β-amyloid-Induced Synthesis of the Ganglioside Gd3 Is a Requisite for Cell Cycle Reactivation and Apoptosis in Neurons

Journal of Neuroscience

Volumn 22, Issue 10, 2002, Pages 3963-3968

  Copani, Agata ^a   Melchiorri, Daniela ^b   Caricasole, Andrea ^b   Martini, Francesca ^b   Sale, Patrizio ^b   Carnevale, Roberto ^b   Gradini, Roberto ^b   Sortino, Maria Angela ^a   Lenti, Luisa ^b   De Maria, Ruggero ^c   Nicoletti, Ferdinando ^b,d  

^a UNIVERSITY OF CATANIA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d IRCCS NEUROMED   (Italy)

Author keywords

Alzheimer's disease; Apoptosis; Cell cycle; Ganglioside GD3; Neurodegeneration; amyloid

Indexed keywords

ALPHA 2,8 SIALYLTRANSFERASE; AMYLOID BETA PROTEIN; ANTISENSE OLIGODEOXYNUCLEOTIDE; CERAMIDE; GANGLIOSIDE GD3; GANGLIOSIDE GM3; SIALIC ACID DERIVATIVE; SPHINGOMYELIN; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR BLOCKING AGENT; AMYLOID BETA PROTEIN (25 35); AMYLOID BETA-PROTEIN (25-35); ANTISENSE OLIGONUCLEOTIDE; BETA D GALACTOSIDE ALPHA 2 6 SIALYLTRANSFERASE; BETA-D-GALACTOSIDE ALPHA 2-6-SIALYLTRANSFERASE; GANGLIOSIDE; GANGLIOSIDE, GD3; MESSENGER RNA; PEPTIDE FRAGMENT; SIALYLTRANSFERASE;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; BRAIN CELL; CELL CYCLE; CELL CYCLE S PHASE; CELL LEVEL; CELL PROTECTION; CHROMATIN; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME INDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RAT; ANIMAL; BIOSYNTHESIS; CELL COUNT; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; CELL COUNT; CELL CYCLE; CELLS, CULTURED; CHROMATIN; EXCITATORY AMINO ACID ANTAGONISTS; GANGLIOSIDES; MICROSCOPY, FLUORESCENCE; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDE FRAGMENTS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; S PHASE; SIALYLTRANSFERASES; SPHINGOMYELINS;

EID: 0037095678     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-10-03963.2002     Document Type: Article

References (51)

