Gut-derived serotonin is a multifunctional determinant to fasting adaptation

Cell Metabolism

Volumn 16, Issue 5, 2012, Pages 588-600

  Sumara, Grzegorz ^a   Sumara, Olga ^a   Kim, Jason K ^b   Karsenty, Gerard ^a  

^a NewYork Presbyterian Hospital   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; GLUCOSE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 2; GUT DERIVED SEROTONIN; HTR2B PROTEIN; LIPID; SEROTONIN; SEROTONIN RECEPTOR; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ADIPOCYTE; ARTICLE; DIET RESTRICTION; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; INTESTINE; LIPOLYSIS; LIVER; LIVER CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTONIN BLOOD LEVEL; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84871451681     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.09.014     Document Type: Article

References (48)

1. Alegre, M., Ciudad, C.J., Fillat, C., and Guinovart, J.J. (1988). Determination of glucose-6-phosphatase activity using the glucose dehydrogenase-coupled reaction. Anal. Biochem. 173, 185-189.
2. Amireault, P., Hatia, S., Bayard, E., Bernex, F., Collet, C., Callebert, J., Launay, J.M., Hermine, O., Schneider, E., Mallet, J., et al. (2011). Ineffective erythropoiesis with reduced red blood cell survival in serotonin-deficient mice. Proc. Natl. Acad. Sci. USA 108, 13141-13146.
3. Anthonsen, M.W., Rönnstrand, L., Wernstedt, C., Degerman, E., and Holm, C. (1998). Identification of novel phosphorylation sites in hormone-sensitive lipase that are phosphorylated in response to isoproterenol and govern activation properties in vitro. J. Biol. Chem. 273, 215-221.
4. Bäckhed, F., Ding, H., Wang, T., Hooper, L.V., Koh, G.Y., Nagy, A., Semenkovich, C.F., and Gordon, J.I. (2004). The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 101, 15718-15723.
5. Berger, M., Gray, J.A., and Roth, B.L. (2009). The expanded biology of serotonin. Annu. Rev. Med. 60, 355-366.
6. Black, A., Allison, D.B., Shapses, S.A., Tilmont, E.M., Handy, A.M., Ingram, D.K., Roth, G.S., and Lane, M.A. (2001). Calorie restriction and skeletal mass in rhesus monkeys (Macaca mulatta): evidence for an effect mediated through changes in body size. J. Gerontol. A Biol. Sci. Med. Sci. 56, B98-B107.
7. Carlson, L.A., Ekelund, L.G., and Orö, L. (1967). Metabolic and cardio-vascular effects of serotonin. Life Sci. 6, 261-271.
8. Côté, F., Fligny, C., Bayard, E., Launay, J.M., Gershon, M.D., Mallet, J., and Vodjdani, G. (2007). Maternal serotonin is crucial for murine embryonic development. Proc. Natl. Acad. Sci. USA 104, 329-334.
9. Dees, C., Akhmetshina, A., Zerr, P., Reich, N., Palumbo, K., Horn, A., Jüngel, A., Beyer, C., Krönke, G., Zwerina, J., et al. (2011). Platelet-derived serotonin links vascular disease and tissue fibrosis. J. Exp. Med. 208, 961-972.
10. Djouder, N., Tuerk, R.D., Suter, M., Salvioni, P., Thali, R.F., Scholz, R., Vaahtomeri, K., Auchli, Y., Rechsteiner, H., Brunisholz, R.A., et al. (2010). PKA phosphorylates and inactivates AMPKalpha to promote efficient lipolysis. EMBO J. 29, 469-481.
11. Ducy, P., Desbois, C., Boyce, B., Pinero, G., Story, B., Dunstan, C., Smith, E., Bonadio, J., Goldstein, S., Gundberg, C., et al. (1996). Increased bone formation in osteocalcin-deficient mice. Nature 382, 448-452.
12. Eguchi, J., Wang, X., Yu, S., Kershaw, E.E., Chiu, P.C., Dushay, J., Estall, J.L., Klein, U., Maratos-Flier, E., and Rosen, E.D. (2011). Transcriptional control of adipose lipid handling by IRF4. Cell Metab. 13, 249-259.
13. Fisher, F.M., Kleiner, S., Douris, N., Fox, E.C., Mepani, R.J., Verdeguer, F., Wu, J., Kharitonenkov, A., Flier, J.S., Maratos-Flier, E., and Spiegelman, B.M. (2012). FGF21 regulates PGC-1a and browning of white adipose tissues in adaptive thermogenesis. Genes Dev. 26, 271-281.
