Lysophosphatidic acid induces necrosis and apoptosis in hippocampal neurons

Journal of Neurochemistry

Volumn 70, Issue 1, 1998, Pages 66-76

  Holtsberg, Frederick W ^a   Steiner, Marion R ^b   Keller, Jeffrey N ^a   Mark, Robert J ^c,d   Mattson, Mark P ^c,d   Steiner, Sheldon M ^a,b  

^a Center for Ecology Evolution and Behavior   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Apoptosis; Cyclosporin A; Lysophosphatidic acid; Mitochondrial membrane potential; Neurons

Indexed keywords

CYCLOSPORIN A; DIZOCILPINE; GLUTAMATE RECEPTOR ANTAGONIST; LYSOPHOSPHATIDIC ACID; TACROLIMUS;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CHROMATIN CONDENSATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME INHIBITION; ENZYME RELEASE; HIPPOCAMPUS; MITOCHONDRIAL MEMBRANE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT;

ANIMALIA;

EID: 0031982675     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70010066.x     Document Type: Article

References (103)

1. An S., Dickens M. A., Bleu T., Hallmark O. G., and Goetzl E. J. (1997) Molecular cloning of the human edg2 protein and its identification as a functional cellular receptor for lysophosphatidic acid. Biochem. Biophys. Res. Commun. 231, 619-622.
2. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A., and Nicotera P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
3. Ankarcrona M., Dypbukt J. M., Orrenius S., and Nicotera P. (1996) Calcineurin and mitochondrial function in glutamate-induced neuronal cell death. FEBS Lett. 394, 321-324.
4. Bavbek M., Nietgen G. W., Bogaev C., Fineman M. B., Polin R., Chen Z. F., Lee K. S., Kassell N. F., and Durieux M. E. (1996) Increased lysophosphatidate levels in CSF after subarachnoid hemorrhage. Soc. Neurosci. Abstr. 22, 1566.
5. Bazan N. G. and Allan G. (1996) Platelet-activating factor in the modulation of excitatory amino acid neurotransmitter release and of gene expression. J. Lipid Mediat. Cell Signal. 14, 321-330.
6. Bindokas V. P., Jordán J., Lee C. C., and Miller R. J. (1996) Superoxide production in rat hippocampal neurons: sensitive imaging with ethidine. J. Neurosci. 16, 1324-1336.
7. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and Lipton S. A. (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cultures. Proc. Natl. Acad. Sci. USA 92, 7162-7166.
8. Bredesen D. (1995) Neural apoptosis. Ann. Neurol. 38, 839-851.
9. Broekmeier K. M., Dempsey M. E., and Pfeiffer D. R. (1989) Cyclosporin A is a potent inhibitor of the inner membrane permeability transition in liver mitochondria. J. Biol. Chem. 264, 7826-7830.
10. Bruce A. J., Sakhi S., Schreiber S. S., and Baudry M. (1995) Development of kainic acid and N-methyl-D-aspartic acid toxicity in organotypic hippocampal cultures. Exp. Neurol. 132, 209-219.
11. Budd S. L. and Nicholls D. G. (1996) Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 67, 2282-2291.
12. Burek M. J. and Oppenheim R. W. (1996) Programmed cell death in the developing nervous system. Brain Pathol. 6, 427-446.
13. Chalmers-Redman R. M. E., Fraser A. D., Ju W. Y. H., Wadia J., Tatton N. A., and Tatton W. G. (1997) Mechanisms of nerve cell death: apoptosis or necrosis after cerebral ischaemia. Int. Rev. Neurobiol. 40, 1-25.
14. Chen Q., Olashaw N., and Wu J. (1995) Participation of reactive oxygen species in the lysophosphatidic acid-stimulated mitogen-activated protein kinase kinase activation pathway. J. Biol. Chem. 270, 28499-28502.
15. Cheng B. and Mattson M. P. (1992) IGF-I and IGF-II protect cultured hippocampal and septal neurons against calcium-mediated hypoglycemic damage. J. Neurosci. 12, 1558-1566.
16. Choi D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
