The role of sphingomyelin and sphingomyelin synthases in cell death, proliferation and migration - From cell and animal models to human disorders

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 5, 2014, Pages 692-703

  Taniguchi, Makoto ^a   Okazaki, Toshiro ^a  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

Cell functions; Ceramide; Malignancies; Membrane; Sphingomyelin; Sphingomyelin synthase

Indexed keywords

CERAMIDE; SPHINGOMYELIN; SPHINGOMYELIN SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; AUTOPHAGY; CARDIOVASCULAR DISEASE; CAVEOLA; CELL DEATH; CELL FUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOLOGY; ENZYME ACTIVITY; ENZYME MECHANISM; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

ANIMALIA;

CELL FUNCTIONS; CERAMIDE; MALIGNANCIES; MEMBRANE; SPHINGOMYELIN; SPHINGOMYELIN SYNTHASE;

ANIMALS; CELL DEATH; CELL MOVEMENT; CELL PROLIFERATION; DISEASE; HUMANS; MODELS, BIOLOGICAL; SPHINGOMYELINS; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

EID: 84897954261     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.12.003     Document Type: Review

References (149)

1. Y.A. Hannun, and L.M. Obeid Principles of bioactive lipid signalling: lessons from sphingolipids Nat. Rev. Mol. Cell Biol. 9 2008 139 150 (Pubitemid 351158911)
2. M.M. Young, M. Kester, and H.G. Wang Sphingolipids: regulators of crosstalk between apoptosis and autophagy J. Lipid Res. 54 2013 5 19
3. D.K. Perry Serine palmitoyltransferase: role in apoptotic de novo ceramide synthesis and other stress responses Biochim. Biophys. Acta 1585 2002 146 152 (Pubitemid 36092079)
4. D.S. Menaldino, A. Bushnev, A. Sun, D.C. Liotta, H. Symolon, K. Desai, D.L. Dillehay, Q. Peng, E. Wang, J. Allegood, S. Trotman-Pruett, M.C. Sullards, and A.H. Merrill Jr. Sphingoid bases and de novo ceramide synthesis: enzymes involved, pharmacology and mechanisms of action Pharmacol. Res. 47 2003 373 381 (Pubitemid 36379199)
5. R. Bose, M. Verheij, A. Haimovitz-Friedman, K. Scotto, Z. Fuks, and R. Kolesnick Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals Cell 82 1995 405 414
6. G.M. Jenkins, L.A. Cowart, P. Signorelli, B.J. Pettus, C.E. Chalfant, and Y.A. Hannun Acute activation of de novo sphingolipid biosynthesis upon heat shock causes an accumulation of ceramide and subsequent dephosphorylation of SR proteins J. Biol. Chem. 277 2002 42572 42578 (Pubitemid 35285625)
7. K. Kitatani, M. Nemoto, S. Akiba, and T. Sato Stimulation by de novo-synthesized ceramide of phospholipase A(2)-dependent cholesterol esterification promoted by the uptake of oxidized low-density lipoprotein in macrophages Cell. Signal. 14 2002 695 701 (Pubitemid 34518623)
8. T. Gomez del Pulgar, G. Velasco, C. Sanchez, A. Haro, and M. Guzman De novo-synthesized ceramide is involved in cannabinoid-induced apoptosis Biochem. J. 363 2002 183 188 (Pubitemid 34280625)
9. D.J. Verlaan, S. Berlivet, G.M. Hunninghake, A.M. Madore, M. Lariviere, S. Moussette, E. Grundberg, T. Kwan, M. Ouimet, B. Ge, R. Hoberman, M. Swiatek, J. Dias, K.C. Lam, V. Koka, E. Harmsen, M. Soto-Quiros, L. Avila, J.C. Celedon, S.T. Weiss, K. Dewar, D. Sinnett, C. Laprise, B.A. Raby, T. Pastinen, and A.K. Naumova Allele-specific chromatin remodeling in the ZPBP2/GSDMB/ORMDL3 locus associated with the risk of asthma and autoimmune disease Am. J. Hum. Genet. 85 2009 377 393
10. D.K. Breslow, S.R. Collins, B. Bodenmiller, R. Aebersold, K. Simons, A. Shevchenko, C.S. Ejsing, and J.S. Weissman Orm family proteins mediate sphingolipid homeostasis Nature 463 2010 1048 1053
11. F.M. Roelants, D.K. Breslow, A. Muir, J.S. Weissman, and J. Thorner Protein kinase Ypk1 phosphorylates regulatory proteins Orm1 and Orm2 to control sphingolipid homeostasis in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U. S. A. 108 2011 19222 19227
12. K. Kitatani, J. Idkowiak-Baldys, and Y.A. Hannun The sphingolipid salvage pathway in ceramide metabolism and signaling Cell. Signal. 20 2008 1010 1018
13. T.D. Mullen, Y.A. Hannun, and L.M. Obeid Ceramide synthases at the centre of sphingolipid metabolism and biology Biochem. J. 441 2012 789 802
14. S. Bourteele, A. Hausser, H. Doppler, J. Horn-Muller, C. Ropke, G. Schwarzmann, K. Pfizenmaier, and G. Muller Tumor necrosis factor induces ceramide oscillations and negatively controls sphingolipid synthases by caspases in apoptotic Kym-1 cells J. Biol. Chem. 273 1998 31245 31251 (Pubitemid 28533140)
