Promotion of neuronal survival by GM1 ganglioside - Phenomenology and mechanism of action

Annals of the New York Academy of Sciences

Volumn 845, Issue , 1998, Pages 263-273

  Ferrari, Giovanna ^a   Greene, Lloyd A ^b  

^a Fidia Advanced Biopolymers   (Italy)

^b College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GANGLIOSIDE GM1; NEUROPROTECTIVE AGENT; NEUROTROPHIC FACTOR; PROTEIN TYROSINE KINASE;

CELL SURVIVAL; CONFERENCE PAPER; DIMERIZATION; NERVE CELL; NEUROPROTECTION;

EID: 0031880893     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.1998.tb09679.x     Document Type: Article

References (82)

1. OPPENHEIM, R. W. 1991. Cell death during development of the nervous system. Annu. Rev. Neurosci. 14: 453-501.
2. RAFF, M. C., B. A. BARRES, J. F. BURNE, H. S. COLES, Y. ISHIZAKI & M. D. JACOBSON. 1993. Programmed cell death and the control of cell survival: Lessons from the nervous system. Science 262: 695-700.
3. CHOI, D. W. 1996. Ischemia-induced neuronal apoptosis. Curr. Opin. Neurobiol. 6: 667-672.
4. CROWE, M. J., J. C. BRESNAHAN, S. L. SHUMAN, J. N. MASTERS & M. S. BEATTIE. 1997. Nat. Med. 3: 73-76.
5. THOMPSON, C. B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267: 1456-1462.
6. HAKOMORI, S. 1981. Glycosphingolipids in cellular interaction, differentiation and oncogenesis. Annu. Rev. Biochem. 50: 733-764.
7. WIEGANDT, H. 1982. The gangliosides. Adv. Neurochem. 4: 149-223.
8. LEDEEN, R. W. 1985. Gangliosides of the neuron. Trends Neurosci. 8: 169-174.
9. GORIO, A. 1986. Ganglioside enhancement of neuronal differentiation, plasticity and repair. CRC Crit. Rev. Clin. Neurobiol. 2: 241-296.
10. SKAPER, S. D., A. LEON & G. TOFFANO. 1989. Ganglioside function in the development and repair of the nervous system. Mol. Neurobiol. 3: 173-199.
11. KARPIAK, S. E., S. P. MAHADIK & C. G. WAKADE. 1990. Ganglioside reduction of ischemic injury. CRC. Crit. Rev. Neurobiol. 5: 221-237.
12. MANEV, H., M. FAVARON, S. VICINI & A. GUIDOTTI. 1990. Ganglioside-mediated protection from glutamate-induced neuronal death. Acta Neurobiol. Exp. 50: 475-488.
13. CUELLO, A. C. 1990. Gangliosphingolipids that can regulate nerve growth and repair. Adv. Pharmacol. 21: 1-50.
14. SCHENGRUND, C. L. 1990. The role(s) of gangliosides in neuronal differentiation and repair: A perspective. Brain Res. Bull. 24: 131-141.
15. LEDEEN, R. W., G. WU, M. S. CANNELLA, B. ODERFELD-NOWAK & A. C. CUELLO. 1990. Gangliosides as neurotrophic agents: Studies on the mechanism of action. Acta Neurobiol. Exp. 50: 439-449.
16. CAROLEI, A., C. FIESCHI, R. BRUNO & G. TOFFANO. 1991. Monosialoganglioside GM1 in cerebral ischemia. Cerebrovasc. Brain Met. Rev. 3: 134-157.
17. SKAPER, S. D. & A. LEON. 1992. Monosialogangliosides, neuroprotection, and neuronal repair processes. J. Neurotrauma 9: S507-S516.
18. SCHNEIDER, J. S., A. POPE, K. SIMPSON, J. TAGGART, M. G. SMITH & L. DISTEFANO. 1992. Recovery from experimental Parkinsonism in primates with GM1 ganglioside treatment. Science 256: 843-846.
