Elevation of GM2 ganglioside during ethanol-induced apoptotic neurodegeneration in the developing mouse brain

Journal of Neurochemistry

Volumn 121, Issue 4, 2012, Pages 649-661

  Saito, Mitsuo ^a,c   Chakraborty, Goutam ^a   Shah, Relish ^a   Mao, Rui Fen ^a   Kumar, Asok ^a,c   Yang, Dun Sheng ^a,c   Dobrenis, Kostantin ^b   Saito, Mariko ^a,c  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Activated microglia; Apoptotic neurodegeneration; Ethanol; GM2 ganglioside; Lysosome; Mitochondria

Indexed keywords

ALCOHOL; CASPASE 3; CYTOCHROME C; CYTOCHROME C OXIDASE; GANGLIOSIDE GD3; GANGLIOSIDE GM2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; CELL ACTIVATION; CELL FRACTIONATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; ENZYME RELEASE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYSOSOME; MICROGLIA; MITOCHONDRION; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SYNAPSE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BRAIN; BRAIN CHEMISTRY; CASPASE 3; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CYTOCHROMES C; ENDOSOMES; ENZYME ACTIVATION; ETHANOL; G(M2) GANGLIOSIDE; IMMUNOHISTOCHEMISTRY; LYSOSOMES; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; MITOCHONDRIA; NERVE DEGENERATION; SUBCELLULAR FRACTIONS;

MUS;

EID: 84862826947     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07710.x     Document Type: Article

References (59)

