Sphingomyelin regulates the transbilayer movement of diacylglycerol in the plasma membrane of Madin-Darby canine kidney cells

FASEB Journal

Volumn 27, Issue 8, 2013, Pages 3284-3297

  Ueda, Yoshibumi ^a   Makino, Asami ^a   Murase Tamada, Kotono ^a   Sakai, Shota ^a   Inaba, Takehiko ^a   Hullin Matsuda, Françoise ^a,b   Kobayashi, Toshihide ^a,b  

^a RIKEN   (Japan)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

C1AB domain; Ceramides; Flip flop; Lipid probe

Indexed keywords

DIACYLGLYCEROL; PHOSPHOLIPASE C; PROTEIN KINASE C GAMMA; SPHINGOMYELIN; YELLOW FLUORESCENT PROTEIN; 1,2-DIACYLGLYCEROL; LIPID BILAYER; MEMBRANE LIPID; PHOTOPROTEIN; PROTEIN KINASE C; SPHINGOMYELIN PHOSPHODIESTERASE;

ARTICLE; ARTIFICIAL MEMBRANE; BACILLUS CEREUS; BINDING AFFINITY; CELL MEMBRANE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; LIPID ANALYSIS; LIPID BILAYER; LIPID VESICLE; LIPOGENESIS; MDCK CELL; MOLECULAR DYNAMICS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN PURIFICATION; ANIMAL; BINDING SITE; CELL LINE; CHEMISTRY; CLOSTRIDIUM PERFRINGENS; CONFOCAL MICROSCOPY; DOG; ENZYMOLOGY; ERYTHROCYTE MEMBRANE; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; RAT; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BACILLUS CEREUS; BINDING SITES; BIOLOGICAL TRANSPORT; CELL LINE; CELL MEMBRANE; CLOSTRIDIUM PERFRINGENS; DIGLYCERIDES; DOGS; ERYTHROCYTE MEMBRANE; HELA CELLS; HUMANS; LIPID BILAYERS; LUMINESCENT PROTEINS; MEMBRANE LIPIDS; MICROSCOPY, CONFOCAL; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELINS; TYPE C PHOSPHOLIPASES;

EID: 84881157822     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-226548     Document Type: Article

References (81)

