Age-Dependent Changes in the Sphingolipid Composition of Mouse CD4+ T Cell Membranes and Immune Synapses Implicate Glucosylceramides in Age-Related T Cell Dysfunction

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Molano, Alberto ^a   Huang, Zhaofeng ^a,d   Marko, Melissa G ^a   Azzi, Angelo ^a   Wu, Dayong ^a   Wang, Elaine ^b   Kelly, Samuel L ^b   Merrill, Alfred H ^b   Bunnell, Stephen C ^c   Meydani, Simin Nikbin ^a,c  

^a TUFTS UNIVERSITY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c TUFTS UNIVERSITY   (United States)

^d SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSYLCERAMIDE; SPHINGOLIPID; SPHINGOMYELIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; ENRICHMENT CULTURE; HYDROLYSIS; IMMUNOLOGICAL SYNAPSE; IN VITRO STUDY; LIPID ANALYSIS; LIPID COMPOSITION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MALE; MICROENVIRONMENT; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; PURIFICATION; SIGNAL TRANSDUCTION;

AGING; ANIMALS; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELL MEMBRANE; CELL SURVIVAL; CERAMIDES; MALE; MICE; MICE, INBRED C57BL; SPHINGOLIPIDS; SYNAPSES; T-LYMPHOCYTES;

EID: 84868152429     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047650     Document Type: Article

References (48)

