Abstract
The present review focuses on adipocytes-released peptides known to be involved in the control of gastrointestinal motility, acting both centrally and peripherally. Thus, four peptides have been taken into account: leptin, adiponectin, nesfatin-1, and apelin. The discussion of the related physiological or pathophysiological roles, based on the most recent findings, is intended to underlie the close interactions among adipose tissue, central nervous system, and gastrointestinal tract. The better understanding of this complex network, as gastrointestinal motor responses represent peripheral signals involved in the regulation of food intake through the gut-brain axis, may also furnish a cue for the development of either novel therapeutic approaches in the treatment of obesity and eating disorders or potential diagnostic tools.
Keywords: Adiponectin, apelin, gastrointestinal motility, leptin, nesfatin-1, smooth muscle.
Graphical Abstract
[1]
Rodríguez, A.; Ezquerro, S.; Méndez-Giménez, L.; Becerril, S.; Frühbeck, G. Revisiting the adipocyte: A model for integration of cytokine signalling in the regulation of energy metabolism. Am. J. Physiol. Endocrinol. Metab., 2015, 309, E691-E714.
[2]
Giralt, M.; Villarroya, F. White, brown, beige/brite: Different adipose cells for different functions? Endocrinology, 2013, 154, 2992-3000.
[3]
Frühbeck, G.; Gómez-Ambrosi, J.; Muruzabal, F.J.; Burrell, M.A. The adipocyte: A model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am. J. Physiol. Endocrinol. Metab., 2001, 280, E827-E847.
[4]
Di Franco, A.; Guasti, D.; Squecco, R.; Mazzanti, B.; Rossi, F.; Idrizaj, E.; Gallego-Escuredo, J.M.; Villarroya, F.; Bani, D.; Forti, G.; Vannelli, G.B.; Luconi, M. Searching for classical brown fat in humans: Development of a novel human fetal brown stem cell model. Stem Cells, 2016, 34, 1679-1691.
[5]
Wu, J.; Bostrom, P.; Sparks, L.M.; Ye, L.; Choi, J.H.; Giang, A.H.; Khandekar, M.; Virtanen, K.A.; Nuutila, P.; Schaart, G.; Huang, K.; Tu, H.; van Marken Lichtenbelt, W.D.; Hoeks, J.; Enerback, S.; Schrauwen, P.; Spiegelman, B.M. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell, 2012, 150, 366-376.
[6]
Zhang, Y.; Proenca, R.; Maffei, M.; Barone, M.; Leopold, L.; Friedman, J.M. Positional cloning of the mouse obese gene and its human homologue. Nature, 1994, 372(6505), 425-432.
[7]
Novelle, M.G.; Diéguez, C. Unravelling the role and mechanism of adipokine and gastrointestinal signals in animal models in the nonhomeostatic control of energy homeostasis: Implications for binge eating disorder. Eur. Eat. Disord. Rev., 2018, 26(6), 551-568.
[8]
Spalding, K.L.; Arner, E.; Westermark, P.O.; Bernard, S.; Buchholz, B.A.; Bergmann, O.; Blomqvist, L.; Hoffstedt, J.; Naslund, E.; Britton, T.; Concha, H.; Hassan, M.; Ryden, M.; Frisen, J:,. Arner, P. Dynamics of fat cell turnover in humans. Nature, 2008, 453, 783-787.
[9]
Gray, S.L.; Vidal-Puig, A.J. Adipose tissue expandability in the maintenance of metabolic homeostasis. Nutr. Rev., 2007, 107, S7-S12.
[10]
Furness, J.B. The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroenterol. Hepatol., 2012, 9(5), 286-294.
[11]
Furness, J.B.; Callaghan, B.P.; Rivera, L.R.; Cho, H.J. The enteric nervous system and gastrointestinal innervation: Integrated local and central control. Adv. Exp. Med. Biol., 2014, 817, 39-71.
[12]
Wood, J.D. In: Physiology of the Gastrointestinal Tract., Johnson
L.R. Ed.; Raven Press, New York. 1987, 67-109.
[13]
Burnstock, G.; Campbell, G.; Bennet, M.; Holman, M.E. Inhibition of the smooth muscle of the Taenia coli. Nature, 1963, 200, 581-582.
[14]
Martinson, J.; Muren, A. Excitatory and inhibitory effects of vagus stimulation on gastric motility in the cat. Acta Physiol. Scand., 1963, 57, 309-316.
[15]
Rand, M.J. Nitrergic transmission: Nitric oxide as mediator of non-adrenergic, non-cholinergic neuro-effector transmission. Clin. Exp. Pharmacol. Physiol., 1992, 19, 147-169.
[16]
Currò, D.; Ipavec, V.; Preziosi, P. Neurotransmitters of the non-adrenergic non-cholinergic relaxation of proximal stomach. Eur. Rev. Med. Pharmacol. Sci., 2008, 12(1), 53-62.
[17]
Garella, R.; Idrizaj, E.; Traini, C.; Squecco, R.; Vannucchi, M.G.; Baccari, M.C. Glucagon-like peptide-2 modulates the nitrergic neurotransmission in strips from the mouse gastric fundus. World J. Gastroenterol., 2017, 23(40), 7211-7220.
[18]
Garella, R.; Squecco, R.; Baccari, M.C. Site-related effects of relaxin in the gastrointestinal tract through nitric oxide signalling: An updated report. Curr. Protein Pept. Sci., 2017, 18(12), 1254-1262.
[19]
Sanders, K.M. Regulation of smooth muscle excitation and contraction. Neurogastroenterol. Motil., 2008, 20, 39-53.
[20]
Sanders, K.M.; Sang, D.K.; Seungil, R.; Sean, M.W. Regulation of gastrointestinal motility-insights from smooth muscle biology. Nat. Rev. Gastroenterol. Hepatol., 2012, 9(11), 633-645.
[21]
Camilleri, M. Peripheral mechanisms in appetite regulation. Gastroenterology, 2015, 148, 1219-1233.
[22]
Zhang, A.Q.; Li, X.L.; Jiang, C.Y.; Lin, L.; Shi, R.H.; Chen, J.D.; Oomura, Y. Expression of nesfatin-1/NUCB2 in rodent digestive system. World J. Gastroenterol., 2010, 16, 1735-1741.