17. Clark G. D., Happel L. T., Zorumski C. F., and Bazan N. G. (1992) Enhancement of hippocampal excitatory synaptic transmission by platelet-activating factor. Neuron 9, 1211-1216.
18. Das A. K. and Hajra A. K. (1989) Quantification, characterization and fatty acid composition of lysophosphatidic acid in different rat tissues. Lipids 24, 329-333.
19. Dawson T. M., Steiner J. P., Dawson V. L., Dinerman J. L., Uhl G. R., and Snyder S. H. (1993) Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc. Natl. Acad. Sci. USA 90, 9808-9812.
20. de Bilbao F. and Dubois-Dauphin M. (1996) Acute application of an interleukin-1 β-converting enzyme-specific inhibitor delays axotomy-induced motoneurone death. Neuroreport 7, 3051-3054.
21. Dugan L. L., Sensi S. L., Canzoniero L. M. T., Handran S. D., Rothman S. M., Lin T.-S., Goldberg M. P., and Choi D. W. (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15, 6377-6388.
22. Eichholtz T., Jalink K., Fahrenfort I., and Moolenaar W. H. (1993) The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem. J. 291, 677-680.
23. Fearnhead H. O., Dinsdale D., and Cohen G. M. (1995) An interleukin-1 β-converting enzyme-like protease is a common mediator of apoptosis in thymocytes. FEBS Lett. 375, 283-288.
24. 2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 80, 919-927.
25. Frandsen A. and Schousboe A. (1993) Excitatory amino acid-mediated cytotoxicity and calcium homeostasis in cultured neurons. J. Neurochem. 60, 1202-1211.
26. Gaits F., Salles J.-P., and Chap H. (1997) Dual effect of lysophosphatidic acid on proliferation of glomerular mesangial cells. Kidney Int. 51, 1022-1027.
27. Gavrieli Y., Sherman Y., and Ben-Sasson S. A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
28. Gelbard H. A., Nottet H. S., Swindells S., Jett M., Dzenko K. A., Genis P., White R., Wang L., Choi Y. B., Zhang D., Lipton S. A., Tourtellotte W. W., Epstein L. G., and Gendelman H. E. (1994) Platelet-activating factor: a candidate human immunodeficiency virus type 1-induced neurotoxin. J. Virol. 68, 4628-4635.
29. Gerlach M., Riederer P., and Youdim M. B. H. (1996) Molecular mechanisms for neurodegeneration. Adv. Neurol. 69, 177-194.
30. Gerrard J. M. and Robinson P. (1989) Identification of the molecular species of lysophosphatidic acid produced when platelets are stimulated by thrombin. Biochim. Biophys. Acta 1001, 282-285.
31. Ghosh A. and Greenberg M. E. (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268, 239-247.
32. Griffiths E. J. and Halestrap A. P. (1991) Further evidence that cyclosporin A protects mitochondria from calcium overload by inhibiting a matrix peptidyl-prolyl cis-trans isomerase. Biochem. J. 274, 611-614.
33. Guo Z., Liliom K., Fischer D. J., Bathurst I. C., Tomei L. D., Kiefer M. C., and Tigyi G. (1996) Molecular cloning of a high-affinity receptor for the growth factor-like lipid mediator lysophosphatidic acid from Xenopus oocytes. Proc. Natl. Acad. Sci. USA 93, 14367-14372.
34. Gustavsson L., Lundqvist C., and Hansson E. (1993) Receptor-mediated phospholipase D activity in primary astroglial cultures. Glia 8, 249-255.
35. Gustavsson L., Boyano-Adánez M. C., Larsson C., Aradottir S., and Lundqvist C. (1996) Regulation of phospholipase D activity in neuroblastoma cells. J. Lipid Mediat. Cell Signal. 14, 229-235.
36. Hara H., Friedlander R. M., Gagliardini V., Ayata C., Fink K., Huang Z., Shimizu-Sasamata M., Yuan J., and Moskowitz M. A. (1997) Inhibition of interleukin 1β converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. Natl. Acad. Sci. USA 94, 2007-2012.
37. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 13, 1993-2000.
38. Hecht J. H., Weiner J. A., Post S. R., and Chun J. (1996) Ventricular zone gene-1 (vgz-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex. J. Cell Biol. 135, 1071-1083.
