Trophic effect of cholera toxin B subunit in cultured cerebellar granule neurons: Modulation of intracellular calcium by GM1 ganglioside

Journal of Neuroscience Research

Volumn 44, Issue 3, 1996, Pages 243-254

  Wu, G ^a   Lu, Z H ^a   Nakamura, K ^b   Spray, D C ^c   Ledeen, R W ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

calcium modulation; cerebellar granule neurons; L type calcium channel

Indexed keywords

CALCIUM CHANNEL; CHOLERA TOXIN B SUBUNIT; GANGLIOSIDE GM1;

ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL SURVIVAL; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM RADIOISOTOPES; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; CHOLERA TOXIN; FLUORESCENT DYES; FURA-2; G(M1) GANGLIOSIDE; IMAGE PROCESSING, COMPUTER-ASSISTED; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SPECTROMETRY, FLUORESCENCE;

EID: 0029913460     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19960501)44:3<243::AID-JNR5>3.0.CO;2-G     Document Type: Article

References (82)

1. Ando S (1983): Gangliosides in the nervous system. Neurochem Int 5:507-537.
2. Byrne MC, Ledeen RW, Roisen FJ, Yorke G, Sclafani IR (1983): Ganglioside-induced neuritogenesis: verification that gangliosides are the active agents, and comparison of molecular species. J Neurochem 41:1214-1222.
3. Cannella MS, Roisen FJ, Ogawa T, Sugimoto M, Ledeen RW (1988): Comparison of epi-GM3 with GM3 and GM1 as stimulators of neurite outgrowth. Dev Brain Res 39:137-143.
4. Cannella MS, Oderfeld-Nowak B, Gradkowska M, Skup M, Garofalo L, Cuello AC, Ledeen RW (1990): Derivatives of ganglioside GM1 as neurotrophic agents: comparison of in vivo and in vitro effects. Brain Res 513:286-294.
5. Carlson RO, Masco D, Brooker G, Spiegel S (1994): Endogenous ganglioside GM1 modulates L-type calcium channel activity in N18 neuroblastoma cells. J Neurosci 14:2272-2281.
6. Ceccarelli B, Aporti F, Finesso M (1976): Effects of brain gangliosides on functional recovery in experimental regeneration and reinnervation. In Porcellati G, Ceccarelli B, Tettamanti G (eds): "Ganglioside Function." New York: Plenum, pp 275-293.
7. Chan K-FJ (1987): Ganglioside-modulated protein phosphorylation. J Biol Chem 262:5248-5255.
8. Ciardo A, Meldolesi J (1991): Regulation of intracellular calcium in cerebellar granule neurons: effects of depolarization and of glutamatergic and cholinergic stimulation. J Neurochem 56:184-191.
9. Cochran FB, Ledeen RW, YU RK (1983): Gangliosides and proteins in developing chicken brain myelin. Dev Brain Res 6:27-32.
10. Collins F, Schmidt MF, Guthrie PB, Kater SB (1991): Sustained increase in intracellular calcium promotes neuronal survival. J Neurosci 11:2582-2587.
11. 2+ of rat cerebellar granule cells in explant cultures. J Neurosci 7:1384-1400.
12. Consolazione A, Toffano G (1988): Ganglioside role in functional recovery of damaged nervous system. In Ledeen RW, Hogan EL, Tettamanti G, Yates AJ, Yu RK, (eds): "New Trends in Ganglioside Research: Neurochemical and Neuroregenerative Aspects." Padova, Italy: Liviana Press, pp 523-533.
13. Cuello AC, Stephens PH, Tagari PC, Sofroniew MV, Pearson RCA (1986): Retrograde changes in the nucleus basalis of the rat, caused by cortical damage, are prevented by exogenous ganglioside GM1. Brain Res 376:373-377.
14. 2+ dynamics after toxic doses of glutamate in cerebellar granule cells. Proc Natl Acad Sci USA 87:8017-8021.