14. Fligny, C., Fromes, Y., Bonnin, P., Darmon, M., Bayard, E., Launay, J.M., Côté, F., Mallet, J., and Vodjdani, G. (2008). Maternal serotonin influences cardiac function in adult offspring. FASEB J. 22, 2340-2349.
15. González-Rodriguez, A., Nevado, C., Escrivá, F., Sesti, G., Rondinone, C.M., Benito, M., and Valverde, A.M. (2008). PTP1B deficiency increases glucose uptake in neonatal hepatocytes: involvement of IRA/GLUT2 complexes. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G338-G347.
16. Greenberg, A.S., Shen, W.J., Muliro, K., Patel, S., Souza, S.C., Roth, R.A., and Kraemer, F.B. (2001). Stimulation of lipolysis and hormone-sensitive lipase via the extracellular signal-regulated kinase pathway. J. Biol. Chem. 276, 45456-45461.
17. Guillam, M.T., Burcelin, R., and Thorens, B. (1998). Normal hepatic glucose production in the absence of GLUT2 reveals an alternative pathway for glucose release from hepatocytes. Proc. Natl. Acad. Sci. USA 95, 12317-12321.
18. Haemmerle, G., Lass, A., Zimmermann, R., Gorkiewicz, G., Meyer, C., Rozman, J., Heldmaier, G., Maier, R., Theussl, C., Eder, S., et al. (2006). Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312, 734-737.
19. Inagaki, T., Dutchak, P., Zhao, G., Ding, X., Gautron, L., Parameswara, V., Li, Y., Goetz, R., Mohammadi, M., Esser, V., et al. (2007). Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 5, 415-425.
20. Iwata, T., Taniguchi, H., Kuwajima, M., Taniguchi, T., Okuda, Y., Sukeno, A., Ishimoto, K., Mizusawa, N., and Yoshimoto, K. (2012). The action of D-dopachrome tautomerase as an adipokine in adipocyte lipid metabolism. PLoS ONE 7, e33402.
21. Kim, H., Toyofuku, Y., Lynn, F.C., Chak, E., Uchida, T., Mizukami, H., Fujitani, Y., Kawamori, R., Miyatsuka, T., Kosaka, Y., et al. (2010). Serotonin regulates pancreatic beta cell mass during pregnancy. Nat. Med. 16, 804-808.
22. Lee, N.K., Sowa, H., Hinoi, E., Ferron, M., Ahn, J.D., Confavreux, C., Dacquin, R., Mee, P.J., McKee, M.D., Jung, D.Y., et al. (2007). Endocrine regulation of energy metabolism by the skeleton. Cell 130, 456-469.
23. Lesurtel, M., Graf, R., Aleil, B., Walther, D.J., Tian, Y., Jochum, W., Gachet, C., Bader, M., and Clavien, P.A. (2006). Platelet-derived serotonin mediates liver regeneration. Science 312, 104-107.
24. Lin, H.V., and Accili, D. (2011). Hormonal regulation of hepatic glucose production in health and disease. Cell Metab. 14, 9-19.
25. Liu, Q., Yang, Q., Sun, W., Vogel, P., Heydorn, W., Yu, X.Q., Hu, Z., Yu, W., Jonas, B., Pineda, R., et al. (2008). Discovery and characterization of novel tryptophan hydroxylase inhibitors that selectively inhibit serotonin synthesis in the gastrointestinal tract. J. Pharmacol. Exp. Ther. 325, 47-55.
26. Martinez-Botas, J., Anderson, J.B., Tessier, D., Lapillonne, A., Chang, B.H., Quast, M.J., Gorenstein, D., Chen, K.H., and Chan, L. (2000). Absence of perilipin results in leanness and reverses obesity in Lepr(db/db) mice. Nat. Genet. 26, 474-479.
27. Matschinsky, F.M. (2009). Assessing the potential of glucokinase activators in diabetes therapy. Nat. Rev. Drug Discov. 8, 399-416.
28. Moore, M.C., Geho, W.B., Lautz, M., Farmer, B., Neal, D.W., and Cherrington, A.D. (2004). Portal serotonin infusion and glucose disposal in conscious dogs. Diabetes 53, 14-20.
29. Osuga, J., Ishibashi, S., Oka, T., Yagyu, H., Tozawa, R., Fujimoto, A., Shionoiri, F., Yahagi, N., Kraemer, F.B., Tsutsumi, O., and Yamada, N. (2000). Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity. Proc. Natl. Acad. Sci. USA 97, 787-792.