15. Y. Uchida, A.D. Nardo, V. Collins, P.M. Elias, and W.M. Holleran De novo ceramide synthesis participates in the ultraviolet B irradiation-induced apoptosis in undifferentiated cultured human keratinocytes J. Invest. Dermatol. 120 2003 662 669 (Pubitemid 36344011)
16. J.P. Truman, N. Gueven, M. Lavin, S. Leibel, R. Kolesnick, Z. Fuks, and A. Haimovitz-Friedman Down-regulation of ATM protein sensitizes human prostate cancer cells to radiation-induced apoptosis J. Biol. Chem. 280 2005 23262 23272 (Pubitemid 40853238)
17. M. Garzotto, M. White-Jones, Y. Jiang, D. Ehleiter, W.C. Liao, A. Haimovitz-Friedman, Z. Fuks, and R. Kolesnick 12-O-tetradecanoylphorbol-13- acetate-induced apoptosis in LNCaP cells is mediated through ceramide synthase Cancer Res. 58 1998 2260 2264 (Pubitemid 28232917)
18. H.J. Ch'ang, J.G. Maj, F. Paris, H.R. Xing, J. Zhang, J.P. Truman, C. Cardon-Cardo, A. Haimovitz-Friedman, R. Kolesnick, and Z. Fuks ATM regulates target switching to escalating doses of radiation in the intestines Nat. Med. 11 2005 484 490 (Pubitemid 40685970)
19. J. Mesicek, H. Lee, T. Feldman, X. Jiang, A. Skobeleva, E.V. Berdyshev, A. Haimovitz-Friedman, Z. Fuks, and R. Kolesnick Ceramide synthases 2, 5, and 6 confer distinct roles in radiation-induced apoptosis in HeLa cells Cell. Signal. 22 2010 1300 1307
20. G. Rath, C. Schneider, B. Langlois, H. Sartelet, H. Morjani, H.E. Btaouri, S. Dedieu, and L. Martiny De novo ceramide synthesis is responsible for the anti-tumor properties of camptothecin and doxorubicin in follicular thyroid carcinoma Int. J. Biochem. Cell Biol. 41 2009 1165 1172
21. N. Marchesini, and Y.A. Hannun Acid and neutral sphingomyelinases: roles and mechanisms of regulation Biochem. Cell Biol. 82 2004 27 44 (Pubitemid 38580872)
22. M.Y. Kim, C. Linardic, L. Obeid, and Y. Hannun Identification of sphingomyelin turnover as an effector mechanism for the action of tumor necrosis factor alpha and gamma-interferon. Specific role in cell differentiation J. Biol. Chem. 266 1991 484 489 (Pubitemid 21906148)
23. B. Brenner, K. Ferlinz, H. Grassme, M. Weller, U. Koppenhoefer, J. Dichgans, K. Sandhoff, F. Lang, and E. Gulbins Fas/CD95/Apo-I activates the acidic sphingomyelinase via caspases Cell Death Differ. 5 1998 29 37 (Pubitemid 28359080)
24. T. Goldkorn, N. Balaban, M. Shannon, V. Chea, K. Matsukuma, D. Gilchrist, H. Wang, and C. Chan H2O2 acts on cellular membranes to generate ceramide signaling and initiate apoptosis in tracheobronchial epithelial cells J. Cell Sci. 111 Pt 21 1998 3209 3220 (Pubitemid 28532431)
25. S. Yamaoka, M. Miyaji, T. Kitano, H. Umehara, and T. Okazaki Expression cloning of a human cDNA restoring sphingomyelin synthesis and cell growth in sphingomyelin synthase-defective lymphoid cells J. Biol. Chem. 279 2004 18688 18693 (Pubitemid 38623292)
26. K. Huitema, J. van den Dikkenberg, J.F. Brouwers, and J.C. Holthuis Identification of a family of animal sphingomyelin synthases EMBO J. 23 2004 33 44 (Pubitemid 38165745)
27. B.A. Muehlenberg, M. Sribney, and M.K. Duffe Occurrence and biosynthesis of ceramide phosphorylethanolamine in chicken and rat liver Can. J. Biochem. 50 1972 166 173
28. K. Satouchi, K. Hirano, M. Sakaguchi, H. Takehara, and F. Matsuura Phospholipids from the free-living nematode Caenorhabditis elegans Lipids 28 1993 837 840 (Pubitemid 23277649)
29. H.G. Elmendorf, and K. Haldar Plasmodium falciparum exports the Golgi marker sphingomyelin synthase into a tubovesicular network in the cytoplasm of mature erythrocytes J. Cell Biol. 124 1994 449 462 (Pubitemid 24064458)
30. S.G. Karlander, K.A. Karlsson, H. Leffler, A. Lilja, B.E. Samuelsson, and G.O. Steen The structure of sphingomyelin of the honey bee (Apis mellifera) Biochim. Biophys. Acta 270 1972 117 131
31. R.C. Dickson Sphingolipid functions in Saccharomyces cerevisiae: comparison to mammals Annu. Rev. Biochem. 67 1998 27 48 (Pubitemid 28411122)
32. T.M. Dunn, D.V. Lynch, L.V. Michaelson, and J.A. Napier A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana Ann. Bot. 93 2004 483 497 (Pubitemid 41295603)
33. F.G. Tafesse, P. Ternes, and J.C. Holthuis The multigenic sphingomyelin synthase family J. Biol. Chem. 281 2006 29421 29425 (Pubitemid 44536948)
34. J. Bielawski, J.S. Pierce, J. Snider, B. Rembiesa, Z.M. Szulc, and A. Bielawska Sphingolipid analysis by high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS) Adv. Exp. Med. Biol. 688 2010 46 59
