Glycosphingolipids and mitochondria: Role in apoptosis and disease

Glycoconjugate Journal

Volumn 20, Issue 9, 2003, Pages 579-588

  Morales, Albert ^a   Colell, Anna ^a   Mari, Montserrat ^a   Garcia Ruiz, Carmen ^b   Fernandez Checa, José C ^a,b  

^a HOSPITAL CLÍNIC   (Spain)

^b INST D INVESTIGACIONS B   (Spain)

Author keywords

Apoptosome; Cancer therapy; Cell death; GD3; NF B; Oxidative stress

Indexed keywords

CERAMIDE; GANGLIOSIDE GD3; GLYCOSPHINGOLIPID; GANGLIOSIDE; GANGLIOSIDE, GD3; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID; N ACETYLNEURAMINIC ACID;

APOPTOSIS; CANCER THERAPY; CELL DEATH; CELL MEMBRANE; CONFERENCE PAPER; FIBROGENESIS; GOLGI COMPLEX; HUMAN; LIPOGENESIS; MITOCHONDRION; MULTIDRUG RESISTANCE; NATURAL KILLER CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; METABOLISM; NEOPLASM; PATHOLOGY; REVIEW;

ANIMALS; APOPTOSIS; CELL DEATH; DRUG RESISTANCE, MULTIPLE; GANGLIOSIDES; GLUCOSE; GLYCOSPHINGOLIPIDS; GOLGI APPARATUS; HUMANS; LIPIDS; MITOCHONDRIA; MODELS, BIOLOGICAL; N-ACETYLNEURAMINIC ACID; NEOPLASMS; NF-KAPPA B; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 16644368067     PISSN: 02820080     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:GLYC.0000043294.62504.2c     Document Type: Conference Paper

References (114)