30. Paulmann, N., Grohmann, M., Voigt, J.P., Bert, B., Vowinckel, J., Bader, M., Skelin, M., Jevsek, M., Fink, H., Rupnik, M., and Walther, D.J. (2009). Intracellular serotonin modulates insulin secretion from pancreatic beta-cells by protein serotonylation. PLoS Biol. 7, e1000229.
31. Perea, A., Clemente, F., Martinell, J., Villanueva-Peñacarrillo, M.L., and Valverde, I. (1995). Physiological effect of glucagon in human isolated adipocytes. Horm. Metab. Res. 27, 372-375.
32. Potthoff, M.J., Inagaki, T., Satapati, S., Ding, X., He, T., Goetz, R., Mohammadi, M., Finck, B.N., Mangelsdorf, D.J., Kliewer, S.A., and Burgess, S.C. (2009). FGF21 induces PGC-1alpha and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc. Natl. Acad. Sci. USA 106, 10853-10858.
33. Reyes, A., Burgos, M.E., Hubert, E., and Slebe, J.C. (1987). Selective thiol group modification renders fructose-1,6-bisphosphatase insensitive to fructose 2,6-bisphosphate inhibition. J. Biol. Chem. 262, 8451-8454.
34. Ríos-Lugo, M.J., Cano, P., Jiménez-Ortega, V., Fernández-Mateos, M.P., Scacchi, P.A., Cardinali, D.P., and Esquifino, A.I. (2010). Melatonin effect on plasma adiponectin, leptin, insulin, glucose, triglycerides and cholesterol in normal and high fat-fed rats. J. Pineal Res. 49, 342-348.
35. Rosen, E.D., and Spiegelman, B.M. (2000). Molecular regulation of adipogenesis. Annu. Rev. Cell Dev. Biol. 16, 145-171.
36. Saltiel, A.R., and Kahn, C.R. (2001). Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799-806.
37. Samuel, V.T., and Shulman, G.I. (2012). Mechanisms for insulin resistance: common threads and missing links. Cell 148, 852-871.
38. Schweiger, M., Schreiber, R., Haemmerle, G., Lass, A., Fledelius, C., Jacobsen, P., Tornqvist, H., Zechner, R., and Zimmermann, R. (2006). Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism. J. Biol. Chem. 281, 40236-40241.
39. Söhle, J., Machuy, N., Smailbegovic, E., Holtzmann, U., Grönniger, E., Wenck, H., Stäb, F., and Winnefeld, M. (2012). Identification of new genes involved in human adipogenesis and fat storage. PLoS ONE 7, e31193.
40. Unger, R.H., and Cherrington, A.D. (2012). Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. J. Clin. Invest. 122, 4-12.
41. Vegiopoulos, A., and Herzig, S. (2007). Glucocorticoids, metabolism and metabolic diseases. Mol. Cell. Endocrinol. 275, 43-61.
42. Vestergaard, E.T., Gormsen, L.C., Jessen, N., Lund, S., Hansen, T.K., Moller, N., and Jorgensen, J.O. (2008). Ghrelin infusion in humans induces acute insulin resistance and lipolysis independent of growth hormone signaling. Diabetes 57, 3205-3210.
43. Wahren, J., and Ekberg, K. (2007). Splanchnic regulation of glucose production. Annu. Rev. Nutr. 27, 329-345.
44. Wei, W., Dutchak, P.A., Wang, X., Ding, X., Wang, X., Bookout, A.L., Goetz, R., Mohammadi, M., Gerard, R.D., Dechow, P.C., et al. (2012). Fibroblast growth factor 21 promotes bone loss by potentiating the effects of peroxisome proliferator- activated receptor g. Proc. Natl. Acad. Sci. USA 109, 3143-3148.
45. Xu, C., He, J., Jiang, H., Zu, L., Zhai, W., Pu, S., and Xu, G. (2009). Direct effect of glucocorticoids on lipolysis in adipocytes. Mol. Endocrinol. 23, 1161-1170.
46. Yadav, V.K., Ryu, J.H., Suda, N., Tanaka, K.F., Gingrich, J.A., Schütz, G., Glorieux, F.H., Chiang, C.Y., Zajac, J.D., Insogna, K.L., et al. (2008). Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 135, 825-837.
47. Yadav, V.K., Balaji, S., Suresh, P.S., Liu, X.S., Lu, X., Li, Z., Guo, X.E., Mann, J.J., Balapure, A.K., Gershon, M.D., et al. (2010). Pharmacological inhibition of gut-derived serotonin synthesis is a potential bone anabolic treatment for osteoporosis. Nat. Med. 16, 308-312.
48. Zechner, R., Zimmermann, R., Eichmann, T.O., Kohlwein, S.D., Haemmerle, G., Lass, A., and Madeo, F. (2012). FAT SIGNALS - lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 15, 279-291.