Apelin and energy metabolism

Chantal Bertrand, Philippe Valet, Isabelle Castan-Laurell, Chantal Bertrand, Philippe Valet, Isabelle Castan-Laurell

Abstract

A wide range of adipokines identified over the past years has allowed considering the white adipose tissue as a secretory organ closely integrated into overall physiological and metabolic control. Apelin, a ubiquitously expressed peptide was known to exert different physiological effects mainly on the cardiovascular system and the regulation of fluid homeostasis prior to its characterization as an adipokine. This has broadened its range of action and apelin now appears clearly as a new player in energy metabolism in addition to leptin and adiponectin. Apelin has been shown to act on glucose and lipid metabolism but also to modulate insulin secretion. Moreover, different studies in both animals and humans have shown that plasma apelin concentrations are usually increased during obesity and type 2 diabetes. This mini-review will focus on the various systemic apelin effects on energy metabolism by addressing its mechanisms of action. The advances concerning the role of apelin in metabolic diseases in relation with the recent reports on apelin concentrations in obese and/or diabetic subjects will also be discussed.

Keywords: adipokine; apelin; insulin sensitivity; obesity; type 2 diabetes.

Figures

Figure 1
Figure 1
Metabolic effects of apelin and its main signaling targets. Apelin, the ligand of the G protein coupled receptor APJ, can stimulate several metabolic functions (green arrows/boxes) and inhibit (orange arrows/boxes) lipolysis as well as insulin secretion through different signaling pathways: PDE3B, phosphodiesterase 3B; AMPK, AMP-activated protein kinase; PGC1-α, peroxisome proliferator-activated receptor γ co-activator 1α; eNOS, endothelial NO synthase; PI3K, phosphatidylinositol 3-kinase and Akt.