1. Klenk E, Über die ganglioside, eine neue Gruppe von zucherhaltigen Gerhirnlipoiden, Hoppe-Seylers Z Physiol Chem 273, 78-86 (1942).
2. Svennerholm L, Raal A, Composition of brain ganglio-sides, Biochim Biophys Acta 53, 422-4 (1961).
3. Hakomori S, Traveling for the glycosphingolipid path, Glycoconj J 17, 627-47 (2000).
4. Fernandez-Checa JC, Redox regulation and signalling lipids in mitochondrial apoptosis, Biochem Biophys Res Commun 304, 471-9 (2003).
5. Weiss B, Stoffel W, Human and murine serine-palmitoyl-CoA transferase-cloning, expression and characterization of the key enzyme in sphingolipid synthesis, Eur J Biochem 249, 239-47 (1997).
6. Basu S, Kaufman B, Roseman S, Enzymatic synthesis of glucocerebroside by a glucosyltransferase from embryonic chicken brain, J Biol Chem, 248, 1388-94 (1973).
7. Basu S, Schutz AM, Basu M, Roseman S, Enzymatic synthesis of galactosylcerebroside by a galactosyltransferase from embryonic chicken brain, J Biol Chem 246, 4272-9 (1971).
8. Keenan TW, Morre JD, Basu S, Ganglioside biosynthesis: Concentration of glycosphingolipid glycosyltransferase in golgi apparatus of rat liver, J Biol Chem 249, 310-4 (1974).
9. Jeckel D, Karrembauer A, Burger KN, van Meer G, Wieland F, Glucosylceramide is synthesized at the cytosolic surface of various Golgi subfractions, J Cell Biol 117, 259-67 (1992).
10. Yamashita T, Wada R, Sasaki T, Deng C, Bierfreund U, Sandhoff K, Proia RL, A vital role for glycosphingolipid synthesis during development and differentiation, Proc Natl Acad Sci USA 96, 9142-7 (1999).
11. Basu S, Basu M, Dastgheib S, Hawes JW. Biosynthesis and Regulation of Glycosphingolipid in "Comprehensive Natural Products Chemistry" (eds. Barton D, Nakanishi K, Meth-Cohen O, Vol.3) (ed. Pinto BM), Pergamon Press, New York 107-28 (1999).
12. Basu S, Das K, Basu M, Glycosyltransferase in Glycosphingolipid Biosynthesis in "Oligosaccharides in Chemistry and Biology. A Comprehensive Handbook" (eds. Ernst B, Sinay P, Hart G), Wiley-VCH Verlag GmbH, Germany 330-47, 2000.
13. Basu S, The serendipity of ganglioside biosynthesis: pathway to CARS and HY-CARS glycosyltransferases, Glycobiology 1, 469-75 (1991).
14. Funato K, Rietzman H, Vesicular and nonvesicular transport of ceramide from ER to the Golgi apparatus in yeasts, J Cell Biol 155, 949-59 (2001).
15. van Meer G, Holthuis JC, Sphingolipid transport in eukaryotic cells, Biochim Biophys Acta 1486, 145-70 (2000).
16. Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M, Fukasawa M, Nishijima M, Molecular machinery for non-vesicular trafficking of ceramide, Nature 426, 803-9 (2003).
17. Kolesnick RN, Kronke M, Regulation of ceramide production and apoptosis, Annu. Rev Physiol 60, 643-65 (1998).
18. Cremesti AE, Goñi FM, Kolesnick RN, Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome?, FEBS Lett 531, 47-53 (2002).
19. Bezombes C, Segui B, Cuvillier O, Bruno AP, Uro-Coste E, Gouaze V, Andrieu-Abadie N, Carpentier S, Laurent G, Salvayre R, Lysosomal sphingomyelinase is not solicited for apoptotic signaling, FASEB J 15, 297-9 (2001).
20. Lozano J, Menéndez S, Morales A, Ehleiter D, Liao WC, Wagman R, Haimovitz-Friedman A, Fuks Z, Kolesnick R, Cell autonomous apoptosis defects in acid sphingomyelinase knockout fibroblasts, J Biol Chem 276, 442-8 (2001).
21. Grullich C, Sullards MC, Fuks Z, Merrill AH Jr, Kolesnick R, CD95 (Fas/APO-1) signals ceramide generation independent of the effector stage of apoptosis, J Biol Chem 275, 8650-6 (2000).
22. Morita Y, Perez GI, Paris F, Miranda SR, Ehleiter D, Haimovitz-Friedman A, Fuks Z, Xie Z, Reed JC, Schuchman EH, Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy, Nat Med 6, 1109-14 (2000).
