Obestatin regulates adipocyte function and protects against diet-induced insulin resistance and inflammation

FASEB Journal

Volumn 26, Issue 8, 2012, Pages 3393-3411

  Granata, Riccarda ^a   Gallo, Davide ^a   Luque, Raul M ^c,d   Baragli, Alessandra ^a   Scarlatti, Francesca ^a   Grande, Cristina ^a   Gesmundo, Iacopo ^a   Córdoba Chacón, Jose ^c,d   Bergandi, Loredana ^b   Settanni, Fabio ^a   Togliatto, Gabriele ^a   Volante, Marco ^b   Garetto, Stefano ^a   Annunziata, Marta ^a   Chanclón, Belén ^c,d   Gargantini, Eleonora ^a   Rocchietto, Stefano ^b   Matera, Lina ^a   Datta, Giacomo ^b   Morino, Mario ^b   Brizzi, Maria Felice ^a   Ong, Huy ^e   Camussi, Giovanni ^a   Castaño, Justo P ^c,d   Papotti, Mauro ^b   Ghigo, Ezio ^a   more..

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF CÓRDOBA   (Spain)

^d Instituto de Salud Carlos III   (Spain)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Glucose uptake; High fat diet; Lipolysis; PI3K Akt and AMP activated protein kinase; Sirtuin 1

Indexed keywords

ADIPONECTIN; GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOPRENALINE; LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OBESTATIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SIRTUIN 1; SMALL INTERFERING RNA;

ADIPOCYTE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INFLAMMATION; INSULIN RELEASE; INSULIN RESISTANCE; LIPID DIET; LIPOLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OMENTUM; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SUBCUTANEOUS TISSUE;

3T3-L1 CELLS; ADIPOCYTES; ADIPONECTIN; ANIMALS; APOPTOSIS; DIET, HIGH-FAT; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GHRELIN; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INFLAMMATION; INSULIN RESISTANCE; ISLETS OF LANGERHANS; LEPTIN; LIPOLYSIS; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

MUS;

EID: 84864768395     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-201343     Document Type: Article

References (61)