19. TETTAMANTI, G. & L. RIBONI. 1993. Gangliosides and modulation of the neural cells. Adv. Lip. Res. 25: 235-267.
20. SIMON, R. P., J. CHEN & S. H. GRAHAM. 1993. GM1 ganglioside treatment of focal ischemia: A dose-response and microdialysis study. J. Pharmacol. Exp. Ther. 265: 24-29.
21. LAZZARO, A., S. SEREN, T. KOGA, R. ZANONI, N. SCHIAVO & H. MANEV. 1994. GM1 reduces infarct volume after focal cerebral ischemia. Exp. Neurol. 125: 278-285.
22. THE SASS INVESTIGATORS. 1994. Ganglioside GM1 in acute ischemic stroke. SASS Trial Stroke 25: 1141-1148.
23. LENZI, G. L., F. GRIGOLETTO, M. GENT, R. S. ROBERTS, M. D. WALKER, J. D. EASTON, A. CAROLEI, F. C. DORSEY, W. A. ROCCA, R. BRUNO, F. PATERNELLO & C. FIESCHI FOR THE EARLY STROKE TRIAL GROUP. 1994. Early treatment of stroke with monosialoganglioside GM1: Efficacy and safety results of the Early Stroke Trial. Stroke 25: 1552-1558.
24. GEISLER, F. H., F. C. DORSEY & W. P. COLEMAN. 1991. Recovery of motor function after spinal-cord injury. A randomized, placebo-controlled trial with GM1-ganglioside. N. Engl. J. Med. 324: 1829-1832.
25. GEISLER, F. H., F. C. DORSEY & W. P. COLEMAN. 1993. Past and current clinical studies with GM-1 ganglioside in acute spinal cord injury. Ann. Emerg. Med. 22: 1041-1047.
26. SCHNEIDER, J. S. 1994. The therapeutic role of gangliosides in neurological disorders. CNS Drugs 3: 213-222.
27. SCHNEIDER, J. S., D. P. ROELTGEN, D. S. ROTHBLAT, J. CHAPAS-CRILLY, L. SERAYDARIAN & J. RAO. 1995. GM1 ganglioside treatment of Parkinson's disease: An open pilot study of safety and efficacy. Neurology 45: 1149-1154.
28. FERRARI, G. & L. A. GREENE. 1996. Prevention of neuronal apoptotic death by neurotrophic agents and ganglioside GM1: Insights and speculations regarding a common mechanism. Perspec. Dev. Neurobio. 3: 91-98.
29. ROISEN, F. J., H. BARTFELD, R. NAGELE & G. YORK. 1981. Ganglioside stimulation of axonal sprouting in vitro. Science 214: 577-578.
30. FACCI, L., A. LEON, G. TOFFANO, S. SONNINO, R. GHIDONI & G. TETTAMANTI. 1984. Promotion of neuritogenesis in mouse neuroblastoma cells by exogenous gangliosides. Relationship between the effect and the cell association of ganelioside GM1. J. Neurochem. 42: 299-305.
31. LEDEEN, R. W., G. WU, M. S. CANNELLA, B. ODERFELD-NOWAK & A. C. CUELLO. 1990. Gangliosides as neurotrophic agents: Studies on the mechanism of action. Acta Neurobiol. Exp. 50: 439-449.
32. WU, G. & R. W. LEDEEN. 1991. Stimulation of neurite outgrowth in neuroblastoma cells by neuraminidase: Putative role of GM1 ganglioside in differentiation. J. Neurochem. 56: 95-104.
33. FERRARI, G., M. FABRIS & A. GORIO. 1983. Gangliosides enhance neurite outgrowth in PC12 cells. Devel. Brain Res. 8: 215-221.
34. SKAPER, S. D., R. KATOH-SEMBA & S. VARON. 1985. GM1 ganglioside accelerates neurite outgrowth from primary peripheral and central neurons under selected culture conditions. Dev. Brain Res. 23: 19-26.
35. DOHERTY, P., J. G. DICKSON, T. P. FLANIGAN & F. S. WALSH. 1985. Ganglioside GM1 does not initiate, but enhances neurite regeneration of nerve growth factor-dependent sensory neurons. J. Neurochem. 44: 1259-1265.