1. Carman, G. M., and Han, G. S. (2006) Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem. Sci. 31, 694-699
2. Berridge, M. J., and Irvine, R. F. (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312, 315-321
3. Nishizuka, Y. (1992) Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258, 607-614
4. Griner, E. M., and Kazanietz, M. G. (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 7, 281-294
5. Newton, A. C. (2009) Lipid activation of protein kinases. J. Lipid Res. 50(Suppl.), S266-S271
6. Rhee, S. G., and Bae, Y. S. (1997) Regulation of phosphoinositide- specific phospholipase C isozymes. J. Biol. Chem. 272, 15045-15048
7. Fukami, K. (2002) Structure, regulation, and function of phospholipase C isozymes. J. Biochem. 131, 293-299
8. Reue, K., and Brindley, D. N. (2008) Thematic review series: glycerolipids. Multiple roles for lipins/phosphatidate phosphatase enzymes in lipid metabolism. J. Lipid Res. 49, 2493-2503
9. Manmontri, B., Sariahmetoglu, M., Donkor, J., Bou Khalil, M., Sundaram, M., Yao, Z., Reue, K., Lehner, R., and Brindley, D. N. (2008) Glucocorticoids and cyclic AMP selectively increase hepatic lipin-1 expression, and insulin acts antagonistically. J. Lipid Res. 49, 1056-1067
10. Ullman, M. D., and Radin, N. S. (1974) The enzymatic formation of sphingomyelin from ceramide and lecithin in mouse liver. J. Biol. Chem. 249, 1506-1512
11. Voelker, D. R., and Kennedy, E. P. (1982) Cellular and enzymic synthesis of sphingomyelin. Biochemistry 21, 2753-2759
12. Marggraf, W. D., and Kanfer, J. N. (1984) The phosphorylcholine acceptor in the phosphatidylcholine: ceramide cholinephosphotransferase reaction. Is the enzyme a transferase or a hydrolase? Biochim. Biophys. Acta 793, 346-353
13. Huitema, K., van den Dikkenberg, J., Brouwers, J. F. H. M., and Holthuis, J. C. M. (2004) Identification of a family of animal sphingomyelin synthases. EMBO J. 23, 33-44
14. Tafesse, F. G., Huitema, K., Hermansson, M., van der Poel, S., van den Dikkenberg, J., Uphoff, A., Somerharju, P., and Holthuis, J. C. (2007) Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells. J. Biol. Chem. 282, 17537-17547
15. Van Helvoort, A., van't Hof, W., Ritsema, T., Sandra, A., and van Meer, G. (1994) Conversion of diacylglycerol to phosphatidylcholine on the basolateral surface of epithelial (Madin-Darby canine kidney) cells. Evidence for the reverse action of a sphingomyelin synthase. J. Biol. Chem. 269, 1763-1769
16. Vos, J. P., Giudici, M. L., van der Bijl, P., Magni, P., Marchesini, S., van Golde, L. M., and Lopes-Cardozo, M. (1995) Sphingomyelin is synthesized at the plasma membrane of oligodendrocytes and by purified myelin membranes: a study with fluorescent-and radio-labelled ceramide analogues. FEBS Lett. 368, 393-396
17. Zachowski, A. (1993) Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294, 1-14
18. Van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008) Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell. Biol. 9, 112-124
19. Shaner, R. L., Allegood, J. C., Park, H., Wang, E., Kelly, S., Haynes, C. A., Sullards, M. C., and Merrill, A. H., Jr. (2009) Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J. Lipid Res. 50, 1692-1707
20. Lingwood, D., and Simons, K. (2010) Lipid rafts as a membraneorganizing principle. Science 327, 46-50
21. Abe, M., Makino, A., Hullin-Matsuda, F., Kamijo, K., Ohno-Iwashita, Y., Hanada, K., Mizuno, H., Miyawaki, A., and Kobayashi, T. (2012) A role for sphingomyelin-rich lipid domains in the accumulation of phosphatidylinositol-4, 5-bisphosphate to the cleavage furrow during cytokinesis. Mol. Cell. Biol. 32, 1396-1407
22. Mauco, G., Dangelmaier, C. A., and Smith, J. B. (1984) Inositol lipids, phosphatidate and diacylglycerol share stearoylarachidonoylglycerol as a common backbone in thrombin-stimulated human platelets. Biochem. J. 224, 933-940
