Glial-derived neurotrophic factor rescues calbindin-D(28k)- Immunoreactive neurons in alcohol-treated cerebellar explant cultures

Journal of Neurobiology

Volumn 33, Issue 6, 1997, Pages 835-847

  McAlhany Jr , Robert E ^a   West, James R ^a   Miranda, Rajesh C ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Cerebellum; Explant cultures; Fetal alcohol syndrome; Glial derived neurotrophic factor; Purkinje cell

Indexed keywords

ALCOHOL; CALBINDIN; NEURITE PROMOTING FACTOR;

ALCOHOL CONSUMPTION; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; EXPLANT; IMMUNOHISTOCHEMISTRY; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FETAL ALCOHOL SYNDROME; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; IMMUNOHISTOCHEMISTRY; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA;

EID: 1842410681     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(19971120)33:6<835::AID-NEU10>3.0.CO;2-3     Document Type: Article

References (64)

1. ABEL, E. L. and HANNIGAN, J. H. (1995). Maternal risk factors in fetal alcohol syndrome: provocative and permissive influences. Neurotoxicol. Teratol. 17:445-462.
2. ALLERAND, C. D. (1971). Patterns of neuronal differentiation in developing cultures of neonatal mouse cerebellum: a living and silver impregnation study. J. Comp. Neurol. 142:167-204.
3. ALLERAND, C. D. and MURRAY, M. R. (1968). Myelin formation in vitro. Arch. Neurol 19:292-301.
4. ALTMAN, J. and BAYER, S. A. (1997). Development of the Cerebellar System: In Relation to Its Evolution, Structure and Functions. CRC Press, Boca Raton, FL.
5. BAEK, J.-K., HEATON, M. B., and WALKER, D. W. (1994). Chronic alcohol ingestion: nerve growth factor gene expression and neurotrophic activity in rat hippocampus. Alcohol Clin. Exp. Res. 18:1368-1376.
6. BALOH, R. H., TANSEY, M. G., GOLDEN, J. P., CREEDON, D. J., HEUCKEROTH, R. O., KECK, C. L., ZIMONJIC, D. B., POPESCU, N. C., JOHNSON, E. M., JR., and MILBRANDT, J. (1997). TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret. Neuron 18:793-802.
7. BONTHIUS, D. J. and WEST, J. R. (1990). Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcohol Clin. Exp. Res. 14:107-118.
8. BONTHIUS, D. J. and WEST, J. R. (1991). Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology 44:147-163.
9. BUJBELLO, A., ADU, J., PINON, L. G. P., HORTON, A., THOMPSON, J., ROSENTHAL, A., CHINCHETRU, M., BUCHMAN, V. L., and DAVIES, A. M. (1997). Neurturin responsiveness requires a GPI-linked receptor and the Ret receptor tyrosine kinase. Nature 387:721-724.
10. CELIO, M. R. (1990). Calbindin-D28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
11. CHEN, S. and HILLMAN, D. E. (1989). Regulation of granule cell number by a predetermined number of Purkinje cells in development. Brain Res. Dev. Brain Res. 45:137-147.
12. CHEN, W.-J. A. and WEST, J. R. (1997). Alcohol-induced brain damage during development: potential risk factors. In: Alcoholism and Alcoholism: Brain and Development. J. H. Hannigan, C. R. Goodlett, L. P. Spear, and N. E. Spear, Eds. Erlbaum, Mahwah, NJ.
13. CHOI, D. W. (1992). Excitotoxic cell death. J. Neurobiol. 23:1261-1276.
14. CHOI-LUNDBERG, D. L. and BOHN, M. C. (1995). Ontogeny and distribution of glial cell line-derived neurotrophic factor (GDNF) mRNA in rat. Brain Res. Dev. Brain Res. 85:80-88.
15. DOBBING, J. and SANDS, J. (1973). Quantitative growth and development of human brain. Arch. Dis. Child 48:757-767.
16. DOBBING, J. and SANDS, J. (1979). Comparative aspects of the brain growth spurt. Early Hum. Dev. 3:79-83.
17. DURBEC, P., MARCOS-GUTIERREZ, C. V., KILKENNY, C., GRIGORIOU, M., WARTIOWAARA, K., SUVANTO, P., SMITH, D., PONDER, B., COSTANTINI, F., SAARMA, M., SARIOLA, H., and PACHNIS, V. (1996). GDNF signaling through the Ret receptor tyrosine kinase. Nature 381:789-793.
