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Gastric Inhibitory Polypeptide and Effects of Glycation on Glucose Transport and Metabolism in Isolated Mouse Abdominal Muscle

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Gastric Inhibitory Polypeptide and Effects of Glycation on Glucose Transport and Metabolism in Isolated Mouse Abdominal Muscle 237 Gastric inhibitory polypeptide and effects of glycation on glucose transport and metabolism in isolated mouse abdominal muscle F P M O’Harte, A M Gray and P R Flatt School of Biomedical Sciences, University of Ulster, Coleraine, Co. Londonderry, BT52 1SA, UK (Requests for offprints should be addressed toFPMO’Harte) Abstract This study investigates the effects of gastric inhibitory effect on glucose oxidation was diminished by 32% with polypeptide (GIP) and glycated GIP (glucitol adduct of 10"8 mol/l glycated GIP (P<0·05). GIP (10"9 and 10"8 GIP) on glucose uptake and metabolism in muscle. Gly- mol/l) induced a 1·4- to 1·8-fold increase in [14C]glucose cated GIP (molecular mass 5147·2 Da) was purified by incorporation into muscle glycogen (glycogenesis) com- HPLC following in vitro incubation under hyperglycaemic pared with controls. Glycated GIP (10"8 mol/l) exhibited reducing conditions (24 h at pH 7·4). GIP (10"10–10"8 a 41% decrease in glycogenic activity (P<0·01). GIP mol/l) significantly stimulated (1·4- to 1·5-fold, P<0·001) (10"10–10"8 mol/l) stimulated lactate production in 2-deoxy-D-[1-3H]glucose uptake in abdominal muscle isolated abdominal muscle (1·2- to 1·3-fold, P<0·05); pieces from 3- to 5-week-old lean mice compared however glycated GIP did not exert a significant effect. with control incubations (without GIP). This stimu- This study demonstrates for the first time that GIP latory effect on glucose uptake at 10"10–10"9 mol/l was promotes glucose uptake, glucose oxidation and glycogen- decreased by 13–20% following glycation of the peptide esis in muscle tissue. Furthermore, modification of GIP (P<0·05). GIP (10"9 and 10"8 mol/l) induced a stepwise through glycation diminishes its biological effectiveness. 1·4- to 1·7-fold increase (P<0·01, P<0·001 respectively) Journal of Endocrinology (1998) 156, 237–243 in [14C]glucose oxidation compared with controls. This Introduction dependent transport mechanism resulting in a sharp rise in plasma immunoreactive GIP and insulin concentrations Incretins are endogenous peptides released from the (Cataland et al. 1974). The secretory response to fats is gastrointestinal tract into the circulation following a meal, greater and more prolonged than glucose and may reflect which potentiate glucose-stimulated insulin secretion. the fact that fat slows gastric emptying and thus provides Currently there are two well established incretin an extended stimulus for GIP release (Penman et al. 1981, hormones, gastric inhibitory polypeptide (GIP; glucose- Pedersen 1994). Ingestion of protein alone is a relatively dependent insulinotrophic polypeptide) and glucagon-like weak stimulus for GIP release, although nearly all amino peptide-1(7–36)amide (tGLP-1). The forty-two amino acids possess some GIP-releasing activity (Flatt et al. 1991). acid GIP was initially isolated from porcine intestine for its Studies of the biological activity of GIP have identified ability to inhibit gastric acid secretion (Brown et al. 1970), a number of extrapancreatic target tissues including but its most important physiological role resides in its stomach, adipose tissue and liver. GIP can inhibit gastric insulinotrophic activity (Morgan et al. 1988). GIP acts acid secretion in man but only at supra-physiological under mild or moderate hyperglycaemic conditions concentrations (Maxwell et al. 1980, Nauck et al. 1992). through specific receptors on the pancreatic B-cell However, GIP has a number of other potentially import- (Wheeler et al. 1995) to stimulate insulin secretion and ant actions which mirror some of the effects of insulin. enhance proinsulin gene expression (Andersen et al. 1978). These include the stimulation of glucose uptake in GIP secretion is stimulated from the endocrine K cells of adipocytes, increased synthesis of fatty acids and activation the duodenum and jejunum by the active transport of of lipoprotein lipase in adipose tissue (Eckel et al. 1979, macronutrients rather than just their presence in the gut Oben et al. 1991, Morgan 1996). Both exogenous and lumen (Sykes et al. 1980). The most important stimuli for endogenous GIP promote plasma triglyceride clearance in GIP release are carbohydrate (Sykes et al. 1980), fat and response to oral fat loading, indicating that fat-induced triglycerides (Krarup et al. 1985, Kwasowski et al. 1985) GIP secretion plays a physiological role in lipid metabolism and proteins (Flatt et al. 1991). Oral glucose is absorbed in adipose tissue (Ebert et al. 1991). In liver, GIP has from the small intestine through an active sodium- been shown to enhance insulin-dependent inhibition of Journal of Endocrinology (1998) 156, 237–243 ? 