35. A.L. Ziulkoski, A.R. Zimmer, and F.C. Guma De novo synthesis and recycling pathways of sphingomyelin in rat Sertoli cells Biochem. Biophys. Res. Commun. 281 2001 971 975 (Pubitemid 32917827)
36. A.B. Shakor, M. Taniguchi, K. Kitatani, M. Hashimoto, S. Asano, A. Hayashi, K. Nomura, J. Bielawski, A. Bielawska, K. Watanabe, T. Kobayashi, Y. Igarashi, H. Umehara, H. Takeya, and T. Okazaki Sphingomyelin synthase 1-generated sphingomyelin plays an important role in transferrin trafficking and cell proliferation J. Biol. Chem. 286 2011 36053 36062
37. Z. Li, T.K. Hailemariam, H. Zhou, Y. Li, D.C. Duckworth, D.A. Peake, Y. Zhang, M.S. Kuo, G. Cao, and X.C. Jiang Inhibition of sphingomyelin synthase (SMS) affects intracellular sphingomyelin accumulation and plasma membrane lipid organization Biochim. Biophys. Acta 1771 2007 1186 1194 (Pubitemid 47404966)
38. F.G. Tafesse, K. Huitema, M. Hermansson, S. van der Poel, J. van den Dikkenberg, A. Uphoff, P. Somerharju, and J.C. Holthuis Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells J. Biol. Chem. 282 2007 17537 17547 (Pubitemid 47100300)
39. A.M. Vacaru, F.G. Tafesse, P. Ternes, V. Kondylis, M. Hermansson, J.F. Brouwers, P. Somerharju, C. Rabouille, and J.C. Holthuis Sphingomyelin synthase-related protein SMSr controls ceramide homeostasis in the ER J. Cell Biol. 185 2009 1013 1027
40. P. Ternes, J.F. Brouwers, J. van den Dikkenberg, and J.C. Holthuis Sphingomyelin synthase SMS2 displays dual activity as ceramide phosphoethanolamine synthase J. Lipid Res. 50 2009 2270 2277
41. N. Guillen, M.A. Navarro, J.C. Surra, C. Arnal, M. Fernandez-Juan, J.A. Cebrian-Perez, and J. Osada Cloning, characterization, expression and comparative analysis of pig Golgi membrane sphingomyelin synthase 1 Gene 388 2007 117 124 (Pubitemid 46014020)
42. C. Man, and J. Lee Molecular cloning, sequence characterization, and tissue expression analysis of chicken sphingomyelin synthase 1 (SMS1) Mol. Cell. Biochem. 357 2011 353 361
43. P. Bork, and E.V. Koonin Predicting functions from protein sequences - where are the bottlenecks? Nat. Genet. 18 1998 313 318 (Pubitemid 28158157)
44. F.N. Barrera, J.A. Poveda, J.M. Gonzalez-Ros, and J.L. Neira Binding of the C-terminal sterile alpha motif (SAM) domain of human p73 to lipid membranes J. Biol. Chem. 278 2003 46878 46885 (Pubitemid 37452269)
45. F. Qiao, and J.U. Bowie The many faces of SAM Sci. STKE 2005 re7
46. A.F. Neuwald An unexpected structural relationship between integral membrane phosphatases and soluble haloperoxidases Protein Sci. 6 1997 1764 1767 (Pubitemid 27333079)
47. C. Yeang, S. Varshney, R. Wang, Y. Zhang, D. Ye, and X.C. Jiang The domain responsible for sphingomyelin synthase (SMS) activity Biochim. Biophys. Acta 1781 2008 610 617
48. E.C. Mandon, I. Ehses, J. Rother, G. van Echten, and K. Sandhoff Subcellular localization and membrane topology of serine palmitoyltransferase, 3-dehydrosphinganine reductase, and sphinganine N-acyltransferase in mouse liver J. Biol. Chem. 267 1992 11144 11148
49. K. Hanada, K. Kumagai, N. Tomishige, and M. Kawano CERT and intracellular trafficking of ceramide Biochim. Biophys. Acta 1771 2007 644 653 (Pubitemid 46856888)
50. Y. Ishibashi, A. Kohyama-Koganeya, and Y. Hirabayashi New insights on glucosylated lipids: metabolism and functions Biochim. Biophys. Acta 1831 2013 1475 1485
51. C. Yeang, T. Ding, W.J. Chirico, and X.C. Jiang Subcellular targeting domains of sphingomyelin synthase 1 and 2 Nutr. Metab. (Lond.) 8 2011 89
52. M. Miyaji, Z.X. Jin, S. Yamaoka, R. Amakawa, S. Fukuhara, S.B. Sato, T. Kobayashi, N. Domae, T. Mimori, E.T. Bloom, T. Okazaki, and H. Umehara Role of membrane sphingomyelin and ceramide in platform formation for Fas-mediated apoptosis J. Exp. Med. 202 2005 249 259 (Pubitemid 41043821)
53. F.G. Tafesse, S. Sanyal, J. Ashour, C.P. Guimaraes, M. Hermansson, P. Somerharju, and H.L. Ploegh Intact sphingomyelin biosynthetic pathway is essential for intracellular transport of influenza virus glycoproteins Proc. Natl. Acad. Sci. U. S. A. 110 2013 6406 6411
54. S. Asano, K. Kitatani, M. Taniguchi, M. Hashimoto, K. Zama, S. Mitsutake, Y. Igarashi, H. Takeya, J. Kigawa, A. Hayashi, H. Umehara, and T. Okazaki Regulation of cell migration by sphingomyelin synthases: sphingomyelin in lipid rafts decreases responsiveness to signaling by the CXCL12/CXCR4 pathway Mol. Cell. Biol. 32 2012 3242 3252