23. Segui B, Cuvillier O, Adam-Klages S, Garcia V, Malagarie-Cazenave S, Leveque S, Caspar-Bauguil S, Coudert J, Salvayre R, Kronke M, Involvement of FAN in TNF-induced apoptosis, J Clin Invest 108, 143-51 (2001).
24. Malagarie-Cazenave S, Segui B, Leveque S, Garcia V, Carpentier S, Altie MF, Brouchet A, Gouaze V, Andrieu-Abadie N, Barreira Y Benoist H, Levade T, Role of FAN in tumor necrosis factor-alpha and lipopolysaccharide-induced interleukin-6 secretion and lethality in D-galactosamine-sensitized mice, J Biol Chem in press (2004).
25. Lin T, Genestier L, Pinkoski MJ, Castro A, Nicholas S, Mogil R, Paris F, Fuks Z, Schuchman EH, Kolesnick R, Green DR, Role of acidic sphingomyelinase in Fas/CD95-mediated cell death, J Biol Chem 275, 8657-63 (2000).
26. Paris F, Genestier L, Pinkoski MJ, Castro A, Nicholas S, Mogil R, Paris F, Fuks Z, Schuchman EH, Kolesnick RN, Natural ceramide reverses Fas resistance of acid sphingomyelinase (-/-) hepatocytes, J Biol Chem 276, 8297-05 (2001).
27. García-Ruiz C, Colell A, Mari M, Morales A, Calvo M, Enrich C, Fernandez-Checa JC, Defective TNF-α-mediated hepatocellular apoptosis and liver damage in acidic sphingomyelinase knockout mice, J Clin Invest 111, 197-208 (2003).
28. Mari M, Colell A, Morales A, Pañeda C, Varela-Nieto I, Garcia-Ruiz C, Fernandez-Checa JC, Acidic sphingomyelinase downregulates the liver specific methionine adenosyltransferase 1A, contributing to tumor necrosis factor-induced lethal hepatitis, J Clin Invest 113, 895-904 (2004).
29. Heinrich M, Neumeyer J, Jakob M, Hallas C, Tchikov V, Winoto-Morbach S, Wickel M, Schneider-Brachert W, Trauzold A, Hethke A, Schutze S, Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and-3 activation, Cell Death Differ, in press (2004).
30. Wang X, The expanding role of mitochondria in apoptosis, Genes Dev 15, 2922-33 (2002).
31. Kroemer G, Mitochondrial control of apoptosis: an introduction, Biochem Biophys Res Commun 304, 433-5 (2003).
32. Deshager S, Martinou JC, Mitochondria as the central control point of apoptosis, Trends Cell Biol 10, 369-77 (2000).
33. Hannun YA, Luberto C, Ceramide in the eukaryotic stress response, Trends Cell Biol 10, 73-80 (2000).
34. Garcia-Ruiz C, Colell A, Mari M, Morales A, Fernández-Checa JC, Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione, J Biol Chem 272, 11369-77 (1997).
35. Quillet-Mary A, Jaffrezou JP, Manzat V, Bordier C, Naval J, Laurent G, Implications of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis, J Biol Chem 272, 21388-95 (1997).
36. Gudz TI, Tserng KY, Hoppel CL, Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide, J Biol Chem 272, 24154-8 (1997).
37. Gharourifar P, Klein SD, Schucht O, Schenk U, Pruschy M, Rocha S, Richter C, Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state, J Biol Chem 274, 6080-4 (1999).
38. Birbes H, Bawab SE, Hannun YA, Obeid LM, Selective hydrolysis of a mitochondrial pool of sphingomyelin induces apoptosis, FASEB J 14, 2669-79 (2001).
39. Scorrano L, Petronilli P, DiLisa F, Bernardi P, Commitment to apoptosis by GD3 ganglioside depends on opening of the mitochondrial permeability transition pore, J Biol Chem 274, 22581-5 (1999).
40. Kristal BS, Brown AM, Apoptogenic ganglioside GD3 directly induces the mitochondrial permeability transition, J Biol Chem 274, 23169-75 (1999).
41. García-Ruiz C, Colell A, París R, Fernández-Checa JC, Direct interaction of GD3 ganglioside with mitochondria generates reactive oxygen species followed by mitochondrial permeability transition, cytochrome c release and caspase activation, FASEB J 14, 847-58 (2000).