15. Dixon SJ, Stewart D, Grinstein S, Spiegel S (1987): Transmembrane signaling by the B subunit of cholera toxin: increased cytoplasmic free calcium in rat lymphocytes. J Cell Biol 105:1153-1161.
16. Doherty P, Dickson JG, Flanigan TP, Walsh FS (1985): Ganglioside GM1 does not initiate, but enhances neurite regeneration of nerve growth factor-dependent sensory neurons. J Neurochem 44:1259-1265.
17. 2+ channels. Cell 67:21-33.
18. Doherty P, Ashton SV, Skaper SD, Leon A, Walsh FS (1992): Ganglioside modulation of neural cell adhesion molecule and N-cadherin-dependent neurite outgrowth. J Cell Biol 117:1093-1099.
19. Dreyfus H, Louis JC, Harth S, Mandel P (1980): Gangliosides in cultured neurons. Neuroscience 5:1647-1655.
20. 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.
21. Ferrari G, Batistatou A, Greene LA (1993): Gangliosides rescue neuronal cells from death after trophic factor deprivation. J Neurosci 13:1879-1887.
22. Fishman PH (1982): Role of membrane gangliosides in the binding and action of bacterial toxin. J Membr Biol 69:85-97.
23. Forti L, Pietrobon D (1993): Functional diversity of L-type calcium channels in rat cerebellar neurons. Neuron 10:437-450.
24. Forti L, Tottene A, Moretti A, Pietrobon D (1994): Three novel types of voltage-dependent calcium channels in rat cerebellar neurons. J Neurosci 14:5243-5256.
25. Fueshko SM, Schengrund C-L (1992): Identification of a GM1-binding protein on the surface of murine neuroblastoma cells. J Neurochem 59:527-535.
26. Gallo V, Kingsbury A, Balazs R, Jorgensen OS (1987): The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J Neurosci 7:2203-2213.
27. Geisler FH, Dorsey FC, Coleman WP (1991): Recovery of motor function after spinal cord injury - a randomized, placebo-controlled trial with GM-1 ganglioside. N Engl J Med 27:1829-1838.
28. Guan Z, Stokes BT, Brooklyn JV, Yates AJ (1992): Gangliosides inhibit platelet-derived growth-factor-stimulated increase in intracellular calcium in Swiss 3T3 cells. Biochim Biophys Acta 1136:315-318.
29. Guerold B, Massarelli R, Forster V, Freysz L, Dreyfus H (1992): Exogenous gangliosides modulate calcium fluxes in cultured neuronal cells. J Neurosci Res 32:110-115.
30. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
31. Hadjiconstantinou M, Mariani AP, Neff NH (1989): GM1 ganglioside-induced recovery of nigrostriatal dopaminergic neurons after MPTP: an immunohistochemical study. Brain Res 484:297-303.
32. Higashi H, Yamagata T (1992): Mechanism for ganglioside-mediated modulation of a calmodulin-dependent enzyme. J Biol Chem 267:9839-9843.
33. M1 ganglioside in PC12 cells. J Biol Chem 267:24789-24795.
34. Hirano T, Kubo Y, Wu MM (1986): Cerebellar granule cells in culture: monosympatic connections with Purkinje cells and ionic currents. Proc Natl Acad Sci USA 83:4957-4961.
35. 2+ in focal cortical stroke: GM1 ganglioside reduces ischemic injury. J Neurosci Res 30:512-520.
36. Kharlamov A, Guidotti A, Costa E, Hayes R, Armstrong D (1993): Semisynthetic sphingolipids prevent protein kinase C translocation and neuronal damage in the perifocal area following a photochemically induced thrombotic brain cortical lesion. J Neurosci 13:2483-2494.
37. Kreutter D, Kim JYH, Goldenring JR, Ramussen H, Ukomadu C, DeLorenzo RJ, Yu RK (1987): Regulation of protein kinase C activity by gangliosides. J Biol Chem 262:1633-1637.
38. Kueng W, Silber E, Eppenberger U (1989): Quantification of cells cultured on 96-well plates. Anal Biochem 182:16-19.
39. Ledeen RW (1984): Biology of gangliosides: neuritogenic and neuronotrophic properties. J Neurosci Res 12:147-159.