55. S. Mitsutake, K. Zama, H. Yokota, T. Yoshida, M. Tanaka, M. Mitsui, M. Ikawa, M. Okabe, Y. Tanaka, T. Yamashita, H. Takemoto, T. Okazaki, K. Watanabe, and Y. Igarashi Dynamic modification of sphingomyelin in lipid microdomains controls development of obesity, fatty liver, and type 2 diabetes J. Biol. Chem. 286 2011 28544 28555
56. M. Tani, and O. Kuge Sphingomyelin synthase 2 is palmitoylated at the COOH-terminal tail, which is involved in its localization in plasma membranes Biochem. Biophys. Res. Commun. 381 2009 328 332
57. T. Ding, Z. Li, T. Hailemariam, S. Mukherjee, F.R. Maxfield, M.P. Wu, and X.C. Jiang SMS overexpression and knockdown: impact on cellular sphingomyelin and diacylglycerol metabolism, and cell apoptosis J. Lipid Res. 49 2008 376 385 (Pubitemid 351213622)
58. M. Villani, M. Subathra, Y.B. Im, Y. Choi, P. Signorelli, M. Del Poeta, and C. Luberto Sphingomyelin synthases regulate production of diacylglycerol at the Golgi Biochem. J. 414 2008 31 41
59. M. Yano, K. Watanabe, T. Yamamoto, K. Ikeda, T. Senokuchi, M. Lu, T. Kadomatsu, H. Tsukano, M. Ikawa, M. Okabe, S. Yamaoka, T. Okazaki, H. Umehara, T. Gotoh, W.J. Song, K. Node, R. Taguchi, K. Yamagata, and Y. Oike Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice J. Biol. Chem. 286 2011 3992 4002
60. M. Yano, T. Yamamoto, N. Nishimura, T. Gotoh, K. Watanabe, K. Ikeda, Y. Garan, R. Taguchi, K. Node, T. Okazaki, and Y. Oike Increased oxidative stress impairs adipose tissue function in sphingomyelin synthase 1 null mice PLoS One 8 2013 e61380
61. Z. Li, Y. Fan, J. Liu, Y. Li, C. Huan, H.H. Bui, M.S. Kuo, T.S. Park, G. Cao, and X.C. Jiang Impact of sphingomyelin synthase 1 deficiency on sphingolipid metabolism and atherosclerosis in mice Arterioscler. Thromb. Vasc. Biol. 32 2012 1577 1584
62. M.H. Lu, M. Takemoto, K. Watanabe, H. Luo, M. Nishimura, M. Yano, H. Tomimoto, T. Okazaki, Y. Oike, and W.J. Song Deficiency of sphingomyelin synthase-1 but not sphingomyelin synthase-2 causes hearing impairments in mice J. Physiol. 590 2012 4029 4044
63. T.K. Hailemariam, C. Huan, J. Liu, Z. Li, C. Roman, M. Kalbfeisch, H.H. Bui, D.A. Peake, M.S. Kuo, G. Cao, R. Wadgaonkar, and X.C. Jiang Sphingomyelin synthase 2 deficiency attenuates NFkappaB activation Arterioscler. Thromb. Vasc. Biol. 28 2008 1519 1526
64. Y. Fan, F. Shi, J. Liu, J. Dong, H.H. Bui, D.A. Peake, M.S. Kuo, G. Cao, and X.C. Jiang Selective reduction in the sphingomyelin content of atherogenic lipoproteins inhibits their retention in murine aortas and the subsequent development of atherosclerosis Arterioscler. Thromb. Vasc. Biol. 30 2010 2114 2120
65. S. Gowda, C. Yeang, S. Wadgaonkar, F. Anjum, N. Grinkina, M. Cutaia, X.C. Jiang, and R. Wadgaonkar Sphingomyelin synthase 2 (SMS2) deficiency attenuates LPS-induced lung injury Am. J. Physiol. Lung Cell. Mol. Physiol. 300 2011 L430 L440
66. J. Liu, C. Huan, M. Chakraborty, H. Zhang, D. Lu, M.S. Kuo, G. Cao, and X.C. Jiang Macrophage sphingomyelin synthase 2 deficiency decreases atherosclerosis in mice Circ. Res. 105 2009 295 303
67. Y. Zhang, J. Dong, X. Zhu, W. Wang, and Q. Yang The effect of sphingomyelin synthase 2 (SMS2) deficiency on the expression of drug transporters in mouse brain Biochem. Pharmacol. 82 2011 287 294
68. Y. Li, J. Dong, T. Ding, M.S. Kuo, G. Cao, X.C. Jiang, and Z. Li Sphingomyelin synthase 2 activity and liver steatosis: An effect of ceramide-mediated peroxisome proliferator-activated receptor gamma2 suppression Arterioscler. Thromb. Vasc. Biol. 33 2013 1513 1520
69. J. Liu, H. Zhang, Z. Li, T.K. Hailemariam, M. Chakraborty, K. Jiang, D. Qiu, H.H. Bui, D.A. Peake, M.S. Kuo, R. Wadgaonkar, G. Cao, and X.C. Jiang Sphingomyelin synthase 2 is one of the determinants for plasma and liver sphingomyelin levels in mice Arterioscler. Thromb. Vasc. Biol. 29 2009 850 856
70. S. Imgrund, D. Hartmann, H. Farwanah, M. Eckhardt, R. Sandhoff, J. Degen, V. Gieselmann, K. Sandhoff, and K. Willecke Adult ceramide synthase 2 (CERS2)-deficient mice exhibit myelin sheath defects, cerebellar degeneration, and hepatocarcinomas J. Biol. Chem. 284 2009 33549 33560
71. P. Ebel, K. Vom Dorp, E. Petrasch-Parwez, A. Zlomuzica, K. Kinugawa, J. Mariani, D. Minich, C. Ginkel, J. Welcker, J. Degen, M. Eckhardt, E. Dere, P. Dormann, and K. Willecke Inactivation of ceramide synthase 6 in mice results in an altered sphingolipid metabolism and behavioral abnormalities J. Biol. Chem. 288 2013 21433 21447