42. Colell A, Garcia-Ruiz C, Roman J, Ballesta A, Fernandez-Checa JC, Ganglioside GD3 enhances apoptosis by suppressing the nuclear factor-kappaB-dependent survival pathway, FASEB J 15, 1068-70 (2001).
43. Colell A, Garcia-Ruiz C, Mari M, Fernandez-Checa JC, Mitochondrial permeability transition induced by reactive oxygen species is independent of cholesterol-regulated membrane fluidity, FEBS Lett, 560, 63-8 (2004).
44. Inoki Y, Miura T, Kajimoto T, Kawase M, Kawase Y, Yoshida Y, Tsuji S, Kinouchi T, Endo H, Kagawa Y, Hamamoto T, Ganglioside GD3 and its mimetics induce cytochrome c release from mitochondria, Biochem Biophys Res Commun 276, 1210-6 (2000).
45. Malisan F, Franchi L, Tomassini B, Ventura N, Condo I, Rippo MR, Rufini A, Liberati L, Nachtigall C, Kniep B, Testi R, Acetylation suppresses the proapoptotic activity of GD3 ganglioside, J Exp Med 196, 1535-41 (2002).
46. Esposti MD, Erler JT, Hickman JA, Dive C, Bid, a widely expressed proapoptotic protein of the Bcl-2 family, displays lipid transfer activity, Mol Cell Biol 21, 7268-76 (2001).
47. DeMaria R, Lenti T, Malissan F, d'Agostino F, Tomassini B, Zeuner A, Rippo MR, Testi R, Requirement for GD3 ganglioside in ceramide-induced apoptosis, Science 277, 1652-5 (1997).
48. Rippo MR, Malisan F, Ravagnan L, Tomassini B, Condo IP, Constantini P, Susin SA, Rufini A, Todaro M, Kroemer G, Testi R, GD3 ganglioside directly targets mitochondria in a bcl-2 controlled fashion, FASEB J 14, 2047-54 (2000).
49. Garcia-Ruiz C, Colell A, Morales A, Calvo M, Enrich C, Fernandez-Checa JC, Trafficking of GD3 to mitochondria by tumor necrosis factor-α, J Biol Chem 277, 36443-8 (2002).
50. Colell A, Morales A, Fernandez-Checa JC, Garcia-Ruiz C, Ceramide generated by acidic sphingomyelinase contributes to tumor necrosis factor-mediated apoptosis in HT-29 cells through glycosphingolipid generation. Possible role of ganglioside GD3, FEBS Lett 526, 135-41 (2002).
51. Giammarioli AM, Garofalo T, Sorice M, Misasi R, Gambardella L, Gradini R, Fais S, Pavan A, Malorni W, GD3 glycosphingolipid contributes to Fas-mediated apoptosis via association with ezrin cytoskeletal protein, FEBS Lett 506, 45-50 (2001).
52. Rusinol A E, Cui Z, Chen M H, Vance J, An unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins, J Biol Chem 269, 27494-502 (1994).
53. 2+ responses, Science 280, 1763-6 (1998).
54. Chen HY, Varki A, O-acetylation of GD3: An enigmatic modification regulating apoptosis? J Exp Med 196, 1529-33 (2002).
55. Ghosh S, May N, Kopp E, NF-κB and Rel proteins: Evolutionary conserved mediators of immune responses, Annu Rev Immunol 16, 225-60 (1998).
56. Baldwin AS, Control of oncogenesis and cancer therapy resistance by the transcription factor NF-κB, J Clin Invest 107, 241-6 (2001).
57. Beg AA, Sha WC, Bronson RT, Ghosh S, Baltimore D, Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B, Nature 376, 167-70 (1995).
58. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS, NF-kappaB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and C-IAP2 to suppress caspase-8 activation Science 281, 1680-3 (1998).
59. Van Antwerp DJ, Martin SJ, Verman IM, Green DR, Inhibition of TNF-induced apoptosis by NF-kappa B, Trends Cell Biol 8, 107-11 (1998).
60. Wang CY, Guttridge DC, Mayo MW, Baldwin AS, NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis, Mol Cell Biol 19, 5923-9 (1999).
61. Chen C, Edelstein LC, Gelinas C, The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L), Mol Cell Biol 20, 2687-95 (2000).
