A Novel Regulatory Function of Sweet Taste-Sensing Receptor in Adipogenic Differentiation of 3T3-L1 Cells

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Masubuchi, Yosuke ^a   Nakagawa, Yuko ^a   Ma, Jinhui ^a   Sasaki, Tsutomu ^a   Kitamura, Tadahiro ^a   Yamamoto, Yoritsuna ^b   Kurose, Hitoshi ^c   Kojima, Itaru ^a   Shibata, Hiroshi ^a  

^a GUNMA UNIVERSITY   (Japan)

^b NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CCAAT ENHANCER BINDING PROTEIN ALPHA; CHOLERA TOXIN; CYCLIC AMP; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; GUSTDUCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SACCHARIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; SUCRALOSE; T1R2 RECEPTOR; T1R3 RECEPTOR; UNCLASSIFIED DRUG;

ADIPOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN 3T3; CELL STRAIN HEK293; CONTROLLED STUDY; GENE EXPRESSION; MALE; MOUSE; NONHUMAN; PROADIPOCYTE; TASTE BUD; UPREGULATION;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CYCLIC AMP; GENE EXPRESSION; GTP-BINDING PROTEINS; HUMANS; MALE; MICE; RECEPTORS, G-PROTEIN-COUPLED; TASTE BUDS;

EID: 84872392828     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054500     Document Type: Article

References (53)

1. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, et al. (2001) Mammalian sweet taste receptors. Cell 106: 381-390.
2. Kojima I, Nakagawa Y, (2011) The Role of the Sweet Taste Receptor in Enteroendocrine Cells and Pancreatic beta-Cells. Diabetes Metab J 35: 451-457.
3. Roper SD, (2007) Signal transduction and information processing in mammalian taste buds. Pflugers Arch 454: 759-776.
4. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Varadarajan V, et al. (2003) Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 301: 850-853.
5. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, et al. (2003) The receptors for mammalian sweet and umami taste. Cell 115: 255-266.
6. Delay ER, Hernandez NP, Bromley K, Margolskee RF, (2006) Sucrose and monosodium glutamate taste thresholds and discrimination ability of T1R3 knockout mice. Chem Senses 31: 351-357.
7. Wong GT, Gannon KS, Margolskee RF, (1996) Transduction of bitter and sweet taste by gustducin. Nature 381: 796-800.
8. Danilova V, Damak S, Margolskee RF, Hellekant G, (2006) Taste responses to sweet stimuli in alpha-gustducin knockout and wild-type mice. Chem Senses 31: 573-580.
9. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Perez CA, et al. (2006) Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 31: 253-264.
10. Margolskee RF, Dyer J, Kokrashvili Z, Salmon KS, Ilegems E, et al. (2007) T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci U S A 104: 15075-15080.
11. Nakagawa Y, Nagasawa M, Yamada S, Hara A, Mogami H, et al. (2009) Sweet taste receptor expressed in pancreatic beta-cells activates the calcium and cyclic AMP signaling systems and stimulates insulin secretion. PLoS One 4: e5106.
12. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, et al. (2007) Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci U S A 104: 15069-15074.
13. Kokrashvili Z, Mosinger B, Margolskee RF, (2009) Taste signaling elements expressed in gut enteroendocrine cells regulate nutrient-responsive secretion of gut hormones. Am J Clin Nutr 90: 822S-825S.
14. Shibata H, Suzuki Y, Omata W, Tanaka S, Kojima I, (1995) Dissection of GLUT4 recycling pathway into exocytosis and endocytosis in rat adipocytes. Evidence that GTP-binding proteins are involved in both processes. J Biol Chem 270: 11489-11495.
15. Maruyama Y, Yasuda R, Kuroda M, Eto Y, (2012) Kokumi substances, enhancers of basic tastes, induce responses in calcium-sensing receptor expressing taste cells. PLoS One 7: e34489.
16. Djian P, Phillips M, Green H, (1985) The activation of specific gene transcription in the adipose conversion of 3T3 cells. J Cell Physiol 124: 554-556.
17. Liu LB, Omata W, Kojima I, Shibata H, (2007) The SUMO conjugating enzyme Ubc9 is a regulator of GLUT4 turnover and targeting to the insulin-responsive storage compartment in 3T3-L1 adipocytes. Diabetes 56: 1977-1985.
18. Rodbell M, (1964) Metabolism of Isolated Fat Cells. I. Effects of Hormones on Glucose Metabolism and Lipolysis. J Biol Chem 239: 375-380.
19. Hattori H, Ishihara M, Fukuda T, Suda T, Katagiri T, (2006) Establishment of a novel method for enriching osteoblast progenitors from adipose tissues using a difference in cell adhesive properties. Biochem Biophys Res Commun 343: 1118-1123.
20. Jones DT, Reed RR, (1987) Molecular cloning of five GTP-binding protein cDNA species from rat olfactory neuroepithelium. J Biol Chem 262: 14241-14249.
21. Miller RT, Masters SB, Sullivan KA, Beiderman B, Bourne HR, (1988) A mutation that prevents GTP-dependent activation of the alpha chain of Gs. Nature 334: 712-715.
22. Lee E, Taussig R, Gilman AG, (1992) The G226A mutant of Gs alpha highlights the requirement for dissociation of G protein subunits. J Biol Chem 267: 1212-1218.
23. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ, (2004) Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279: 37215-37218.
24. Bystrova MF, Romanov RA, Rogachevskaja OA, Churbanov GD, Kolesnikov SS, (2010) Functional expression of the extracellular-Ca2+-sensing receptor in mouse taste cells. J Cell Sci 123: 972-982.
25. Ohsu T, Amino Y, Nagasaki H, Yamanaka T, Takeshita S, et al. (2010) Involvement of the calcium-sensing receptor in human taste perception. J Biol Chem 285: 1016-1022.
26. San Gabriel A, Uneyama H, Maekawa T, Torii K, (2009) The calcium-sensing receptor in taste tissue. Biochem Biophys Res Commun 378: 414-418.
27. Shindo Y, Miura H, Carninci P, Kawai J, Hayashizaki Y, et al. (2008) G alpha14 is a candidate mediator of sweet/umami signal transduction in the posterior region of the mouse tongue. Biochem Biophys Res Commun 376: 504-508.