[23]
Pelleymounter, M.A.; Cullen, M.J.; Baker, M.B.; Hecht, R.; Winters, D.; Boone, T.; Collins, F. Effects of the obese gene product on body weight regulation in ob/ob mice. Science, 1995, 269(5223), 540-543.
[24]
Chan, J.L.; Heist, K.; De Paoli, A.M.; Veldhuis, J.D.; Mantzoros, C.S. The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men. J. Clin. Invest., 2003, 111, 1409-1421.
[25]
Ahima, R.S.; Saper, C.B.; Flier, J.S.; Elmquist, J.K. Leptin regulation of neuroendocrine systems. Front. Neuroendocrinol., 2000, 21, 263-307.
[26]
Frederich, R.C.; Hamann, A.; Anderson, S.; Lollmann, B.; Lowell, B.B.; Flier, J.S. Leptin levels reflect body lipid content in mice: Evidence for diet-induced resistance to leptin action. Nat. Med., 1995, 1(12), 1311-1314.
[27]
Maffei, M.; Halaas, J.; Ravussin, E.; Pratley, R.E.; Lee, G.H.; Zhang, Y.; Fei, H.; Kim, S.; Lallone, R.; Ranganathan, S. Leptin levels in human and rodent: Measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat. Med., 1995, 1(11), 1155-1161.
[28]
Morris, D.L.; Rui, L. Recent advances in understanding leptin signaling and leptin resistance. Am. J. Physiol. Endocrinol. Metab., 2009, 297(6), E1247-E1259.
[29]
Badman, M.K.; Flier, J.S. The adipocyte as an active participant in energy balance and metabolism. Gastroenterology, 2007, 132, 2103-2115.
[30]
Mark, A.L.; Agassandian, K.; Morgan, D.A.; Liu, X.; Cassel, M.D.; Rahmouni, K. Leptin signaling in the nucleus Tractus solitarii increases sympathetic nerve activity to the kidney. Hypertension, 2009, 53, 375-380.
[31]
Münzberg, H.; Morrison, C.D. Structure, production and signaling of leptin. Metabolism, 2015, 64(1), 13-23.
[32]
Gong, Y.; Ishida-Takahashi, R.; Villanueva, E.C.; Fingar, D.C.; Munzberg, H.; Myers, M.G., Jr The long form of the leptin receptor regulates STAT5 and ribosomal protein S6 via alternate mechanisms. J. Biol. Chem., 2007, 282, 31019-31027.
[33]
Wada, N.; Hirako, S.; Takenoya, F.; Kageyama, H.; Okabe, M.; Shioda, S. Leptin and its receptors. J. Chem. Neuroanat., 2014, 61-62, 191-199.
[34]
Buettner, C.; Pocai, A.; Muse, E.D.; Etgen, A.M.; Myers, M.G., Jr; Rossetti, L. Critical role of STAT3 in leptin’s metabolic actions. Cell Metab., 2006, 4, 49-60.
[35]
Sahu, M.; Sahu, A. Leptin receptor expressing neurons express phosphodiesterase-3B (PDE3B) and leptin induces STAT3 activation in PDE3B neurons in the mouse hypothalamus. Peptides, 2015, 73, 35-42.
[36]
Korner, J.; Chua, S.C., Jr; Williams, J.A.; Leibel, R.L.; Wardlaw, S.L. Regulation of hypothalamic proopiomelanocortin by leptin in lean and obese rats. Neuroendocrinology, 1999, 70(6), 377-383.
[37]
Mercer, A.J.; Stuart, R.C.; Attard, C.A.; Otero-Corchon, V.; Nillni, E.A.; Low, M.J. Temporal changes in nutritional state affect hypothalamic POMC peptide levels independently of leptin in adult male mice. Am. J. Physiol. Endocrinol. Metab., 2014, 306(8), E904-E915.
[38]
Lee, S.J.; Verma, S.; Simonds, S.E.; Kirigiti, M.A.; Kievit, P.; Lindsley, S.R.; Loche, A.; Smith, M.S.; Cowley, M.A.; Grove, K.L. Leptin stimulates neuropeptide Y and cocaine amphetamine-regulated transcript coexpressing neuronal activity in the dorsomedial hypothalamus in diet-induced obese mice. J. Neurosci., 2013, 33(38), 15306-15317.
[39]
Gong, L.; Yao, F.; Hockman, K.; Heng, H.H.; Morton, G.J.; Takeda, K.; Akira, S.; Low, M.J.; Rubinstein, M.; MacKenzie, R.G. Signal transducer and activator of transcription-3 is required in hypothalamic agouti-related protein/neuropeptide Y neurons for normal energy homeostasis. Endocrinology, 2008, 149(7), 3346-3354.
[40]
Bates, S.H.; Stearns, W.H.; Dundon, T.A.; Schubert, M.; Tso, A.W.; Wang, Y.; Banks, A.S.; Lavery, H.J.; Haq, A.K.; Maratos-Flier, E.; Neel, B.G.; Schwartz, M.W.; Myers, M.G., Jr STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature, 2003, 421(6925), 856-859.
[41]
Cummings, D.E.; Foster, K.E. Ghrelin-leptin tango in body-weight regulation. Gastroenterology, 2003, 124(5), 1532-1535.
[42]
Rodrigues, K.D.C.D.; Pereira, R.M.; de Campos, T.D.P.; de Moura, R.F.; da Silva, A.S.R.; Cintra, D.E.; Ropelle, E.R.; Pauli, J.R.; de Araújo, M.B.; de Moura, L.P. The role of physical exercise improve the browning of white adipose tissue via POMC neurons. Front. Cell. Neurosci., 2018, 12, 88.
[43]
Ahima, R.S.; Mitchell, A.L. Adipokines and the peripheral and neural control of energy balance. Mol. Endocrinol., 2008, 22(5), 1023-1031.
[44]
Barrenetxe, J.; Barber, A.; Lostao, M.P. Leptin effect on galactose absorption in mice jejunum. J. Physiol. Biochem., 2001, 57(4), 345-346.
[45]
Fanjul, C.; Barrenetxe, J.; Inigo, C.; Sakar, Y.; Ducroc, R.; Barber, A.; Lostao, M.P. Leptin regulates sugar and amino acids transport in the human intestinal cell line Caco-2. Acta Physiol., 2012, 205(1), 82-91.
