Metabolic depletion of sphingolipids impairs ligand binding and signaling of human serotonin1A receptors

Biochemistry

Volumn 49, Issue 11, 2010, Pages 2389-2397

  Paila, Yamuna Devi ^a   Ganguly, Sourav ^a   Chattopadhyay, Amitabha ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR FUNCTION; CHO CELL; ESSENTIAL COMPONENT; EUKARYOTIC CELLS; FUMONISIN; G PROTEIN; LIGAND BINDING; MEMBRANE RECEPTORS; SPECIFIC INTERACTION; SPHINGOLIPID METABOLISM; SPHINGOLIPIDS; SPHINGOSINE; TRANS-MEMBRANE DOMAINS;

ACTIVATION ANALYSIS; BIOCHEMISTRY; BIOLOGICAL MEMBRANES; CELL MEMBRANES; CYTOLOGY; LIGANDS; METABOLISM; PROTEINS; SIGNALING;

LIPIDS;

FUMONISIN B1; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE RECEPTOR; SEROTONIN 1A RECEPTOR; SPHINGOLIPID; SPHINGOSINE;

ARTICLE; BIOSYNTHESIS; CHO CELL; HUMAN; HUMAN CELL; LIGAND BINDING; METABOLIC DISORDER; PRIORITY JOURNAL;

ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; ENZYME INHIBITORS; FUMONISINS; GENE EXPRESSION REGULATION; GTP-BINDING PROTEINS; HUMANS; LIGANDS; OXIDOREDUCTASES; PROTEIN BINDING; RECEPTOR, SEROTONIN, 5-HT1A; SPHINGOLIPIDS;

EUKARYOTA;

EID: 77949503339     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1001536     Document Type: Article

References (63)