23. Bai, J., and Pagano, R. E. (1997) Measurement of spontaneous transfer and transbilayer movement of BODIPY-labeled lipids in lipid vesicles. Biochemistry 36, 8840-8848
24. Ganong, B. R., and Bell, R. M. (1984) Transmembrane movement of phosphatidylglycerol and diacylglycerol sulfhydryl analogues. Biochemistry 23, 4977-4983
25. Pagano, R., and Longmuir, K. (1985) Phosphorylation, transbilayer movement, and facilitated intracellular transport of diacylglycerol are involved in the uptake of a fluorescent analog of phosphatidic acid by cultured fibroblasts. J. Biol. Chem. 260, 1909-1916
26. Ogushi, F., Ishitsuka, R., Kobayashi, T., and Sugita, Y. (2012) Rapid flip-flop motions of diacylglycerol and ceramide in phospholipid bilayers. Chem. Phys. Lett. 522, 96-102
27. Holland, W. L., Knotts, T. A., Chavez, J. A., Wang, L. P., Hoehn, K. L., and Summers, S. A. (2007) Lipid mediators of insulin resistance. Nutr. Rev. 65, S39-S46
28. Allan, D., Thomas, P., and Michell, R. H. (1978) Rapid transbilayer diffusion of 1,2-diacylglycerol and its relevance to control of membrane curvature. Nature 276, 289-290
29. Oancea, E., Teruel, M. N., Quest, A. F., and Meyer, T. (1998) Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. J. Cell Biol. 140, 485-498
30. Sampaio, J. L., Gerl, M. J., Klose, C., Ejsing, C. S., Beug, H., Simons, K., and Shevchenko, A. (2011) Membrane lipidome of an epithelial cell line. Proc. Natl. Acad. Sci. U. S. A. 108, 1903-1907
31. Kiyokawa, E., Baba, T., Otsuka, N., Makino, A., Ohno, S., and Kobayashi, T. (2005) Spatial and functional heterogeneity of sphingolipid-rich membrane domains. J. Biol. Chem. 280, 24072-24084
32. Klein, U., Gimpl, G., and Fahrenholz, F. (1995) Alteration of the myometrial plasma membrane cholesterol content with betacyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry 34, 13784-13793
33. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
34. Ishitsuka, R., Saito, T., Osada, H., Ohno-Iwashita, Y., and Kobayashi, T. (2011) Fluorescence image screening for chemical compounds modifying cholesterol metabolism and distribution. J. Lipid Res. 52, 2084-2094
35. Baumann, N. A., Vidugiriene, J., Machamer, C. E., and Menon, A. K. (2000) Cell surface display and intracellular trafficking of free glycosylphosphatidylinositols in mammalian cells. J. Biol. Chem. 275, 7378-7389
36. Kates, M. (1986) Techniques of Lipidology-Isolation, Analysis and Identification of Lipids, Vol. 3, Elsevier, Amsterdam
37. Kremer, J. M., Esker, M. W., Pathmamanoharan, C., and Wiersema, P. H. (1977) Vesicles of variable diameter prepared by a modified injection method. Biochemistry 16, 3932-3935
38. Kobayashi, T., and Pagano, R. E. (1988) ATP-dependent fusion of liposomes with the Golgi apparatus of perforated cells. Cell 55, 797-805
39. McIntyre, J. C., and Sleight, R. G. (1991) Fluorescence assay for phospholipid membrane asymmetry. Biochemistry 30, 11819-11827
40. Kobayashi, T., Storrie, B., Simons, K., and Dotti, C. G. (1992) A functional barrier to movement of lipids in polarized neurons. Nature 359, 647-650
41. Sakurai, J., Nagahama, M., and Oda, M. (2004) Clostridium perfringens alpha-toxin: characterization and mode of action. J. Biochem. 136, 569-574
42. Naylor, C. E., Eaton, J. T., Howells, A., Justin, N., Moss, D. S., Titball, R. W., and Basak, A. K. (1998) Structure of the key toxin in gas gangrene. Nat. Struct. Biol. 5, 738-746
43. Otnaess, A. B., Little, C., Sletten, K., Wallin, R., Johnsen, S., Flengsrud, R., and Prydz, H. (1977) Some characteristics of phospholipase C from Bacillus cereus. Eur. J. Biochem. 79, 459-468
44. Van Engeland, M., Nieland, L. J., Ramaekers, F. C., Schutte, B., and Reutelingsperger, C. P. (1998) Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31, 1-9
