Dynamics of lipid raft components during lymphocyte apoptosis: The paradigmatic role of GD3

Apoptosis

Volumn 12, Issue 5, 2007, Pages 941-949

  Malorni, Walter ^a   Giammarioli, Anna Maria ^a   Garofalo, Tina ^b   Sorice, Maurizio ^b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Apoptosis; Gangliosides; GD3; Lipid rafts; Mitochondria

Indexed keywords

CHOLESTEROL; GANGLIOSIDE GD3; SPHINGOLIPID; SPHINGOMYELIN;

APOPTOSIS; CELL DEATH; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CYTOSKELETON; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; LIPID ANALYSIS; LIPID RAFT; LYMPHOCYTE; MEMBRANE TRANSPORT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; APOPTOSIS; CYTOSKELETON; GANGLIOSIDES; HUMANS; INTRACELLULAR MEMBRANES; LYMPHOCYTES; MEMBRANE MICRODOMAINS; MITOCHONDRIA; MODELS, THEORETICAL;

EID: 34247518635     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-007-0757-1     Document Type: Review

References (91)

1. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569-572
2. Hakomori S, Handa K, Iwabuchi K, Yamamura S, Prinetti A (1998) New insights in glycosphingolipid function "signaling domain," a cell surface assembly of glycosphingolipids with signal transducer molecules, involved in cell adhesion coupled with signaling. Glycobiology 8:XI-XVIII
3. Iwabuchi K, Yamamura S, Prinetti A, Handa K, Hakomori S (1998) GM3-enriched microdomain involved in cell adhesion and signal transduction through carbohydrate-carbohydrate interaction in mouse melanoma B12 cells. J Biol Chem 273:9130-9139
4. Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544
5. Parton RG (1994) Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem 42:155-166
6. Garofalo T, Lenti L, Longo A, Misasi R, Mattei V, Pontieri GM et al (2002) Association of GM3 with Zap-70 induced by T cell activation in plasma membrane microdomains. J Biol Chem 227:11233-11238
7. Pike L, Han X, Gross RW (2005) Epidermal growth factor receptors are localized to lipid rafts that contain a balance of inner and outer leaflet lipids. J Biol Chem 280:26796-26804
8. Xavier R, Brennan T, Li Q, McCormack C, Seed B (1998) Membrane compartimentation is required for efficient T cell activation. Immunity 8:723-732
9. Chun M, Liyanage UK, Lisanti MP, Lodish HF (1994) Signal transduction of a G-protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc Natl Acad Sci USA 91:11728-11732
10. Parolini I, Sargiacomo, M, Lisanti, MP, Peschle C (1996) Signal transduction and glycophosphatidylinositol-linked proteins (lyn,lck,CD4,CD45,G- proteins, and CD55) selectively localize in Triton-insoluble plasma membrane domains of human leukemic cell lines and normal granulocytes. Blood 87:3783-3794
11. Parolini I, Topa S, Sorice M et al (1999) Phorbol ester-induced disruption of the CD4- lck complex occur within a detergent-resistant microdomain of the plasma membrane. Involvement of the translocation of activated protein Kinase C isoform. J Biol Chem 274:14176-14187
12. Cinek T, Horejsi VJ (1992) The nature of large non covalent complexes containing glycosyl-phosphatidylnositol-anchored membrane glycoproteins and protein tyrosine kinases. Immunology 149:2262-2270
13. Horejsi V, Drbal K, Cebecauer M et al (1999) GPI-microdomains: a role in signaling via immunoreceptors. Immunol Today 20:356-361
14. Furley A, Morton JS, Manalo BD, Karagogeos D, Dodd J, Jessel T (1990) The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member neurite outgrowth- promoting activity. Cell 61:157-170
15. Olive S, Dubois C, Schachner M, Rougon G (1995) The F3 neuronal glycosylphosphatidyl inositol-linked molecule is localized to glycolipid-enriched membrane subdomains and interacts with L1 and Fyn kinase in cerebellum. J Neurochem 65:2307-2317
16. Leitinger B, Hogg N (2002) The involvement of lipid rafts in the regulation of integrin function. J Cell Science 115:963-972
17. Shamri R, Grabovsky V, Feigelson, Dwir O, Van Kooyk Y, Alon R (2002) Chemokine-stimulation of lymphocytes a4 integrin avidity but not LFA-1 avidity to endothelial ligands under shear flow requires cholesterol membrane rafts. J Biol Chem 227:40027-40035.