[46]
Martí, A.; Berraondo, B.; Martínez, J.A. Leptin: Physiological actions. J. Physiol. Biochem., 1999, 55(1), 43-49.
[47]
De Fanti, B.A.; Lamas, O.; Milagro, F.I.; Martïnez-Ansó, E.; Martínez, J.A. Immunoneutralization and anti-idiotype production: two-sided applications of leptin. Trends Immunol., 2002, 23(4), 180-181.
[48]
Yarandi, S.S.; Hebbar, G.; Sauer, C.G.; Cole, C.R.; Ziegler, T.R. Diverse roles of leptin in the gastrointestinal tract: Modulation of motility, absorption, growth, and inflammation. Nutrition, 2011, 27(3), 269-275.
[49]
Buettner, C.; Muse, E.D.; Cheng, A.; Chen, L.; Scherer, T.; Pocai, A.; Su, K.; Cheng, B.; Li, X.; Harvey-White, J.; Schwartz, G.J.; Kunos, G.; Rossetti, L. Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms. Nat. Med., 2008, 14, 667-675.
[50]
Dong, Z.; Fu, S.; Xu, X.; Yang, Y.; Du, L.; Li, W.; Kan, S.; Li, Z.; Zhang, X.; Wang, L.; Li, J.; Liu, H.; Qu, X.; Wang, C. Leptin-mediated regulation of ICAM-1 is Rho/ROCK dependent and enhances gastric cancer cell migration. Br. J. Cancer, 2014, 110(7), 1801-1810.
[51]
Bado, A.; Levasseur, S.; Attoub, S.; Kermorgant, S.; Laigneau, J.P.; Bortoluzzi, M.N.; Moizo, L.; Lehy, T.; Guerre-Millo, M.; Le Marchand, B.Y.; Lewin, M.J. The stomach is a source of leptin. Nature, 1998, 394, 790-793.
[52]
Sobhani, I.; Bado, A.; Vissuzaine, C.; Buyse, M.; Kermorgant, S.; Laigneau, J.P.; Attoub, S.; Lehy, T.; Henin, D.; Mignon, M.; Lewin, M.J. Leptin secretion and leptin receptor in the human stomach. Gut, 2000, 47, 178-183.
[53]
Barrenetxe, J.; Villaro, A.C.; Guembe, L.; Pascual, I.; Munoz-Navas, M.; Barber, A.; Lostao, M.P. Distribution of the long leptin receptor isoform in brush border, basolateral membrane, and cytoplasm of enterocytes. Gut, 2008, 50, 797-809.
[54]
Buyse, M.; Ovesjo, M.L.; Goiot, H.; Guilmeau, S.; Peranzi, G.; Moizo, L.; Walker, F.; Lewin, M.J.; Meister, B.; Bado, A. Expression and regulation of leptin receptor proteins in afferent and efferent neurons of the vagus nerve. Eur. J. Neurosci., 2001, 14, 64-73.
[55]
Wang, Y.H.; Tache, Y.; Sheibel, A.B.; Go, V.L.; Wei, J.Y. Two types of leptin-responsive gastric vagal afferent terminals: an in vitro single-unit study in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 1997, 273, R833-R837.
[56]
Li, H.Y.; Wang, L.L.; Yeh, R.S. Leptin immunoreactivity in the central nervous system in normal and diabetic rats. Neuroreport, 1999, 10, 437-442.
[57]
Martinez, V.; Barrachina, M.D.; Wang, L.; Tache, Y. Intracerebroventricular leptin inhibits gastric emptying of a solid nutrient meal in rats. Neuroreport, 1999, 10, 3217.
[58]
Banks, W.A.; Kastin, A.J.; Huang, W.; Jaspan, J.B.; Maness, L.M. Leptin enters the brain by a saturable system independent of insulin. Peptides, 1996, 17, 305-311.
[59]
Davis, J.D.; Smith, G.P.; Sayler, J.L. Reduction of intake in the rat due to gastric filling. Am. J. Physiol., 1997, 272, R1599-R1605.
[60]
Asakawa, A.; Inui, A.; Ueno, N.; Makino, S.; Fujino, M.A.; Kasuga, M. Urocortin reduces food intake and gastric emptying in lean and ob/ob obese mice. Gastroenterology, 1999, 116, 1287.
[61]
Barrachina, M.D.; Martinez, V.; Wei, J.Y.; Tache, Y. Leptin-induced decrease in food intake is not associated with changes in gastric emptying in lean mice. Am. J. Physiol., 1997, 272, R1007-R1011.
[62]
Hata, N.; Murata, S.; Maeda, J.; Yatani, H.; Kohno, Y.; Yokono, K.; Okano, H. Predictors of gastric myoelectrical activity in type 2 diabetes mellitus. J. Clin. Gastroenterol., 2009, 43, 429-436.
[63]
He, L.; Sun, Y.; Zhu, Y.; Ren, R.; Zhang, Y.; Wang, F. Improved gastric emptying in diabetic rats by irbesartan via decreased serum leptin and ameliorated gastric microcirculation. Genet. Mol. Res., 2014, 13(3), 7163-7172.
[64]
Hammersjö, R.; Roth, B.; Höglund, P.; Ohlsson, B. Esophageal and gastric dysmotilities are associated with altered glucose homeostasis and plasma levels of incretins and leptin. Rev. Diabet. Stud., 2016, 13(1), 79-90.
[65]
Gallagher, T.K.; Geoghegan, J.G.; Baird, A.W.; Winter, D.C. Implications of altered gastrointestinal motility in obesity. Obes. Surg., 2007, 17, 1399-1407.
[66]
Kiely, J.M.; Noh, J.H.; Graewin, S.J.; Pitt, H.A.; Swartz-Basile, D.A. Altered intestinal motility in leptin-deficient obese mice. J. Surg. Res., 2005, 124, 98-103.
[67]
Côté-Daigneault, J.; Poitras, P.; Rabasa-Lhoret, R.; Bouin, M. Plasma leptin concentrations and esophageal hypomotility in obese patients. Can. J. Gastroenterol. Hepatol., 2015, 29(1), 49-51.