45. Zambon, A. C., Hughes, R. J., Meszaros, J. G., Wu, J. J., Torres, B., Brunton, L. L., and Insel, P. A. (2000) P2Y(2) receptor of MDCK cells: cloning, expression, and cell-specific signaling. Am. J. Physiol. Renal Physiol. 279, F1045-F1052
46. Kol, M. A., van Laak, A. N., Rijkers, D. T., Killian, J. A., de Kroon, A. I., and de Kruijff, B. (2003) Phospholipid flop induced by transmembrane peptides in model membranes is modulated by lipid composition. Biochemistry 42, 231-237
47. Meshulam, T., Simard, J. R., Wharton, J., Hamilton, J. A., and Pilch, P. F. (2006) Role of caveolin-1 and cholesterol in transmembrane fatty acid movement. Biochemistry 45, 2882-2893
48. Rothblat, G. H., de la Llera-Moya, M., Atger, V., Kellner-Weibel, G., Williams, D. L., and Phillips, M. C. (1999) Cell cholesterol efflux: integration of old and new observations provides new insights. J. Lipid Res. 40, 781-796
49. van Meer, G., and Simons, K. (1982) Viruses budding from either the apical or the basolateral plasma membrane domain of MDCK cells have unique phospholipid compositions. EMBO J. 1, 847-852
50. Miyake, Y., Kozutsumi, Y., Nakamura, S., Fujita, T., and Kawasaki, T. (1995) Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem. Biophys. Res. Commun. 211, 396-403
51. Shogomori, H., and Kobayashi, T. (2008) Lysenin: a sphingomyelin specific pore-forming toxin. Biochim. Biophys. Acta 1780, 612-618
52. Ding, T., Li, Z., Hailemariam, T., Mukherjee, S., Maxfield, F. R., Wu, M.-P., and Jiang, X.-C. (2008) SMS overexpression and knockdown: impact on cellular sphingomyelin and diacylglycerol metabolism, and cell apoptosis. J. Lipid Res. 49, 376-385
53. Hailemariam, T. K., Huan, C., Liu, J., Li, Z., Roman, C., Kalbfeisch, M., Bui, H. H., Peake, D. A., Kuo, M. S., Cao, G., Wadgaonkar, R., and Jiang, X. C. (2008) Sphingomyelin synthase 2 deficiency attenuates NF-B activation. Arterioscler. Thromb. Vasc. Biol. 28, 1519-1526
54. Contreras, F. X., Villar, A. V., Alonso, A., Kolesnick, R. N., and Goni, F. M. (2003) Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes. J. Biol. Chem. 278, 37169-37174
55. Contreras, F. X., Villar, A. V., Alonso, A., and Goni, F. M. (2009) Ceramide-induced transbilayer (flip-flop) lipid movement in membranes. Methods Mol. Biol. 462, 155-165
56. Amtmann, E. (1996) The antiviral, antitumoural xanthate D609 is a competitive inhibitor of phosphatidylcholine-specific phospholipase C. Drugs Exp. Clin. Res. 22, 287-294
57. Luberto, C., and Hannun, Y. A. (1998) Sphingomyelin synthase, a potential regulator of intracellular levels of ceramide and diacylglycerol during SV40 transformation. Does sphingomyelin synthase account for the putative phosphatidylcholine-specific phospholipase C? J. Biol. Chem. 273, 14550-14559
58. Thompson, A. K., Mostafapour, S. P., Denlinger, L. C., Bleasdale, J. E., and Fisher, S. K. (1991) The aminosteroid U-73122 inhibits muscarinic receptor sequestration and phosphoinositide hydrolysis in SK-N-SH neuroblastoma cells. A role for Gp in receptor compartmentation. J. Biol. Chem. 266, 23856-23862
59. Vieu, C., Jaspard, B., Barbaras, R., Manent, J., Chap, H., Perret, B., and Collet, X. (1996) Identification and quantification of diacylglycerols in HDL and accessibility to lipase. J. Lipid Res. 37, 1153-1161
60. Wuttke, A., Idevall-Hagren, O., and Tengholm, A. (2013) P2Y1 receptor-dependent diacylglycerol signaling microdomains in beta cells promote insulin secretion. FASEB J. 27, 1610-1620
61. Lewis, R. N., Mak, N., and McElhaney, R. N. (1987) A differential scanning calorimetric study of the thermotropic phase behavior of model membranes composed of phosphatidylcholines containing linear saturated fatty acyl chains. Biochemistry 26, 6118-6126
62. De Kruyff, B., Demel, R. A., Slotboom, A. J., van Deenen, L. L., and Rosenthal, A. F. (1973) The effect of the polar headgroup on the lipid-cholesterol interaction: a monolayer and differential scanning calorimetry study. Biochim. Biophys. Acta 307, 1-19