62. Tanaka H, Matsumura I, Ezoe S, Satoh Y, Sakamaki TL, Albanese C, Machii T, Pestell RG, Kanakura Y, E2F1 and c-Myc Potentiate Apoptosis through Inhibition of NF-κB Activity that Facilitates MnSOD-Mediated ROS Elimination, Mol Cell 9, 1017-29 (2002).
63. Vasudevan KM, Gurumurthy S, Rangnekar VM, Suppression of PTEN expression by NF-kappa B prevents apoptosis, Mol Cell Biol 24, 1007-21 (2004).
64. Uzzo RG, Rayman P, Kolenko V, Clark PE, Cathcart MK, Bloom T, Novick AC, Bukowski RM, Hamilton T, Finke J H, Renal cell carcinoma-derived gangliosides suppress nuclear factor-kappaB activation in T cells J Clin Invest 104, 769-76 (1999).
65. Thornton MV, Kudo D, Rayman P, Horton C, Molto L, Cathcart MK, Ng C, Paszkiewicz-Kozik E, Bukowski R, Derweesh I, Tannenbaum CS, Finke JH, Degradation of NF-kappa B in T cells by gangliosides expressed in renal cell carcinomas, J Immunol 172, 3480-90 (2004).
66. Wang XQ, Sun P, Paller AS, Inhibition of integrin-linked kinase/protein kinase B/Akt signaling. Mechanism for ganglioside-induced apoptosis, J Biol Chem 276, 44504-11 (2001).
67. Paris R, Morales A, Coll O, Sánchez-Reyes A, García-Ruiz C, Fernández-Checa JC, Ganglioside GD3 sensitizes human hepatoma cells to cancer therapy, J Biol Chem 277, 49870-6 (2002).
68. Watanabe R, Ohyama R, Aoki H, Takahashi T, Satoh M, Saito S, Hoshi S, Ishii A, Saito M, Arai Y, Ganglioside G(M3) overexpression induces apoptosis and reduces malignant potential in murine bladder cancer, Cancer Res 62, 3850-4 (2002).
69. Peguet-Navarro J, Sportouch M, Popa I, Berthier O, Schmitt D, Portoukalian J, Gangliosides from human melanoma tumors impair dendritic cell differentiation from monocytes and induce their apoptosis, J Immunol 170, 3488-94 (2003).
70. Zhou J, Cox NR, Ewald SJ, Morrison NE, Baker HJ, Evaluation of GM1 ganglioside-mediated apoptosis in feline thymocytes, Vet Immunol Immunopathol 66, 25-42 (1998).
71. Peterson RH, Meyers MB, Spengler BA, Biedler JL, Alteration of plasma membrane glycopeptides and gangliosides of Chinese hamster cells accompanying development of resistance to daunorubicin and vincristine, Cancer Res 43, 222-8 (1983).
72. Lavie Y, Cao H, Bursten SL, Giuliano AE, Cabot MC, Accumulation of glucosylceramides in multidrug-resistant cancer cells, J Biol Chem 271, 19530-6 (1996).
73. Liu YY, Han TY, Giuliano AE, Cabot MC, Expression of glucosylceramide synthase, converting ceramide to glucosylceramide, confers adriamycin resistanse in human breast cancer cells, J Biol. Chem 274, 1140-6 (1999).
74. Lavie Y, Cao H, Volner A, Lucci A, Han TY, Geffen V, Giuliano AE, Cabot MC, Agents that reverse multidrug resistance, tamoxifen, verapamil and cyclosporin A, block glycosphingolipid metabolism by inhibiting ceramide glycosylation in human cancer cells, J Biol Chem 272, 1682-7 (1997).
75. Veldman RJ, Mita A, Cuvillier O, Garcia V, Klappe K, Medin JA, Campbell JD, Carpentier S, Kok JW, Levade T, The absence of functional glucosylceramide synthase does not sensitize melanoma cells for anticancer drugs, FASEB J. 17, 1144-6 (2003).
76. Grazide S, Terrisse AD, Lerouge S, Laurent G, Jaffrezou JP, Cytoprotective effect of glucosylceramide synthase inhibition against daunorubicin induced apoptosis in human leukemic cell lines, J Biol Chem in press.
77. Inokuchi J, Radin NS, Preparation of the active isomer of 1-phenyl-2-decanoylamino-3-morpholino-1-propanol, inhibitor of murine glucocerebroside synthetase, J Lipid Res 28 565-71 (1987).
78. Di Sano F, Fazi B, Citro G, Lovat PE, Cesareni G, Piacentini P, Glucosylceramide synthase and its functional interaction with RTN-1C regulate chemotherapeutic-induced apoptosis in neuroepithelioma cells, Cancer Res 63, 3860-5 (2003).