1. Ahima, R. S., and Flier, J. S. (2000) Adipose tissue as an endocrine organ. Trends Endocrinol. Metab. 11, 327-332
2. Hotamisligil, G. S. (2006) Inflammation and metabolic disorders. Nature 444, 860-867
3. Schenk, S., Saberi, M., and Olefsky, J. M. (2008) Insulin sensitivity: modulation by nutrients and inflammation. J. Clin. Invest. 118, 2992-3002
4. Zhang, J. V., Ren, P. G., Avsian-Kretchmer, O., Luo, C. W., Rauch, R., Klein, C., and Hsueh, A. J. (2005) Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin's effects on food intake. Science 310, 996-999 (Pubitemid 41611907)
5. Ataka, K., Inui, A., Asakawa, A., Kato, I., and Fujimiya, M. (2008) Obestatin inhibits motor activity in the antrum and duodenum in the fed state of conscious rats. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1210-G1218
6. Zhang, J. V., Jahr, H., Luo, C. W., Klein, C., Van Kolen, K., Ver Donck, L., De, A., Baart, E., Li, J., Moechars, D., and Hsueh, A. J. (2008) Obestatin induction of early-response gene expression in gastrointestinal and adipose tissues and the mediatory role of G protein-coupled receptor, GPR39. Mol. Endocrinol. 22, 1464-1475 (Pubitemid 351787005)
7. Chartrel, N., Alvear-Perez, R., Leprince, J., Iturrioz, X., Reaux-Le Goazigo, A., Audinot, V., Chomarat, P., Coge, F., Nosjean, O., Rodriguez, M., Galizzi, J. P., Boutin, J. A., Vaudry, H., and Llorens-Cortes, C. (2007) Comment on "Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin's effects on food intake." Science 315, 766; author reply 766
8. Holst, B., Egerod, K. L., Schild, E., Vickers, S. P., Cheetham, S., Gerlach, L. O., Storjohann, L., Stidsen, C. E., Jones, R., Beck-Sickinger, A. G., and Schwartz, T. W. (2007) GPR39 signaling is stimulated by zinc ions but not by obestatin. Endocrinology 148, 13-20 (Pubitemid 46021433)
9. Tremblay, F., Perreault, M., Klaman, L. D., Tobin, J. F., Smith, E., and Gimeno, R. E. (2007) Normal food intake and body weight in mice lacking the G protein-coupled receptor GPR39. Endocrinology 148, 501-506 (Pubitemid 46143155)
10. Alloatti, G., Arnoletti, E., Bassino, E., Penna, C., Perrelli, M. G., Ghe, C., and Muccioli, G. (2010) Obestatin affords cardioprotection to the ischemic-reperfused isolated rat heart and inhibits apoptosis in cultures of similarly stressed cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 299, H470-H481
11. Granata, R., Settanni, F., Gallo, D., Trovato, L., Biancone, L., Cantaluppi, V., Nano, R., Annunziata, M., Campiglia, P., Arnoletti, E., Ghe, C., Volante, M., Papotti, M., Muccioli, G., and Ghigo, E. (2008) Obestatin promotes survival of pancreatic beta-cells and human islets and induces expression of genes involved in the regulation of beta-cell mass and function. Diabetes 57, 967-979
12. Seim, I., Walpole, C., Amorim, L., Josh, P., Herington, A., and Chopin, L. (2012) The expanding roles of the ghrelin-gene derived peptide obestatin in health and disease. Mol. Cell. Endocrinol. 340, 111
13. Granata, R., Baragli, A., Settanni, F., Scarlatti, F., and Ghigo, E. (2010) Unraveling the role of the ghrelin gene peptides in the endocrine pancreas. J. Mol. Endocrinol. 45, 107-118
14. Gronberg, M., Tsolakis, A. V., Magnusson, L., Janson, E. T., and Saras, J. (2008) Distribution of obestatin and ghrelin in human tissues: immunoreactive cells in the gastrointestinal tract, pancreas, and mammary glands. J. Histochem. Cytochem. 56, 793-801
15. Volante, M., Rosas, R., Ceppi, P., Rapa, I., Cassoni, P., Wiedenmann, B., Settanni, F., Granata, R., and Papotti, M. (2009) Obestatin in human neuroendocrine tissues and tumours: expression and effect on tumour growth. J. Pathol. 218, 458-466
16. Granata, R., Volante, M., Settanni, F., Gauna, C., Ghe, C., Annunziata, M., Deidda, B., Gesmundo, I., Abribat, T., van der Lely, A. J., Muccioli, G., Ghigo, E., and Papotti, M. (2010) Unacylated ghrelin and obestatin increase islet cell mass and prevent diabetes in streptozotocin-treated newborn rats. J. Mol. Endocrinol. 45, 9-17