1. Ariga T. and Yu R. K. (2000) Ganglioside analysis by high-performance thin layer chromatography. Methods Enzymol. 312, 115-134.
2. Berrettini M., Fedeli D., Falcioni G., Bevilacqua C., Massi M. and Polidori C. (2004) Hippocampal and striated skeletal muscle changes in fatty acid composition induced by ethanol in alcohol-preferring rats. Toxicology 199, 161-168. (Pubitemid 38624527)
3. Birbes H., El Bawab S., Obeid L. M. and Hannun Y. A. (2002) Mitochondria and ceramide: intertwined roles in regulation of apoptosis. Adv. Enzyme Regul. 42, 113-129. (Pubitemid 35033533)
4. Biswas S., Biswas K., Richmond A. et al. (2009) Elevated levels of select gangliosides in T cells from renal cell carcinoma patients is associated with T cell dysfunction. J. Immunol. 183, 5050-5058.
5. Carloni S., Mazzoni E. and Balduini W. (2004) Caspase-3 and calpain activities after acute and repeated ethanol administration during the rat brain growth spurt. J. Neurochem. 89, 197-203. (Pubitemid 38420689)
6. Constantopoulos G., Eiben R. M. and Schafer I. A. (1978) Neurochemistry of the mucopolysaccharidoses: brain glycosaminoglycans, lipids and lysosomal enzymes in mucopolysaccharidosis type III B (alpha-N-acetylglucosaminidase deficiency). J. Neurochem. 31, 1215-1222. (Pubitemid 9039040)
7. Duffy O., Menez J. F., Floch H. H. and Leonard B. E. (1991) Changes in whole brain membranes of rats following pre- and post-natal exposure to ethanol. Alcohol Alcohol. 26, 605-613.
8. Farber N. B., Creeley C. E. and Olney J. W. (2010) Alcohol-induced neuroapoptosis in the fetal macaque brain. Neurobiol. Dis. 40, 200-206.
9. Garcia-Ruiz C., Colell A., Morales A., Calvo M., Enrich C. and Fernández-Checa J. C. (2002) Trafficking of ganglioside GD3 to mitochondria by tumor necrosis factor-alpha. J. Biol. Chem. 277, 36443-36448.
10. Garige M., Azuine M. A. and Lakshman M. R. (2006) Chronic ethanol consumption down-regulates CMP-NeuAc:GM3 alpha 2,8-sialyltransferase (ST8Sia-1) gene in the rat brain. Neurochem. Int. 49, 312-318. (Pubitemid 43975196)
11. Guerri C., Bazinet A. and Riley E. P. (2009) Fetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol. 44, 108-114.
12. Hakomori S. (2003) Structure, organization, and function of glycosphingolipids in membrane. Curr. Opin. Hematol. 10, 16-24.
13. Han J. Y., Jeong J. Y., Lee Y. K., Roh G. S., Kim H. J., Kang S. S., Cho G. J. and Choi W. S. (2006) Suppression of survival kinases and activation of JNK mediate ethanol-induced cell death in the developing rat brain. Neurosci. Lett. 398, 113-117.
14. Hara A., Kitazawa N. and Taketomi T. (1984) Abnormalities of glycosphingolipids in mucopolysaccharidosis type III B. J. Lipid Res. 25, 175-184. (Pubitemid 14150097)
15. Huang J. Q., Trasler J. M., Igdoura S., Michaud J., Hanal N. and Gravel R. A. (1997) Apoptotic cell death in mouse models of GM2 gangliosidosis and observations on human Tay-Sachs and Sandhoff diseases. Hum. Mol. Gent. 6, 1879-1885. (Pubitemid 27460363)
16. Ieraci A. and Herrera D. G. (2006) Nicotinamide protects against ethanol-induced apoptotic neurodegeneration in the developing mouse brain. PLoS Med. 3, e101.
17. Ikonomidou C., Bittigau P., Ishimaru M. J. et al. (2000) Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 287, 1056-1060. (Pubitemid 30094364)
18. Inoki Y., Miura T., Kajimoto T. et al. (2000) Ganglioside GD3 and its mimetics induce cytochrome c release from mitochondria. Biochem. Biophys. Res. Commun. 276, 1210-1216.
19. Jennermann R. and Wiegandt H. (1994) A rapid method for the preparation of ganglioside Glac2 (GD3). Lipids 29, 365-368.
20. Jeyakumar M., Butters T. D., Cortina-Borja M., Hunnam V., Prola R. L., Perry V. H., Dwek R. A. and Platt F. M. (1999) Delayed symptom onset and increased life expectancy in Sandhoff disease mice treated with N-butyldeoxynojirimycin. Proc. Natl Acad. Sci. USA 96, 6388-6393. (Pubitemid 29256675)