39. Holtsberg F. W., Steiner M. R., Furukawa K., Keller J. N., Mattson M. P., and Steiner S. M. (1997) Lysophosphatidic acid induces a sustained elevation of neuronal intracellular calcium. J. Neurochem. 69, 68-75.
40. Honegger A. and Humbel R. E. (1986) Insulin-like growth factors I and II in fetal and adult bovine serum. Purification, primary structures and immunological cross-reactivities. J. Biol. Chem. 261, 569-575.
41. 2+-mobilizing stimulus for fibroblasts. J. Biol. Chem. 265, 12232-12239.
42. Jalink K., Eichholtz T., Postma F. R., van Corven E. J., and Moolenaar W. H. (1993) Lysophosphatidic acid induces neuronal shape changes via a novel, receptor-mediated signaling pathway: similarity to thrombin action. Cell Growth Differ. 4, 247-255.
43. Johnson E. M. Jr., Deckwerth T., and Deshmukh M. (1996) Neuronal death in developmental models: possible implications in neuropathology. Brain Pathol. 6, 397-409.
44. Keller J. N., Steiner M. R., Mattson M. P., and Steiner S. M. (1996) Lysophosphatidic acid decreases glutamate and glucose uptake by astrocytes. J. Neurochem. 67, 2300-2305.
45. Keller J. N., Steiner M. R., Holtsberg F. W., Mattson M. P., and Steiner S. M. (1997) Lysophosphatidic acid-induced proliferation-related signals in astrocytes. J. Neurochem. 69, 1073-1084.
46. Kitamura Y., Itano Y., Kubo T., and Nomura Y. (1994) Suppressive effect of FK-506, a novel immunosuppressant, against MPTP-induced dopamine depletion in the striatum of young C57BL/6 mice. J. Neuroimmunol. 50, 221-224.
47. 2 and glutamate on inducing cell death and sustained arachidonic acid metabolic changes in primary cortical neuronal cultures. J. Biol. Chem. 271, 32722-32728.
48. Köller H., Siebler M., Schmalenbach C., and Müller H.-W. (1990) GABA and glutamate receptor development of cultured neurons from rat hippocampus, septal region, and cortex. Synapse 5, 59-64.
49. Koopman G., Reutelingsperger C. P., Kuijten G. A., Keehnen R. M., Pals S. T., and van Oers M. H. (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84, 1415-1420.
50. Kroemer G., Petit P., Zamzami N., Vayssière J. L., and Mignotte R. (1995) The biochemistry of programmed cell death. FASEB J. 9, 1277-1287.
51. Kroemer G., Zamzami N., and Susin S. A. (1997) Mitochondrial control of apoptosis. Immunol. Today 18, 44-51.
52. Kunz J. and Hall M. N. (1993) Cyclosporin A, FK506 and rapamycin: more than just immunosuppression. Trends Biochem. Sci. 18, 334-338.
53. Kurtz A., Hartl W., Jelkmann W., Zapf J., and Bauer C. (1985) Activity in fetal bovine serum that stimulates erythroid colony formation in fetal mouse livers is insulinlike growth factor I. J. Clin. Invest. 76, 1643-1648.
54. Lafon-Cazal M., Pietri S., Culcasi M., and Bockaert J. (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364, 535-537.
55. 2 in rat brain after severe forebrain ischemia and in endotoxic shock. Brain Res. 651, 353-356.
56. Liliom K., Murakami-Murofushi K., Kobayashi S., Murofushi H., and Tigyi G. (1996) Xenopus oocytes express multiple receptors for LPA-like lipid mediators. Am. J. Physiol. 270, C772-C777.
57. Liu J., Farmer J. D., Lane W. S., Friedman J., Weissman I., and Schreiber S. L. (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 807-815.
58. Mangoura D. and Dawson G. (1993) Opioid peptides activate phospholipase D and protein kinase C-∈ in chicken embryo neuron cultures. Proc. Natl. Acad. Sci. USA 90, 2915-2919.
59. +-ATPase that results in its activation in cerebellar neurons in cultures. J. Neurochem. 66, 99-104.
60. Martin S. J., Finucane D. M., Amarante-Mendes G. P., O'Brien G. A., and Green D. R. (1996) Phosphatidylserine externalization during CD95-induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J. Biol. Chem. 271, 28753-28756.
