Ceramide and its interconvertible metabolite sphingosine function as indispensable lipid factors involved in survival and dendritic differentiation of cerebellar Purkinje cells

Journal of Neurochemistry

Volumn 71, Issue 1, 1998, Pages 366-377

  Furuya, Shigeki ^a   Mitoma, Junya ^a   Makino, Asami ^a   Hirabayashi, Yoshio ^a  

^a INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

Author keywords

Apoptosis; Ceramide; Cerebellar Purkinje cells; Dendritic differentiation; Neurotrophin; Sphingomyelinase

Indexed keywords

ACYLTRANSFERASE; CERAMIDE; ENZYME INHIBITOR; GLUCOSYLCERAMIDE; GLYCOSPHINGOLIPID; ISP 1; LACTOSYLCERAMIDE; LIPID; NERVE GROWTH FACTOR; NEUROTROPHIN 3; SERINE PALMITOYLTRANSFERASE; SPHINGOLIPID; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; FETUS; METABOLITE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT;

EID: 0031866963     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.71010366.x     Document Type: Article

References (72)

1. Ando S. (1983) Gangliosides in the nervous system. Neurochem. Int. 5, 507-537.
2. Baptista C. A., Hatten M. E., Blazeski R., and Mason C. A. (1994) Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron 12, 243-260.
3. Brugg B., Michel P. P., Agid Y., and Ruberg M. (1996) Ceramide induces apoptosis in cultured mesencephalic neurons. J. Neurochem. 66, 733-739.
4. Casaccia-Bonnefil P., Aibel L., and Chao M. V. (1996a) Central glial and neuronal populations display differential sensitivity to ceramide-dependent cell death. J. Neurosci. Res. 43, 382-389.
5. Casaccia-Bonnefil P., Carter B. D., Dobrowsky R. T., and Chao M. V. (1996b) Death of oligodendrocytes mediated by the inter action of nerve growth factor with its receptor p75. Nature 383, 716-719.
6. Cohen-Cory S., Dreyfus C. F., and Black I. B. (1991) NGF and excitatory neurotransmitters regulate survival and morphogenesis of cultured cerebellar Purkinje cells. J. Neurosci. 11, 462-471.
7. Dobrowsky R. T., Kamibayashi C., Mumby M. C., and Hannun Y. A. (1993) Ceramide activates heterotrimeric protein phosphatase 2A. J. Biol. Chem. 268, 15523-15530.
8. Dobrowsky R. T., Werner M. H., Castellino A. M., Chao M. V., and Hannun Y. A. (1994) Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 265, 1596-1599.
9. Dobrowsky R. T., Jenkins G. M., and Hannun Y. A. (1995) Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. J. Biol. Chem. 270, 22135-22142.
10. Fishbein J. D., Dobrowsky R. T., Bielawska A., Garrett S., and Hannun Y. A. (1993) Ceramide-mediated growth inhibition and CAPP are conserved in Saccharomyces cerevisiae. J. Biol. Chem. 268, 9255-9261.
11. Furuya S. and Hirabayashi Y. (1996) Regulation of cerebellar Purkinje cell growth by ceramide generated from sphingomyelin. Soc. Neurosci. Abstr. 22, 297.
12. Furuya S., Irie F., Hashikawa T., Nakazawa K., Kozakai A., Hasegawa A., Sudo K., and Hirabayashi Y. (1994) Ganglioside GD1α in cerebellar Purkinje cells: its specific absence in mouse mutants with Purkinje cell abnormality and altered immunore-activity in response to conjunctive stimuli causing long-term desensitization. J. Biol. Chem. 269, 32418-32425.
13. Furuya S., Ono K., and Hirabayashi Y. (1995) Sphingolipid biosynthesis is necessary for dendritic growth and survival of cerebellar Purkinje cells in culture. J. Neurochem. 65, 1551-1561.
14. Furuya S., Hashikawa T., and Hirabayashi Y. (1996a) Restricted occurrence of an unusual ganglioside GD1α in rat brain and its possible involvement in dendritic growth of cerebellar Purkinje neurons. J. Neurosci. Res. 44, 73-83.
15. 2+ release from rat brain microsomes. J. Lipid Mediat. Cell Signal. 14, 303-311.