21. Kadowaki T., Nakadate K., Sakakibara S., Hirata K. and Ueda S. (2007) Expression of Iba1 protein in microglial cells of zitter mutant rat. Neurosci. Lett. 411, 26-31. (Pubitemid 44751933)
22. Keelan J., Bates T. E. and Clark J. B. (1996) Intrasynaptosomal free calcium concentration during rat brain development: effects of hypoxia, aglycaemia, and ischaemia. J. Neurochem. 66, 2460-2467. (Pubitemid 26159082)
23. Kiebish M. A., Han X., Cheng H., Lunceford A., Clarke C. F., Moon H., Chuang J. H. and Seyfried T. N. (2008) Lipidomic analysis and electron transport chain activities in C57BL/6J mouse brain mitochondria. J. Neurochem. 106, 299-312. (Pubitemid 351840212)
24. Ledeen R. W. and Wu G. (2002) Ganglioside function in calcium homeostasis and signaling. Neurochem. Res. 27, 637-647.
25. Ledeen R. W. and Yu R. K. (1982) Gangliosides: structure, isolation, and analysis, in Methods in Enzymology (Ginsburg V., ed.), Vol. 83, pp. 139-191. Academic Press, New York.
26. Lloyd-Evans E. and Platt F. M. (2010) Lipids on trial: the search for the offending metabolite in Niemann-Pick type C disease. Traffic 11, 419-428.
27. Malorni W., Giammarioli A. M., Garofalo T. and Sorice M. (2007) Dynamics of lipid raft components during lymphocyte apoptosis: the paradigmatic role of GD3. Apoptosis 12, 941-949. (Pubitemid 46653301)
28. Marks D. and Pagano R. E. (2002) Endocytosis and sorting of glycosphingolipids in sphingolipid storage disease. Trends Cell Biol. 12, 605-613. (Pubitemid 35461860)
29. -/- knockout mouse model of mucolipidosis type IV. J. Neuropathol. Exp. Neurol. 68, 125-135.
30. Molotkovskaya I. M., Kholodenko R. V., Zelenova N. A., Sapozhnikov A. M., Mikhalev I. I. and Molotkovsky J. G. (2000) Gangliosides induce cell apoptosis in the cytotoxic line CTLL-2, but not in the promyelocyte leukemia cell line HL-60. Membr. Cell Biol. 13, 811-822. (Pubitemid 30495267)
31. Natoli E. J., Livingston P. O., Pukel C. S., Lloyd K. O., Wiegandt H., Szalay J., Oettgen H. F. and Old L. J. (1986) A murine monoclonal antibody detecting N-acetyl- and N-glycolyl-GM2: Characterization of cell surface reactivity. Cancer Res. 46, 4116-4120. (Pubitemid 16075916)
32. 2+loading capacity and promotes apoptosis. J. Biol. Chem. 286, 4644-4658.
33. Olney J. W., Tenkova T., Dikranian K., Qin Y. Q., Labruyere J. and Ikonomidou C. (2002) Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Brain Res. Dev. Brain Res. 133, 115-126. (Pubitemid 34211997)
34. Piccinini M., Scandroglio F., Prioni S. et al. (2010) Deregulated sphingolipid metabolism and membrane organization in neurodegenerative disorders. Mol. Neurobiol. 41, 314-340.
35. Rajapakse N., Shimizu K., Payne M. and Busija D. (2001) Isolation and characterization of intact mitochondria from neonatal rat brain. Brain Res. Brain Res. Protoc. 8, 176-183. (Pubitemid 33152942)
36. Ravasi D., Ferraretto A., Omodeo-salè M. F., Tettamanti G., Pitto M. and Masserini M. (2002) Ethanol-induced increase of sphingosine recycling for ganglioside biosynthesis: a study performed on cerebellar granule cells in culture. J. Neurosci. Res. 69, 80-85. (Pubitemid 34734167)
37. Rippo M. R., Malisan F., Ravagnan L. et al. (2000) GD3 ganglioside directly targets mitochondria in a bcl-2-controlled fashion. FASEB J. 14, 2047-2054.
38. Saito M., Saito M., Berg M., Guidotti A. and Marks N. (1999) Gangliosides attenuate ethanol-induced apoptosis in rat cerebellar granule neurons. Neurochem. Res. 24, 1109-1117.
39. Saito M., Saito M., Cooper T. B. and Vadasz C. (2005) Ethanol-induced changes in the content of triglycerides, ceramides, and glucosylceramides in cultured neurons. Alcohol. Clin. Exp. Res. 29, 1374-1383. (Pubitemid 41243361)
40. Saito M., Chakraborty G., Mao R. F., Wang R., Cooper T. B., Vadasz C. and Saito M. (2007a) Ethanol alters lipid profiles and phosphorylation status of AMP-activated protein kinase in the neonatal mouse brain. J. Neurochem. 103, 1208-1218. (Pubitemid 47568737)