72. R. Jennemann, M. Rabionet, K. Gorgas, S. Epstein, A. Dalpke, U. Rothermel, A. Bayerle, F. van der Hoeven, S. Imgrund, J. Kirsch, W. Nickel, K. Willecke, H. Riezman, H.J. Grone, and R. Sandhoff Loss of ceramide synthase 3 causes lethal skin barrier disruption Hum. Mol. Genet. 21 2012 586 608
73. T.D. Mullen, S. Spassieva, R.W. Jenkins, K. Kitatani, J. Bielawski, Y.A. Hannun, and L.M. Obeid Selective knockdown of ceramide synthases reveals complex interregulation of sphingolipid metabolism J. Lipid Res. 52 2011 68 77
74. A. Delgado, J. Casas, A. Llebaria, J.L. Abad, and G. Fabrias Inhibitors of sphingolipid metabolism enzymes Biochim. Biophys. Acta 1758 2006 1957 1977 (Pubitemid 44879369)
75. J. Robert MS-209 Schering Curr. Opin. Investig. Drugs 5 2004 1340 1347 (Pubitemid 40074976)
76. E. Amtmann The antiviral, antitumoural xanthate D609 is a competitive inhibitor of phosphatidylcholine-specific phospholipase C Drugs Exp. Clin. Res. 22 1996 287 294 (Pubitemid 27060176)
77. A. Gonzalez-Roura, J. Casas, and A. Llebaria Synthesis and phospholipase C inhibitory activity of D609 diastereomers Lipids 37 2002 401 406 (Pubitemid 34441803)
78. R.M. Adibhatla, J.F. Hatcher, and A. Gusain Tricyclodecan-9-yl- xanthogenate (D609) mechanism of actions: a mini-review of literature Neurochem. Res. 37 2012 671 679
79. C. Luberto, and Y.A. Hannun 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 1998 14550 14559 (Pubitemid 28319178)
80. L. Riboni, P. Viani, R. Bassi, P. Giussani, and G. Tettamanti Basic fibroblast growth factor-induced proliferation of primary astrocytes. Evidence for the involvement of sphingomyelin biosynthesis J. Biol. Chem. 276 2001 12797 12804
81. A. Meng, C. Luberto, P. Meier, A. Bai, X. Yang, Y.A. Hannun, and D. Zhou Sphingomyelin synthase as a potential target for D609-induced apoptosis in U937 human monocytic leukemia cells Exp. Cell Res. 292 2004 385 392 (Pubitemid 38018853)
82. A. Bai, G.P. Meier, Y. Wang, C. Luberto, Y.A. Hannun, and D. Zhou Prodrug modification increases potassium tricyclo[5.2.1.0(2,6)]-decan-8-yl dithiocarbonate (D609) chemical stability and cytotoxicity against U937 leukemia cells J. Pharmacol. Exp. Ther. 309 2004 1051 1059 (Pubitemid 38669691)
83. D. Milhas, C.J. Clarke, and Y.A. Hannun Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids FEBS Lett. 584 2010 1887 1894
84. Z.X. Jin, C.R. Huang, L. Dong, S. Goda, T. Kawanami, T. Sawaki, T. Sakai, X.P. Tong, Y. Masaki, T. Fukushima, M. Tanaka, T. Mimori, H. Tojo, E.T. Bloom, T. Okazaki, and H. Umehara Impaired TCR signaling through dysfunction of lipid rafts in sphingomyelin synthase 1 (SMS1)-knockdown T cells Int. Immunol. 20 2008 1427 1437
85. L. Dong, K. Watanabe, M. Itoh, C.R. Huan, X.P. Tong, T. Nakamura, M. Miki, H. Iwao, A. Nakajima, T. Sakai, T. Kawanami, T. Sawaki, Y. Masaki, T. Fukushima, Y. Fujita, M. Tanaka, M. Yano, T. Okazaki, and H. Umehara CD4 + T-cell dysfunctions through the impaired lipid rafts ameliorate concanavalin A-induced hepatitis in sphingomyelin synthase 1-knockout mice Int. Immunol. 24 2012 327 337
86. E. Molnar, M. Swamy, M. Holzer, K. Beck-Garcia, R. Worch, C. Thiele, G. Guigas, K. Boye, I.F. Luescher, P. Schwille, R. Schubert, and W.W. Schamel Cholesterol and sphingomyelin drive ligand-independent T-cell antigen receptor nanoclustering J. Biol. Chem. 287 2012 42664 42674
87. T.R. Bilderback, R.J. Grigsby, and R.T. Dobrowsky Association of p75(NTR) with caveolin and localization of neurotrophin-induced sphingomyelin hydrolysis to caveolae J. Biol. Chem. 272 1997 10922 10927
88. V. Puri, R. Watanabe, R.D. Singh, M. Dominguez, J.C. Brown, C.L. Wheatley, D.L. Marks, and R.E. Pagano Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways J. Cell Biol. 154 2001 535 547 (Pubitemid 34286160)
89. M. Koivusalo, M. Jansen, P. Somerharju, and E. Ikonen Endocytic trafficking of sphingomyelin depends on its acyl chain length Mol. Biol. Cell 18 2007 5113 5123 (Pubitemid 350246710)
90. M. Koval, and R.E. Pagano Lipid recycling between the plasma membrane and intracellular compartments: transport and metabolism of fluorescent sphingomyelin analogues in cultured fibroblasts J. Cell Biol. 108 1989 2169 2181 (Pubitemid 19168910)
91. C. Nusshold, A. Uellen, E. Bernhart, A. Hammer, S. Damm, A. Wintersperger, H. Reicher, A. Hermetter, E. Malle, and W. Sattler Endocytosis and intracellular processing of BODIPY-sphingomyelin by murine CATH.a neurons Biochim. Biophys. Acta 1831 2013 1665 1678
92. R.E. Pagano, R. Watanabe, C. Wheatley, and C.S. Chen Use of N-[5-(5,7-dimethyl boron dipyrromethene difluoride-sphingomyelin to study membrane traffic along the endocytic pathway Chem. Phys. Lipids 102 1999 55 63 (Pubitemid 29438659)