1. Ando S, Toyoda Y, Nagai Y, Ikuta F (1984) Alterations in brain gangliosides and other lipids of patients with Creutzfeldt-Jakob disease and subacute sclerosing panencephalitis (SSPE). Jpn J Exp Med 54:229-234.
2. Arendt T, Holzer M, Gartner U, Bruckner MK (1998) Aberrancies in signal transduction and cell cycle related events in Alzheimer's disease. J Neural Transm 54:147-158.
3. Auffray C, Rougeon F (1980) Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem 107:303-314.
4. Behl C (2000) Apoptosis in Alzheimer's disease. J Neurol Transm 107:1325-1344.
5. Bilderback TR, Gazula VR, Dobrowsky R (2001) Phosphoinositide 3-kinase regulates crosstalk between Trk A tyrosine kinase and p75(NTR)-dependent sphingolipid signaling pathways. J Neurochem 76:1540-1551.
6. Birkle S, Gao L, Zeng G, Yu RK (2000) Down regulation of GD3 ganglioside and its O-acetylated derivative by stable transfection with antisense vector against GD3-synthase gene expression in hamster melanoma cells: effects on cellular growth, melanogenesis, and dendricity. J Neurochem 75:547-554.
7. Brann AB, Scott R, Neuberger Y, Abulafia D, Boldin S, Fainzilber M, Futerman AH (1999) Ceramide signaling downstream of the p75 neurotrophin receptor mediates the effects of nerve growth factor on outgrowth of cultured hippocampal neurons. J Neurosci 19:8199-8206.
8. Busser J, Geldmacher DS, Herrup K (1998) Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J Neurosci 18:2801-2807.
9. Colell A, Garcia-Ruiz C, Roman J, Ballesta A, Fernandez-Checa JC (2001) Ganglioside GD3 enhances apoptosis by suppressing the nuclear factor-κ B-dependent survival pathway. FASEB J 15:1068-1070.
10. Copani A, Condorelli F, Caruso A, Vancheri C, Sala A, Giuffrida Stella AM, Canonico PL, Nicoletti F, Sortino MA (1999) Mitotic signaling by β-amyloid causes neuronal death. FASEB J 13:2225-2234.
11. Copani A, Uberti D, Sortino MA, Bruno V, Nicoletti F, Memo M (2001) Activation of cell-cycle-associated proteins in neuronal death: a mandatory or dispensable path? Trends Neurosci 24:25-31.
12. De Maria R, Lenti L, Malisan F, d'Agostino F, Tomassini B, Zeuner A, Rippo MR, Testi R (1997) Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science 277:1652-1655.
13. De Maria R, Rippo MR, Schuchman EH, Testi R (1998) Acidic sphingomyelinase (ASM) is necessary for fas-induced GD3 ganglioside accumulation and efficient apoptosis in lymphoid cells. J Exp Med 187:897-902.
14. Dotta F, Previti M, Neerman-Arbez M, Dionisi S, Cucinotta D, Lenti L, Di Mario U, Halban PA (1998) The GM2-1 ganglioside islet autoantigen in insulin-dependent diabetes mellitus is expressed in secretory granules and is not beta-cell specific. Endocrinology 139:316-319.
15. Favaron M, Manev H, Alho H, Bertolino M, Ferret B, Guidotti A, Costa E (1988) Gangliosides prevent glutamate and kainate neurotoxicity in primary neuronal cultures of neonatal rat cerebellum and cortex. Proc Natl Acad Sci USA 85:7351-7355.
16. Forloni G, Chiesa R, Smiroldo S, Verga L, Salmona M, Tagliavini F, Angeretti N (1993) Apoptosis mediated neurotoxicity induced by chronic application of β-amyloid 25-35. NeuroReport 4:523-526.
17. Fukumoto S, Mutoh T, Hasegawa T, Miyazaki H, Okada M, Goto J, Furukawa K, Urano T (2000) GD3 synthase gene expression in PC12 cells results in the continuous activation of TrkA and ERK1/2 and enhanced proliferation. J Biol Chem 275:5832-5838.
18. Giovanni A, Wirtz-Brugger F, Keramaris E, Slack R, Park DS (1999) Involvement of cell cycle elements, cyclin-dependent kinases, pRb, and E2F X DP, in β-amyloid-induced neuronal death. J Biol Chem 274:19011-19016.
19. Giovanni A, Keramaris E, Morris EJ, Hou ST, O'Hare M, Dyson N, Robertson GS, Slack RS, Park DS (2000) E2F1 mediates death of β-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase 3. J Biol Chem 275:11553-11560.
20. Goldman JE, Reynolds R (1996) A reappraisal of ganglioside GD3 expression in the CNS. Glia 16:291-295.
21. Herrup K, Busser JC (1995) The induction of multiple cell cycle events precedes target-related neuronal death. Development 121:2385-2395.
22. Joseph J, Shukitt-Hale B, Denisova NA, Martin A, Perry G, Smith MA (2001) Copernicus revisited: amyloid beta in Alzheimer's disease. Neurobiol Aging 22:131-146.
23. Kalanj S, Kracun I, Rosner H, Cosovic C (1991) Regional distribution of brain gangliosides in Alzheimer's disease. Neurol Croat 40:269-281.
