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Gastric leptin: a putative role in the short-term regulation of food intake

Published online by Cambridge University Press:  09 March 2007

Catalina Picó ,
Paula Oliver ,
Juana Sánchez  and
Andreu Palou
Catalina Picó
Affiliation:
Department of Fundamental Biology and Health Sciences, University of the Balearic Islands, Palma de Mallorca, Spain
Paula Oliver
Affiliation:
Department of Fundamental Biology and Health Sciences, University of the Balearic Islands, Palma de Mallorca, Spain
Juana Sánchez
Affiliation:
Department of Fundamental Biology and Health Sciences, University of the Balearic Islands, Palma de Mallorca, Spain
Andreu Palou*
Affiliation:
Department of Fundamental Biology and Health Sciences, University of the Balearic Islands, Palma de Mallorca, Spain
*
*Corresponding author: Professor Andreu Palou, fax +34 971173184, email andreu.palou@uib.es
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Abstract

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The discovery of the production of leptin by the stomach, in addition to its production by adipose tissue, has initiated new investigation into the possible role of this protein in the digestive physiology, in particular in the short-term control of energy balance. Leptin has been identified in the lower half of the stomach glands both in the pepsinogen granules of chief cells and in the granules of a specific endocrine cell type, suggesting that leptin action is exerted by both exocrine and endocrine pathways. Gastric leptin is sensitive to the nutritional state, being rapidly mobilized in response to food intake following fasting, or after the administration of satiety factors; this suggests a role for this protein in the short-term regulation of feeding, acting in collaboration with satiety peptides such as cholecystokinin. Leptin, produced by gastric cells and by adipocytes, could act on both acute and chronic regulation of feeding behaviour respectively, giving information to the brain on the availability of external (food) and internal (fat depots) energy resources, thus participating in short- and long-term satiation.

Keywords

LeptinStomachFood intakeSatietyEnergy balance
Type
Review article
Information
British Journal of Nutrition , Volume 90 , Issue 4 , October 2003 , pp. 735 - 741
Copyright
Copyright © The Nutrition Society 2003