[68]
Baudry, C.; Reichardt, F.; Marchix, J.; Bado, A.; Schemann, M.; des Varannes, S.B.; Neunlist, M.; Moriez, R. Diet-induced obesity has neuroprotective effects in murine gastric enteric nervous system: Involvement of leptin and glial cell line-derived neurotrophic factor. J. Physiol., 2012, 590(3), 533-544.
[69]
Li, J.; Ma, W.; Wang, S. Slower gastric emptying in high-fat diet induced obese rats is associated with attenuated plasma ghrelin and elevated plasma leptin and cholecystokinin concentrations. Regul. Pept., 2011, 171(1-3), 53-57.
[70]
Wang, L.; Barachina, M.D.; Martínez, V.; Wei, J.Y.; Taché, Y. Synergistic interaction between CCK and leptin to regulate food intake. Regul. Pept., 2000, 92(1-3), 79-85.
[71]
Heldsinger, A.; Grabauskas, G.; Song, I.; Owyang, C. Synergistic interaction between leptin and cholecystokinin in the rat nodose ganglia is mediated by PI3K and STAT3 signaling pathways: Implications for leptin as a regulator of short term satiety. J. Biol. Chem., 2011, 286(13), 11707-11715.
[72]
Gaigé, S.; Abysique, A.; Bouvier, M. Effects of leptin on cat intestinal motility. J. Physiol., 2003, 546, 267-277.
[73]
Guilmeau, S.; Buyse, M.; Tsocas, A.; Laigneau, J.P.; Bado, A. Duodenal leptin stimulates cholecystokinin secretion evidence of a positive leptin-cholecystokinin feedback loop. Diabetes, 2003, 52, 1664-1672.
[74]
Reichardt, F.; Krueger, D.; Schemann, M. Leptin excites enteric neurons of guinea-pig submucous and myenteric plexus. Neurogastroenterol. Motil., 2011, 23, E165-E170.
[75]
Cammisotto, P.G.; Levy, É.; Bukowiecki, L.J.; Bendayan, M. Cross-talk between adipose and gastric leptins for the control of food intake and energy metabolism. Prog. Histochem. Cytochem., 2010, 45(3), 143-200.
[76]
Florian, V.; Caroline, F.; Francis, C.; Camille, S.; Fabielle, A. Leptin modulates enteric neurotransmission in the rat proximal colon: An in vitro study. Regul. Pept., 2013, 185, 73-78.
[77]
Voinot, F.; Fischer, C.; Schmidt, C.; Ehret-Sabatier, L.; Angel, F. Controlled ingestion of kaolinite (5%) modulates enteric nitrergic innervation in rats. Fundam. Clin. Pharmacol., 2014, 28(4), 405-413.
[78]
Buckley, M.M.; O’Brien, R.; Devlin, M.; Creed, A.A.; Rae, M.G.; Hyland, N.P.; Quigley, E.M.; McKernan, D.P.; O’Malley, D. Leptin modifies the prosecretory and prokinetic effects of the inflammatory cytokine interleukin-6 on colonic function in Sprague-Dawley rats. Exp. Physiol., 2016, 101(12), 1477-1491.
[79]
Scherer, P.E.; Williams, S.; Fogliano, M.; Baldini, G.; Lodish, H.F. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem., 1995, 270, 26746-26749.
[80]
Hotta, K.; Funahashi, T.; Bodkin, N.L. Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys. Diabetes, 2001, 50, 1126-1133.
[81]
Fu, Y.; Luo, N.; Klein, R.L.; Garvey, W.T. Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J. Lipid Res., 2005, 46, 1369-1379.
[82]
Maeda, K.; Okubo, K.; Shimomura, I.; Funahashi, T.; Matsuzawa, Y.; Matsubara, K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (AdiPose Most abundant Gene transcript 1). Biochem. Biophys. Res. Commun., 1996, 221, 286-289.
[83]
Maeda, K.; Okubo, K.; Shimomura, I.; Mizuno, K.; Matsuzawa, Y.; Matsubara, K. Analysis of an expression profile of genes in the human adipose tissue. Gene, 1997, 190, 227-235.
[84]
Hu, E.; Liang, P.; Spiegelman, B.M. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem., 1996, 271, 10697-10703.
[85]
Arita, Y.; Kihara, S.; Ouchi, N.; Maeda, K.; Kuriyama, H.; Okamoto, Y.; Kumada, M.; Hotta, K.; Nishida, M.; Takahashi, M.; Nakamura, T.; Shimomura, I.; Muraguchi, M.; Ohmoto, Y.; Funahashi, T.; Matsuzawa, Y. Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation, 2002, 105, 2893-2898.
[86]
Brochu-Gaudreau, K.; Rehfeldt, C.; Blouin, R.; Bordignon, V.; Murphy, B.D.; Palin, M.F. Adiponectin action from head to toe. Endocrine, 2010, 37(1), 11-32.
[87]
Kentish, S.J.; Ratcliff, K.; Li, H.; Wittert, G.A.; Page, A.J. High fat diet induced changes in gastric vagal afferent response to adiponectin. Physiol. Behav., 2015, 152, 354-362.
[88]
Arita, Y.; Kihara, S.; Ouchi, N.; Takahashi, M.; Maeda, K.; Miyagawa, J.; Hotta, K.; Shimomura, I.; Nakamura, T.; Miyaoka, K.; Kuriyama, H.; Nishida, M.; Yamashita, S.; Okubo, K.; Matsubara, K.; Muraguchi, M.; Ohmoto, Y.; Funahashi, T.; Matsuzawa, Y. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun., 1999, 257, 79-83.
[89]
Ryo, M.; Nakamura, T.; Kihara, S. Adiponectin as a biomarker of the metabolic syndrome. Circ. J., 2004, 68, 975-981.
[90]
Cnop, M.; Havel, P.J.; Utzschneider, K.M. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: Evidence for independent roles of age and sex. Diabetologia, 2003, 46, 459-469.
[91]
Weyer, C.; Funahashi, T.; Tanaka, S.; Hotta, K.; Matsuzawa, Y.; Pratley, R.E.; Tataranni, P.A. Hypoadiponectinemia in obesity and type 2 diabetes: Close association with insulin resistance and hyperinsulinemia. J. Clin. Endocrinol. Metab., 2001, 86, 1930-1935.