93. K. Yuyama, H. Sun, S. Mitsutake, and Y. Igarashi Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia J. Biol. Chem. 287 2012 10977 10989
94. A.T. Hutchinson, P.A. Ramsland, D.R. Jones, M. Agostino, M.E. Lund, C.V. Jennings, V. Bockhorni, E. Yuriev, A.B. Edmundson, and R.L. Raison Free Ig light chains interact with sphingomyelin and are found on the surface of myeloma plasma cells in an aggregated form J. Immunol. 185 2010 4179 4188
95. M. Subathra, A. Qureshi, and C. Luberto Sphingomyelin synthases regulate protein trafficking and secretion PLoS One 6 2011 e23644
96. J.M. Duran, F. Campelo, J. van Galen, T. Sachsenheimer, J. Sot, M.V. Egorov, C. Rentero, C. Enrich, R.S. Polishchuk, F.M. Goni, B. Brugger, F. Wieland, and V. Malhotra Sphingomyelin organization is required for vesicle biogenesis at the Golgi complex EMBO J. 31 2012 4535 4546
97. B. Soreghan, S.N. Thomas, and A.J. Yang Aberrant sphingomyelin/ceramide metabolic-induced neuronal endosomal/lysosomal dysfunction: potential pathological consequences in age-related neurodegeneration Adv. Drug Deliv. Rev. 55 2003 1515 1524 (Pubitemid 37464576)
98. G. Sumara, I. Formentini, S. Collins, I. Sumara, R. Windak, B. Bodenmiller, R. Ramracheya, D. Caille, H. Jiang, K.A. Platt, P. Meda, R. Aebersold, P. Rorsman, and R. Ricci Regulation of PKD by the MAPK p38delta in insulin secretion and glucose homeostasis Cell 136 2009 235 248
99. J. Chen, F. Deng, J. Li, and Q.J. Wang Selective binding of phorbol esters and diacylglycerol by individual C1 domains of the PKD family Biochem. J. 411 2008 333 342 (Pubitemid 351580185)
100. Y. Maeda, G.V. Beznoussenko, J. Van Lint, A.A. Mironov, and V. Malhotra Recruitment of protein kinase D to the trans-Golgi network via the first cysteine-rich domain EMBO J. 20 2001 5982 5990 (Pubitemid 33049273)
101. O. Rey, and E. Rozengurt Protein kinase D interacts with Golgi via its cysteine-rich domain Biochem. Biophys. Res. Commun. 287 2001 21 26 (Pubitemid 32912457)
102. N.C. Lucki, and M.B. Sewer Nuclear sphingolipid metabolism Annu. Rev. Physiol. 74 2012 131 151
103. M. Watanabe, T. Kitano, T. Kondo, T. Yabu, Y. Taguchi, M. Tashima, H. Umehara, N. Domae, T. Uchiyama, and T. Okazaki Increase of nuclear ceramide through caspase-3-dependent regulation of the "sphingomyelin cycle" in Fas-induced apoptosis Cancer Res. 64 2004 1000 1007 (Pubitemid 38176903)
104. E. Albi, and M.P. Viola-Magni Chromatin-associated sphingomyelin: metabolism in relation to cell function Cell Biochem. Funct. 21 2003 211 215 (Pubitemid 36988373)
105. E. Albi, A. Lazzarini, R. Lazzarini, A. Floridi, E. Damaskopoulou, F. Curcio, and S. Cataldi Nuclear lipid microdomain as place of interaction between sphingomyelin and DNA during liver regeneration Int. J. Mol. Sci. 14 2013 6529 6541
106. E.B. Romanenko, A.V. Alessenko, and B.F. Vanyushin Effect of sphingomyelin and antioxidants on the in vitro and in vivo DNA methylation Biochem. Mol. Biol. Int. 35 1995 87 94
107. G.A. Patwardhan, and Y.Y. Liu Sphingolipids and expression regulation of genes in cancer Prog. Lipid Res. 50 2011 104 114
108. D.H. Nguyen-Tran, N. Hait, H. Sperber, J. Qi, K. Fischer, N. Ieronimakis, M. Pantoja, A. Hays, J. Allegood, M. Reyes, S. Spiegel, and H. Ruohola-Baker Molecular mechanism of sphingosine-1-phosphate action in duchenne muscular dystrophy Dis. Model. Mech. 2013 10.1242/dmm.013631
109. N.C. Zembruski, C.D. Nguyen, D. Theile, R.M. Ali, M. Herzog, G. Hofhaus, U. Heintz, J. Burhenne, W.E. Haefeli, and J. Weiss Liposomal sphingomyelin influences the cellular lipid profile of human lymphoblastic leukemia cells without effect on P-glycoprotein activity Mol. Pharm. 10 2013 1020 1034
110. Y. Osawa, A. Suetsugu, R. Matsushima-Nishiwaki, I. Yasuda, T. Saibara, H. Moriwaki, M. Seishima, and O. Kozawa Liver acid sphingomyelinase inhibits growth of metastatic colon cancer J. Clin. Invest. 123 2013 834 843
111. A.E. Alewijnse, S.L. Peters, and M.C. Michel Cardiovascular effects of sphingosine-1-phosphate and other sphingomyelin metabolites Br. J. Pharmacol. 143 2004 666 684 (Pubitemid 39611603)
112. R.G. Sitrin, T.M. Sassanella, and H.R. Petty An obligate role for membrane-associated neutral sphingomyelinase activity in orienting chemotactic migration of human neutrophils Am. J. Respir. Cell Mol. Biol. 44 2011 205 212