18. EBENDAL, T., TOMAC, A., HOFFER, B. J., and OLSON, L. (1995). Glial cell line-derived neurotrophic factor stimulates fiber formation and survival in cultured neurons from peripheral autonomic ganglia. J. Neurosci. Res. 40:276-284.
19. FARBER, J. L. (1981). The role of calcium in cell death. Life Sci. 29:1289-1295.
20. GASH, D. M., ZHANG, Z., OVADIA, A., CASS, W. A., YI, A., SIMMERMAN, L., RUSSELL, D., MARDIN, D., LAPCHAK, P. A., COLLINS, F., HOFFER, B. J., and GERHARDT, G. A. (1996). Functional recovery in Parkonsonian monkeys treated with GDNF. Nature 380:252-255.
21. GOODLETT, C. R., MARCUSSEN, B. L., and WEST, J. R. (1990). A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss. Alcohol 7:107-114.
22. GOODLETT, C. R., THOMAS, J. D., and WEST, J. R. (1991). Long term deficits in cerebellar growth and Rotarod performance of rats following "binge-like" alcohol exposure during the neonatal brain growth spurt. Neurotoxicol. Teratol. 13:69-74.
23. GRAINGER, D. J., WITCHELL, C. M., and METCALFE, J. C. (1995). Tamoxifen elevates transforming growth factor-beta and suppresses diet-induced formation of lipid lesions in mouse aorta. Nat. Med. 1:1067-1073.
24. GRUOL, D. L. and CURRY, J. G. (1995). Calcium signals elicited by quisqualate in cultured Purkinje neurons show developmental changes in sensitivity to acute alcohol. Brain Res. 673:1-12.
25. HAMRE, K. M. and WEST, J. R. (1993). The effects of the timing of ethanol exposure during the brain growth spurt on the number of cerebellar Purkinje and granule cell nuclear profiles. Alcohol Clin. Exp. Res. 17:610-622.
26. HAUSER, K. F., GURWELL, J. A., and TURBEK, C. S. (1994). Morphine inhibits Purkinje cell survival and dendritic differentiation in organotypic cultures of mouse cerebellum. Exp. Neurol. 130:95-105.
27. HEATON, M. B., PAIVA, M., SWANSON, D. J., and WALKER, D. W. (1993). Modulation of ethanol neurotoxicity by nerve growth factor. Brain Res. 620:78-85.
28. HEATON, M. B., PAIVA, M., SWANSON, D. J., and WALKER, D. W. (1994). Responsiveness of cultured septal and hippocampal neurons to ethanol and neurotrophic substances. J. Neurosci. Res. 39:305-318.
29. HEATON, M. B., PAIVA, M., SWANSON, D. J., and WALKER, D. W. (1995). Alterations in responsiveness to ethanol and neurotrophic substances in fetal septohippocampal neurons following chronic prenatal ethanol exposure. Brain Res. Dev. Brain Res. 85:1-13.
30. HENDERSON, C. E., PHILLIPS, H. S., POLLOCK, R. A., DAVIES, A. M., LEMEULLE, C., ARMANINI, M., SIMPSON, L. C., MOFFET, B., VANDLEN, R. A., KOLIATSOS, V. E., and ROSENTHAL, A. (1994). GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266:1062-1064.
31. IACOPINO, A. M., RHOTEN, W. B., and CHRISTAKOS, S. (1990). Calcium binding protein (calbindin-D28k) gene expression in the developing and aging mouse cerebellum. Brain Res. Mol. Brain Res. 8:283-290.
32. JING, S., WEN, D., YU, Y., HOLST, P. L., LUO, Y., FANG, M., TAMIR, R., ANTONIO, L., HU, Z., CUPPLES, R., LOUIS, J.-C., HU, S., ALTROCK, B. W., and FOX, G. M. (1996). GDNF-induced activation of the Ret protein tyrosine kinase is mediated by GDNFR-a, a novel receptor for GDNF. Cell 85:1113-1124.
33. JONES, K. L. and SMITH, D. W. (1973). Recognition of the fetal alcohol syndrome in early infancy. Lancet ii:999-1001.
34. JONES, K. L., SMITH, D. W., ULLELAND, C. N., and STREISSGUTH, A. P. (1973). Pattern of malformation in offspring of chronic alcoholic mothers. Lancet i:1267-1271.
35. KLEIN, R. D., SHERMAN, D., HO, W. H., STONE, D., BENNETT, G. L., MOFFAT, B., VANDLEN, R., SIMMONS, L., GU, Q. M., HONGO, J. A., DEVAUX, B., POULSEN, K., ARMANINI, M., NOZAKI, C., ASAI, N., GODDARD, A., PHILLIPS, H., HENDERSON, C. E., TAKAHASHI, M., and ROSENTHAL, A. (1997). A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature 387:717-721.