16. Goldkorn T., Dressler K. A., Muindi J., Radin N. S., Mendelsohn J., Menaldino D., Liotta D., and Kolesnick R. N. (1991) Ceramide stimulates epidermal growth factor receptor phosphorylation in A431 human epidermoid carcinoma cells: evidence that ceramide may mediate sphingosine action. J. Biol. Chem. 266, 16092-16097.
17. Goodman Y. and Mattson M. P. (1996) Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid β-peptide toxicity. J. Neurochem. 66, 869-872.
18. Hanada K., Nishijima M., Kiso M., Hasegawa A., Fujita S., Ogawa T., and Akamatsu Y. (1992) Sphingolipids are essential for the growth of Chinese hamster ovary cells: restoration of the growth of a mutant defective in sphingoid base biosynthesis by exogenous sphingolipids. J. Biol. Chem. 267, 23527-23533.
19. Hannun Y. A. (1996) Functions of ceramide in coordinating cellular responses to stress. Science 274, 1855-1859.
20. Hannun Y. A. and Obeid L. M. (1995) Ceramide: an intracellular signal for apoptosis. Trends Biochem. Sci. 20, 73-77.
21. Harel R. and Futerman A. H. (1993) Inhibition of sphingolipid synthesis affects axonal outgrowth in cultured hippocampal neurons. J. Biol Chem. 268, 14476-14481.
22. Hirabayashi Y., Nakao T., Matsumoto M., Obata K., and Ando S. (1988) Improved method for large-scale purification of brain gangliosides by Q-Sepharose column chromatography: immunological detection of c-series polysialogangliosides in adult bovine brains. J. Chromatogr. 445, 377-384.
23. Horinouchi K., Erlich S., Perl D. P., Ferlinz K., Bisgaier C. L., Sandhoff K., Desnick R. J., Stewart C. L., and Schuchman E. H. (1995) Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease. Nat. Genet. 10, 288-293.
24. Huwiler A., Brunner J., Hummel R., Vervoordeldonk M., Stabel S., van den Bosch H., and Pfeilschifter J. (1996) Ceramide-binding and activation defines protein kinase c-Raf as a ceramide-activated protein kinase. Proc. Natl. Acad. Sci. USA 93, 6959-6963.
25. Ito A. and Horigome K. (1995) Ceramide prevents neuronal programmed cell death induced by nerve growth factor deprivation. J. Neurochem. 65, 463-466.
26. Ji L., Zhang G., Uematsu S., Akahori Y., and Hirabayashi Y. (1995) Induction of apoptotic DNA fragmentation and cell death by natural ceramide. FEBS Lett. 358, 211-214.
27. Kates M. (1986) Techniques of Lipidology: Isolation, Analysis and Identification, 2nd edit. Elsevier, Amsterdam.
28. Koh S. and Higgins G. A. (1991) Differential regulation of the low-affinity nerve growth factor receptor during postnatal development of the rat brain. J. Comp. Neural. 313, 494-508.
29. Kolesnick R. and Golde D. W. (1994) The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signaling. Cell 77, 325-328.
30. Kyriakis J. M., Banerjee P., Nikolakaki E., Dai T., Rubie E. A., Ahmad M. F., Avruch J., and Woodgett J. R. (1994) The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369, 156-160.
31. Lärkfors L., Lindsay R. M., and Alderson R. F. (1996) Characterization of the responses of Purkinje cells to neurotrophin treatment. J. Neurochem. 66, 1362-1373.
32. Lee K. F., Li E., Huber L. J., Landis S. C., Sharpe A. H., Chao M. V., and Jaenisch R. (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737-749.
33. Lindholm D., Castren E., Tsoulfas P., Kolbeck R., Berzaghi M. P., Leingartner A., Heisenberg C.-P., Tesarollo L., Parada L. F., and Thoenen H. (1993) Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. J. Cell Biol. 122, 443-450.
34. Martin S. J., Reutelingsperger C. P., McGahon A. J., Rader J. A., van Schie R. C., LaFace D. M., and Green D. R. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182, 1545-1556.