40. Ledeen RW (1989): Biosynthesis, metabolism, and biological effects of gangliosides. In Margolis RU, Margolis RK (eds): "Neurobiology of Glycoconjugates." New York: Plenum, pp 43-83.
41. Ledeen RW, Wu G (1992): Ganglioside function in the neuron. Trends Glycosci Glycotech 4:174-187.
42. Ledeen RW Aquino DA, Sbaschnig-Agler M, Gammon CM, Vaswani KK (1987): Fundamentals of neuronal transport of gangliosides. Functional implications. NATO ASI H7:259-274.
43. Lees MB, Paxman S (1972): Modification of the Lowry procedure for the analysis of proteolipid protein. Analyt Biochem 47:184-192.
44. Leon AD, Benvegnu D, Dal Toso R, Presti D, Facci L, Giorgi O, Toffano G (1984): Dorsal root ganglia and nerve growth factor: a model for understanding the mechanism of GM1 effects on neuronal repair. J Neurosci Res 12:277-287.
45. Magal E, Louis J-C, Aguilera J, Yavin E (1990): Gangliosides prevent ischemia-induced down-regulation of protein kinase C in fetal rat brain. J Neurochem 55:2126-2131.
46. Marchetti C, Carignani C, Robello M (1991): Voltage-dependent calcium currents in dissociated granule cells from rat cerebellum. Neurosci 43:121-133.
47. 2+ in monolayers and suspensions of various types of animal cells. J Cell Biol 105:2145-2155.
48. Masco D, Van de Walle M, Spiegel S (1991): Interaction of ganglioside GM1 with the B subunit of cholera toxin modulates growth and differentiation of neuroblastoma N18 cells. J Neurosci 11:2443-2452.
49. Milani D, Minozzi M-C, Petrelli L, Guidolin D, Skaper SD, Spoerri PE (1992): Interaction of ganglioside GM1 with the B subunit of cholera toxin modulates intracellular free calcium in sensory neurons. J Neurosci Res 33:466-475.
50. Mutoh T, Tokuda A, Guroff G, Fujiki N (1993): The effect of the B subunit of cholera toxin on the action of nerve growth factor on PC12 cells. J Neurochem 60:1540-1547.
51. Nagai Y, Tsuji S (1988): Cell biological significance of gangliosides in neural differentiation and development: critique and proposals. In Ledeen RW, Hogan EL, Tettamanti G, Yates AJ, Yu Rk, (eds): "New Trends in Ganglioside Research: Neurochemical and Neuroregenerative Aspects. Padova, Italy: Liviana Press, pp 329-350.
52. Nakamura K, Wu G, Ledeen RW (1992): Protection of Neuro-2a cells against calcium ionophore cytotoxicity by gangliosides. J Neurosci Res 31:245-253.
53. Narahashi T, Tsunoo A, Yushii M (1987): Characterization of two types of calcium channels in mouse neuroblastoma cells. J Physiol (Lond) 383:231-249.
54. 2+ channel currents in rat cerebellar granule neurons. J Neurosci 15:2995-3012.
55. Riboni L, Bassi R, Conti M, Tettamanti G (1993): Metabolism of exogenous ganglioside GM1 in cultured cerebellar granule cells. FEBS Lett 3:257-260.
56. Roisen FJ, Matta SG, Nagele R, Yorke G (1981): Ganglioside stimulation of axonal sprouting in vitro. Science 214:577-578.
57. Saito M, Yu RK (1993): Possible role of myelin-associated neuraminidase in membrane adhesion. J Neurosci Res 36:127-132.
58. Saito M, Saito M, Liu Y, Wu G, Ledeen RW (1994): GM1-associated proteins in neurons involved in neurite outgrowth. Trans Am Soc Neurochem 25:139.
59. Schengrund C-L (1990): The role(s) of gangliosides in neural differentiation and repair: a perspective. Brain Res Bull 24:131-141.
60. Schneider JS, Pope A, Simpson K, Taggart J, Smith MG, DiStefano L (1992): Recovery from experimental parkinsonism in primates with GM1 ganglioside treatment. Science 256:843-846.