[92]
Yamauchi, T.; Kamon, J.; Ito, Y.; Tsuchida, A.; Yokomizo, T.; Kita, S.; Sugiyama, T.; Miyagishi, M.; Hara, K.; Tsunoda, M.; Murakami, K.; Ohteki, T.; Uchida, S.; Takekawa, S.; Waki, H.; Tsuno, N.H.; Shibata, Y.; Terauchi, Y.; Froguel, P.; Tobe, K.; Koyasu, S.; Taira, K.; Kitamura, T.; Shimizu, T.; Nagai, R.; Kadowaki, T. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature, 2003, 423, 762-769.
[93]
Yamauchi, T.; Iwabu, M.; Okada-Iwabu, M.; Kadowaki, T. Adiponectin receptors: A review of their structure, function and how they work. Best Pract. Res. Clin. Endocrinol. Metab., 2014, 28(1), 15-23.
[94]
Wang, Z.V.; Scherer, P.E. Adiponectin, the past two decades. J. Mol. Cell Biol., 2016, 8(2), 93-100.
[95]
González, C.R.; Caminos, J.E.; Gallego, R.; Tovar, S.; Vázquez, M.J.; Garcés, M.F.; Lopez, M.; García-Caballero, T.; Tena-Sempere, M.; Nogueiras, R.; Diéguez, C. Adiponectin receptor 2 is regulated by nutritional status, leptin and pregnancy in a tissue-specific manner. Physiol. Behav., 2010, 99, 91-99.
[96]
Qi, Y.; Takahashi, N.; Hileman, S.M.; Patel, H.R.; Berg, A.H.; Pajvani, U.B.; Scherer, P.E.; Ahima, R.S. Adiponectin acts in the brain to decrease body weight. Nat. Med., 2004, 10, 524-529.
[97]
Coope, A.; Milanski, M.; Araújo, E.P.; Tambascia, M.; Saad, M.J.; Geloneze, B.; Velloso, L.A. AdipoR1 mediates the anorexigenic and insulin/leptin-like actions of adiponectin in the hypothalamus. FEBS Lett., 2008, 582, 1471-1476.
[98]
Kadowaki, T.; Yamauchi, T.; Kubota, N. The physiological and pathophysiological role of adiponectin and adiponectin receptors in the peripheral tissues and CNS. FEBS Lett., 2008, 582, 74-80.
[99]
Oh, D.K.; Ciaraldi, T.; Henry, R.R. Adiponectin in health and disease. Diabetes Obes. Metab., 2007, 9, 282-289.
[100]
Palin, M.F.; Bordignon, V.V.; Murphy, B.D. Adiponectin and the control of female reproductive functions. Vitam. Horm., 2012, 90, 239-287.
[101]
Yamauchi, T.; Nio, Y.; Maki, T.; Kobayashi, M.; Takazawa, T.; Iwabu, M.; Okada, I.M.; Kawamoto, S. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med., 2007, 13, 332-339.
[102]
Yamauchi, T.; Kadowaki, T. Adiponectin receptor as a key player in healthy longevity and obesity-related diseases. Cell Metab., 2013, 17, 185-196.
[103]
Holland, W.L.; Miller, R.A.; Wang, Z.V.; Sun, K.; Barth, B.M.; Bui, H.H.; Davis, K.E.; Bikman, B.T. Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat. Med., 2011, 17, 55-63.
[104]
Denzel, M.S.; Scimia, M.C.; Zumstein, P.M.; Walsh, K.; Ruiz-Lozano, P.; Ranscht, B. T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J. Clin. Invest., 2010, 120, 4342-4352.
[105]
Hui, X.; Lam, K.S.; Vanhoutte, P.M.; Xu, A. Adiponectin and cardiovascular health: An update. Br. J. Pharmacol., 2012, 165, 574-590.
[106]
Ouchi, N.; Kihara, S.; Arita, Y.; Okamoto, Y.; Maeda, K.; Kuriyama, H.; Hotta, K.; Nishida, M.; Takahashi, M.; Muraguchi, M.; Ohmoto, Y.; Nakamura, T.; Yamashita, S.; Funahashi, T.; Matsuzawa, Y. Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-kappaB signaling through a cAMP-dependent pathway. Circulation, 2000, 102, 1296-1301.
[107]
Minokoshi, Y.; Alquier, T.; Furukawa, N.; Kim, Y.B.; Lee, A.; Xue, B.; Mu, J.; Foufelle, F.; Ferré, P.; Birnbaum, M.J.; Stuck, B.J.; Kahn, B.B. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature, 2004, 428, 569-574.
[108]
Wolf, G. The regulation of food intake by hypothalamic malonyl-coenzyme A: The MaloA hypothesis. Nutr. Rev., 2006, 64, 379-383.
[109]
Chen, H.; Montagnani, M.; Funahashi, T.; Shimomura, I.; Quon, M.J. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J. Biol. Chem., 2003, 278, 45021-45026.
[110]
Ewart, M.A.; Kohlhaas, C.F.; Salt, I.P. Inhibition of tumor necrosis factor alpha-stimulated monocyte adhesion to human aortic endothelial cells by AMP-activated protein kinase. Arterioscler. Thromb. Vasc. Biol., 2008, 28, 2255-2257.
[111]
Francisco, C.; Neves, J.S.; Falcão-Pires, I.; Leite-Moreira, A. Can adiponectin help us to target diastolic dysfunction? Cardiovasc. Drugs Ther., 2016, 6, 635-644.
[112]
Shklyaev, S.; Aslanidi, G.; Tennant, M.; Prima, V.; Kohlbrenner, E.; Kroutov, V.; Campbell-Thompson, M.; Crawford, J.; Shek, E.W.; Scarpace, P.J.; Zolotukhin, S. Sustained peripheral expression of transgene adiponectin offsets the development of diet-induced obesity in rats. Proc. Natl. Acad. Sci. USA, 2003, 100, 14217-14222.
[113]
Kubota, N.; Yano, W.; Kubota, T.; Yamauchi, T.; Itoh, S.; Kumagai, H.; Kozono, H.; Takamoto, I.; Okamoto, S.; Shiuchi, T.; Suzuki, R.; Satoh, H.; Tsuchida, A.; Moroi, M.; Sugi, K.; Noda, T.; Ebinuma, H.; Ueta, Y.; Kondo, T.; Araki, E.; Ezaki, O.; Nagai, R.; Tobe, K.; Terauchi, Y.; Ueki, K.; Minokoshi, Y.; Kadowaki, T. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab., 2007, 6, 55-68.