79. Jan Veldman R, Klappe K, Hinrichs J, Hummel I, van der Schaaf G, Sietsma H, Kok JW, Altered sphingolipid metabolism in multidrug-resistant ovarian cancer cells is due to uncoupling of glycolipid biosynthesis in the Golgi apparatus, FASEB J 16, 1111-3 (2002).
80. Iimuro Y, Gallucci RM, Luster MI, Kono H, Thurman RG, Antibodies to tumor necrosis factor alpha attenuate hepatic necrosis and inflammation caused by chronic exposure to ethanol in the rat, Hepatology 26, 1530-7 (1997).
81. Yin M, Wheeler MD, Kono H, Bradford B, Gallucci RM, Luster MI, Thurman RG, Essential role of tumor necrosis factor in alcoholic-induced liver injury in mice, Gastroenterology 117, 942-52 (1999).
82. Deaciuc IV, Nikolova-Karakashian M, Fortunato F, Lee EY, Hill DB, McClain CJ, Apoptosis and dysregulated ceramide metabolism in a murine model of alcohol-enhanced lipopolysaccharide hepatotoxicity, Alcohol Clin Exp Res 24, 1557-65 (2000).
83. Pastorino JG, Marcineviciute A, Cahill A, Hoek JB, Potentiation by chronic ethanol treatment of the mitochondrial permeability transition, Biochem Biophys Res Commun 265, 405-9 (1999).
84. Memon RA, Holleran WM, Uchida Y, Moser AH, Ichikawa S, Hirabayashi Y, Grunfeld C, Feingold KR, Regulation of glycosphingolipid metabolism in liver during the acute phase response, J Biol Chem 274, 19707-13 (1999).
85. Colell A, García-Ruiz C, Miranda M, Ardite E, Marí M, Morales A, Corrales F, Kaplowitz N, and Fernández-Checa JC, Selective glutathione depletion of mitochondria by ethanol sensitizes hepatocytes to Tumor Necrosis Factor, Gastroenterology 115, 1541-51 (1998).
86. Fernandez-Checa JC, Colell A, Garcia-Ruiz C, S-adenosyl-L-methionine and mitochondrial reduced glutathione depletion in alcoholic liver disease, Alcohol 27, 179-83 (2002).
87. Nakagami M, Wheeler MD, Bradford BU, Uesugi T, Mason RP, Connor HD, Dikalova A, Kadiiska M, Thurman RG, Overexpression of manganese superoxide dismutase prevents alcohol-induced liver injury in the rat, J Biol Chem 276, 36664-72 (2001).
88. Zhao P, Kahorn TF, Slattery JT, Selective mitochondrial glutathione depletion by ethanol enhances acetaminophen toxicity in rat liver, Hepatology 36, 3/26-35 (2002).
89. + T cells for liver injury induced by Salmonella infection in mice, Hepatology 29, 1799-08 (1999).
90. Kakimi K, Guidotti LG, Koezuka Y, Chisari FV, Natural killer T cell activation inhibits hepatitis B virus replication in vivo, J Exp Med 192, 921-30 (2000).
91. Kaneko BY, Harada M, Kawano T, Yamashita M, Shibata Y, Gejyo F, Nakayama T, Augmentation of V isn't in document 14 NKT cell-mediated cytotoxicity by interleukin 4 in an autocrine mechanism resulting in the development of concanavalin A-induced hepatitis, J Exp Med 191, 105-14 (2000).
92. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, Ueno H, CD1d-restricted and TCR-mediated activation of Val4 NKT cells by glycosylceramides, Science 278, 1626-9 (1997).
93. Osman Y, Kawamura T, Naito T, Takeda K, Van-Kaer L, Okumura K, Bendelac A. Activation of hepatic NKT cells and subsequent liver injury following administration of α-galcatosylceramide, Eur J Immunol 163, 1919-28 (2000).
94. Chida Y, Sudo N, Sonoda J, Sogawa H, Kubo C, Electric foot shock stress-induced exacerbation of a-galactosylceramide-triggered apoptosis in mouse liver, Hepatology 39, 1131-40 (2004).
95. Wu DY, Segal NH, Sidobre S, Kronenberg M, Chapman PB, Cross-presentation of disialoganglioside GD3 to natural killer T cells, J Exp Med 198, 173-81 (2003).