18. Simons K, Van Meer G (1988) Lipid sorting in epithelial cells. Biochemistry 27:6197-6202
19. Manes S, Lacalle RA, Gomez-Mouton C, Martinez AC (2003) From rafts to crafts: membrane asymmetry in moving cells. Trends Immunol 24:320-326
20. Gomez-Mouton C, Abad JL, Mira E et al (2001) Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad SciUSA 98:9642-9647
21. Fais S, Malorni W (2003) Leukocyte uropod formation and membrane/cytoskeleton linkage in immune interactions. J Leukoc Biol 73:556-563
22. Pizzo P, Giurisato E, Bigsten A et al (2004) Physiological T cell activation starts and propagates in lipid rafts. Immunol Lett 91:3-9
23. Pizzo P, Viola A (2004) Lipid rafts in lymphocyte activation. Microbes Inf 6:686-692
24. Brown DA, London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275:17221-17224
25. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K (2003) Resistance of cell membranes to different detergents. Proc Natl Acad Sci USA 100:5795-5800
26. Parton RG (2003) Caveolae - from ultrastructure to molecular mechanisms. Nat Rev Mol Cell Biol 4:162-167
27. Garofalo T, Misasi R, Mattei V et al (2003) Association of the death-inducing signaling complex with microdomains after triggering through CD95/Fas. Evidence for caspase-8-ganglioside interaction in T cells. J Biol Chem 278:8309-8315
28. Edidin M (2003) The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32:257-283
29. Jacobson K, Dietrich C (1999) Looking at lipid rafts? Trends Cell Biol 9:87-91
30. Dietrich C, Yang B, Fujiwara T, Kusumi A, Jacobson K (2002) Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys J 82:274-284
31. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157:1071-1081
32. Marguet D, Lenne PF, Rigneault H, He HT (2006) Dynamics in the plasma membrane: how to combine fluidity and order. EMBO J 25:3446-3457
33. Fra AM, Williamson E, Simons K, Parton RG (1994) Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J Biol Chem 269:30745-30748
34. Sorice M, Parolini, I, Sansolini T et al (1997) Evidence for the existence of ganglioside-enriched plasma membrane domains in human peripheral lymphocytes. J Lipid Res 38:969-980
35. Montixi C, Langlet C, Bernard AM et al (1998) Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J 17:5334-5348
36. Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A (1999) T lymphocytes costimulation mediated by reorganization of membrane microdomains. Science 283:680-682
37. Resh MD (1994) Myrystilation and palmitoylation of Src family members: the fats of the matter. Cell 76:411-413
38. Zhang W, Trible RP, Samelson LE (1998) LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9:239-246
39. Kawabuchi M, Satomi Y, Takao T et al (2000) Transmembrane posphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 404:999-1003
40. Brdickova N, Brdicka T, Angelisova P et al (2003) LIME: a new membrane raft-associated adaptor protein involved in CD4 and CD8 coreceptor signalling. J Exp Med 198:1453-1462
41. Coudronniere N, Villalba M, Englund N, Altman A (2000) NF-kappa B activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-theta. Proc Natl Acad Sci USA 97:3394-3399
42. Na SY, Patra A, Scheuring Y et al (2003) Constitutively active protein kinase B enhances Lck and Erk activities and influences thymocyte selection and activation. J Immunol 171:1285-1296
43. Jordan S, Rodgers W (2003) T cell glycolipid-enriched membrane domains are constitutively assembled as membrane patches that translocate to immune synapses. J Immunol 171:78-87
44. Hakomori S (1981) Glycosphingolipids in cellular interactions differentiation and oncogenesis. Annu Rev Biochem 50:733-764
45. Grassmé H, Jekle A, Riehle A et al (2001) CD95 signaling via ceramide-rich membrane rafts. J Biol Chem 276:20589-20596
46. Hueber AO, Bernard AM, Herincs Z, Couzinet A, He HT (2002) An essential role for membrane rafts in the initiation of Fas/CD95-triggered cell death in mouse thymocytes. EMBO Rep 3:190-196