1998 Journal of Endocrinology Ltd Printed in Great Britain 0022–0795/98/0156–0237 $08.00/0 Downloaded from Bioscientifica.com at 09/28/2021 05:09:00PM via free access 238 F P M O’HARTE and others · GIP and glucose metabolism in muscle glycogenolysis (Elahi et al. 1986). GIP also reduces both (C18) analytical column (The Separations Group, glucagon-stimulated lipolysis in adipose tissue as well as Hesperia, CA, USA) and eluted at a flow rate of 1·0 ml/ hepatic glucose production (Hartmann et al. 1986). min. The mobile phase consisted of solvent A: 0·12% (v/v) The other major incretin hormone, tGLP-1, has been TFA in water; solvent B consisted of 0·1% (v/v) TFA in reported to have potent stimulatory effects on glucose 70% acetonitrile, 29·9% water. Elution profiles were oxidation, glycogen synthesis and lactate formation in monitored at 206 nm and peptide peaks collected by hand. rat skeletal muscle (Villanueva-Pen˜acarrillo et al. 1994) GIP and glycated GIP were separated using linear gradi- mediated through specific tGLP-1 receptors (Delgado ents of 0% to 31·5% acetonitrile over 10 min, followed by et al. 1995). The present study was carried out to investi- 31·5% to 45·5% acetonitrile over 20 min. Two major gate the possible influence of GIP on glucose uptake and peaks were collected eluting after 16·7 min and 16·9 min metabolism in skeletal muscle. Since recent studies in our corresponding to glycated GIP and GIP respectively. laboratory have demonstrated that peptide hormones such Fractions of glycated GIP were pooled, taken to dryness as proinsulin and insulin can be glycated during the stages using a Speed-Vac (AES 1000 Savant, Life Sciences of synthesis and storage in secretory cells (Abdel-Wahab International, Runcorn, Cheshire, UK) and reconstituted et al. 1996a, 1997), we have also investigated whether GIP in 0·12% (v/v) TFA/water. Glycated GIP was purified can be glycated. A recent study demonstrated that modi- to homogeneity by repeated HPLC runs on a (4·6# fication of tGLP-1 through glycation reduces it effective- 150 mm) Supelcosil (C8) analytical column (Supelco Inc., ness at promoting glucose uptake and utilization in isolated Poole, Dorset, UK). GIP and glycated GIP were quanti- muscle tissue (O’Harte et al. 1997) and in this context it fied by comparison of peak areas obtained from reverse- was of interest to examine the efficacy of the glycated phase (RP)-HPLC with a standard curve using known form of the other major incretin hormone, GIP, on muscle concentrations of GIP. glucose metabolism. The present study demonstrates for the first time that GIP promotes glucose uptake and Electrospray ionization mass spectrometry (ESI-MS) metabolism in isolated muscle from mice and that glyca- tion of GIP (glucitol adduct of GIP) reduces its biological Samples of GIP and glycated GIP for ESI-MS were activity in muscle in vitro. dissolved in 100 µl 0·1% (v/v) TFA/water and applied to the LC/MS using gradient elution HPLC (C18 column, 150#2·0 mm). Samples (10 µl injection) were applied Materials and Methods at a flow rate of 0·2 ml/min, using a linear gradient from 0% to 90% acetonitrile over 10 min and holding at 90% Reagents acetonitrile for 10 min. Mass spectra were recorded on a Finnigan Mat LCQ benchtop mass spectrometer (Finnigan HPLC grade acetonitrile was obtained from Rathburn Mat, Hemel Hempstead, Herts, UK) and spectra were (Walkersburn, Scotland). Sequencing grade trifluoroacetic obtained from the quadripole ion trap mass analyzer. acid (TFA) was obtained from Aldrich (Poole, Dorset, Spectra were collected using full ion scan mode UK). All water used in these experiments was purified (400–1850 m/z mode) and UV absorbance (280 nM). using a Milli-Q Water Purification System (Millipore Corporation, Millford, MA, USA). Human insulin (E. coli recombinant) and sodium cyanoborohydride were ob- Animals tained from Sigma (Poole, Dorset, UK). Human GIP was Male lean mice aged between 3 and 5 weeks were obtained from the American Peptide Company (Sunnyvale, 3 obtained from the Behavioural and Biomedical Research CA, USA). Radiolabelled 2-deoxy--[1- H]glucose, Unit, University of Ulster, Coleraine. The animals were -[U14C]glucose and L-[114C]glucose were obtained from housed in an air-conditioned room at 22&2 )C and were Amersham Life Science (Amersham, Bucks, UK). fed a standard rodent maintenance diet from weaning (3 weeks) (Specialist Diet Services, Witham, Essex, UK). Food and tap water were available ad libitum. Animals were Preparation of glycated GIP killed by cervical dislocation and the abdominal muscle Human GIP (50 µg) was incubated with 220 mmol/l quickly excised. The muscle was dissected into 10 pieces -glucose together with a 1000-fold molar excess of of approximately 10 mg each (accurately weighed) and NaBH3CN (dissolved in 10 mmol/l NaOH) in 10 mmol/l used for either glucose uptake or metabolism studies. sodium phosphate buffer pH 7·4 for 24 h at 37 )C (total volume 1·0 ml).
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