1. Bitterman KJ, Medvedik O, Sinclair DA, (2003) Longevity regulation in Saccharomyces cerevisiae: linking metabolism, genome stability, and heterochromatin. Microbiol Mol Biol Rev 67: 376-399, table of contents.
2. Jazwinski SM, (2000) Aging and longevity genes. Acta Biochim Pol 47: 269-279.
3. Hannun YA, Obeid LM, (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150.
4. Jiang JC, Kirchman PA, Allen M, Jazwinski SM, (2004) Suppressor analysis points to the subtle role of the LAG1 ceramide synthase gene in determining yeast longevity. Exp Gerontol 39: 999-1009.
5. Cowart LA, Hannun YA, (2007) Selective substrate supply in the regulation of yeast de novo sphingolipid synthesis. J Biol Chem 282: 12330-12340.
6. Dbaibo GS, Pushkareva MY, Rachid RA, Alter N, Smyth MJ, et al. (1998) p53-dependent ceramide response to genotoxic stress. J Clin Invest 102: 329-339.
7. Dbaibo GS, Pushkareva MY, Jayadev S, Schwarz JK, Horowitz JM, et al. (1995) Retinoblastoma gene product as a downstream target for a ceramide-dependent pathway of growth arrest. Proc Natl Acad Sci U S A 92: 1347-1351.
8. Lee JY, Bielawska AE, Obeid LM, (2000) Regulation of cyclin-dependent kinase 2 activity by ceramide. Exp Cell Res 261: 303-311.
9. Chen Y, Liu Y, Sullards MC, Merrill AH Jr, (2010) An introduction to sphingolipid metabolism and analysis by new technologies. Neuromolecular Med 12: 306-319.
10. Elson EL, Fried E, Dolbow JE, Genin GM, (2010) Phase separation in biological membranes: integration of theory and experiment. Annu Rev Biophys 39: 207-226.
11. Marsh NL, Elias PM, Holleran WM, (1995) Glucosylceramides stimulate murine epidermal hyperproliferation. J Clin Invest 95: 2903-2909.
12. Natoli TA, Smith LA, Rogers KA, Wang B, Komarnitsky S, et al. (2010) Inhibition of glucosylceramide accumulation results in effective blockade of polycystic kidney disease in mouse models. Nat Med 16: 788-792.
13. Shayman JA, Deshmukh GD, Mahdiyoun S, Thomas TP, Wu D, et al. (1991) Modulation of renal epithelial cell growth by glucosylceramide. Association with protein kinase C, sphingosine, and diacylglycerol. J Biol Chem 266: 22968-22974.
14. Zhu Y, Gumlaw N, Karman J, Zhao H, Zhang J, et al. (2011) Lowering glycosphingolipid levels in CD4+ T cells attenuates T cell receptor signaling, cytokine production, and differentiation to the Th17 lineage. J Biol Chem 286: 14787-14794.
15. Zitomer NC, Mitchell T, Voss KA, Bondy GS, Pruett ST, et al. (2009) Ceramide synthase inhibition by fumonisin B1 causes accumulation of 1-deoxysphinganine: a novel category of bioactive 1-deoxysphingoid bases and 1-deoxydihydroceramides biosynthesized by mammalian cell lines and animals. J Biol Chem 284: 4786-4795.
16. Huang S, Cheng TY, Young DC, Layre E, Madigan CA, et al. (2011) Discovery of deoxyceramides and diacylglycerols as CD1b scaffold lipids among diverse groove-blocking lipids of the human CD1 system. Proc Natl Acad Sci U S A 108: 19335-19340.
17. Taha TA, Mullen TD, Obeid LM, (2006) A house divided: ceramide, sphingosine, and sphingosine-1-phosphate in programmed cell death. Biochim Biophys Acta 1758: 2027-2036.
18. Agarwal S, Busse PJ, (2010) Innate and adaptive immunosenescence. Ann Allergy Asthma Immunol 104: 183-190; quiz 190-182, 210.
19. Marko MG, Ahmed T, Bunnell SC, Wu D, Chung H, et al. (2007) Age-associated decline in effective immune synapse formation of CD4(+) T cells is reversed by vitamin E supplementation. J Immunol 178: 1443-1449.
20. Tamir A, Eisenbraun MD, Garcia GG, Miller RA, (2000) Age-dependent alterations in the assembly of signal transduction complexes at the site of T cell/APC interaction. J Immunol 165: 1243-1251.
21. Adolfsson O, Huber BT, Meydani SN, (2001) Vitamin E-enhanced IL-2 production in old mice: naive but not memory T cells show increased cell division cycling and IL-2-producing capacity. J Immunol 167: 3809-3817.
22. Zech T, Ejsing CS, Gaus K, de Wet B, Shevchenko A, et al. (2009) Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. EMBO J 28: 466-476.
23. Merrill AH Jr, Sullards MC, Allegood JC, Kelly S, Wang E, (2005) Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry. Methods 36: 207-224.
24. Shaner RL, Allegood JC, Park H, Wang E, Kelly S, et al. (2009) Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J Lipid Res 50: 1692-1707.
25. Ikeda K, Shimizu T, Taguchi R, (2008) Targeted analysis of ganglioside and sulfatide molecular species by LC/ESI-MS/MS with theoretically expanded multiple reaction monitoring. J Lipid Res 49: 2678-2689.
26. Harder T, Kuhn M, (2000) Selective accumulation of raft-associated membrane protein LAT in T cell receptor signaling assemblies. J Cell Biol 151: 199-208.
27. Nguyen K, Sylvain NR, Bunnell SC, (2008) T cell costimulation via the integrin VLA-4 inhibits the actin-dependent centralization of signaling microclusters containing the adaptor SLP-76. Immunity 28: 810-821.
28. Seminario MC, Bunnell SC, (2008) Signal initiation in T-cell receptor microclusters. Immunol Rev 221: 90-106.
29. Lingwood D, Simons K, (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
30. Shaw AS, (2006) Lipid rafts: now you see them, now you don't. Nat Immunol 7: 1139-1142.
31. Hannun YA, Obeid LM, (2011) Many ceramides. J Biol Chem 286: 27855-27862.
32. Miyake Y, Kozutsumi Y, Nakamura S, Fujita T, Kawasaki T, (1995) Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem Biophys Res Commun 211: 396-403.
33. Nakamura S, Kozutsumi Y, Sun Y, Miyake Y, Fujita T, et al. (1996) Dual roles of sphingolipids in signaling of the escape from and onset of apoptosis in a mouse cytotoxic T-cell line, CTLL-2. J Biol Chem 271: 1255-1257.
34. Blank N, Schiller M, Gabler C, Kalden JR, Lorenz HM, (2005) Inhibition of sphingolipid synthesis impairs cellular activation, cytokine production and proliferation in human lymphocytes. Biochem Pharmacol 71: 126-135.
35. Rani CS, Abe A, Chang Y, Rosenzweig N, Saltiel AR, et al. (1995) Cell cycle arrest induced by an inhibitor of glucosylceramide synthase. Correlation with cyclin-dependent kinases. J Biol Chem 270: 2859-2867.
36. Flores I, Canela A, Vera E, Tejera A, Cotsarelis G, et al. (2008) The longest telomeres: a general signature of adult stem cell compartments. Genes Dev 22: 654-667.
37. Sahin E, Depinho RA, (2010) Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464: 520-528.
38. Jaskelioff M, Muller FL, Paik JH, Thomas E, Jiang S, et al. (2011) Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 469: 102-106.
39. Castillo SS, Levy M, Thaikoottathil JV, Goldkorn T, (2007) Reactive nitrogen and oxygen species activate different sphingomyelinases to induce apoptosis in airway epithelial cells. Exp Cell Res 313: 2680-2686.
40. Michel C, van Echten-Deckert G, Rother J, Sandhoff K, Wang E, et al. (1997) Characterization of ceramide synthesis. A dihydroceramide desaturase introduces the 4,5-trans-double bond of sphingosine at the level of dihydroceramide. J Biol Chem 272: 22432-22437.
41. Liu YY, Han TY, Giuliano AE, Cabot MC, (2001) Ceramide glycosylation potentiates cellular multidrug resistance. FASEB J 15: 719-730.
42. Kanfer JN, Legler G, Sullivan J, Raghavan SS, Mumford RA, (1975) The Gaucher mouse. Biochem Biophys Res Commun 67: 85-90.
43. Kaucic K, Liu Y, Ladisch S, (2006) Modulation of growth factor signaling by gangliosides: positive or negative? Methods Enzymol 417: 168-185.
44. Garofalo T, Lenti L, Longo A, Misasi R, Mattei V, et al. (2002) Association of GM3 with Zap-70 induced by T cell activation in plasma membrane microdomains: GM3 as a marker of microdomains in human lymphocytes. J Biol Chem 277: 11233-11238.
45. Barbat C, Trucy M, Sorice M, Garofalo T, Manganelli V, et al. (2007) p56lck, LFA-1 and PI3K but not SHP-2 interact with GM1- or GM3-enriched microdomains in a CD4-p56lck association-dependent manner. Biochem J 402: 471-481.
46. Camoletto PG, Vara H, Morando L, Connell E, Marletto FP, et al. (2009) Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18. PLoS One 4: e5310.
47. Wheeler D, Knapp E, Bandaru VV, Wang Y, Knorr D, et al. (2009) Tumor necrosis factor-alpha-induced neutral sphingomyelinase-2 modulates synaptic plasticity by controlling the membrane insertion of NMDA receptors. J Neurochem 109: 1237-1249.
48. Stefanic S, Spycher C, Morf L, Fabrias G, Casas J, et al. (2010) Glucosylceramide synthesis inhibition affects cell cycle progression, membrane trafficking, and stage differentiation in Giardia lamblia. J Lipid Res 51: 2527-2545.