1. Holthuis, J. C., Pomorski, T., Raggers, R. J., Sprong, H., and van Meer, G. (2001) The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81, 1689-1723.
2. Bartke, N., and Hannun, Y. A. (2009) Bioactive sphingolipids: Metabolism and function. J. Lipid Res. 50, S91-S96.
3. Brown, R. E. (1998) Sphingolipid organization in biomembranes: What physical studies of model membranes reveal. J. Cell Sci. 111, 1-9.
4. Masserini, M., and Ravasi, D. (2001) Role of sphingolipids in the biogenesis of membrane domains. Biochim. Biophys. Acta 1532, 149-161.
5. Jacobson, K., Mouritsen, O. G., and Anderson, R. G. W. (2007) Lipid rafts: At a crossroad between cell biology and physics. Nat. Cell Biol. 9, 7-14.
6. Simons, K., and van Meer, G. (1988) Lipid sorting in epithelial cells. Biochemistry 27, 6191-6202.
7. Simons, K., and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
8. Riethmüller, J., Riehle, A., Grassmé, H., and Gulbins, E. (2006) Membrane rafts in host-pathogen interactions. Biochim. Biophys. Acta 1758, 2139-2147.
9. Desai, K., Sullards, C., Allegood, J., Wang, E., Schmelz, E. M., Hartl, M., Humpf, H.-U., Liotta, D. C., Peng, Q., and Merrill, A. H., Jr. (2002) Fumonisins and fumonisin analogs as inhibitors of ceramide synthase and inducers of apoptosis. Biochim. Biophys. Acta 1585, 188-192.
10. Gelderblom, W. C., Jaskiewicz, K., Marasas, W. F., Thiel, P. G., Horak, R. M., Vleggaar, R., and Kriek, N. P. (1988) Fumonisinsnovel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Appl. Environ. Microbiol. 54, 1806-1811.
11. 1. Hum. Exp. Toxicol. 27, 799-809.
12. 1 as an example. Toxicol. Sci. 61, 6-17.
13. Wang, E., Norred, W. P., Bacon, C. W., Riley, R. T., and Merrill, A. H., Jr. (1991) Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. J. Biol. Chem. 266, 14486-14490.
14. Gelderblom, W. C., Semple, E., Marasas, W. F., and Farber, E. (1992) The cancer-initiating potential of the fumonisin B mycotoxins. Carcinogenesis 13, 433-437.
15. Soriano, J. M., Gonzalez, L., and Catalá, A. I. (2005) Mechanism of action of sphingolipids and their metabolites in the toxicity of fumonisin B,. Prog. Livid Res. 44, 345-356.
16. Harel, R., and Futerman, A. H. (1993) Inhibition of sphingolipid synthesis affects axonal outgrowth in cultured hippocampal neurons. J. Biol. Chem. 268, 14476-14481.
17. Hirabayashi, Y., and Furuya, S. (2008) Roles of L-serine and sphingolipid. synthesis in brain development and neuronal survival. Prog. Lipid Res. 47, 188-203.
18. Posee de Chaves, E. I. (2006) Sphingolipids in apoptosis, survival and regeneration in the nervous system, Biochim. Biophys. Acta 1758, 1995-2015.
19. 1A receptor: A representative member of the serotonin receptor family. Cell. Mol. Neurobiol. 25, 553-580.
20. 1Areceptors. Prog. Neurobiol. 81, 133-178.
21. Gardier, A. M. (2009) Mutant mouse models and antidepressant drug research: Focus on serotonin and brain-derived neurotrophic factor. Behav. Pharmacol. 20, 18-32.
22. 1A receptor is impaired in cellular model of Smith-Lemli-Opitz Syndrome. Biochim. Biophys. Acta 1778, 1508-1516.
23. 1A receptor heterologously expressed in CHO cells. Biosci. Rep. 24, 101-115.
24. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
25. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
26. Ito, J., Nagayasu, Y., Kato, K., Sato, R., and Yokoyama, S. (2002) Apolipoprotein A-I induces translocation of cholesterol, phospholipid, and caveolin-1 to cytosol in rat astrocytes. J. Biol. Chem. 277, 7929-7935.
27. van Echten-Deckert, G. (2000) Sphingolipid extraction and analysis by thin-layer chromatography. Methods Enzymol. 312, 64-79.
28. McClare, C. W. F. (1971) An accurate and convenient organic phosphorus assay. Anal. Biochem. 39, 527-530.
29. 1A receptor expressed in neuronal cells: Toward a native environment for neuronal receptors. Cell. Mol. Neurobiol. 26, 925-942.
30. 2+ and the βγ-subunit complex on the interactions of guanine nucleotides with G proteins. J. Biol. Chem. 262, 762-766.
31. Nordstedt, C., and Fredholm, B. B. (1990) A modification of a protein-binding method for rapid quantification of cAMP in cellculture supernatants and body fluid. Anal. Biochem. 189, 231-234.
32. 1A receptor. Mol. Membr. Biol. 22, 241-249.
33. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3rd ed., Springer, New York.
34. 1A receptor tagged to yellow fluorescent protein. Biochemistry 43, 15852-15862.