17. Catalan, V., Gomez-Ambrosi, J., Rotellar, F., Silva, C., Gil, M. J., Rodriguez, A., Cienfuegos, J. A., Salvador, J., and Fruhbeck, G. (2007) The obestatin receptor (GPR39) is expressed in human adipose tissue and is down-regulated in obesity-associated type 2 diabetes mellitus. Clin. Endocrinol. (Oxf.) 66, 598-601 (Pubitemid 46434943)
18. Egerod, K. L., Holst, B., Petersen, P. S., Hansen, J. B., Mulder, J., Hokfelt, T., and Schwartz, T. W. (2007) GPR39 splice variants versus antisense gene LYPD1: expression and regulation in gastrointestinal tract, endocrine pancreas, liver, and white adipose tissue. Mol. Endocrinol. 21, 1685-1698 (Pubitemid 47001091)
19. Miegueu, P., St Pierre, D., Broglio, F., and Cianflone, K. (2011) Effect of desacyl ghrelin, obestatin and related peptides on triglyceride storage, metabolism and GHSR signaling in 3T3-L1 adipocytes. J. Cell. Biochem. 112, 704-714
20. Gurriaran-Rodriguez, U., Al-Massadi, O., Roca-Rivada, A., Crujeiras, A. B., Gallego, R., Pardo, M., Seoane, L. M., Pazos, Y., Casanueva, F. F., and Camina, J. P. (2011) Obestatin as a regulator of adipocyte metabolism and adipogenesis. J. Cell. Mol. Med. 15, 1927-1940
21. Hauner, H., Entenmann, G., Wabitsch, M., Gaillard, D., Ailhaud, G., Negrel, R., and Pfeiffer, E. F. (1989) Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J. Clin. Invest. 84, 1663-1670 (Pubitemid 19272257)
22. Granata, R., Settanni, F., Biancone, L., Trovato, L., Nano, R., Bertuzzi, F., Destefanis, S., Annunziata, M., Martinetti, M., Catapano, F., Ghe, C., Isgaard, J., Papotti, M., Ghigo, E., and Muccioli, G. (2007) Acylated and unacylated ghrelin promote proliferation and inhibit apoptosis of pancreatic beta-cells and human islets: involvement of 3′,5′-cyclic adenosine monophosphate/protein kinase A, extracellular signal-regulated kinase 1/2, and phosphatidyl inositol 3-kinase/Akt signaling. Endocrinology 148, 512-529 (Pubitemid 46143157)
23. Mulumba, M., Jossart, C., Granata, R., Gallo, D., Escher, E., Ghigo, E., Servant, M. J., Marleau, S., and Ong, H. (2010) GPR103b functions in the peripheral regulation of adipogenesis. Mol. Endocrinol. 24, 1615-1625
24. Luque, R. M., Lin, Q., Cordoba-Chacon, J., Subbaiah, P. V., Buch, T., Waisman, A., Vankelecom, H., and Kineman, R. D. (2011) Metabolic impact of adult-onset, isolated, growth hormone deficiency (AOiGHD) due to destruction of pituitary somatotropes. PLoS ONE 6, e15767
25. Irako, T., Akamizu, T., Hosoda, H., Iwakura, H., Ariyasu, H., Tojo, K., Tajima, N., and Kangawa, K. (2006) Ghrelin prevents development of diabetes at adult age in streptozotocin-treated newborn rats. Diabetologia 49, 1264-1273
26. Adeghate, E., and Ponery, A. S. (2002) Ghrelin stimulates insulin secretion from the pancreas of normal and diabetic rats. J. Neuroendocrinol. 14, 555-560 (Pubitemid 34679218)
27. Bonzon-Kulichenko, E., Fernandez-Agullo, T., Molto, E., Serrano, R., Fernandez, A., Ros, M., Carrascosa, J. M., Arribas, C., Martinez, C., Andres, A., and Gallardo, N. (2011) Regulation of insulin-stimulated glucose uptake in rat white adipose tissue upon chronic central leptin infusion: effects on adiposity. Endocrinology 152, 1366-1377
28. Nishiumi, S., Bessyo, H., Kubo, M., Aoki, Y., Tanaka, A., Yoshida, K., and Ashida, H. (2010) Green and black tea suppress hyperglycemia and insulin resistance by retaining the expression of glucose transporter 4 in muscle of high-fat diet-fed C57BL/6J mice. J. Agric. Food Chem. 58, 12916-12923
29. Bourron, O., Daval, M., Hainault, I., Hajduch, E., Servant, J. M., Gautier, J. F., Ferre, P., and Foufelle, F. (2010) Biguanides and thiazolidinediones inhibit stimulated lipolysis in human adipocytes through activation of AMP-activated protein kinase. Diabetologia 53, 768-778