35. Merrill A. H. Jr., van Echten G., Wang E., and Sandhoff K. (1993a) Fumonisin B1 inhibits sphingosine (sphinganine) N-acyltransferase and de novo sphingolipid biosynthesis in cultured neurons in situ. J. Biol. Chem. 268, 27299-27306.
36. Merrill A. H. Jr., Wang E., Gilchrist D. G., and Reiley R. T. (1993b) Fumonisins and other inhibitors of de novo sphingolipid biosynthesis. Adv. Lipid Res. 26, 215-234.
37. Miyake Y., Kozutsumi Y., Nakamura S., Fujita T., and Kawasaki T. (1995) Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem. Biophys. Res. Commun. 211, 396-403.
38. Mount H. T. J., Dreyfus C. F., and Black I. B. (1994) Neurotrophin-3 selectively increases cultured Purkinje cell survival. Neuroreport 5, 2497-2500.
39. Nakamura S., Kozutsumi Y., Sun Y., Miyake Y., Fujita T., and Kawasaki T. (1996) Dual roles of sphingolipids in signaling of the escape from and onset of apoptosis in a mouse cytotoxic T-cell line, CTLL-2. J. Biol. Chem. 271, 1255-1257.
40. Neveu I. and Arenas E. (1996) Neurotrophins promote the survival and development of neurons in the cerebellum of hypothyroid rats in vivo. J. Cell Biol. 133, 631-646.
41. Olivera A., Buckley N. E., and Spiegel S. (1992) Sphingomyelinase and cell-permeable ceramide analogs stimulate cellular proliferation in quiescent Swiss 3T3 fibroblasts. J. Biol. Chem. 267, 26121-26127.
42. Otterbach B. and Stoffel W. (1995) Acid sphingomyelinase-deficient mice mimic the neurovisceral form of human lysosomal storage disease (Niemann-Pick disease). Cell 81, 1053-1061.
43. Paul P., Kamisaka Y., Marks D. L., and Pagano R. E. (1996) Purification and characterization of UDP-glucose:ceramide glucosyltransferase from rat liver Golgi membranes. J. Biol. Chem. 271, 2287-2293.
44. Pint W. J., Srinivasan B., Shephered S., Schmidt A., Dickson R. C., and Lester R. L. (1992) Sphingolipid long-chain base auxotrophs of Saccharomyces cerevisiae: genetics, physiology, and a method for their selection. J. Bacteriol. 174, 2565-2574.
45. Posse de Chaves E. I., Bussière M., Vance D. E., Campenot R. B., and Vance J. E. (1997) Elevation of ceramide within distal neuntes inhibits neurite growth in cultured rat sympathetic neurons. J. Biol. Chem. 272, 3028-3035.
46. Raines M. A., Kolesnick R. N., and Golde D. W. (1993) Sphingomyelinase and ceramide activate mitogen-activated protein kinase in myeloid HL-60 cells. J. Biol. Chem. 268, 14572-14575.
47. Riboni L., Bassi R., Conti M., and Tettamanti G. (1993) Metabolism of exogenous ganglioside GM1 in cultured cerebellar granule cells: the fatty acid and sphingosine moieties formed during degradation are re-used for lipid biosynthesis. FEBS Lett. 322, 257-260.
48. Riboni L., Prinetti A., Bassi R., Caminiti A., and Tettamanti G. (1995) A mediator role for ceramide in the regulation of Neuro2a cell differentiation. J. Biol Chem. 270, 26868-26875.
49. Ridgway N. D. and Merrian D. L. (1995) Metabolism of short-chain ceramide and dihydroceramide analogues in Chinese hamster ovary (CHO) cells. Biochim. Biophys. Acta 1256, 57-70.
50. Rimon G., Bazenet C. E., Philpott K. L., and Rubin L. L. (1997) Increased surface phosphatidylserine is an early marker of neuronal apoptosis. J. Neurosci. Res. 48, 563-570.
51. Rocamora N., Garcia-Ladona F. J., Palacios J. M., and Mengod G. (1993) Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and low-affinity nerve growth factor receptor during the postnatal development of the rat cerebellar system. Mol. Brain Res. 17, 1-8.
52. Sasaki T., Hazeki K., Hazeki O., Ui M., and Katada T. (1995) Permissive effect of ceramide on growth factor-induced cell proliferation. Biochem. J. 311, 829-834.