References

Adibi, SA (1997) The oligopeptide transporter (Pept-1) in human intestine: biology and function. Gastroenterology 113, 332–340.CrossRefGoogle ScholarPubMed
Ahima, RS & Flier, JS (2000) Leptin. Annu Rev Physiol 62, 413–437.CrossRefGoogle ScholarPubMed
Ariyasu, H, Takaya, K, Tagami, T, et al. (2001) Stomach is a major source of circulating ghrelin, and feeding state determines plasma ghrelin-like immunoreactivity levels in humans. J Clin Endocrinol Metab 86, 4753–4758.CrossRefGoogle Scholar
Attoub, S, Levasseur, S, Buyse, M, et al. (1999) Physiological role of cholecystokinin B/gastrin receptor in leptin secretion. Endocrinology 140, 4406–4410.CrossRefGoogle ScholarPubMed
Bado, A, Levasseur, S, Attoub, S, et al. (1998) The stomach is a source of leptin. Nature 394, 790–793.CrossRefGoogle ScholarPubMed
Barrachina, MD, Martinez, V, Wang, L, Wei, JY & Tache, Y (1997) Synergistic interaction between leptin and cholecystokinin to reduce short-term food intake in lean mice. Proc Natl Acad Sci USA 94, 10455–10460.CrossRefGoogle ScholarPubMed
Batterham, RL, Cowley, MA, Small, CJ, et al. (2002) Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418, 650–654.CrossRefGoogle ScholarPubMed
Berthoud, HR & Powley, TL (1992) Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. J Comp Neurol 319, 261–276.CrossRefGoogle ScholarPubMed
Boden, G, Chen, X, Mozzoli, M & Ryan, I (1996) Effect of fasting on serum leptin in normal human subjects. J Clin Endocrinol Metab 81, 3419–3423.Google ScholarPubMed
Buyse, M, Berlioz, F, Guilmeau, S, et al. (2001 a) PepT1-mediated epithelial transport of dipeptides and cephalexin is enhanced by luminal leptin in the small intestine. J Clin Invest 108, 1483–1494.CrossRefGoogle ScholarPubMed
Buyse, M, Ovesjo, ML, Goiot, H, et al. (2001 b) Expression and regulation of leptin receptor proteins in afferent and efferent neurons of the vagus nerve. Eur J Neurosci 14, 64–72.CrossRefGoogle ScholarPubMed
Campfield, LA & Smith, FJ (1990) Transient declines in blood glucose signal meal initiation. Int J Obes 14, Suppl. 3, 15–31.Google Scholar
Campfield, LA & Smith, FJ (2003) Blood glucose dynamics and control of meal initiation: a pattern detection and recognition theory. Physiol Rev 83, 25–58.CrossRefGoogle ScholarPubMed
Campfield, LA, Smith, FJ, Rosenbaum, M & Hirsch, J (1996) Human eating: evidence for a physiological basis using a modified paradigm. Neurosci Biobehav Rev 20, 133–137.CrossRefGoogle ScholarPubMed
Casabiell, X, Pineiro, V, Tome, MA, Peino, R, Dieguez, C & Casanueva, FF (1997) Presence of leptin in colostrum and/or breast milk from lactating mothers: a potential role in the regulation of neonatal food intake. J Clin Endocrinol Metab 82, 4270–4273.CrossRefGoogle ScholarPubMed
Cinti, S, de Matteis, R, Ceresi, E, et al. (2001) Leptin in the human stomach. Gut 49, 155.CrossRefGoogle ScholarPubMed
Cinti, S, de Matteis, R, Pico, C, et al. (2000) Secretory granules of endocrine and chief cells of human stomach mucosa contain leptin. Int J Obes Relat Metab Disord 24, 789–793.CrossRefGoogle ScholarPubMed
Considine, RV, Sinha, MK, Heiman, ML, et al. (1996) Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334, 292–295.CrossRefGoogle ScholarPubMed
Corp, ES, McQuade, J, Moran, TH & Smith, GP (1993) Characterization of type A and type B CCK receptor binding sites in rat vagus nerve. Brain Res 623, 161–166.CrossRefGoogle ScholarPubMed
Crawley, JN (1999) The role of galanin in feeding behavior. Neuropeptides 33, 369–375.CrossRefGoogle ScholarPubMed
Cummings, DE, Purnell, JQ, Frayo, RS, Schmidova, K, Wisse, BE & Weigle, DS (2001) A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50, 1714–1719.CrossRefGoogle ScholarPubMed
Date, Y, Kojima, M, Hosoda, H, et al. (2000) Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 141, 4255–4261.CrossRefGoogle Scholar
Frederich, RC, Lollmann, B, Hamann, A, et al. (1995) Expression of ob mRNA and its encoded protein in rodents. Impact of nutrition and obesity. J Clin Invest 96, 1658–1663.CrossRefGoogle Scholar