35. Merrill, A. H., Jr., Liotta, D. C., and Riley, R. T. (1996) Fumonisins: Fungal toxins that shed light on sphingolipid function. Trends Cell Biol. 6, 218-223.
36. Kouadio, J. H., Mobio, T. A., Baudrimont, L., Moukha, S., Dano, S. D., and Creppy, E. E. (2005) Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin Bl in human intestinal cell line Caco-2. Toxicology 213, 56-65.
37. 1 on cell death in cultured cells: The significance of the elevated sphinganine. Arch. Pharm. Res. 24, 136-143.
38. Sjögren, B., and Svenningsson, P. (2007) Depletion of the lipid raft constituents, sphingomyelin and ganglioside, decreases serotonin binding at human 5-HT7(a) receptors in HeLa cells. Acta Physiol. 190, 47-53.
39. Fantini, J., and Barrantes, F. J. (2009) Sphingolipid/cholesterol regulation of neurotransmitter receptor conformation and function. Biochim. Biophys. Acta 1788, 2345-2361.
40. 1A receptors to inhibitory G protein α-subunits and lack of coupling to Gsα. Biochemistry 32, 11064-11073.
41. 1A receptors from bovine hippocampus by an agonist and an antagonist. FEBS Lett. 457, 389-392.
42. 1A receptor correlates with receptor signaling. Biophys. J. 95, 451-463.
43. Ramstedt, B., and Slotte, J. P. (2006) Sphingolipids and the formation of sterol-enriched ordered membrane domains. Biochim. Biophys. Acta 1758, 1945-1956.
44. 1A binding sites. Brain Res. Mol. Brain Res. 69, 186-201.
45. Lee, A. G. (2004) How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 1666, 62-87.
46. Palsdottir, H., and Hunte, C. (2004) Lipids in membrane protein structures. Biochim. Biophys. Acta 1666, 2-18.
47. Pucadyil, T. J., and Chattopadhyay, A. (2006) Role of cholesterol in the function and organization of G-protein coupled receptors. Prog. Lipid Res. 45, 295-333.
48. Chattopadhyay, A., and Paila, Y. D. (2007) Lipid-protein interactions, regulation and dysfunction of brain cholesterol. Biochem. Biophys. Res. Commun. 354, 627-633.
49. Porter, F. D. (2002) Malformation syndromes due to inborn errors of cholesterol synthesis. J. Clin. Invest. 110, 715-724.
50. Fantini, J. (2003) How sphingolipids bind and shape proteins: Molecular basis of lipid-protein interactions in lipid shells, rafts and related biomembrane domains. Cell. Mol. Life Sci. 60, 1027-1032.
51. Snook, C. F., Jones, J. A., and Hannun, Y. A. (2006) Sphingolipidbinding proteins. Biochim. Biophys. Acta 1761, 927-946.
52. Koval, M., and Pagano, R. E. (1991) Intracellular transport and metabolism of sphingomyelin. Biochim. Biophys. Acta 1082, 113-125.
53. Lange, Y., Swaisgood, M. H., Ramos, B. V., and Steck, T. L. (1989) Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J. Biol. Chem. 264, 3786-3793.
54. Futerman, A. H., and Hannun, Y. A. (2004) The complex life of simple sphingolipids. EMBO Ren. 5, 777-782.
55. Zeidan, Y. H., and Hannun, Y. A. (2007) Translational aspects of sphingolipid metabolism. Trends Mol. Med. 13, 327-336.
56. 1 induced neurodegeneration in mice after intracerebroventricular infusion is concurrent with disruption of sphingolipid metabolism and activation of proinflammatory signaling. Neurotoxicology 26, 211-221.
57. Harikumar, K. G., Puri, V., Singh, R. D., Hanada, K., Pagano, R. E., and Miller, L. J. (2005) Differential effects of modification of membrane cholesterol and sphingolipids on the conformation, function, and trafficking of the G protein-coupled cholecystokinin receptor. J. Biol. Chem. 280, 2116-2185.
58. Baier, C. J. and Barrantes, F. J. (2007) Sphingolipids are necessary for nicotinic acetylcholine receptor export in the early secretory pathway. J. Neurochem. 101, 1072-1084.
59. 1, a mycotoxin. Biochem. Biophys. Res. Commun. 220, 160-165.
60. Mutoh, T., Tokuda, A., Miyadai, T., Hamaguchi, M., and Fujiki, N. (1995) Ganglioside GM1 binds to the Trk protein and regulates receptor function. Proc. Natl. Acad. Sci. U.S.A. 92, 5087-5091.
61. 1A receptors from bovine hippocampus. Biochim. Biophys. Acta 1663, 188-200.
62. Paila, Y. D., Tiwari, S., and Chattopadhyay, A. (2009) Are specific nonannular cholesterol binding sites present in G-protein coupled receptors? Biochim. Biophys. Acta 1788, 295-302.
63. Mahfoud, R., Mylvaganam, M., Lingwood, C. A., and Fantini, J. (2002) A novel soluble analog of the HIV-1 fusion cofactor, globotriaosylceramide (Gb(3)), eliminates the cholesterol requirement for high affinity gp120/Gb(3) interaction. J. Lipid Res. 43, 1670-1679.