24. Kawai H, Sango K, Mullin KA, Proia RL (1998) Embryonic stem cells with a disrupted GD3 synthase gene undergo neuronal differentiation in the absence of b-series gangliosides. J Biol Chem 273:19634-19638.
25. Kozireski-Chuback D, Wu G, Ledeen RM (1999) Axogenesis in neuro-2a cells correlates with GM1 upregulation in the nuclear and plasma membranes, J Neurosci Res 57:541-550.
26. Kristal BS, Brown AM (1999) Apoptogenic GD3 directly induces the mitochondrial permeability transition. J Biol Chem 274:23169-23175.
27. Loo DT, Copani A, Pike CJ, Whittemore ER, Walencewicz AJ, Cotman CW (1993) Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc Natl Acad Sci USA 90:7951-7955.
28. Malisan F, Testi R (1999) Lipid signaling in CD95-mediated apoptosis. FEBS Lett 452:100-103.
29. Manev H, Favaron M, Vicini S, Guidotti A, Costa E (1990) Glutamate-induced neuronal death in primary cultures of cerebellar granule cells: protection by synthetic derivatives of endogenous sphingolipids. J Pharmacol Exp Ther 252:419-427.
30. Mattson MP (2000) Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1:120-129.
31. McShea A, Wahl AF, Smith MA (1999) Re-entry into the cell cycle: a mechanism for neurodegeneration in Alzheimer disease. Med Hypotheses 52:525-527.
32. Nagy Z, Esiri MM, Smith AD (1998) The cell division cycle and the pathophysiology of Alzheimer's disease. Neuroscience 87:731-739.
33. Ohsawa T, Ikeda H, Senshu T (1988) Effects of ganglioside GM1 on DNA synthesis in isolated nuclei and on the activity of DNA polymerase alpha derived from S-phase HeLa cells. Biochim Biophys Acta 949:305-310.
34. Percy AK, Gottfries J, Vilbergsson G, Mansson JE, Svennerholm L (1991) Glycosphingolipid glycosyltransferases in human fetal brain. J Neurochem 56:1461-1465.
35. Rippo MR, Malisan F, Ravagnan L, Tomassini B, Condo I, Costantini P, Susin SA, Rufini A, Todaro M, Kroemer G, Testi R (2000) GD3 ganglioside directly targets mitochondria in a bcl-2-controlled fashion. FASEB J 14:2047-2054.
36. Roelen BA, Lin HY, Knezevic V, Freund E, Mummery CL (1994) Expression of TGF-βs and their receptors during implantation and organogenesis of the mouse embryo. Dev Biol 166:716-728.
37. Roth KA (2001) Caspases, apoptosis, and Alzheimer disease: causation, correlation and confusion. J Neuropathol Exp Neurol 60:829-838.
38. Ryu BR, Choi DW, Hartley DM, Costa E, Jou I, Gwag BJ (1999) Attenuation of cortical neuronal apoptosis by gangliosides. J Pharmacol Exp Ther 290:811-816.
39. Saito M, Guidotti A, Berg MJ, Marks N (1998) The semisynthetic ganglioside LIGA20 potently protects neurons against apoptosis. Ann NY Acad Sci 845:253-262.
40. Saito M, Berg MJ, Guidotti A, Marks N (1999) Gangliosides attenuate ethanol-induced apoptosis in rat cerebellar granule neurons. Neurochem Res 24:1107-1115.
41. 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 274:22582-22585.
42. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81:741-766.
43. Small DH, Mok SS, Bornstein JC (2001) Alzheimer's disease and Abeta toxicity: from top to bottom. Nat Rev Neurosci 2:595-598.
44. Sottocornola E, Colombo I, Vergani V, Taraboletti G, Berra B (1998) Increased tumorigenicity and invasiveness of C6 rat glioma cells transfected with the human α-2,8 sialyltransferase cDNA. Invasion Metastasis 18:142-154.
45. Svennerholm L, Fredman P (1980) A procedure for the quantitative isolation of brain gangliosides. Biochim Biophys Acta 617:97-109.
46. Svennerholm L, Rynmark BM, Vilbergsson G, Fredman P, Gottfries J, Mansson JE, Percy A (1991) Gangliosides in human fetal brain. J Neurochem 56:1763-1768.
47. Vincent I, Rosado M, Davies P (1996) Mitotic mechanisms in Alzheimer's disease? J Cell Biol 132:413-425.
48. Wu G, Lu ZH, Ledeen RW (1995) GM1 ganglioside in the nuclear membrane modulates nuclear calcium homeostasis during neurite outgrowth. J Neurochem 65:1419-1422.
49. Wu G, Lu ZH, Xie X, Ledeen R (2001) Comparison of ganglioside profiles in nuclei and whole cells of NG-108 and NG-CR72 lines: changes in response to different neuritogenic stimuli. Brain Res Dev Brain Res 126:183-190.
50. Yaar M, Zhai S, Pilch PF, Doyle SM, Eisenhauer PB, Fine RE, Gilchrest BA (1997) Binding of β-amyloid to the p75 neurotrophin receptor induces apoptosis: a possible substrate for Alzheimer's disease. J Clin Invest 100:2333-2340.
51. Yang Y, Geldmacher DS, Herrup K (2001) DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci 21:2661-2668.