References

    1. Alexiadou K., Kokkinos A., Liatis S., Perrea D., Katsilambros N., Tentolouris N. (2012). Differences in plasma apelin and visfatin levels between patients with type 1 diabetes mellitus and healthy subjects and response after acute hyperglycemia and insulin administration. Hormones (Athens) 11, 444–450. 10.14310/horm.2002.1376
    1. Alfarano C., Foussal C., Lairez O., Calise D., Attane C., Anesia R., et al. . (2015). Transition from metabolic adaptation to maladaptation of the heart in obesity: role of apelin. Int. J. Obes. (Lond.) 39, 312–320. 10.1038/ijo.2014.122
    1. Attane C., Daviaud D., Dray C., Dusaulcy R., Masseboeuf M., Prevot D., et al. . (2011). Apelin stimulates glucose uptake but not lipolysis in human adipose tissue ex vivo. J. Mol. Endocrinol. 46, 21–28. 10.1677/JME-10-0105
    1. Attane C., Foussal C., Le Gonidec S., Benani A., Daviaud D., Wanecq E., et al. . (2012). Apelin treatment increases complete Fatty Acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice. Diabetes 61, 310–320. 10.2337/db11-0100
    1. Azizi M., Iturrioz X., Blanchard A., Peyrard S., De Mota N., Chartrel N., et al. . (2008). Reciprocal regulation of plasma apelin and vasopressin by osmotic stimuli. J. Am. Soc. Nephrol. 19, 1015–1024. 10.1681/ASN.2007070816
    1. Boucher J., Masri B., Daviaud D., Gesta S., Guigne C., Mazzucotelli A., et al. . (2005). Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 146, 1764–1771. 10.1210/en.2004-1427
    1. Burcelin R., Dolci W., Thorens B. (2000). Portal glucose infusion in the mouse induces hypoglycemia: evidence that the hepatoportal glucose sensor stimulates glucose utilization. Diabetes 49, 1635–1642. 10.2337/diabetes.49.10.1635
    1. Castan-Laurell I., Dray C., Attane C., Duparc T., Knauf C., Valet P. (2011). Apelin, diabetes, and obesity. Endocrine 40, 1–9. 10.1007/s12020-011-9507-9
    1. Chapman N. A., Dupre D. J., Rainey J. K. (2014). The apelin receptor: physiology, pathology, cell signalling, and ligand modulation of a peptide-activated class A GPCR. Biochem. Cell. Biol. 92, 431–440. 10.1139/bcb-2014-0072
    1. Delaere F., Magnan C., Mithieux G. (2010). Hypothalamic integration of portal glucose signals and control of food intake and insulin sensitivity. Diabetes Metab. 36, 257–262. 10.1016/j.diabet.2010.05.001
    1. De Mota N., Reaux-Le Goazigo A., El Messari S., Chartrel N., Roesch D., Dujardin C., et al. . (2004). Apelin, a potent diuretic neuropeptide counteracting vasopressin actions through inhibition of vasopressin neuron activity and vasopressin release. Proc. Natl. Acad. Sci. U.S.A. 101, 10464–10469. 10.1073/pnas.0403518101
    1. Dray C., Knauf C., Daviaud D., Waget A., Boucher J., Buleon M., et al. . (2008). Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab. 8, 437–445. 10.1016/j.cmet.2008.10.003
    1. Dray C., Sakar Y., Vinel C., Daviaud D., Masri B., Garrigues L., et al. . (2013). The intestinal glucose-apelin cycle controls carbohydrate absorption in mice. Gastroenterology 144, 771–780. 10.1053/j.gastro.2013.01.004
    1. Farooqi I. S., O'Rahilly S. (2014). 20 years of leptin: human disorders of leptin action. J. Endocrinol. 223, T63–T70. 10.1530/JOE-14-0480
    1. Fukaya M., Mizuno A., Arai H., Muto K., Uebanso T., Matsuo K., et al. . (2007). Mechanism of rapid-phase insulin response to elevation of portal glucose concentration. Am. J. Physiol. Endocrinol. Metab. 293, E515–E522. 10.1152/ajpendo.00536.2006
    1. Guo L., Li Q., Wang W., Yu P., Pan H., Li P., et al. . (2009). Apelin inhibits insulin secretion in pancreatic beta-cells by activation of PI3-kinase-phosphodiesterase 3. Endocr. Res. 34, 142–154. 10.3109/07435800903287079
    1. Habchi M., Duvillard L., Cottet V., Brindisi M. C., Bouillet B., Beacco M., et al. . (2014). Circulating apelin is increased in patients with type 1 or type 2 diabetes and is associated with better glycaemic control. Clin. Endocrinol. (Oxf.) 81, 696–701. 10.1111/cen.12404
    1. Heinonen M. V., Laaksonen D. E., Karhu T., Karhunen L., Laitinen T., Kainulainen S., et al. . (2009). Effect of diet-induced weight loss on plasma apelin and cytokine levels in individuals with the metabolic syndrome. Nutr. Metab. Cardiovasc. Dis. 19, 626–633. 10.1016/j.numecd.2008.12.008
    1. Higuchi K., Masaki T., Gotoh K., Chiba S., Katsuragi I., Tanaka K., et al. . (2007). Apelin, an APJ receptor ligand, regulates body adiposity and favors the messenger ribonucleic acid expression of uncoupling proteins in mice. Endocrinology 148, 2690–2697. 10.1210/en.2006-1270