53. Schwarz A. and Futerman A. H. (1997) Distinct roles for ceramide and glucosylceramide at different stages of neuronal growth. J. Neurosci. 17, 2929-2938.
54. Schwarz A., Rapaport E., Hirschberg K., and Futerman A. H. (1995) A regulatory role for sphingolipids in neuronal growth: inhibition of sphingolipid synthesis and degradation have opposite effects on axonal branching. J. Biol. Chem. 270, 10990-10998.
55. Shirakabe K., Yamaguchi K., Shibuya H., Irie K., Matsuda S., Moriguchi T., Gotoh Y., Matsumoto K., and Nishida E. (1997) TAK1 mediates the ceramide signaling to stress-activated protein kinase/c-Jun N-terminal kinase. J. Biol. Chem. 272, 8141-8144.
56. Sobreviela T., Clay D. O., Reichardt L. F., Brandabur M. M., Kordower J. H., and Mufson E. J. (1994) TrkA-immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. J. Comp. Neurol. 350, 587-611.
57. Spence M. W. and Burgess J. K. (1978) Acid and neutral sphingomyelinases of rat brain: activity in developing brain and regional distribution in adult brain. J. Neurochem. 30, 917-919.
58. Spiegel S. and Merrill A. H. Jr. (1996) Sphingolipid metabolism and cell growth regulation. FASEB J. 10, 1388-1397.
59. Spiegel S., Foster D., and Kolesnick R. (1996) Signal transduction through lipid second messengers. Curr. Opin. Cell Biol. 8, 159-167.
60. Sugita M., Williams M., Dulaney J. T., and Moser H. W. (1975) Ceramidase and ceramide synthesis in human kidney and cerebellum. Biochim. Biophys. Acta 398, 125-131.
61. Svennerholm L. (1964) The gangliosides. J. Lipid Res. 5, 145-153.
62. Tessarollo L., Tsoulfas P., Martin-Zanca D., Gilbert D. J., Jenkins N. A., Copeland N. G., and Parada L. F. (1993) trkC, a receptor for neurotrophin-3, is widely expressed in the developing nervous system and in non-neuronal tissues. Development 118, 463-475.
63. Tettamanti G. and Riboni L. (1993) Gangliosides and modulation of the function of neural cells. Adv. Lipid Res. 25, 235-267.
64. Verheij M., Bose R., Lin X. H., Yao B., Jarvis W. D., Grant S., Birrer M. J., Szabo E., Zon L. I., Kyriakis J. M., Haimovitz-Friedman A., Fuks Z., and Kolesnick R. N. (1996) Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380, 75-79.
65. Vermes I., Haanen C., Steffens-Nakken H., and Reutelingsperger C. (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J. Immunol. Methods 17, 39-51.
66. Wang E., Norred W. P., Bacon C. W., Riley R. T., and Merrill A. H. Jr. (1991) Inhibition of sphingolipid biosynthesis by fumonisins. J. Biol. Chem. 266, 14486-14490.
67. Westwick J. K., Bielawska A. E., Dbaibo G., Hannun Y. A., and Brenner D. A. (1995) Ceramide activates the stress-activated protein kinases. J. Biol. Chem. 270, 22689-22692.
68. Wolff R. A., Dobrowsky R. T., Bielawska A., Obeid L. M., and Hannun Y. A. (1994) Role of ceramide-activated protein phosphatase in ceramide-mediated signal transduction. J. Biol. Chem. 269, 19605-19609.
69. Xia Z., Dickens M., Raingeaud J., Davis R. J., and Greenberg M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
70. Yao B., Zhang Y., Delikat S., Mathias S., Basu S., and Kolesnick R. (1995) Phosphorylation of Raf by ceramide-activated protein kinase. Nature 378, 307-310.
71. Zhang G., Ji L., Kurono S., Fujita S. C., Furuya S., and Hirabayashi Y. (1997) Developmentally regulated O-acetylated sialoglycoconjugates in the central nervous system revealed by a new monoclonal antibody 493D4 recognizing a wide range of O-acetylated glycoconjugates. Glycoconj. J. 14, 847-857.
72. Zhang Y., Yao B., Delikat S., Bayoumy S., Lin X. H., Basu S., McGinley M., Chan-Hui P. Y., Lichenstein H., and Kolesnick R. (1997) Kinase suppressor of Ras is ceramide-activated protein kinase. Cell 89, 63-72.