric inhibitory polypeptide signaling prevents obesity.

        Secretion of gastric inhibitory polypeptide (GIP), a duodenal hormone, is primarily induced by absorption of ingested fat. Here we describe a novel pathway of obesity promotion via GIP. Wild-type mice fed a high-fat diet exhibited both hypersecretion of GIP and extreme visceral and subcutaneous fat deposition with insulin resistance. In contrast, mice lacking the GIP receptor (Gipr(-/-)) fed a high-fat diet were clearly protected from both the obesity and the insulin resistance. Moreover, double-homozygous mice (Gipr(-/-), Lep(ob)/Lep(ob)) generated by crossbreeding Gipr(-/-) and obese ob/ob (Lep(ob)/Lep(ob)) mice gained less weight and had lower adiposity than Lep(ob)/Lep(ob) mice. The Gipr(-/-) mice had a lower respiratory quotient and used fat as the preferred energy substrate, and were thus resistant to obesity. Therefore, GIP directly links overnutrition to obesity and it is a potential target for anti-obesity drugs.
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          Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass.

          To evaluate the physiologic importance of the satiety gut hormones. Controversy surrounds the physiologic role of gut hormones in the control of appetite. Bariatric surgery remains the most effective treatment option for obesity, and gut hormones are implicated in the reduction of appetite and weight after Roux-en-Y gastric bypass. We correlated peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) changes within the first week after gastric bypass with changes in appetite. We also evaluated the gut hormone responses of patients with good or poor weight loss after gastric bypass. Finally, we inhibited the gut hormone responses in gastric bypass patients and then evaluated appetite and food intake. Postprandial PYY and GLP-1 profiles start rising as early as 2 days after gastric bypass (P < 0.05). Changes in appetite are evident within days after gastric bypass surgery (P < 0.05), and unlike other operations, the reduced appetite continues. However, in patients with poor weight loss after gastric bypass associated with increased appetite, the postprandial PYY and GLP-1 responses are attenuated compared with patients with good weight loss (P < 0.05). Inhibiting gut hormone responses, including PYY and GLP-1 after gastric bypass, results in return of appetite and increased food intake (P < 0.05). The attenuated appetite after gastric bypass is associated with elevated PYY and GLP-1 concentrations, and appetite returns when the release of gut hormones is inhibited. The results suggest a role for gut hormones in the mechanism of weight loss after gastric bypass and may have implications for the treatment of obesity.
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            Author and article information

            Affiliations
            [1 ]Department of Endocrinology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China
            [2 ]Antioxidant and Gene Regulation Laboratory, Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana, United States of America
            [3 ]School of Biomedical Sciences, University of Ulster, Coleraine, United Kingdom
            [4 ]Neurobiology of Nutrition Laboratory, Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana, United States of America
            College of Tropical Agriculture and Human Resources, University of Hawaii, UNITED STATES
            Author notes

            Competing Interests: The authors have declared that no competing interests exist.

            Conceived and designed the experiments: JZ ZH H-RB JY. Performed the experiments: JZ ZH. Analyzed the data: JZ ZH H-RB JY. Contributed reagents/materials/analysis tools: NI. Wrote the paper: NI H-RB JY.

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, CA USA )
            1932-6203
            12 August 2015
            2015
            : 10
            : 8
            26266950 4534413 10.1371/journal.pone.0134728 PONE-D-15-03764

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

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            Figures: 7, Tables: 0, Pages: 14
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            Funding
            The authors appreciate technical support from Ms. Xin Ye in qRT-PCR and GIP ELISA assays. This work was supported by NIH grant (DK068036 and DK085495) to JY. qRT-PCR was conducted in the Genetic Core that was supported in part by NORC (NIH 2P30DK072476) center grants from the National Institutes of Health.
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