    1. Knauf C., Drougard A., Fournel A., Duparc T., Valet P. (2013). Hypothalamic actions of apelin on energy metabolism: new insight on glucose homeostasis and metabolic disorders. Horm. Metab. Res. 45, 928–934. 10.1055/s-0033-1351321
    1. Krist J., Wieder K., Kloting N., Oberbach A., Kralisch S., Wiesner T., et al. . (2013). Effects of weight loss and exercise on apelin serum concentrations and adipose tissue expression in human obesity. Obes. Facts 6, 57–69. 10.1159/000348667
    1. Lafontan M., Viguerie N. (2006). Role of adipokines in the control of energy metabolism: focus on adiponectin. Curr. Opin. Pharmacol. 6, 580–585. 10.1016/j.coph.2006.08.002
    1. Ma W. Y., Yu T. Y., Wei J. N., Hung C. S., Lin M. S., Liao Y. J., et al. . (2014). Plasma apelin: a novel biomarker for predicting diabetes. Clin. Chim. Acta 435, 18–23. 10.1016/j.cca.2014.03.030
    1. Masri B., Knibiehler B., Audigier Y. (2005). Apelin signalling: a promising pathway from cloning to pharmacology. Cell. Signal. 17, 415–426. 10.1016/j.cellsig.2004.09.018
    1. O'Carroll A. M., Lolait S. J., Harris L. E., Pope G. R. (2013). The apelin receptor APJ: journey from an orphan to a multifaceted regulator of homeostasis. J. Endocrinol. 219, R13–R35. 10.1530/JOE-13-0227
    1. Ringstrom C., Nitert M. D., Bennet H., Fex M., Valet P., Rehfeld J. F., et al. . (2010). Apelin is a novel islet peptide. Regul. Pept. 162, 44–51. 10.1016/j.regpep.2010.03.005
    1. Roy D., Perreault M., Marette A. (1998). Insulin stimulation of glucose uptake in skeletal muscles and adipose tissues in vivo is NO dependent. Am. J. Physiol. 274, E692–E699.
    1. Sawane M., Kajiya K., Kidoya H., Takagi M., Muramatsu F., Takakura N. (2013). Apelin inhibits diet-induced obesity by enhancing lymphatic and blood vessel integrity. Diabetes 62, 1970–1980. 10.2337/db12-0604
    1. Sorhede Winzell M., Magnusson C., Ahren B. (2005). The apj receptor is expressed in pancreatic islets and its ligand, apelin, inhibits insulin secretion in mice. Regul. Pept. 131, 12–17. 10.1016/j.regpep.2005.05.004
    1. Tatemoto K., Hosoya M., Habata Y., Fujii R., Kakegawa T., Zou M. X., et al. . (1998). Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res. Commun. 251, 471–476. 10.1006/bbrc.1998.9489
    1. Than A., Cheng Y., Foh L. C., Leow M. K., Lim S. C., Chuah Y. J., et al. . (2012). Apelin inhibits adipogenesis and lipolysis through distinct molecular pathways. Mol. Cell. Endocrinol. 362, 227–241. 10.1016/j.mce.2012.07.002
    1. Tishinsky J. M., Robinson L. E., Dyck D. J. (2012). Insulin-sensitizing properties of adiponectin. Biochimie 94, 2131–2136. 10.1016/j.biochi.2012.01.017
    1. Wattez J. S., Ravallec R., Cudennec B., Knauf C., Dhulster P., Valet P., et al. . (2013). Apelin stimulates both cholecystokinin and glucagon-like peptide 1 secretions in vitro and in vivo in rodents. Peptides 48, 134–136. 10.1016/j.peptides.2013.08.005
    1. Wei L., Hou X., Tatemoto K. (2005). Regulation of apelin mRNA expression by insulin and glucocorticoids in mouse 3T3-L1 adipocytes. Regul. Pept. 132, 27–32. 10.1016/j.regpep.2005.08.003
    1. Xu S., Han P., Huang M., Wu J. C., Chang C., Tsao P. S., et al. . (2012). In vivo, ex vivo, and in vitro studies on apelin's effect on myocardial glucose uptake. Peptides 37, 320–326. 10.1016/j.peptides.2012.08.004
    1. Yamamoto T., Habata Y., Matsumoto Y., Yasuhara Y., Hashimoto T., Hamajyo H., et al. . (2011). Apelin-transgenic mice exhibit a resistance against diet-induced obesity by increasing vascular mass and mitochondrial biogenesis in skeletal muscle. Biochim. Biophys. Acta 1810, 853–862. 10.1016/j.bbagen.2011.05.004
    1. Yue P., Jin H., Aillaud M., Deng A. C., Azuma J., Asagami T., et al. . (2010). Apelin is necessary for the maintenance of insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 298, E59–E67. 10.1152/ajpendo.00385.2009
    1. Yue P., Jin H., Xu S., Aillaud M., Deng A. C., Azuma J., et al. . (2011). Apelin decreases lipolysis via Gq, Gi, and AMPK-Dependent mechanisms. Endocrinology 152, 59–68. 10.1210/en.2010-0576
    1. Zhu S., Sun F., Li W., Cao Y., Wang C., Wang Y., et al. . (2011). Apelin stimulates glucose uptake through the PI3K/Akt pathway and improves insulin resistance in 3T3-L1 adipocytes. Mol. Cell. Biochem. 353, 305–313. 10.1007/s11010-011-0799-0

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