113. A. Boecke, D. Sieger, C.D. Neacsu, H. Kashkar, and M. Kronke Factor associated with neutral sphingomyelinase activity mediates navigational capacity of leukocytes responding to wounds and infection: live imaging studies in zebrafish larvae J. Immunol. 189 2012 1559 1566
114. Z. Yang, and D.J. Klionsky Eaten alive: a history of macroautophagy Nat. Cell Biol. 12 2010 814 822
115. G. Kroemer, G. Marino, and B. Levine Autophagy and the integrated stress response Mol. Cell 40 2010 280 293
116. W. Jiang, and B. Ogretmen Ceramide stress in survival versus lethal autophagy paradox: ceramide targets autophagosomes to mitochondria and induces lethal mitophagy Autophagy 9 2013 258 259
117. G. Barcelo-Coblijn, M.L. Martin, R.F. de Almeida, M.A. Noguera-Salva, A. Marcilla-Etxenike, F. Guardiola-Serrano, A. Luth, B. Kleuser, J.E. Halver, and P.V. Escriba Sphingomyelin and sphingomyelin synthase (SMS) in the malignant transformation of glioma cells and in 2-hydroxyoleic acid therapy Proc. Natl. Acad. Sci. U. S. A. 108 2011 19569 19574
118. Y. Barenholz Sphingomyelin and cholesterol: from membrane biophysics and rafts to potential medical applications Subcell. Biochem. 37 2004 167 215
119. M. Itoh, T. Kitano, M. Watanabe, T. Kondo, T. Yabu, Y. Taguchi, K. Iwai, M. Tashima, T. Uchiyama, and T. Okazaki Possible role of ceramide as an indicator of chemoresistance: decrease of the ceramide content via activation of glucosylceramide synthase and sphingomyelin synthase in chemoresistant leukemia Clin. Cancer Res. 9 2003 415 423 (Pubitemid 36109759)
120. Y. Uchida, M. Itoh, Y. Taguchi, S. Yamaoka, H. Umehara, S. Ichikawa, Y. Hirabayashi, W.M. Holleran, and T. Okazaki Ceramide reduction and transcriptional up-regulation of glucosylceramide synthase through doxorubicin-activated Sp1 in drug-resistant HL-60/ADR cells Cancer Res. 64 2004 6271 6279 (Pubitemid 39129431)
121. J. Schwamb, V. Feldhaus, M. Baumann, M. Patz, S. Brodesser, R. Brinker, J. Claasen, C.P. Pallasch, M. Hallek, C.M. Wendtner, and L.P. Frenzel B-cell receptor triggers drug sensitivity of primary CLL cells by controlling glucosylation of ceramides Blood 120 2011 3978 3985
122. T.A. Burns, M. Subathra, P. Signorelli, Y. Choi, X. Yang, Y. Wang, M. Villani, K. Bhalla, D. Zhou, and C. Luberto Sphingomyelin synthase 1 activity is regulated by the BCR-ABL oncogene J. Lipid Res. 54 2013 794 805
123. E. Lafont, K. Kitatani, T. Okazaki, and B. Segui Regulation of death and growth signals at the plasma membrane by sphingomyelin synthesis: implications for hematological malignancies Recent Pat Anticancer Drug Discov. 6 2011 324 333
124. E. Lafont, D. Milhas, S. Carpentier, V. Garcia, Z.X. Jin, H. Umehara, T. Okazaki, K. Schulze-Osthoff, T. Levade, H. Benoist, and B. Segui Caspase-mediated inhibition of sphingomyelin synthesis is involved in FasL-triggered cell death Cell Death Differ. 17 2010 642 654
125. D. Separovic, L. Semaan, A.L. Tarca, M.Y. Awad Maitah, K. Hanada, J. Bielawski, M. Villani, and C. Luberto Suppression of sphingomyelin synthase 1 by small interference RNA is associated with enhanced ceramide production and apoptosis after photodamage Exp. Cell Res. 314 2008 1860 1868
126. W.J. van Blitterswijk, J.B. Klarenbeek, A.H. van der Luit, M.C. Alderliesten, M. van Lummel, and M. Verheij Fas/CD95 down-regulation in lymphoma cells through acquired alkyllysophospholipid resistance: partial role of associated sphingomyelin deficiency Biochem. J. 425 2009 225 234
127. M.J. Miro-Obradors, J. Osada, H. Aylagas, I. Sanchez-Vegazo, and E. Palacios-Alaiz Microsomal sphingomyelin accumulation in thioacetamide-injured regenerating rat liver: involvement of sphingomyelin synthase activity Carcinogenesis 14 1993 941 946 (Pubitemid 23169152)
128. V. Teichgraber, M. Ulrich, N. Endlich, J. Riethmuller, B. Wilker, C.C. De Oliveira-Munding, A.M. van Heeckeren, M.L. Barr, G. von Kurthy, K.W. Schmid, M. Weller, B. Tummler, F. Lang, H. Grassme, G. Doring, and E. Gulbins Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis Nat. Med. 14 2008 382 391 (Pubitemid 351499396)
129. M.M. Zegers, and D. Hoekstra Sphingolipid transport to the apical plasma membrane domain in human hepatoma cells is controlled by PKC and PKA activity: a correlation with cell polarity in HepG2 cells J. Cell Biol. 138 1997 307 321 (Pubitemid 27323533)
130. L.A. Lemonnier, D.L. Dillehay, M.J. Vespremi, J. Abrams, E. Brody, and E.M. Schmelz Sphingomyelin in the suppression of colon tumors: prevention versus intervention Arch. Biochem. Biophys. 419 2003 129 138 (Pubitemid 37329979)