Gibbs, J, Young, RC & Smith, GP (1973) Cholecystokinin decreases food intake in rats. J Comp Physiol Psychol 84, 488–495.CrossRefGoogle ScholarPubMed
Gundlach, AL, Burazin, TC & Larm, JA (2001) Distribution, regulation and role of hypothalamic galanin systems: renewed interest in a pleiotropic peptide family. Clin Exp Pharmacol Physiol 28, 100–105.CrossRefGoogle Scholar
Hampton, LL, Ladenheim, EE, Akeson, M, et al. (1998) Loss of bombesin-induced feeding suppression in gastrin-releasing peptide receptor-deficient mice. Proc Natl Acad Sci USA 95, 3188–3192.CrossRefGoogle ScholarPubMed
Hardie, LJ, Rayner, DV, Holmes, S & Trayhurn, P (1996) Circulating leptin levels are modulated by fasting, cold exposure and insulin administration in lean but not Zucker (fa/fa) rats as measured by ELISA. Biochem Biophys Res Commun 223, 660–665.CrossRefGoogle Scholar
Himms-Hagen, J (1999) Physiological roles of the leptin endocrine system: differences between mice and humans. Crit Rev Clin Lab Sci 36, 575–655.CrossRefGoogle ScholarPubMed
Kamegai, J, Tamura, H, Shimizu, T, Ishii, S, Sugihara, H & Wakabayashi, I (2001) Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and Agouti-related protein mRNA levels and body weight in rats. Diabetes 50, 2438–2443.CrossRefGoogle ScholarPubMed
Kojima, M, Hosoda, H, Date, Y, Nakazato, M, Matsuo, H & Kangawa, K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402, 656–660.CrossRefGoogle ScholarPubMed
Kolaczynski, JW, Considine, RV, Ohannesian, J, et al. (1996 a) Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketones themselves. Diabetes 45, 1511–1515.CrossRefGoogle Scholar
Kolaczynski, JW, Ohannesian, JP, Considine, RV, Marco, CC & Caro, JF (1996 b) Response of leptin to short-term and prolonged overfeeding in humans. J Clin Endocrinol Metab 81, 4162–4165.Google ScholarPubMed
Kopin, AS, Mathes, WF, McBride, EW, et al. (1999) The cholecystokinin-A receptor mediates inhibition of food intake yet is not essential for the maintenance of body weight. J Clin Invest 103, 383–391.CrossRefGoogle Scholar
Lee, HM, Wang, G, Englander, EW, Kojima, M & Greeley, GH Jr (2002) Ghrelin, a new gastrointestinal endocrine peptide that stimulates insulin secretion: enteric distribution, ontogeny, influence of endocrine, and dietary manipulations. Endocrinology 143, 185–190.CrossRefGoogle ScholarPubMed
Lewin, MJ & Bado, A (2001) Gastric leptin. Microsc Res Tech 53, 372–376.CrossRefGoogle ScholarPubMed
Lostao, MP, Urdaneta, E, Martinez-Anso, E, Barber, A & Martinez, JA (1998) Presence of leptin receptors in rat small intestine and leptin effect on sugar absorption. FEBS Lett 423, 302–306.CrossRefGoogle ScholarPubMed
Maffei, M, Halaas, J, Ravussin, E, et al. (1995) Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1, 1155–1161.CrossRefGoogle ScholarPubMed
Masuzaki, H, Ogawa, Y, Sagawa, N, et al. (1997) Nonadipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans. Nat Med 3, 1029–1033.CrossRefGoogle ScholarPubMed
Moran, TH (2000) Cholecystokinin and satiety: current perspectives. Nutrition 16, 858–865.CrossRefGoogle ScholarPubMed
Morton, NM, Emilsson, V, Liu, YL & Cawthorne, MA (1998) Leptin action in intestinal cells. J Biol Chem 273, 26194–26201.CrossRefGoogle ScholarPubMed
Ohki-Hamazaki, H, Sakai, Y, Kamata, K, et al. (1999) Functional properties of two bombesin-like peptide receptors revealed by the analysis of mice lacking neuromedin B receptor. J Neurosci 19, 948–954.CrossRefGoogle ScholarPubMed
Oliver, P, Picó, C, De Matteis, R, Cinti, S & Palou, A (2002) Perinatal expression of leptin in rat stomach. Dev Dyn 223, 148–154.CrossRefGoogle ScholarPubMed
Palou, A, Serra, F, Bonet, ML & Picó, C (2000) Obesity: molecular bases of a multifactorial problem. Eur J Nutr 39, 127–144.CrossRefGoogle ScholarPubMed
Phillips, RJ & Powley, TL (1996) Gastric volume rather than nutrient content inhibits food intake. Am J Physiol 271, R766–R769.Google ScholarPubMed
Picó, C, Sanchez, J, Oliver, P & Palou, A (2002) Leptin production by the stomach is up-regulated in obese (fa/fa) Zucker rats. Obes Res 10, 932–938.CrossRefGoogle ScholarPubMed