36. SPOERRI, P. E. & F. J. ROISEN. 1988. Ganglioside potentiation of NGF-independent trophic agents on sensory ganglia. Neurosci. Lett. 90: 21-26.
37. CUELLO, A. C., L. GAROFALO, R. L. KENIGSBERG & R. MAYSINGER. 1989. Gangliosides potentiate in vivo and in vitro effects of nerve growth factor on central cholinergic neurons. Proc. Natl. Acad. Sci. USA 86: 2056-2060.
38. SKAPER, S. D., A. LEON & L. FACCI. 1993. Basic fibroblast growth factor modulates sensitivity of cultured hippocampal pyramidal neurons to glutamate cytotoxicity: Interaction with ganglioside GM1. Dev. Brain Res. 71: 1-8.
39. SKAPER, S. D., A. NEGRO, L. FACCI & R. DAL TOSO. 1993. Brain-derived neurotrophic factor selectively rescues mesencephalic dopaminergic neurons from 2, 4, 5-trihydroxyphenylalanine-induced injury. J. Neurosci. Res. 34:478-487.
40. SCHWARTZ, M. & N. SPIRMAN. 1982. Sprouting from chicken embryo dorsal root ganglia induced by nerve growth factor is specifically inhibited by affinity-purified antiganglioside antibodies. Proc. Natl. Acad. Sci. USA 79: 6080-6083.
41. SPOERRI, P. E., M. M. RAPPORT, S. P. MAHADIK & F. J. ROISEN. 1988. Inhibition of conditioned media-mediated neuritogenesis of sensory ganglia by monoclonal antibodies to GM1 ganglioside. Dev. Brain Res. 41: 71-77.
42. LEON, A., R. DAL TOSO, D. PRESTI, D. BENVEGNU, L. FACCI, G. KIRSCHNER, G. TETTAMANTI & G. TOFFANO. 1988. Development and survival of neurons in dissociated fetal mesencephalic serum-free cell cultures: II. Modulatory effects of gangliosides. J. Neurosci. 8: 746-753.
43. FERRARI, G., A. BATISTATOU & L. A. GREENE. 1993. Gangliosides rescue neuronal cells from death after trophic factor deprivation. J. Neurosci. 13: 1879-1887.
44. DALIA, A., N. H. NEFF & M. HADJICONSTANTINOU. 1993. GM1 ganglioside improves dopaminergic markers of rat mesencephalic cultures treated with MPP+. J. Neurosci. 13: 3104-3111.
45. FERRARI G., M.-C. MINOZZI, G. TOFFANO, A. LEON & S. D. SKAPER. 1989. Basic fibroblast growth factor promotes the survival and development of mesencephalic neurons in culture. Dev. Biol. 133: 140-147.
46. FERRARI, G., G. TOFFANO & S. D. SKAPER. 1991. Epidermal growth factor exerts neuronotrophic effects on dopaminergic and gabaergic CNS neurons: Comparison with basic fibroblast growth factor. J. Neurosci. Res. 30: 493-497.
47. HYMAN, C., M. HOFER, Y. A. BARDE, M. JUHASZ, G. D. YANCOPOULOS, S. P. SQUINTO & R. M. LINDSAY. 1991. BDNF is a neurotrophic factor for dopaminergic neurons of substantia nigra. Nature 350: 230-232.
48. LIN, L.-F. H., D. H. DOHERTY, J. D. LILE, S. BEKTESH & F. COLLINS. 1993. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260: 1130-1132.
49. DI PATRE, P. L., F. CASAMENTI, A. CENNI & G. PEPEU. 1989. Interaction between nerve growth factor and GM1 monosoaloganglioside in preventing cortical choline acetyltransferase and high affinity choline uptake decrease after lesion of the nucleus basalis. Brain Res. 480: 219-224.