30. Daval, M., Diot-Dupuy, F., Bazin, R., Hainault, I., Viollet, B., Vaulont, S., Hajduch, E., Ferre, P., and Foufelle, F. (2005) Anti-lipolytic action of AMP-activated protein kinase in rodent adipocytes. J. Biol. Chem. 280, 25250-25257 (Pubitemid 40934619)
31. Kadowaki, T., Yamauchi, T., Kubota, N., Hara, K., Ueki, K., and Tobe, K. (2006) Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J. Clin. Invest. 116, 1784-1792 (Pubitemid 44033298)
32. Muller, G., Ertl, J., Gerl, M., and Preibisch, G. (1997) Leptin impairs metabolic actions of insulin in isolated rat adipocytes. J. Biol. Chem. 272, 10585-10593 (Pubitemid 27181066)
33. Siegrist-Kaiser, C. A., Pauli, V., Juge-Aubry, C. E., Boss, O., Pernin, A., Chin, W. W., Cusin, I., Rohner-Jeanrenaud, F., Burger, A. G., Zapf, J., and Meier, C. A. (1997) Direct effects of leptin on brown and white adipose tissue. J. Clin. Invest. 100, 2858-2864 (Pubitemid 28007556)
34. Yoshizaki, T., Milne, J. C., Imamura, T., Schenk, S., Sonoda, N., Babendure, J. L., Lu, J. C., Smith, J. J., Jirousek, M. R., and Olefsky, J. M. (2009) SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes. Mol. Cell. Biol. 29, 1363-1374
35. Zhao, Y. F., Feng, D. D., and Chen, C. (2006) Contribution of adipocyte-derived factors to beta-cell dysfunction in diabetes. Int. J. Biochem. Cell Biol. 38, 804-819 (Pubitemid 43363413)
36. Gurriaran-Rodriguez, U., Al-Massadi, O., Crujeiras, A. B., Mosteiro, C. S., Amil-Diz, M., Beiroa, D., Nogueiras, R., Seoane, L. M., Gallego, R., Pazos, Y., Casanueva, F. F., and Camina, J. P. (2011) Preproghrelin expression is a key target for insulin action on adipogenesis. J. Endocrinol. 210, R1-7
37. Morash, M. G., Gagnon, J., Nelson, S., and Anini, Y. (2010) Tissue distribution and effects of fasting and obesity on the ghrelin axis in mice. Regul. Pept. 163, 62-73
38. Wang, Z. Q., Zuberi, A. R., Zhang, X. H., Macgowan, J., Qin, J., Ye, X., Son, L., Wu, Q., Lian, K., and Cefalu, W. T. (2007) Effects of dietary fibers on weight gain, carbohydrate metabolism, and gastric ghrelin gene expression in mice fed a high-fat diet. Metabolism 56, 1635-1642 (Pubitemid 350060930)
39. Challa, T. D., Beaton, N., Arnold, M., Rudofsky, G., Langhans, W., and Wolfrum, C. (2012) Regulation of adipocyte formation by GLP-1/GLP-1R signaling. J. Biol. Chem. 287, 6421-6430
40. Boney, C. M., Gruppuso, P. A., Faris, R. A., and Frackelton, A. R., Jr. (2000) The critical role of Shc in insulin-like growth factor-I-mediated mitogenesis and differentiation in 3T3-L1 preadipocytes. Mol. Endocrinol. 14, 805-813 (Pubitemid 32260494)
41. Kim, M. S., Yoon, C. Y., Jang, P. G., Park, Y. J., Shin, C. S., Park, H. S., Ryu, J. W., Pak, Y. K., Park, J. Y., Lee, K. U., Kim, S. Y., Lee, H. K., Kim, Y. B., and Park, K. S. (2004) The mitogenic and antiapoptotic actions of ghrelin in 3T3-L1 adipocytes. Mol. Endocrinol. 18, 2291-2301
42. Manning, B. D., and Cantley, L. C. (2007) AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274 (Pubitemid 46962095)
43. Rosen, E. D., and MacDougald, O. A. (2006) Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7, 885-896 (Pubitemid 44871415)
44. Perrini, S., Laviola, L., Cignarelli, A., Melchiorre, M., De Stefano, F., Caccioppoli, C., Natalicchio, A., Orlando, M. R., Garruti, G., De Fazio, M., Catalano, G., Memeo, V., Giorgino, R., and Giorgino, F. (2008) Fat depot-related differences in gene expression, adiponectin secretion, and insulin action and signalling in human adipocytes differentiated in vitro from precursor stromal cells. Diabetologia 51, 155-164 (Pubitemid 350197987)
45. Wajchenberg, B. L. (2000) Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr. Rev. 21, 697-738