[114]
Idrizaj, E.; Garella, R.; Castellini, G.; Mohr, H.; Pellegata, N.S.; Francini, F.; Ricca, V.; Squecco, R.; Baccari, M.C. Adiponectin affects the mechanical responses in strips from the mouse gastric fundus. World J. Gastroenterol., 2018, 24(35), 4028-4035.
[115]
Vannucchi, M.G.; Garella, R.; Cipriani, G.; Baccari, M.C. Relaxin counteracts the altered gastric motility of dystrophic (mdx) mice: Functional and immunohistochemical evidence for the involvement of nitric oxide. Am. J. Physiol. Endocrinol. Metab., 2011, 300, 380-391.
[116]
Squecco, R.; Garella, R.; Idrizaj, E.; Nistri, S.; Francini, F.; Baccari, M.C. Relaxin affects smooth muscle biophysical properties and mechanical activity of the female mouse colon. Endocrinology, 2015, 156, 4398-4410.
[117]
Idrizaj, E.; Garella, R.; Francini, F.; Squecco, R.; Baccari, M.C. Relaxin influences ileal muscular activity through a dual signaling pathway in mice. World J. Gastroenterol., 2018, 24(8), 882-893.
[118]
Nour-Eldine, W.; Ghantous, C.M.; Zibara, K.; Dib, L.; Issaa, H.; Itani, H.; El-Zein, N.; Zeidan, A. Adiponectin attenuates angiotensin II-induced vascular smooth muscle cell remodeling through nitric oxide and the RhoA/ROCK pathway. Front. Pharmacol., 2016, 7, 86.
[119]
Matsuyama, H.; Thapaliya, S.; Takewaki, T. Cyclic GMP-associated apamin-sensitive nitrergic slow inhibitory junction potential in the hamster ileum. Br. J. Pharmacol., 1999, 128, 830-836.
[120]
Oh-I, S.; Shimizu, H.; Satoh, T.; Okada, S.; Adachi, S.; Inoue, K.; Eguchi, H.; Yamamoto, M.; Imaki, T.; Hashimoto, K.; Tsuchiya, T.; Monden, T.; Horiguchi, K.; Yamada, M.; Mori, M. Identification of nesfatin-1 as a satiety molecule in the hypothalamus. Nature, 2006, 443(7112), 709-712.
[121]
Cowley, M.A.; Grove, K.L. To be or NUCB2, is nesfatin the answer? Cell Metab., 2006, 4, 421-422.
[122]
Brailoiu, G.C.; Dun, S.L.; Brailoiu, E.; Inan, S.; Yang, J.; Chang, J.K.; Dun, N.J. Nesfatin-1: distribution and interaction with a G protein-coupled receptor in the rat brain. Endocrinology, 2007, 148, 5088-5094.
[123]
Lin, P.; Le-Niculescu, H.; Hofmeister, R.; McCaffery, J.M.; Jin, M.; Hennemann, H.; McQuistan, T.; De Vries, L.; Farquhar, M.G. The mammalian calcium-binding protein, nucleobindin (CALNUC), is a Golgi resident protein. J. Cell Biol., 1998, 141, 1515-1527.
[124]
Stengel, A.; Taché, Y. Role of brain NUCB2/nesfatin-1 in the regulation of food intake. Curr. Pharm. Des., 2013, 19(39), 6955-6959.
[125]
Dore, R.; Levata, L.; Lehnert, H.; Schulz, C. Nesfatin-1: Functions and physiology of a novel regulatory peptide. J. Endocrinol., 2017, 232(1), R45-R65.
[126]
Senin, L.L.; Al-Massadi, O.; Barja-Fernandez, S.; Folgueira, C.; Castelao, C.; Tovar, S.A.; Leis, R.; Lago, F.; Baltar, J.; Baamonde, I.; Dieguez, C.; Casanueva, F.F.; Seoane, L.M. Regulation of NUCB2/nesfatin-1 production in rat’s stomach and adipose tissue is dependent on age, testosterone levels and lactating status. Mol. Cell. Endocrinol., 2015, 411, 105-112.
[127]
Ravussin, A.; Youm, Y.H.; Sander, J.; Ryu, S.; Nguyen, K.; Varela, L.; Shulman, G.I.; Sidorov, S.; Horvath, T.L.; Schultze, J.L.; Dixit, V.D. Loss of nucleobindin-2 causes insulin resistance in obesity without impacting satiety or adiposity. Cell Reports, 2018, 24(5), 1085-1092.
[128]
Stengel, A. Identification and characterization of nesfatin-1 immunoreactivity in endocrine cell types of the rat gastric oxyntic mucosa. Endocrinology, 2009, 150, 232-238.
[129]
Garcia-Galiano, D.; Navarro, V.M.; Gaytan, F.; Tena-Sempere, M. Expanding roles of NUCB2/nesfatin-1 in neuroendocrine regulation. J. Mol. Endocrinol., 2010, 45, 281-290.
[130]
Stengel, A.; Taché, Y. Nesfatin-1 role as possible new potent regulator of food intake. Regul. Pept., 2010, 163, 18-23.
[131]
Shimizu, H.; Oh-I, S.; Okada, S.; Mori, M. Nesfatin-1: An overview and future clinical application. Endocr. J., 2009, 56, 537-543.
[132]
Kolgazi, M.; Cantali-Ozturk, C.; Deniz, R.; Ozdemir-Kumral, Z.N.; Yuksel, M.; Sirvanci, S.; Yeğen, B.C. Nesfatin-1 alleviates gastric damage via direct antioxidant mechanisms. J. Surg. Res., 2015, 193(1), 111-118.
[133]
Su, Y.; Zhang, J.; Tang, Y.; Bi, F.; Liu, J.N. The novel function of nesfatin-1: Anti-hyperglycemia. Biochem. Biophys. Res. Commun., 2010, 391(1), 1039-1042.
[134]
Yang, M.; Zhang, Z.; Wang, C.; Li, K.; Li, S.; Boden, G.; Li, L.; Yang, G. Nesfatin-1 action in the brain increases insulin sensitivity through Akt/AMPK/TORC2 pathway in diet-induced insulin resistance. Diabetes, 2012, 61(8), 1959-1968.