Qu, D, Ludwig, DS, Gammeltoft, S, et al. (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380, 243–247.CrossRefGoogle ScholarPubMed
Rentsch, J & Chiesi, M (1996) Regulation of ob gene mRNA levels in cultured adipocytes. FEBS Lett 379, 55–59.CrossRefGoogle Scholar
Sahu, A (1998) Leptin decreases food intake induced by melanin-concentrating hormone (MCH), galanin (GAL) and neuropeptide Y (NPY) in the rat. Endocrinology 139, 4739–4742.CrossRefGoogle Scholar
Sakurai, T, Amemiya, A, Ishii, M, et al. (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573–585.CrossRefGoogle Scholar
Saladin, R, De Vos, P, Guerre-Millo, M, et al. (1995) Transient increase in obese gene expression after food intake or insulin administration. Nature 377, 527–529.CrossRefGoogle ScholarPubMed
Scrocchi, LA, Brown, TJ, MacLusky, N, et al. (1996) Glucose intolerance but normal satiety in mice with a null mutation in the glucagon-like peptide 1 receptor gene. Nat Med 2, 1254–1258.CrossRefGoogle Scholar
Shintani, M, Ogawa, Y, Ebihara, K, et al. (2001) Ghrelin, an endogenous growth hormone secretagogue, is a novel orexigenic peptide that antagonizes leptin action through the activation of hypothalamic neuropeptide Y/Y1 receptor pathway. Diabetes 50, 227–232.CrossRefGoogle ScholarPubMed
Sobhani, I, Bado, A, Vissuzaine, C, et al. (2000) Leptin secretion and leptin receptor in the human stomach. Gut 47, 178–183.CrossRefGoogle ScholarPubMed
Sobhani, I, Buyse, M, Goiot, H, et al. (2002) Vagal stimulation rapidly increases leptin secretion in human stomach. Gastroenterology 122, 259–263.CrossRefGoogle ScholarPubMed
Stanley, BG, Kyrkouli, SE, Lampert, S & Leibowitz, SF (1986) Neuropeptide Y chronically injected into the hypothalamus: a powerful neurochemical inducer of hyperphagia and obesity. Peptides 7, 1189–1192.CrossRefGoogle ScholarPubMed
Tartaglia, LA, Dembski, M, Weng, X, et al. (1995) Identification and expression cloning of a leptin receptor, OB-R. Cell 83, 1263–1271.CrossRefGoogle ScholarPubMed
Tschop, M, Smiley, DL & Heiman, ML (2000) Ghrelin induces adiposity in rodents. Nature 407, 908–913.CrossRefGoogle ScholarPubMed
Wang, G, Lee, HM, Englander, E & Greeley, GH (2002) Ghrelin – not just another stomach hormone. Regul Pept 105, 75–81.CrossRefGoogle Scholar
Wang, J, Liu, R, Hawkins, M, Barzilai, N & Rossetti, L (1998) A nutrient-sensing pathway regulates leptin gene expression in muscle and fat. Nature 393, 684–688.CrossRefGoogle ScholarPubMed
Wang, MY, Zhou, YT, Newgard, CB & Unger, RH (1996) A novel leptin receptor isoform in rat. FEBS Lett 392, 87–90.CrossRefGoogle ScholarPubMed
Wang, YH, Tache, Y, Sheibel, AB, Go, VL & Wei, JY (1997) Two types of leptin-responsive gastric vagal afferent terminals: an in vitro single-unit study in rats. Am J Physiol 273, R833–R837.Google Scholar
West, DB, Fey, D & Woods, SC (1984) Cholecystokinin persistently suppresses meal size but not food intake in free-feeding rats. Am J Physiol 246, R776–R787.Google Scholar
Woods, SC, Schwartz, MW, Baskin, DG & Seeley, RJ (2000) Food intake and the regulation of body weight. Annu Rev Psychol 51, 255–277.CrossRefGoogle ScholarPubMed
Woods, SC, Seeley, RJ, Porte, D Jr & Schwartz, MW (1998) Signals that regulate food intake and energy homeostasis. Science 280, 1378–1383.CrossRefGoogle ScholarPubMed
Wren, AM, Seal, LJ, Cohen, MA, et al. (2001 a) Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab 86, 5992.CrossRefGoogle ScholarPubMed
Wren, AM, Small, CJ & Abbott, CR (2001 b) Ghrelin causes hyperphagia and obesity in rats. Diabetes 50, 2540–2547.CrossRefGoogle ScholarPubMed
Yuan, CS, Attele, AS, Wu, JA, Zhang, L & Shi, ZQ (1999) Peripheral gastric leptin modulates brain stem neuronal activity in neonates. Am J Physiol 277, G626–G630.Google ScholarPubMed
Yuan, CS, Dey, L, Xie, JT & Aung, HH (2002) Gastric effects of galanin and its interaction with leptin on brainstem neuronal activity. J Pharmacol Exp Ther 301, 488–493.CrossRefGoogle ScholarPubMed
Zhang, Y, Proenca, R, Maffei, M, Barone, M, Leopold, L & Friedman, JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432.CrossRefGoogle ScholarPubMed