41. Saito M., Mao R. F., Wang R., Vadasz C. and Saito M. (2007b) Effects of gangliosides on ethanol-induced neurodegeneration in the developing mouse brain. Alcohol. Clin. Exp. Res. 31, 665-674. (Pubitemid 46434903)
42. Saito M., Chakraborty G., Hegde M., Ohsie J., Paik S. M., Vadasz C. and Saito M. (2010a) Involvement of ceramide in ethanol-induced apoptotic neurodegeneration in the neonatal mouse brain. J. Neurochem. 115, 168-177.
43. Saito M., Chakraborty G., Mao R. F., Paik S. M., Vadasz C. and Saito M. (2010b) Tau phosphorylation and cleavage in ethanol-induced neurodegeneration in the developing mouse brain. Neurochem. Res. 35, 651-659.
44. Sano R., Annunziata I., Patterson A., Moshiach S., Gomero E., Opferman J., Forte M. and d'Azzo A. (2009) GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca2 + -dependent mitochondrial apoptosis. Cell 36, 500-511.
45. Schönfeld P. and Reiser G. (2007) Ca2 + storage capacity of rat brain mitochondria declines during the postnatal development without change in ROS production capacity. Antioxid. Redox Signal. 9, 191-199. (Pubitemid 46105418)
46. Scorrano L., Petronilli V., Di Lisa F. and Bernardi P. (1999) Commitment to apoptosis by GD3 ganglioside depends on opening of the mitochondrial permeability transition pore. J. Biol. Chem. 274, 22581-22585.
47. Sokolowski J. D. and Mandell J. W. (2011) Phagocytic clearance in neurodegeneration. Am. J. Pathol. 178, 1416-1428.
48. Stolzing A. and Grune T. (2004) Neuronal apoptotic bodies: phagocytosis and degradation by primary microglial cells. FASEB J. 18, 743-745.
49. Stromme P., Dobrenis K., Sillitoe R. V. et al. (2011) X-linked Angelman- like syndrome caused by Slc9a6 knockout in mice exhibits evidence of endosomal-lysosomal dysfunction. Brain 134, 3369-3383.
50. Tancini B., Magini A., Latterini L., Urbanelli L., Ciccarone V., Elisei F. and Emiliani C. (2009) Occurrence of an anomalous endocytic compartment in fibroblasts from Sandhoff disease patients. Mol. Cell. Biochem. 335, 273-282.
51. Tomás M., Durán J. M., Lázaro-Diéguez F., Babià T., Renau-Piqueras J. and Egea G. (2004) Fluorescent analogues of plasma membrane sphingolipids are sorted to different intracellular compartments in astrocytes; Harmful effects of chronic ethanol exposure on sphingolipid trafficking and metabolism. FEBS Lett. 563, 59-65.
52. Vitner E. B., Platt F. M. and Futerman A. H. (2010) Common and uncommon pathogenic cascades in lysosomal storage diseases. J. Biol. Chem. 285, 20423-20427.
53. Walkley S. U. (2003) Neurobiology and cellular pathogenesis of glycolipid storage diseases. Philos. Trans. R. Soc. Lond. B 358, 893-904.
54. Wilson D. A., Peterson J., Basavaraj B. S. and Saito M. (2011) Local and regional network function in behaviorally relevant cortical circuits of adult mice following postnatal alcohol exposure. Alcohol. Clin. Exp. Res. 35, 1974-1984.
55. Wozniak D. F., Hartman R. E., Boyle M. P., Vogt S. K., Brooks A. R., Tenkova T., Young C., Olney J. W. and Muglia L. J. (2004) Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol. Dis. 17, 403-414. (Pubitemid 39574874)
56. Young C., Klocke B. J., Tenkova T., Choi J., Labruyere J., Qin Y. Q., Holtzman D. M., Roth K. A. and Olney J. W. (2003) Ethanol-induced neuronal apoptosis in vivo requires BAX in the developing mouse brain. Cell Death Differ. 10, 1148-1155. (Pubitemid 37258580)
57. Yu W. H., Cuervo A. M., Kumar A. et al. (2005) Macroautophagy - a novel Beta-amyloid peptide generating pathway activated in Alzheimer's disease. J. Cell Biol. 171, 87-98. (Pubitemid 41434604)
58. Zervas M. and Walkley S. U. (1999) Ferret pyramidal cell dendritogenesis: changes in morphology and ganglioside expression during cortical development. J. Comp. Neurol. 413, 420-48.
59. Zervas M., Somers K. L., Thrall M. A. and Walkley S. U. (2001) Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 11, 1283-1287. (Pubitemid 32774086)