61. Masui T., Wakeneld L. M., Lechner J. F., LaVeck M. A., Sporn M. B., and Harris C. C. (1986) Type β TGF is the primary differentiation-inducing serum factor for normal human bronchial epithelial cells. Proc. Natl. Acad. Sci. USA 83, 2438-2442.
62. Matsuura K., Kabuto H., Making H., and Ogawa N. (1996) Cyclosporin A attenuates degeneration of dopaminergic neurons induced by 6-hydroxydopamine in the mouse brain. Brain Res. 733, 101-104.
63. 2 from rat neuronal cells and its possible function in the regulation of catecholamine secretion. Biochem J. 318, 701-709.
64. Mattson M. P. and Kater S. B. (1988) Isolated hippocampal neurons in cryopreserved long term culture: development of neuroarchitecture and sensitivity to NMDA. Int. J. Dev. Neurosci. 6, 439-452.
65. Mattson M. P., Barger S. W., Begley J., and Mark R. J. (1995) Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol. 46, 187-216.
66. Mauco G., Chap H., Simon M.-F., and Douste-Blazy L. (1978) Phosphatidic and lysophosphatidic acid production in phospholipase C- and thrombin-treated platelets. Possible involvement of a platelet lipase. Biochimie 60, 653-661.
67. Moulin V., Auger F. A., O'Connor-McCourt M., and Germain L. (1997) Fetal and postnatal sera differentially modulate human dermal fibroblast phenotypic and functional features in vitro. J. Cell. Physiol. 171, 1-10.
68. Naito M., Nagashima K., Mashima T., and Tsuruo T. (1996) Phosphatidylserine externalization is a downstream event of interleukin-1 β-converting enzyme family protease activation during apoptosis. Blood 89, 2060-2066.
69. Nilsson O. G., Saveland H., Boris-Moller F., Brandt L., and Wieloch T. (1996) Increased levels of glutamate in patients with subarachnoid haemorrhage as measured by intracerebral microdialysis. Acta Neurochir. Suppl. 67, 45-47.
70. 2 in noradrenaline release from cerebral cortical synaptosomes. J. Pharm. Pharmacol. 41, 450-458.
71. 2 in rat cultured astrocytes. Two distinct pathways of the gene expression. J. Biol. Chem. 266, 9956-9960.
72. O'Keefe S. J., Tamura J., Kincaid R. L., Tocci M. J., and O'Neill E. A. (1992) FK506 and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357, 692-694.
73. Pastorino J. G., Snyder J. W., Serroni A., Hoek J. B., and Farber F. L. (1993) Cyclosporin and carnitine prevent the anoxic death of cultured hepatocytes by inhibiting the mitochondrial permeability transition. J. Biol. Chem. 268, 13791-13798.
74. Pelekanou V., Trezise A. L., Moore A. L., and Kay J. E. (1991) FK 506 and rapamycin do not affect platelet aggregation or mitochondrial function. Transplant. Proc. 23, 2300-2301.
75. Persson L., Valtysson J., Enblad P., Wärme P.-E., Cesarini K., Lewén A., and Hillered L. (1996) Neurochemical monitoring using intracerebral microdialysis in patients with subarachnoid hemorrhage. J. Neurosurg. 84, 606-616.
76. Piazza G. A., Ritter J. L., and Baracka C. A. (1995) Lysophosphatidic acid induction of transforming growth factors α and β: modulation of proliferation and differentiation in cultured human keratinocytes and mouse skin. Exp. Cell Res. 216, 51-64.
77. Prehn J. H., Bindokas V. P., Marcuccilli C. J., Krajewski S., Reed J. C., and Miller R. J. (1994) Regulation of neuronal Bcl2 protein expression and calcium homeostasis by transforming growth factor β confers wide-ranging protection on rat hippocampal neurons. Proc. Natl. Acad. Sci. USA 91, 12599-12603.
78. Raff M. C., Barres B. A., Burne J. F., Coles H. S., Ishizaki Y., and Jacobson M. D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262, 695-700.
79. Randall R. D. and Thayer S. A. (1992) Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J. Neurosci. 12, 1882-1895.
80. Reers M., Smiley S. T., Mottola-Hartshorn C., Chen A., Lin M., and Chen L. B. (1995) Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 260, 406-416.