50. GAROFALO, L., A. RIBEIRO-DA-SILVA & A. C. CUELLO. 1993. Potentiation of nerve growth factor-induced alterations in cholinergic fibre length and presynaptic terminal size in cortex of lesioned rats by the monosialoganglioside GM1. Neuroscience 57: 21-40.
51. GAROFALO, L. & A. C. CUELLO. 1994. Nerve growth factor and the monosialoganglioside GM1: Analogous and different in vivo effects on biochemical, morphological, and behavioral parameters of adult cortically lesioned rats. Exp. Neurol. 125: 195-217.
52. VANTINI, G., M. FUSCO, E. BIGON & A. LEON. 1988. GM1 ganglioside potentiates the effect of nerve growth factor in preventing vinblastine-induced sympathectomy in newborn rats. Brain Res. 448: 252-258.
53. HADJICONSTANTINOU, M. & N. H. NEFF. 1988. Treatment with GM1 ganglioside restores striatal dopamine in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated mouse. J. Neurochem. 51: 1190-1196.
54. HADJICONSTANTINOU, M. & N. H. NEFF. 1990. Differential recovery of dopamine synthetic enzymes following MPTP and the consequences of GM1 ganglioside treatment. Eur. J. Pharmacol. 181: 137-139.
55. HERRERO, M. T., I. PEREZ-OTANO, C. OSET, A. KASTNER, E. C. HIRSCH, Y. AGID, M. R. LIQUIN, J. A. OBESO & J. DEL RIO. 1993. GM1 ganglioside promotes the recovery of surviving midbrain dopaminergic neurons in MPTP-treated monkeys. Neuroscience. 56: 965-972.
56. CHOI, D. W. & S. M. ROTHMAN. 1990. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci. 13: 171-182.
57. FAVARON, M., H. MANEV, H. ALHO, M. BERTOLINO, B. FERRET, A. GUIDOTTI & E. COSTA. 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.
58. SKAPER, S. D., L. FACCI, D. MILANI & A. LEON. 1989. Monosialoganglioside GM1 protects against anoxia-induced neuronal death in vitro. Exp. Neurol. 106: 297-305.
59. CHENG, B. & M. P. MATTSON. 1991. NGF and bFGF protect rat hippocampal and human cortical neurons against hypoglycemic damage by stabilizing calcium homeostasis. Neuron 7: 1031-1041.
60. CHENG, B. & M. P. MATTSON. 1992. IGF-I and IGF-II protect cultured hippocampal and septal neurons against calcium-mediated hypoglycemic damage. J. Neurosci. 12: 1558-1566.
61. LIBERINI, P., E. P. PIORO, D. MAYSINGER, F. R. ERVIN & A. C. CUELLO. 1993. Long-term protective effects of human recombinant nerve growth factor and monosialoganglioside GM1 treatment on primate nucleus basalis cholinergic neurons after neocortical infarction. Neuroscience 53: 625-637.
62. SKAPER, S. D., L. FACCI, N. SCHIAVO, G. VANTINI, F. MORONI, R. DAL TOSO & A. LEON. 1992. Characterization of 2,4,5-trihydroxyphenylalanine neurotoxicity in vitro and protective effects of ganglioside GM1: Implications for Parkinson's disease. J. Pharmacol. Exp. Ther. 263: 1440-1446.
63. BATISTATOU, A. & L. A. GREENE. 1991. Aurintricarboxylic acid rescues PC12 cells and sympathetic neurons from cell death caused by nerve growth factor deprivation: Correlation with suppression of endonuclease activity. J. Cell Biol. 115:461-471.
64. EDWARDS, S. N, A. E. BUCKMASTER & A. M. TOLKOVSKY. 1991. The death program in cultured sympathetic neurons can be suppressed at the posttranslational level by nerve growth factor, cyclic AMP, and depolarization. J. Neurochem. 57: 2140-2143.