[135]
Nakata, M.; Manaka, K.; Yamamoto, S.; Mori, M.; Yada, T. Nesfatin-1 enhances glucose-induced insulin secretion by promoting Ca(2+) influx through L-type channels in mouse islet β-cells. Endocr. J., 2011, 58(4), 305-313.
[136]
Prinz, P.; Goebel-Stengel, M.; Teuffel, P.; Rose, M.; Klapp, B.F.; Stengel, A. Peripheral and central localization of the nesfatin-1 receptor using autoradiography in rats. Biochem. Biophys. Res. Commun., 2016, 470(3), 521-527.
[137]
Ayada, C.; Turgut, G.; Turgut, S.; Guclu, Z. The effect of chronic peripheral nesfatin-1 application on blood pressure in normal and chronic restraint stressed rats: Related with circulating level of blood pressure regulators. Gen. Physiol. Biophys., 2015, 34, 81-88.
[138]
Yamawaki, H.; Takahashi, M.; Mukohda, M.; Morita, T.; Okada, M.; Hara, Y. A novel adipocytokine, nesfatin-1 modulates peripheral arterial contractility and blood pressure in rats. Biochem. Biophys. Res. Commun., 2012, 418, 676-681.
[139]
Stengel, A.; Goebel, M.; Wang, L.; Tache, ´.Y. Ghrelin, des-acyl ghrelin and nesfatin-1 in gastric X/A-like cells: Role as regulators of food intake and body weight. Peptides, 2010, 31, 357-369.
[140]
Atsuchi, K.; Asakawa, A.; Ushikai, M.; Ataka, K.; Tsai, M.; Koyama, K.; Sato, Y.; Kato, I.; Fujimiya, M.; Inui, A. Centrally administered nesfatin-1 inhibits feeding behaviour and gastroduodenal motility in mice. Neuroreport, 2010, 21(15), 1008-1011.
[141]
Yang, G.T.; Zhao, H.Y.; Kong, Y.; Sun, N.N.; Dong, A.Q. Study of the effects of nesfatin-1 on gastric function in obese rats. World J. Gastroenterol., 2017, 23(16), 2940-2947.
[142]
Wang, Q.; Guo, F.; Sun, X.; Gao, S.; Li, Z.; Gong, Y.; Xu, L. Effects of exogenous nesfatin-1 on gastric distention-sensitive neurons in the central nucleus of the amygdala and gastric motility in rats. Neurosci. Lett., 2014, 582, 65-70.
[143]
Watanabe, A.; Mochiki, E.; Kimura, A.; Kogure, N.; Yanai, M.; Ogawa, A.; Toyomasu, Y.; Ogata, K.; Ohno, T.; Suzuki, H.; Kuwano, H. Nesfatin-1 suppresses gastric contractions and inhibits interdigestive migrating contractions in conscious dogs. Dig. Dis. Sci., 2015, 60(6), 1595-1602.
[144]
Gao, S.; Guo, F.; Sun, X.; Zhang, N.; Gong, Y.; Xu, L. The inhibitory effects of nesfatin-1 in ventromedial hypothalamus on gastric function and its regulation by nucleus accumbens. Front. Physiol., 2017, 7, 634.
[145]
Tatemoto, K.; Hosoya, M.; Habata, Y.; Fujii, R.; Kakegawa, T.; Zou, M.X.; Kawamata, Y.; Fukusumi, S.; Hinuma, S.; Kitada, C.; Kurokawa, T.; Onda, H.; Fujino, M. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res. Commun., 1998, 251(2), 471-476.
[146]
Medhurst, A.D.; Jennings, C.A.; Robbins, M.J.; Davis, R.P.; Ellis, C.; Winborn, K.Y.; Lawrie, K.W.; Hervieu, G.; Riley, G.; Bolaky, J.E.; Herrity, N.C.; Murdock, P.; Darker, J.G. Pharmacological and immunohistochemical characterization of the APJ receptor and its endogenous ligand apelin. J. Neurochem., 2003, 84(5), 1162-1172.
[147]
Kleinz, M.J.; Davenport, A.P. Emerging roles of apelin in biology and medicine. Pharmacol. Ther., 2005, 107(2), 198-211.
[148]
Hosoya, M.; Kawamata, Y.; Fukusumi, S.; Fujii, R.; Habata, Y.; Hinuma, S.; Kitada, C.; Honda, S.; Kurokawa, T.; Onda, H.; Nishimura, O.; Fujino, M. Molecular and functional characteristics of APJ. Tissue distribution of mRNA and interaction with the endogenous ligand apelin. J. Biol. Chem., 2000, 275(28), 21061-21067.
[149]
Reaux, A.; De Mota, N.; Skultetyova, I.; Lenkei, Z.; El Messari, S.; Gallatz, K.; Corvol, P.; Palkovits, M.; Llorens-Cortès, C. Physiological role of a novel neuropeptide, apelin, and its receptor in the rat brain. J. Neurochem., 2001, 77(4), 1085-1096.
[150]
O’Carroll, A.M.; Lolait, S.J.; Harris, L.E.; Pope, G.R. The apelin receptor APJ: journey from an orphan to a multifaceted regulator of homeostasis. J. Endocrinol., 2013, 219, R13-R35.
[151]
Reaux-Le Goazigo, A.; Alvear-Perez, R.; Zizzari, P.; Epelbaum, J.; Bluet-Pajot, M.T.; Llorens-Cortes, C. Cellular localization of apelin and its receptor in the anterior pituitary: evidence for a direct stimulatory action of apelin on ACTH release. Am. J. Physiol. Endocrinol. Metab., 2007, 292(1), E7-E15.
[152]
Galanth, C.; Hus-Citharel, A.; Li, B.; Llorens-Cortès, C. Apelin in the control of body fluid homeostasis and cardiovascular functions. Curr. Pharm. Des., 2012, 18(6), 789-798.
[153]
Lee, D.K.; Cheng, R.; Nguyen, T.; Fan, T.; Kariyawasam, A.P.; Liu, Y.; Osmond, D.H.; George, S.R.; O’Dowd, B.F. Characterization of apelin, the ligand for the APJ receptor. J. Neurochem., 2000, 74(1), 34-41.