63. Sripada, P. K., Maulik, P. R., Hamilton, J. A., and Shipley, G. G. (1987) Partial synthesis and properties of a series of N-acyl sphingomyelins. J. Lipid Res. 28, 710-718
64. Reyes Mateo, C., Ulises Acuna, A., and Brochon, J. C. (1995) Liquid-crystalline phases of cholesterol/lipid bilayers as revealed by the fluorescence of trans-parinaric acid. Biophys. J. 68, 978-987
65. Koynova, R. D., Boyanov, A. I., and Tenchov, B. G. (1985) On the phase diagram of an L-dipalmitoylphosphatidylcholine/ cholesterol mixture. FEBS Lett. 187, 65-68
66. De Almeida, R. F., Fedorov, A., and Prieto, M. (2003) Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85, 2406-2416
67. Marsh, D. (2013) Handbook of Lipid Bilayers, CRC Press, Boca Raton, FL, USA
68. Kawato, S., Kinosita, K., Jr., and Ikegami, A. (1978) Effect of cholesterol on the molecular motion in the hydrocarbon region of lecithin bilayers studied by nanosecond fluorescence techniques. Biochemistry 17, 5026-5031
69. Arora, A., Raghuraman, H., and Chattopadhyay, A. (2004) Influence of cholesterol and ergosterol on membrane dynamics: a fluorescence approach. Biochem. Biophys. Res. Commun. 318, 920-926
70. Kutchai, H., Chandler, L. H., and Zavoico, G. B. (1983) Effects of cholesterol on acyl chain dynamics in multilamellar vesicles of various phosphatidylcholines. Biochim. Biophys. Acta 736, 137-149
71. Ramoni, C., Spadaro, F., Menegon, M., and Podo, F. (2001) Cellular localization and functional role of phosphatidylcholine-specific phospholipase C in NK cells. J. Immunol. 167, 2642-2650
72. Paris, L., Cecchetti, S., Spadaro, F., Abalsamo, L., Lugini, L., Pisanu, M. E., Iorio, E., Natali, P. G., Ramoni, C., and Podo, F. (2010) Inhibition of phosphatidylcholine-specific phospholipase C downregulates HER2 overexpression on plasma membrane of breast cancer cells. Breast Cancer Res. 12, R27
73. Yeang, C., Varshney, S., Wang, R., Zhang, Y., Ye, D., and Jiang, X. C. (2008) The domain responsible for sphingomyelin synthase (SMS) activity. Biochim. Biophys. Acta 1781, 610-617
74. Pagano, R. E. (1988) What is the fate of diacylglycerol produced at the Golgi apparatus? Trends Biochem. Sci. 13, 202-205
75. Villani, M., Subathra, M., Im, Y. B., Choi, Y., Signorelli, P., Del Poeta, M., and Luberto, C. (2008) Sphingomyelin synthases regulate production of diacylglycerol at the Golgi. Biochem. J. 414, 31-41
76. Cerbon, J., and del Carmen Lopez-Sanchez, R. (2003) Diacylglycerol generated during sphingomyelin synthesis is involved in protein kinase C activation and cell proliferation in Madin-Darby canine kidney cells. Biochem. J. 373, 917-924
77. Gerl, M. J., Sampaio, J. L., Urban, S., Kalvodova, L., Verbavatz, J. M., Binnington, B., Lindemann, D., Lingwood, C. A., Shevchenko, A., Schroeder, C., and Simons, K. (2012) Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J. Cell Biol. 196, 213-221
78. Fujita, A., Cheng, J., Tauchi-Sato, K., Takenawa, T., and Fujimoto, T. (2009) A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc. Natl. Acad. Sci. U. S. A. 106, 9256-9261
79. Murate, M., Hayakawa, T., Ishii, K., Inadome, H., Greimel, P., Watanabe, M., Nagatsuka, Y., Ito, K., Ito, Y., Takahashi, H., Hirabayashi, Y., and Kobayashi, T. (2010) Phosphatidylglucoside forms specific lipid domains on the outer leaflet of the plasma membrane. Biochemistry 49, 4732-4739
80. Bourbon, N. A., Sandirasegarane, L., and Kester, M. (2002) Ceramide-induced inhibition of Akt is mediated through protein kinase C zeta: implications for growth arrest. J. Biol. Chem. 277, 3286-3292
81. Fox, T. E., Houck, K. L., O'Neill, S. M., Nagarajan, M., Stover, T. C., Pomianowski, P. T., Unal, O., Yun, J. K., Naides, S. J., and Kester, M. (2007) Ceramide recruits and activates protein kinase C zeta (PKC zeta) within structured membrane microdomains. J. Biol. Chem. 282, 12450-12457