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Effects of Glucose and Glucoregulatory Hormones Release of Somatostatin-like Immunoreactivity from Incubated Rat Hypothalamus and Cerebral Cortex: EFFECTS OF GLUCOSE AND GLUCOREGULATORY HORMONES Michael Berelowitz, … , Daniel Dudlak, Lawrence A. Frohman J Clin Invest. 1982;69(6):1293-1301. https://doi.org/10.1172/JCI110569. Somatostatin (SRIF) is localized in the hypothalamus, extrahypothalamic brain, and throughout the gastrointestinal tract. Release of gastrointestinal SRIF-like immunoreactivity (SRIF-LI) is under nutrient regulation but the effect of nutrients on neural SRIF-LI is unknown. The present studies examined the effects of glucose uptake and metabolism and hormones influencing glucose disposition on SRIF-LI release from medial basal hypothalamus (MBH) and cerebral cortex (Cx) incubated in Krebs-Ringer bicarbonate containing bacitracin. After a preincubation to achieve stable secretion, tissues were incubated for 20 min in 14 mM glucose (basal) and then, for 20 min in fresh medium with test materials. MBH SRIF- LI release was inversely related to medium glucose concentration with release in the absence of glucose (235±42 pg/MBH per 20 min) more than five times that in the presence of 25 mM glucose (46±4 pg/20 min). In the presence of 14 mM glucose MBH SRIF-LI release was stimulated above basal by agents interfering with glucose uptake including 3-O- methyl-d-glucose (42 mM; 70±5 vs. 42±3 pg/20 min,P < 0.05), phlorizin (50 mM; 351±63 vs. 29±2 pg/20 min,P < 0.001) or cytochalasin B (20 μM; 110±7 vs. 22±2 pg/20 min, P < 0.001). Inhibition of glucose metabolism by 2-deoxy-d-glucose resulted in dose-related stimulation of MBH SRIF-LI release (maximal at 28 mM; 201±28 pg/20 min vs. 32±4 pg/20 min, P < 0.001). Viability of […] Find the latest version: https://jci.me/110569/pdf Release of Somatostatin-like Immunoreactivity from Incubated Rat Hypothalamus and Cerebral Cortex EFFECTS OF GLUCOSE AND GLUCOREGULATORY HORMONES MICHAEL BERELOWITZ, DANIEL DUDLAK, and LAWRENCE A. FROHMAN, Division of Endocrinology and Metabolism, Department of Medicine, Michael Reese Hospital and Medical Center, University of Chicago, Illinois 60616 A B S T R A C T Somatostatin (SRIF) is localized in the tion of SRIF-LI responsiveness to stimulation by hypothalamus, extrahypothalamic brain, and through- potassium (60 mM) or neurotensin (5 ,M). In contrast, out the gastrointestinal tract. Release of gastrointes- Cx SRIF-LI release was slightly inhibited by decreases tinal SRIF-like immunoreactivity (SRIF-LI) is under in medium glucose and unaffected by inhibition of nutrient regulation but the effect of nutrients on glucose uptake or metabolism. These results provide neural SRIF-LI is unknown. The present studies ex- evidence for nutrient regulation of MBH but not Cx amined the effects of glucose uptake and metabolism SRIF-LI release and may explain inhibition of growth and hormones influencing glucose disposition on SRIF- hormone seen in the rat in response to hypoglycemia. LI release from medial basal hypothalamus (MBH) and Insulin (10 nM-1 gM) stimulated MBH but not Cx cerebral cortex (Cx) incubated in Krebs-Ringer bicar- SRIF-LI release while glucagon was without effect. bonate containing bacitracin. After a preincubation to Our previous demonstration that MBH SRIF-LI re- achieve stable secretion, tissues were incubated for 20 lease was stimulated by somatomedin-C, but not in- min in 14 mM glucose (basal) and then, for 20 min in sulin at physiologic concentrations, is consistent with fresh medium with test materials. MBH SRIF-LI re- an action of insulin through the somatomedin-C re- lease was inversely related to medium glucose con- ceptor at the doses studied. Our studies indicate a re- centration with release in the absence of glucose gional specificity for the control of SRIF secretion (235±42 pg/MBH per 20 min) more than five times within the brain and suggests the possibility of a role that in the presence of 25 mM glucose (46±4 pg/20 for hypothalamic SRIF in metabolic regulation. min). In the presence of 14 mM glucose MBH SRIF- LI release was stimulated above basal by agents in- INTRODUCTION terfering with glucose uptake including 3-0-methyl- D-glucose (42 mM; 70±5 vs. 42±3 pg/20 min, P Somatostatin (SRIF),' the inhibitory hypothalamic reg- <0.05), phlorizin (50 mM; 351±63 vs. 29±2 pg/20 ulator of pituitary growth hormone (1, 2) and thyro- min, P < 0.001) or cytochalasin B (20 ,M; 110±7 vs. tropin (3, 4) release, is one of a group of peptides 22±2 pg/20 min, P < 0.001). Inhibition of glucose present in high concentration in the central nervous metabolism by 2-deoxy-D-glucose resulted in dose-re- system (CNS), the pancreas, and gastrointestinal tract lated stimulation of MBH SRIF-LI release (maximal (5). Although the highest concentration of CNS SRIF- at 28 mM; 201±28 pg/20 min vs. 32±4 pg/20 min, like immunoreactivity (SRIF-LI) is present in the me- P < 0.001). Viability of MBH was unimpaired by in- dian eminence (6), reflecting its hypophysiotropic role, cubation in the absence of glucose or following ex- the total content of SRIF-LI is considerably greater in posure to 2-deoxy-D-glucose as determined by reten- the cerebral cortex (6). SRIF-LI is also present in D cells of the pancreatic islets (7) and throughout the Dr. Berelowitz and Dr. Frohman's current address is Di- gastrointestinal tract, with highest concentrations in vision of Endocrinology and Metabolism, Department of In- the stomach (5, 6). ternal Medicine, University of Cincinnati College of Med- icine, Cincinnati, OH 45267. Address reprint requests to Dr. Berelowitz. 