65. BATISTATOU, A. & L. A. GREENE. 1993. Internucleosomal DNA cleavage and neuronal cell survival/death. J. Cell Biol. 122: 523-532.
66. DECKWERTH, T. L. & E. M. JOHNSON, JR. 1993. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor (NGF). J. Cell Biol. 123: 1207-1222.
67. D' MELLO, S. R., C. GALLI, T. CIOTTI & P. CALISSANO. 1993. Induction of apoptosis in cerebellar granule neurons by low potassium: Inhibition of death by insulin-like growth factor I and cAMP. Proc. Natl. Acad. Sci. USA 90: 10989-10993.
68. BREDESEN, B.D. 1995. Neural apoptosis. Ann. Neurol. 38: 839-851.
69. GREENE, L. A. 1978. Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. J. Cell Biol. 78: 747-755.
70. RUKENSTEIN, A., R. E. RYDEL & L. A. GREENE. 1991. Multiple agents rescue PC12 cells from serum-free cell death by translation- and transcription-independent mechanisms. J. Neurosci. 11: 2552-2563.
71. FERRARI, G., B. L. ANDERSON, R. M. STEPHENS, R. D. KAPLAN & L. A. GREENE. 1995. Prevention of apoptotic neuronal death by GM1 ganglioside. J. Biol. Chem. 17: 3074-3080.
72. LOEB, D. M., J. MARAGOS, D. MARTIN-ZANCA, M. V. CHAO, L. F. PARADA & L. A. GREENE. 1991. The trk proto-oncogene rescues NGF responsiveness in mutant NGF-responsive PC12 cell lines. Cell 66: 961-966.
73. LOEB, D. M. & L. A. GREENE. 1993. Transfection with trk restores "slow" NGF binding, efficient NGF uptake, and multiple NGF responses to NGF-nonresponsive PC12 cell mutants. J. Neurosci. 13: 2919-2929.
74. KAPLAN, D. K., D. MARTIN-ZANCA & L. F. PARADA. 1991. Tyrosine phosphorylation and tyrosine kinase activity of the trk oncogene product induced by NGF. Nature 350:158-160.
75. KLEIN, R., S. JING, V. NANDURI, E. O'ROURKE & M. BARBACID. 1991. The trk protooncogene encodes a receptor for nerve growth factor. Cell 65: 189-197.
76. FERRARI, G., M. FABRIS, M. G. FIORI, N. GABELLINI & C. VOLONTÉ. 1992. Gangliosides prevent the inhibition by K-252a of NGF responses in PC12 cells. Dev. Brain Res. 65: 35-42.
77. GREEN, S., R. E. RYDEL, J. L. CONNOLLY & L. A. GREENE. 1986. PC12 mutants possessing low- but not high-affinity NGF receptors neither respond to, nor internalize NGF. J. Cell Biol. 102: 830-843.
78. JING, S., P. TAPLEY & M. BARBACID. 1992. Nerve growth factor mediates signal transduction through trk homodimer receptors Neuron 9: 1076-1079.
79. MUTOH, T., A. TOKUDA, T. MIYADAI, M. HAMAGUCHI & N. FUJIHI. 1995. Ganglioside GM1 binds to the Trk protein and regulates receptor function. Proc. Natl. Acad. Sci. USA 92: 5087-5091.
80. RABIN, S. J. & I. MOCCHETTI. 1995. GM1 ganglioside activates the high-affinity nerve growth factor receptor TrkA. J. Neuroch. 65: 347-354.
81. FAROOQUI, T., T. FRANKLIN, D. K. PEARL & A. J. YATES. 1997. Ganglioside GM1 enhances induction by nerve growth factor of a putative dimer of TrkA J. Neuroch. 68: 2348-2355.
82. ULLRICH, A. & J. SCHLESSINGER. 1992. Signal transduction by receptors with tyrosine kinase activity. Neuron 9: 1067-1079.