47. Toellner DS, Wang K, Singh R et al (2002) The death-inducing signaling complex is recruited to lipid rafts in Fas-induced apoptosis. Biochem Biophys Res Commun 297:876-879
48. Kiguchi K, Henning-Chubb BC, Huberman E (1990) Glycosphingolipid patterns of peripheral blood lymphocytes, monocytes, and granulocytes are cell specific. J Biochem 107:8-14
49. Muppidi JR, Siegel RM (2004) Ligand-independent redistribution of Fas (CD95) into lipid rafts mediates clonotypic T cell death. Nat Immunol 5:182-189
50. Lincoln JE, Boling M, Parikh AN, Yeh Y, Gilchrist DG, Morse LS (2006) Fas signaling induces raft coalescence that is blocked by cholesterol depletion in human RPE cells undergoing apoptosis. Invest Ophthalmol Vis Sci 47:2172-2178
51. Detre C, Kiss E, Varga Z et al (2006) Death or survival: membrane ceramide controls the fate and activation of antigen-specific T-cells depending on signal strength and duration. Cell Signal 18:294-306
52. Henkler F, Behrle E, Dennhy KM et al (2005) The extracellular domains of FasL and Fas are sufficient for the formation of supramolecular FasL-Fas clusters of high stability. J Cell Biol 168:1087-1098
53. Elyassaki W, Wu S (2006) Lipid rafts mediate ultraviolet light-induced Fas aggregation in M624 melanoma cells. Photochem Photobiol 82:787-792
54. Scheel-Toellner D, Wang K, Singh R et al (2002) The death-inducing signaling complex is recruited to lipid rafts in FAS-induced apoptosis. Biochem Biophys Res Comm 297:876-879
55. Algeciras-Schimnich A, Shen L, Barnhart BC, Murmann AE, Burkhardt JK, Peter ME (2002) Molecular ordering of the initial signaling events of CD95. Mol Cell Biol 22:207-220
56. Gombos I, Kiss E, Detre C, Laszlo G, Matko J (2006) Cholesterol and sphingolipids as lipid organizers of the immune cells' plasma membrane: their impact on the functions of MHC molecules, effector T-lymphocytes and T-cell death. Immunol Lett 104:59-69
57. Legembre P, Daburon S, Moreau P, Moreau JF, Taupin JL (2006) Modulation of Fas-mediated apoptosis by lipid rafts in T lymphocytes. J Immunol 176:716-720
58. Cahuzac N, Baum W, Kirkin V et al (2006) Fas ligand is localized to membrane rafts, where it displays increased cell death-inducing activity. Blood 107:2384-2391
59. Lacour S, Hammann A, Grazide S et al (2004) Cisplatin-induced CD95 redistribution into membrane lipid rafts of HT29 human colon cancer cells. Cancer Res 64:3593-3598
60. Matarrese P, Straface E, Pietraforte D et al (2005) Peroxynitrite induces senescence and apoptosis of red blood cells through the activation of aspartyl and cysteinyl proteases. FASEB J 19:416-418
61. Mandal D, Mazumder A, Das P, Kundu M, Basu J (2005) Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem 280:39460-39467
62. Remacle-Bonnet M, Garrouste F, Baillat G, Andre F, Marvaldi J, Pommier G (2005) Membrane rafts segregate pro- from anti-apoptotic insulin-like growth factor-I receptor signaling in colon carcinoma cells stimulated by members of the tumor necrosis factor superfamily. Am J Pathol 167:761-773
63. Janas E, Priest R, Wilde JI, White JH, Malhotra R (2005) Rituxan (anti-CD20 antibody)-induced translocation of CD20 into lipid rafts is crucial for calcium influx and apoptosis. Clin Exp Immunol 139:439-446
64. Takahashi E, Inanami O, Ohta T, Matsuda A, Kuwabara M (2006) Lipid raft disruption prevents apoptosis induced by 2-chloro-2′-deoxyadenosine (Cladribine) in leukemia cell lines. Leuk Res 30:1555-1561.
65. Tang PS, Tsang ME, Lodyga M et al (2006) Lipopolysaccharide accelerates caspase-independent but cathepsin B-dependent death of human lung epithelial cells. J Cell Physiol 209:457-467
66. De Maria R, Lenti L, Malisan F et al (1997) Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science 277:1652-1655
67. De Maria R, Rippo MR, Schuchman HE, Testi R (1998) Acidic sphingomyelinase (ASM) is necessary for Fas-induced GD3 ganglioside accumulation and efficient apoptosis of lymphoid cells. J Exp Med 187:897-902