28. Tizzano M, Dvoryanchikov G, Barrows JK, Kim S, Chaudhari N, et al. (2008) Expression of Galpha14 in sweet-transducing taste cells of the posterior tongue. BMC Neurosci 9: 110.
29. Kusakabe Y, Yasuoka A, Asano-Miyoshi M, Iwabuchi K, Matsumoto I, et al. (2000) Comprehensive study on G protein alpha-subunits in taste bud cells, with special reference to the occurrence of Galphai2 as a major Galpha species. Chem Senses 25: 525-531.
30. Trubey KR, Culpepper S, Maruyama Y, Kinnamon SC, Chaudhari N, (2006) Tastants evoke cAMP signal in taste buds that is independent of calcium signaling. Am J Physiol Cell Physiol 291: C237-244.
31. Striem BJ, Pace U, Zehavi U, Naim M, Lancet D, (1989) Sweet tastants stimulate adenylate cyclase coupled to GTP-binding protein in rat tongue membranes. Biochem J 260: 121-126.
32. Naim M, Ronen T, Striem BJ, Levinson M, Zehavi U, (1991) Adenylate cyclase responses to sucrose stimulation in membranes of pig circumvallate taste papillae. Comp Biochem Physiol B 100: 455-458.
33. Nakashima K, Ninomiya Y, (1999) Transduction for sweet taste of saccharin may involve both inositol 1,4,5-trisphosphate and cAMP pathways in the fungiform taste buds in C57BL mice. Cell Physiol Biochem 9: 90-98.
34. Nishimura A, Kitano K, Takasaki J, Taniguchi M, Mizuno N, et al. (2010) Structural basis for the specific inhibition of heterotrimeric Gq protein by a small molecule. Proc Natl Acad Sci U S A 107: 13666-13671.
35. Takasaki J, Saito T, Taniguchi M, Kawasaki T, Moritani Y, et al. (2004) A novel Galphaq/11-selective inhibitor. J Biol Chem 279: 47438-47445.
36. Tanahashi T, Yamaguchi K, Ishikawa S, Kusuhara M, Adachi I, et al. (1991) Endothelin-1 inhibits adipogenic differentiation of 3T3-L1 preadipocytes. Biochem Biophys Res Commun 177: 854-860.
37. Bhattacharya I, Ullrich A, (2006) Endothelin-1 inhibits adipogenesis: role of phosphorylation of Akt and ERK1/2. FEBS Lett 580: 5765-5771.
38. Imamura T, Ishibashi K, Dalle S, Ugi S, Olefsky JM, (1999) Endothelin-1-induced GLUT4 translocation is mediated via Galpha(q/11) protein and phosphatidylinositol 3-kinase in 3T3-L1 adipocytes. J Biol Chem 274: 33691-33695.
39. Bose A, Cherniack AD, Langille SE, Nicoloro SM, Buxton JM, et al. (2001) G(alpha)11 signaling through ARF6 regulates F-actin mobilization and GLUT4 glucose transporter translocation to the plasma membrane. Mol Cell Biol 21: 5262-5275.
40. Lawrence JT, Birnbaum MJ, (2001) ADP-ribosylation factor 6 delineates separate pathways used by endothelin 1 and insulin for stimulating glucose uptake in 3T3-L1 adipocytes. Mol Cell Biol 21: 5276-5285.
41. Gether U, (2000) Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr Rev 21: 90-113.
42. Olansky L, Myers GA, Pohl SL, Hewlett EL, (1983) Promotion of lipolysis in rat adipocytes by pertussis toxin: reversal of endogenous inhibition. Proc Natl Acad Sci U S A 80: 6547-6551.
43. Reusch JE, Colton LA, Klemm DJ, (2000) CREB activation induces adipogenesis in 3T3-L1 cells. Mol Cell Biol 20: 1008-1020.
44. Petersen RK, Madsen L, Pedersen LM, Hallenborg P, Hagland H, et al. (2008) Cyclic AMP (cAMP)-mediated stimulation of adipocyte differentiation requires the synergistic action of Epac- and cAMP-dependent protein kinase-dependent processes. Mol Cell Biol 28: 3804-3816.
45. Wang HY, Watkins DC, Malbon CC, (1992) Antisense oligodeoxynucleotides to GS protein alpha-subunit sequence accelerate differentiation of fibroblasts to adipocytes. Nature 358: 334-337.
46. Liu X, Malbon CC, Wang HY, (1998) Identification of amino acid residues of Gsalpha critical to repression of adipogenesis. J Biol Chem 273: 11685-11694.
47. Wang H, Johnson GL, Liu X, Malbon CC, (1996) Repression of adipogenesis by adenylyl cyclase stimulatory G-protein alpha subunit is expressed within region 146-220. J Biol Chem 271: 22022-22029.
48. Zhang L, Paddon C, Lewis MD, Grennan-Jones F, Ludgate M, (2009) Gsalpha signalling suppresses PPARgamma2 generation and inhibits 3T3L1 adipogenesis. J Endocrinol 202: 207-215.
49. Hewavitharana T, Wedegaertner PB, (2012) Non-canonical signaling and localizations of heterotrimeric G proteins. Cell Signal 24: 25-34.
50. Dave RH, Saengsawang W, Yu JZ, Donati R, Rasenick MM, (2009) Heterotrimeric G-proteins interact directly with cytoskeletal components to modify microtubule-dependent cellular processes. Neurosignals 17: 100-108.
51. Zheng B, Lavoie C, Tang TD, Ma P, Meerloo T, et al. (2004) Regulation of epidermal growth factor receptor degradation by heterotrimeric Galphas protein. Mol Biol Cell 15: 5538-5550.
52. Krendel M, Zenke FT, Bokoch GM, (2002) Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 4: 294-301.
53. Sordella R, Jiang W, Chen GC, Curto M, Settleman J, (2003) Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 113: 147-158.