61. Schwartz M, Spirman N (1982): Sprouting from chicken embryo dorsal root ganglia induced by nerve growth factor is specifically inhibited by affinity-purified antiganglioside antibodies. Proc Natl Sci USA 79:6080-6083.
62. Siegel DA, Suzuki K (1994): A GM1-ganglioside-binding protein in rat brain. Prog Brain Res 101:149-162.
63. Skaper SD, Leon A, Toffano G (1989): Ganglioside function in the development and repair of the nervous system. Mol Neurobiol 3:173-199.
64. Slesinger PA, Lansman JB (1989): Dihydropyridine-sensitive calcium channels in dissociated granule cells cultured from mouse cerebellum. Biophys J 55:302a.
65. Spiegel S, Fishman PH (1987): Gangliosides as bimodal regulators of cell growth. Proc Natl Acad Sci USA 84:141-145.
66. Spiegel S, Panagiotopoulos C (1988): Mitogenesis of 3T3 fibroblasts induced by endogenous gangliosides is not mediated by cAMP, protein kinase C, or phosphoinositide turnover. Exp Cell Res 177:414-427.
67. Spoerri PE, Dozier AK, Roisen FJ (1990): Calcium regulation of neuronal differentiation: the role of calcium in GM1-mediated neuritogenesis. Dev Brain Res 56:177-188.
68. Svennerholm L (1994): Gangliosides - a new therapeutic agent against stroke and Alzheimer's disease. Life Sci 55:2125-2134.
69. Tang C-M, Presser F, Morad M (1988): Amiloride selectively blocks the low threshold (T) calcium channel. Science 240:213-215.
70. Thangnipon W, Balazs R (1992): Developmental changes in gangliosides in cultured cerebellar granule neurons. Neurochem Res 17:45-59.
71. Toffano G, Savoini G, Morono F, Lombardi G, Calza L, Agnati LF (1983): GM1 ganglioside stimulates the regeneration of dopaminergic neurons in the central nervous system. Brain Res 261:163-166.
72. Tsuji S, Arita M, Nagai Y (1983): GQ1b, a bioactive ganglioside that exhibits novel nerve growth factor (NGF)-like activities in two neuroblastoma cell lines. J Biochem (Tokyo) 94:303-306.
73. Tzeng S-F, Diebler GE, DeVries GH (1995): Exogenous myelin basic protein promotes oligodendrocyte death via increased calcium influx. J Neurosci Res (in press).
74. Wu G, Ledeen RW (1991): Stimulation of neurite outgrowth in neuroblastoma cells by neuraminidase: putative role of GM1 ganglioside in differentiation. J Neurochem 56:95-104.
75. Wu G, Nakamura K, Ledeen RW (1991): The role of endogenous GM1 in differentiation of cultured neurons. Trans Amer Soc Neurochem 22:126.
76. Wu G, Ledeen RW (1994): Gangliosides as modulators of neuronal calcium. Prog Brain Res 101:101-112.
77. Wu G, Vaswani KK, Lu Z-H, Ledeen RW (1990): Gangliosides stimulate calcium flux in Neuro-2A cells and require exogenous calcium for neuritogenesis. J Neurochem 55:484-491.
78. Wu G, Nakamura K, Ledeen RW (1994): Inhibition of neurite outgrowth of neuroblastoma Neuro-2A cells by cholera toxin B-subunit and anti-GM1 antibody. Mol Chem Neuropathol 21:259-271.
79. Wu G, Lu Z-H, Ledeen RW (1995a): Induced and spontaneous neuritogenesis are associated with enhanced expression of ganglioside GM1 in the nuclear membrane. J Neurosci 15:3739-3746.
80. Wu G, Lu Z-H, Ledeen RW (1995b): GM1 ganglioside in the nuclear membrane modulates nuclear calcium homeostasis during neurite outgrowth. J Neurochem 65:1419-1422.
81. Yates AJ (1986): Gangliosides in the nervous system during development and regeneration. Neurochem Pathol 5:309-329.
82. Yates AJ, Walters JD, Wood CL, Johnson DJ (1989): Ganglioside modulation of cyclic AMP-dependent protein kinase and cyclic nucleotide phosphodiesterase in vitro. J Neurochem 53:162-167.