68. Ikonen E (2001) Roles of lipid rafts in membrane transport. Curr Opin Cell Biol 13:470-477
69. Rippo MR, Malisan F, Ravagnan L et al (2000) GD3 ganglioside directly targets mitochondria in a bcl-2 controlled fashion. FASEB J 14:2047-2054
70. Garcia-Ruiz C, Colell A, Morales A, Calva M, Enrich C, Fernandez-Checa JC (2002) Trafficking of ganglioside GD3 to mitochondria by tumor necrosis factor-alpha. J Biol Chem 277:36443-36448
71. Giammarioli AM, Garofalo T, Sorice M et al (2001) GD3 glycosphingolipid contributes to FAS-mediate apoptosis via association with ezrin cytoskeletal protein. FEBS Lett 506:45-50
72. Parlato S, Giammarioli AM, Logozzi M et al (2000) CD95 (APO-1/Fas) linkage to the actin cytoskeleton through ezrin in human T lymphocytes: a novel regulatory mechanism of the CD95 apoptotic pathway. EMBO J 19:5123-5134
73. Tomas EM, Chau TA, Madrenas J (2002) Clustering of a lipid-raft associated pool of ERM proteins at the immunological synapse upon T cell receptor or CD28 ligation. Immunol Lett 83:143-147
74. Gajate C, Mollinedo F (2005) Cytoskeleton-mediated death receptor and ligand concentration in lipid rafts forms apoptosis-promoting clusters in cancer chemotherapy. J Biol Chem 280:11641-11647
75. Gupta N, Wollscheid B, Watts JD, Scheer B, Aebersold R, DeFranco AL (2006) Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat Immunol 7:625-633
76. Ardail D, Popa I, Bodennee J, Louisot P, Schmitt D, Portoukalian J (2003) The mitochondria-associated endoplasmic-reticulum subcompartment (MAM fraction) of rat liver contains highly active sphingolipid-specific glycosyltransferases. Biochem J 371:1013-1019
77. Morales A, Colell A, Mari M, Garcia-Ruiz C, Fernandez-Checa JC (2004) Glycosphingolipids and mitochondria: role in apoptosis and disease. Glycoconj J 20:579-588
78. Browman DT, Resek ME, Zajchowski LD, Robbins SM (2006) Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER. J Cell Sci 119:3149-3160
79. d'Azzo A, Tessitore A, Sano R (2006) Gangliosides as apoptotic signals in ER stress response. Cell Death Differ 13:404-414
80. Boyce M, Yuan J (2006) Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 13:363-373
81. Goetz JG, Nabi IR (2006) Interactuion of the smooth endoplasmic reticulum and mitochondria. Biochem Soc Trans 34:370-373
82. Ouasti S, Matarrese P, Paddon R et al (2006) Death receptor ligation triggers membrane scrambling between Golgi and mitochondria. Cell Death Diff 2006 (published ahead of print)
83. Garofalo T, Giammarioli AM, Misasi R et al (2005) Lipid microdomains contribute to apoptosis-associated modifications of mitochondria in T cells. Cell Death Diff 12:1378-1389
84. Birbes H, El Bawab S, Hannun YA, Obeid LM (2001) A mitochondrial pool of sphingomyelin is involved in TNFalpha-induced Bax translocation to mitochondria. FASEB J 14:2669-2679
85. Kniep B, Kniep E, Ozkucur N et al (2006) 9-O-acetyl GD3 protects tumor cells from apoptosis. Int J Can 119:67-73
86. Higuchi Y, Miura T, Kajimoto T, Ohta Y (2005) Effects of disialoganglioside GD3 on the mitochondrial membrane potential. FEBS Lett 579:3009-3013
87. Scorrano L, Petronilli V, Di Lisa F, Bernardi P (1999) Commitment to apoptosis by GD3 ganglioside depends on opening of the mitochondrial permeability transition pore. J Biol Chem 274:22581-22585
88. Karbowski M, Lee YJ, Gaune B et al (2002) Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J Cell Biol 159:931-938
89. Alirol E, James D, Huber D, Marchetto A, Vergani L, Martinou JC et al (2006) The Mitochondrial Fission Protein hFis1 Requires the Endoplasmic Reticulum Gateway to Induce Apoptosis. Mol Biol Cell 17:4593-4605
90. van Blitterswijk WJ, van der Luit AH, Veldman RJ, Verheij M, Borst J (2003) Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem J 369:199-211
91. Matarrese P, Straface E, Pietraforte D et al (2005) Galectin-1 sensitizes resting human T lymphocytes to Fas (CD95)-mediated cell death via mitochondrial hyperpolarization, budding, and fission. J Biol Chem 280:6969-6985