1 Abbreviations used in this paper: CNS, central nervous Received for publication 28 September 1981 and in re- system; SRIF, somatostatin; SRIF-LI, somatostatin-like im- vised form 18 December 1981. munoreactivity. J. Clin. Invest. © The American Society for Clinical Investigation, Inc. * 0021-9738/82/06/1293/09 $1.00 1293 Volume 69 June 1982 1293-1301 Pancreatic and gastrointestinal SRIF exert an im- of the medium was varied as appropriate to provide a con- portant role in nutrient homeostasis (8). Pancreatic stant osmolality. After a preincubation to achieve stable se- cretion (60 min for hypothalamus, 80 min for cerebral cor- SRIF inhibits the release of insulin (9) and glucagon tex), tissues were incubated for 20 min (basal) in fresh (10), possibly through a local or paracrine effect, medium containing 14 mM glucose. At the end of the basal thereby influencing nutrient disposition. Gastric SRIF period medium was removed, fresh medium containing the regulates acid secretion directly (11) and through local stimulus under investigation was added and the tissue was inhibition of antral gastrin release (12). In addition, incubated for an additional 20 min. In some experiments one or two additional 20-min incubations were performed gastrointestinal SRIF appears to have an inhibitory in medium containing 14 mM glucose with or without added hormonal influence on nutrient, especially lipid, ab- stimuli. Media were removed after each incubation period, sorption (13). The demonstration that nutrients, in boiled for 5 min, centrifuged and the supernatants stored turn, stimulate the release of gastrointestinal SRIF-LI at -20°C until assayed. (14, 15) further Drugs. Stimuli used in the studies described included 60 supports a role for SRIF in nutrient mM KC1, neurotensin (5 uM, kindly provided by J. Rivier, regulation. Glucose stimulates pancreatic SRIF-LI (14) Salk Institute), 3-O-methyl-D-glucose (42 mM), phlorizin (50 while lipids, especially free fatty acids, stimulate in- mM), and 2-deoxy-D-glucose (3-42 mM) (Sigma Chemical testinal SRIF-LI release (15). Co., St. Louis, MO), cytochalasin B (20 uM, Aldrich Chem- The role of CNS SRIF-LI in nutrient homeostasis is ical Co., Inc., Milwaukee, WI), cytochalasin D (20 ,M, Cal- biochem-Behring Corp., American Hoechst Corp., San Diego, unknown. While hypothalamic SRIF-LI release has CA), crystalline porcine insulin and bovine-porcine glucagon been demonstrated in response to a variety of stimuli (10 nM-1 ,uM, provided by Eli Lilly Research Laboratories, including membrane depolarization (60 mM K+) (16, Indianapolis, IN). 17), biogenic amines (dopamine) (17), peptides (neu- Radioimmunoassay. SRIF radioimmunoassay was per- rotensin) (17), and hormones [growth formed as previously described (22). The assay sensitivity hormone (18, was 1-2 pg SRIF/tube; 12-18 pg SRIF produced 50% dis- 19), somatomedins (20, 21), triiodothyronine (22)], and placement from maximal binding. The interassay variation cerebral cortical SRIF-LI release occurs in response to was 12% and the intraassay variation was 9%. depolarizing stimuli (23), there is a paucity of infor- Statistics. Comparisons between groups were performed mation available concerning the response of hypo- using Student's nonpaired t test and, where appropriate, an thalamic or extrahypothalamic CNS SRIF-LI to nu- analysis of variance. trients. The present studies were designed to investigate the RESULTS effects of glucose uptake and metabolism and of the Effect of medium glucose concentration on hormonal regulators of glucose utilization on SRIF-LI SRIF-LI release from hypothalamus and release in vitro from incubated rat hypothalamus and cerebral cortex. cerebral cortex Following a 20-min basal incubation period in me- METHODS dium containing 14 mM glucose, media were removed and replaced with fresh medium without glucose or Experimental animals. Male Sprague-Dawley rats, with glucose concentrations ranging from 3 to 25 mM. weighing 150-200 g were housed under constant tempera- Hypothalamic SRIF-LI release was inversely ture (24°C) and light (14 h)-dark (10 h) cycles and were related provided free access to laboratory rat chow and water. An- to medium glucose concentration (Fig. 1A) with re- imals from a single supplier (Locke Erikson, Melrose Park, lease in the absence of glucose (235±42 pg/hypo- IL) were used in all experiments.
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