46. Adams, M., Montague, C. T., Prins, J. B., Holder, J. C., Smith, S. A., Sanders, L., Digby, J. E., Sewter, C. P., Lazar, M. A., Chatterjee, V. K., and O'Rahilly, S. (1997) Activators of peroxisome proliferator-activated receptor gamma have depot-specific effects on human preadipocyte differentiation. J. Clin. Invest. 100, 3149-3153 (Pubitemid 28022853)
47. Rodriguez, A., Gomez-Ambrosi, J., Catalan, V., Gil, M. J., Becerril, S., Sainz, N., Silva, C., Salvador, J., Colina, I., and Fruhbeck, G. (2009) Acylated and desacyl ghrelin stimulate lipid accumulation in human visceral adipocytes. Int. J. Obes. (Lond.) 33, 541-552
48. Giorgino, F., Laviola, L., and Eriksson, J. W. (2005) Regional differences of insulin action in adipose tissue: insights from in vivo and in vitro studies. Acta Physiol. Scand. 183, 13-30 (Pubitemid 40188033)
49. Fogarty, S., and Hardie, D. G. (2010) Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim. Biophys. Acta 1804, 581-591
50. Muccioli, G., Pons, N., Ghe, C., Catapano, F., Granata, R., and Ghigo, E. (2004) Ghrelin and des-acyl ghrelin both inhibit isoproterenol-induced lipolysis in rat adipocytes via a non-type 1a growth hormone secretagogue receptor. Eur. J. Pharmacol. 498, 27-35 (Pubitemid 39208057)
51. Thompson, N. M., Gill, D. A., Davies, R., Loveridge, N., Houston, P. A., Robinson, I. C., and Wells, T. (2004) Ghrelin and des-octanoyl ghrelin promote adipogenesis directly in vivo by a mechanism independent of the type 1a growth hormone secretagogue receptor. Endocrinology 145, 234-242 (Pubitemid 38202164)
52. Baragli, A., Ghe, C., Arnoletti, E., Granata, R., Ghigo, E., and Muccioli, G. (2011) Acylated and unacylated ghrelin attenuate isoproterenol-induced lipolysis in isolated rat visceral adipocytes through activation of phosphoinositide 3-kinase gamma and phosphodiesterase 3B. Biochim. Biophys. Acta 1811, 386-396
53. Minokoshi, Y., Kahn, C. R., and Kahn, B. B. (2003) Tissue-specific ablation of the GLUT4 glucose transporter or the insulin receptor challenges assumptions about insulin action and glucose homeostasis. J. Biol. Chem. 278, 33609-33612 (Pubitemid 37553190)
54. Huang, S., and Czech, M. P. (2007) The GLUT4 glucose transporter. Cell Metab. 5, 237-252 (Pubitemid 46477860)
55. Pfluger, P. T., Herranz, D., Velasco-Miguel, S., Serrano, M., and Tschop, M. H. (2008) Sirt1 protects against high-fat diet-induced metabolic damage. Proc. Natl. Acad. Sci. U. S. A. 105, 9793-9798 (Pubitemid 352031379)
56. Liang, F., Kume, S., and Koya, D. (2009) SIRT1 and insulin resistance. Nat. Rev. Endocrinol. 5, 367-373
57. Reimer, M. K., and Ahren, B. (2002) Altered beta-cell distribution of pdx-1 and GLUT-2 after a short-term challenge with a high-fat diet in C57BL/6J mice. Diabetes 51(Suppl. 1), S138-143 (Pubitemid 34761509)
58. Wueest, S., Rapold, R. A., Schumann, D. M., Rytka, J. M., Schildknecht, A., Nov, O., Chervonsky, A. V., Rudich, A., Schoenle, E. J., Donath, M. Y., and Konrad, D. (2010) Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J. Clin. Invest. 120, 191-202
59. Brunetti, L., Leone, S., Orlando, G., Recinella, L., Ferrante, C., Chiavaroli, A., Di Nisio, C., Di Michele, P., and Vacca, M. (2009) Effects of obestatin on feeding and body weight after standard or cafeteria diet in the rat. Peptides 30, 1323-1327
60. Kim, J. Y., van de Wall, E., Laplante, M., Azzara, A., Trujillo, M. E., Hofmann, S. M., Schraw, T., Durand, J. L., Li, H., Li, G., Jelicks, L. A., Mehler, M. F., Hui, D. Y., Deshaies, Y., Shulman, G. I., Schwartz, G. J., and Scherer, P. E. (2007) Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J. Clin. Invest. 117, 2621-2637 (Pubitemid 47494363)
61. Gaidhu, M. P., Anthony, N. M., Patel, P., Hawke, T. J., and Ceddia, R. B. (2010) Dysregulation of lipolysis and lipid metabolism in visceral and subcutaneous adipocytes by high-fat diet: role of ATGL, HSL, and AMPK. Am. J. Physiol. Cell Physiol. 298, C961-C971