81. Reynolds I. J. and Hastings T. G. (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15, 3318-3327.
82. 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.
83. Schinder A. F., Olson E. C., Spitzer N. C., and Montal M. (1996) Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci. 16, 6125-6133.
84. Schulze C., Smales C., Rubin L. L., and Staddon J. M. (1997) Lysophosphatidic acid increases tight junction permeability in cultured brain endothelial cells. J. Neurochem. 68, 991-1000.
85. Shiono S., Kawamoto K., Yoshida N., Kondo T., and Inagami T. (1993) Neurotransmitter release from lysophosphatidic acid stimulated PC12 cells: involvement of lysophosphatidic acid receptors. Biochem. Biophys. Res. Commun. 193, 667-673.
86. Simonian N. A. and Coyle J. T. (1996) Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 36, 88-7 106.
87. Singleton J. R., Dixit V. M., and Feldman E. L. (1996) Type I insulin-like growth factor receptor activation regulates apoptotic proteins. J. Biol. Chem. 271, 31791-31794.
88. 2 for phosphatidic acid. Biochem. J. 321, 737-741.
89. Steiner J. P., Connolly M. A., Valentine H. L., Hamilton G. A., Dawson T. M., Hester L. A., and Snyder S. H. (1997) Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin A. Nat. Med. 3, 421-428.
90. 2 from rat brain. Biochem. J. 306, 305-309.
91. Thomson F. J., Perkins L., Ahern D., and Clark M. (1994) Identification and characterization of a lysophosphatidic acid receptor. Mol. Pharmacol. 45, 718-723.
92. Tigyi G. and Miledi R. (1992) Lysophosphatidates bound to serum albumin activate membrane currents in Xenopus oocytes and neurite retraction in PC12 pheochromocytoma cells. J. Biol. Chem. 267, 21360-21367.
93. Tigyi G., Dyer D. L., and Miledi R. (1994) Lysophosphatidic acid possesses dual action in cell proliferation. Proc. Natl. Acad. Sci. USA 91, 1908-1912.
94. Tigyi G., Hong L., Yakubu M., Parfenova H., Shibata M., and Leffler C. W. (1995) Lysophosphatidic acid alters cerebrovascular reactivity in piglets. Am. J. Physiol. 268, H2048-H2055.
95. Tokumura A., Iimori M., Nishioka Y., Kitahara M., Sakashita M., and Tanaka S. (1994) Lysophosphatidic acids induce proliferation of cultured vascular smooth muscle cells from rat aorta. Am. J. Physiol. 267, C204-C210.
96. 2+ overload indicates early neuronal injury which precedes staining with viability indicators. Brain Res. 607, 319-323.
97. Uchino H., Elmér E., Uchino K., Lindvall O., and Siesjö B. K. (1995) Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischemia in the rat. Acta Physiol. Scand. 155, 469-471.
98. van Corven E. J., Groenink A., Jalink K., Eichholtz T., and Moolenaar W. H. (1989) Lysophosphatidate-induced cell proliferation: identification and dissection of signaling pathways mediated by G proteins. Cell 59, 45-54.
99. van der Bend R. L., Brunner J., Jalink K., van Corven E. J., Moolenaar W. H., and van Blitterswijk W. J. (1992) Identification of a putative membrane receptor for the bioactive phospholipid, lysophosphatidic acid. EMBO J. 11, 2495-2501.
100. White R. J. and Reynolds I. J. (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16, 5688-5697.
101. Whittemore E. R., Loo D. T., and Cotman C. W. (1994) Exposure to hydrogen peroxide induces cell death via apoptosis in cultured rat cortical neurons. Neuroreport 5, 1485-1488.
102. Yue T. L. and Feuerstein G. Z. (1994) Platelet-activating factor: a putative neuromodulator and mediator in the pathophysiology of brain injury. Crit. Rev. Neurobiol. 8, 11-24.
103. Zhang Y., Tatsuno T., Carney J. M., and Mattson M. P. (1993) Basic FGF, NGF, and IGFs protect hippocampal and cortical neurons against iron-induced degeneration. J. Cereb. Blood Flow Metab. 13, 378-388.