131. E.M. Schmelz, D.L. Dillehay, S.K. Webb, A. Reiter, J. Adams, and A.H. Merrill Jr. Sphingomyelin consumption suppresses aberrant colonic crypt foci and increases the proportion of adenomas versus adenocarcinomas in CF1 mice treated with 1,2-dimethylhydrazine: implications for dietary sphingolipids and colon carcinogenesis Cancer Res. 56 1996 4936 4941 (Pubitemid 26374432)
132. J.C. Mazzei, H. Zhou, B.P. Brayfield, R. Hontecillas, J. Bassaganya-Riera, and E.M. Schmelz Suppression of intestinal inflammation and inflammation-driven colon cancer in mice by dietary sphingomyelin: importance of peroxisome proliferator-activated receptor gamma expression J. Nutr. Biochem. 22 2011 1160 1171
133. P. Zhang, B. Li, S. Gao, and R.D. Duan Dietary sphingomyelin inhibits colonic tumorigenesis with an up-regulation of alkaline sphingomyelinase expression in ICR mice Anticancer Res. 28 2008 3631 3635
134. E.M. Schmelz, M.C. Sullards, D.L. Dillehay, and A.H. Merrill Jr. Colonic cell proliferation and aberrant crypt foci formation are inhibited by dairy glycosphingolipids in 1,2-dimethylhydrazine-treated CF1 mice J. Nutr. 130 2000
135. T. Sugawara, T. Tsuduki, S. Yano, M. Hirose, J. Duan, K. Aida, I. Ikeda, and T. Hirata Intestinal absorption of dietary maize glucosylceramide in lymphatic duct cannulated rats J. Lipid Res. 51 2010 1761 1769
136. Y. Hu, R.K. Le Leu, D. Belobrajdic, and G.P. Young The potential of sphingomyelin as a chemopreventive agent in AOM-induced colon cancer model: wild-type and p53 +/- mice Mol. Nutr. Food Res. 52 2008 558 566
137. D.E. Modrak, W. Lew, D.M. Goldenberg, and R. Blumenthal Sphingomyelin potentiates chemotherapy of human cancer xenografts Biochem. Biophys. Res. Commun. 268 2000 603 606 (Pubitemid 30119668)
138. P. Narayan, and R. Dahiya Alterations in sphingomyelin and fatty acids in human benign prostatic hyperplasia and prostatic cancer Biomed. Biochim. Acta 50 1991 1099 1108
139. D. Pchejetski, T. Bohler, J. Stebbing, and J. Waxman Therapeutic potential of targeting sphingosine kinase 1 in prostate cancer Nat. Rev. Urol. 8 2011 569 678
140. L. Brizuela, A. Dayon, N. Doumerc, I. Ader, M. Golzio, J.C. Izard, Y. Hara, B. Malavaud, and O. Cuvillier The sphingosine kinase-1 survival pathway is a molecular target for the tumor-suppressive tea and wine polyphenols in prostate cancer FASEB J. 24 2010 3882 3894
141. D. Pchejetski, M. Golzio, E. Bonhoure, C. Calvet, N. Doumerc, V. Garcia, C. Mazerolles, P. Rischmann, J. Teissie, B. Malavaud, and O. Cuvillier Sphingosine kinase-1 as a chemotherapy sensor in prostate adenocarcinoma cell and mouse models Cancer Res. 65 2005 11667 11675 (Pubitemid 41821727)
142. J. Nunes, M. Naymark, L. Sauer, A. Muhammad, H. Keun, J. Sturge, J. Stebbing, J. Waxman, and D. Pchejetski Circulating sphingosine-1-phosphate and erythrocyte sphingosine kinase-1 activity as novel biomarkers for early prostate cancer detection Br. J. Cancer 106 2012 909 915
143. S. Chatterjee, A. Kolmakova, and M. Miller The role of the phospholipid sphingomyelin in heart disease Curr. Opin. Investig. Drugs 7 2006 219 228
144. X. Wang, J. Dong, Y. Zhao, Y. Li, and M. Wu Adenovirus-mediated sphingomyelin synthase 2 increases atherosclerotic lesions in ApoE KO mice Lipids Health Dis. 10 2011 7
145. J. Dong, J. Liu, B. Lou, Z. Li, X. Ye, M. Wu, and X.C. Jiang Adenovirus-mediated overexpression of sphingomyelin synthases 1 and 2 increases the atherogenic potential in mice J. Lipid Res. 47 2006 1307 1314 (Pubitemid 43830723)
146. J. Novotny, A. Hrabalek, and K. Vavrova Synthesis and structure-activity relationships of skin ceramides Curr. Med. Chem. 17 2010 2301 2324
147. G. Imokawa A possible mechanism underlying the ceramide deficiency in atopic dermatitis: expression of a deacylase enzyme that cleaves the N-acyl linkage of sphingomyelin and glucosylceramide J. Dermatol. Sci. 55 2009 1 9
148. J. Hara, K. Higuchi, R. Okamoto, M. Kawashima, and G. Imokawa High-expression of sphingomyelin deacylase is an important determinant of ceramide deficiency leading to barrier disruption in atopic dermatitis J. Invest. Dermatol. 115 2000 406 413
149. Y. Murata, J. Ogata, Y. Higaki, M. Kawashima, Y. Yada, K. Higuchi, T. Tsuchiya, S. Kawainami, and G. Imokawa Abnormal expression of sphingomyelin acylase in atopic dermatitis: an etiologic factor for ceramide deficiency? J. Invest. Dermatol. 106 1996 1242 1249 (Pubitemid 26195849)