[154]
Taheri, S.; Murphy, K.; Cohen, M.; Sujkovic, E.; Kennedy, A.; Dhillo, W.; Dakin, C.; Sajedi, A.; Ghatei, M.; Bloom, S. The effects of centrally administered apelin-13 on food intake, water intake and pituitary hormone release in rats. Biochem. Biophys. Res. Commun., 2002, 291(5), 1208-1212.
[155]
Wei, L.; Hou, X.; Tatemoto, K. Regulation of apelin mRNA expression by insulin and glucocorticoids in mouse 3T3-L1 adipocytes. Regul. Pept., 2005, 132, 27-32.
[156]
Boucher, J.; Masri, B.; Daviaud, D.; Gesta, S.; Guigne, C.; Mazzucotelli, A.; Castan-Laurell, I.; Tack, I.; Knibiehler, B.; Carpéné, C.; Audigier, Y.; Saulnier-Blache, J.S.; Valet, P. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology, 2005, 146, 1764-1771.
[157]
Bertrand, C.; Valet, P.; Castan-Laurell, I. Apelin and energy metabolism. Front. Physiol., 2015, 6, 115.
[158]
Chapman, N.A.; Dupré, D.J.; Rainey, J.K. The apelin receptor: Physiology, pathology, cell signalling, and ligand modulation of a peptide-activated class A GPCR. Biochem. Cell Biol., 2014, 92(6), 431-440.
[159]
Xu, N.; Wang, H.; Fan, L.; Chen, Q. Supraspinal administration of apelin-13 induces antinociception via the opioid receptor in mice. Peptides, 2009, 30(6), 1153-1157.
[160]
Jászberényi, M.; Bujdosó, E.; Telegdy, G. Behavioral, neuroendocrine and thermoregulatory actions of apelin-13. Neuroscience, 2004, 129(3), 811-816.
[161]
Fournel, A.; Drougard, A.; Duparc, T.; Marlin, A.; Brierley, S.M.; Castro, J.; Le-Gonidec, S.; Masri, B.; Colom, A.; Lucas, A.; Rousset, P.; Cenac, N.; Vergnolle, N.; Valet, P.; Cani, P.D.; Knauf, C. Apelin targets gut contraction to control glucose metabolism via the brain. Gut, 2017, 66(2), 258-269.
[162]
Guo, M.; Chen, F.; Lin, T.; Peng, Y.; Li, W.; Zhu, X.; Lin, L.; Chen, Y. Apelin-13 decreases lipid storage in hypertrophic adipocytes in vitro through the upregulation of AQP7 expression by the PI3K signaling pathway. Med. Sci. Monit., 2014, 20, 1345-1352.
[163]
Wang, G.; Anini, Y.; Wei, W.; Qi, X.; O’Carroll, A.M.; Mochizuki, T.; Wang, H.Q.; Hellmich, M.R.; Englander, E.W.; Greeley, G.H., Jr Apelin, a new enteric peptide: Localization in the gastrointestinal tract, ontogeny, and stimulation of gastric cell proliferation and of cholecystokinin secretion. Endocrinology, 2004, 145(3), 1342-1348.
[164]
Ohno, S.; Yakabi, K.; Ro, S.; Ochiai, M.; Onouchi, T.; Sakurada, T.; Takabayashi, H.; Ishida, S.; Takayama, K. Apelin-12 stimulates acid secretion through an increase of histamine release in rat stomachs. Regul. Pept., 2012, 174(1-3), 71-78.
[165]
Valle, A.; Hoggard, N.; Adams, A.C.; Roca, P.; Speakman, J.R. Chronic central administration of apelin-13 over 10 days increases food intake, body weight, locomotor activity and body temperature in C57BL/6 mice. J. Neuroendocrinol., 2007, 20, 79-84.
[166]
Konturek, S.J.; Konturek, J.W.; Pawlik, T.; Brzozowski, T. Brain–gut axis and its role in the control of food intake. J. Physiol. Pharmacol., 2004, 55, 137-154.
[167]
Yang, Y.J.; Lv, S.Y.; Xiu, M.H.; Xu, N.; Chen, Q. Intracerebroventricular administration of apelin-13 inhibits distal colonic transit in mice. Peptides, 2010, 31(12), 2241-2246.
[168]
Lv, S.Y.; Yang, Y.J.; Qin, Y.J.; Xiong, W.; Chen, Q. Effect of centrally administered apelin-13 on gastric emptying and gastrointestinal transit in mice. Peptides, 2011, 32(5), 978-982.
[169]
Wang, G.; Kundu, R.; Han, S.; Qi, X.; Englander, E.W.; Quertermous, T.; Greeley, G.H., Jr Ontogeny of apelin and its receptor in the rodent gastrointestinal tract. Regul. Pept., 2009, 158(1-3), 32-39.
[170]
Bülbül, M.; Sinen, O. Dual autonomic inhibitory action of central Apelin on gastric motor functions in rats. Auton. Neurosci., 2018, 212, 17-22.
[171]
Bülbül, M.; Sinen, O.; Gök, M.; Travagli, R.A. Apelin-13 inhibits gastric motility through vagal cholinergic pathway in rats. Am. J. Physiol. Gastrointest. Liver Physiol., 2018, 314(2), G201-G210.
[172]
Bülbül, M.; Sinen, O.; İzgüt-Uysal, V.N.; Akkoyunlu, G.; Öztürk, S.; Uysal, F. Peripheral apelin mediates stress-induced alterations in gastrointestinal motor functions depending on the nutritional status. Clin. Exp. Pharmacol. Physiol., 2019, 46(1), 29-39.
[173]
Stengel, A.; Goebel, M.; Wang, L.; Rivier, J.; Kobelt, P.; Mönnikes, H.; Lambrecht, N.W.; Taché, Y. Central nesfatin-1: Differential role of corticotropin-releasing factor2 receptor. Endocrinology, 2009, 150(11), 4911-4919.
[174]
Wattez, J.S.; Ravallec, R.; Cudennec, B.; Knauf, C.; Dhulster, P.; Valet, P.; Breton, C.; Vieau, D.; Lesage, J. Apelin stimulates both cholecystokinin and glucagon-like peptide 1 secretions in vitro and in vivo in rodents. Peptides, 2013, 48, 134-136.
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