96. Friedman SL, Molecular regulation of hepatic fibrosis, an integrated cellular response to liver injury, J Biol Chem 275, 2247-50 (2000).
97. Lee SH, Seo GS, Park PH, Choi JY, Park YN, Kim HK, Chae KS, Sohn DH, Increased expression of O-acetyldisialoganglioside synthase during liver fibrogenesis relates to stellate cell activation, Biochem Biophys Res Commun 303, 954-61 (2003).
98. Tagami S, Inokuchi J, Kabayama K, Yoshimura H, Kitamura F, Uemura S, Ogawa C, Ishii A, Saito M, Ohtsuka Y, Ganglioside GM3 participates in the pathological conditions of insulin resistance, J Biol Chem 277, 3085-92 (2002).
99. Nojiri H, Stroud M, Hakomori S, A specific type of ganglioside as a modulator of insulin-dependent cell growth and insulin receptor tyrosine kinase activity. Possible association of ganglioside-induced inhibition of insulin receptor function and monocytic differentiation induction in HL-60 cells, J Biol Chem 266, 4531-37 (1991).
100. Tsuruoka T, Tsuji T, Nojiri H, Holmes EH, Hakomori S, Selection of a mutant cell line based on differential expression of glycosphingolipid, utilizing anti-lactosylceramide antibody and complement, J Biol Chem 268, 2211-6 (1993).
101. Yamashita T, Hashiramoto A, Haluzik M, Mizukami H, Beck S, Norton A, Kono M, Tsuji S, Daniotti JL, Werth N, Sandhoff R, Sandhoff K, Proia RL, Enhanced insulin sensitivity in mice lacking ganglioside GM3, Proc Natl Acad Sci USA 100, 3445-9 (2003).
102. Brent M, Nonalcoholic steatohepatitis, Sem Liver Dis 24, 3-20 (2004).
103. Zhang X, Kiechle FL, Glycosphingolipids in health and disease, Ann Clin Lab Sci 34, 3-13 (2004).
104. Ellison JA, de Vellis J, Amoeboid microglia expressing GD3 ganglioside are concentrated in regions of oliogdendrogenesis during development of the rat corpus callsum, Glia 14, 123-32 (1995).
105. Kawai K, Mori M, Watari S, Yasuda T, Immunohistochemical demonstration of ganglioside GD3 in the central nervous system, Neurosci Res 19, 119-24 (1994).
106. Molander M, Berthold CH, Persson H, Friedman P, Immunostaining of ganglioside GD1b, GD3 and GM1 in rat cerebellum: Cellular layer and cell type specific interactions, J Neurosci Res 60, 531-42 (2000).
107. Vitry S, Avellana-Adalid V, Hardy R, Lachapelle F, Baron-Van Evercooren A, Mouse oligospheres: From preprogenitors to functional oligodendrocytes, J Neurosci Res 58, 735-51 (1999).
108. Andersson LM, Fredman P, Lekman A, Rosengren L, Gissien M, Increased cerebrospinal fluid ganglioside GD3 concentrations as a marker of microglial activation in HIV type 1 infection, Aids Res Human Retrovir 14, 1065-9 (1998).
109. Miyatani N, Saito M, Ariga T, Yoshino H, Yu RK, Glycosphingolipids in the cerebrospinal fluid of patients with multiple sclerosis, Mol Chem Neuropathol 13, 205-16 (1990).
110. Tarvonen-Schroder S, Biennow K, Lekman A, Friedman P, Raiha I, Sourander L, Gangliosides and sulfatide in cerebrospinal fluid in leukoaraiosis, Dement Geriatr Cogn Disord 8, 174-9 (1997).
111. Yu RK, Ledeen RW, Eng LF, Ganglioside abnormalities in multiple sclerosis, J Neurochem 23, 169-74 (1974).
112. Simon BM, Malisan F, Testi R, Nicotera P, Leist M, Disialoganglioside GD3 is released by microglia and induces oligodendrocyte apoptosis, Cell Death Differ 9, 758-67 (2002).
113. Ladish S, Chang F, Li R, Cogen P, Johnson D, Detection of medulloblastoma and astrocytoma-associated ganglioside GD3 in cerobrospinal fluid, Cancer Lett 120, 71-8 (1997).
114. Hakomori S., Igarashi Y, Gangliosides and glycosphingolipids as modulators of cell growth, adhesion and transmembrane signaling, Adv Lipid Res 25, 147-62 (1993).