36. KOTZBAUER, P. T., LAMPE, P. A., HEUCKEROTH, R. O., GOLDEN, J. P., CREEDON, D. J., JOHNSON, E. M., JR., and MILBRANDT, J. (1996). Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature 384:467-470.
37. LIN, L. F., DOHERTY, D. H., LILE, J. D., BEKTESH, S., and COLLINS, F. (1993). GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260:1130-1132.
38. LINDHOLM, D., CASTREN, E., TSOULFAS, P., KOLBECK, R., BERZAGHI, M. da-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.
39. LUO, J., WEST, J. R., and PANTAZIS, N. J. (1996). Ethanol exposure reduces the density of the low affinity nerve growth factor receptor (p75) on pheochromocytoma (PC12) cells. Brain Res. 737:34-44.
40. MARCUSSEN, B. L., GOODLETT, C. R., MAHONEY, J. C., and WEST, J. R. (1994). Developing rat Purkinje cells are more vulnerable to alcohol-induced depletion during differentiation than during neurogenesis. Alcohol 11:147-156.
41. MARSHALL, C. J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
42. MATTSON, M. P., RYCHLIK, B., CHU, C., and CHRISTAKOS, S. (1991). Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron 6:41-51.
43. MEYER, L. S., KOTCH, L. E., and RILEY, E. P. (1990). Alterations in gait following ethanol exposure during the brain growth spurt in rats. Alcohol Clin. Exp. Res. 14:23-27.
44. MICHAELIS, M. L. and MICHAELIS, E. K. (1994). Effects of ethanol on NMDA receptors in brain: possibilities for Mg(2+)-ethanol interactions. Alcohol Clin. Exp. Res. 18:1069-1075.
45. MILLER, M. W. and RIECK, R. W. (1993). Effects of chronic ethanol administration on acetylcholinesterase activity in the somatosensory cortex and basal forebrain of the rat. Brain Res. 627:104-112.
46. MIRANDA, R., SOHRABJI, F., SINGH, M., and TORAN-ALLERAND, D. (1996). Nerve growth factor (NGF) regulation of the estrogen receptors in explant cultures of the developing forebrain. J. Neurobiol. 31:77-87.
47. MOUNT, H. T. J., DEAN, D. O., ALBERCH, J., DREYFUS, C. F., and BLACK, I. B. (1995). Glial cell line-derived neurotrophic factor promotes the survival and morphologic differentiation of Purkinje cells. Proc. Natl. Acad. Sci. 92:9092-9096.
48. NAPPER, R. M. A. and WEST, J. R. (1995). Permanent neuronal cell loss in the cerebellum of rats exposed to continuous low blood alcohol levels during the brain growth spurt. J. Comp. Neurol. 362:283-292.
49. PANTAZIS, N. J., DOHRMAN, D. P., LUO, J., GOODLETT, C. R., and WEST, J. R. (1992). Alcohol reduces the number of pheochromocytoma (PC12) cells in culture. Alcohol 9:171-180.
50. POLLOCK, J. D. and RANE, S. G. (1996). p21ras signaling is necessary but not sufficient to mediate neurotrophin induction of calcium channels in PC12 cells. J. Biol. Chem. 271:8008-8014.
51. RAHMAN, H., KENTROTI, S., and VERNADAKIS, A. (1994). Neuroblast cell death in ovo and in culture: interaction of alcohol and neurotrophic factors. Neurochem. Res. 19:1495-1502.
52. RIPAMONTI, U. and REDDI, A. H. (1994). Periodontal regeneration: Potential role of bone morphogenetic proteins. J. Periodont. Res. 29:225-235.
53. SMITH, D. W. (1980). Alcohol effects on the fetus. Prog. Clin. Biol. Res. 36:73-82.
54. SOFRONIEW, M. V., COOPER, J. D., SVENDSEN, C. N., CROSSMAN, P., IP, N. Y., LINDSAY, R. M., ZAFRA, F., and LINDHOLM, D. (1993). Atrophy but not death of adult septal cholinergic neurons after ablation of target capacity to produce mRNAs for NGF, BDNF, and NT3. J. Neurosci. 13:5263-5276.
55. SPRINGER, J. E., MU, X., BERGMANN, L. W., and TROJANOWSKI, J. Q. (1994). Expression of GDNF mRNA in rat and human nervous tissue. Exp. Neurol. 127:167-170.
56. STRATTON, K., HOWE, C., and BATTAGLIA, F. (1996). Fetal Alcohol Syndrome. Diagnosis, Epidemiology, Prevention, and Treatment. Institute of Medicine, National Academy Press, Washington, DC.
57. TAZI, A., LE BRAS, S., LAMGHITNIA, H. O., VINCENT, J. D., CZERNICHOW, P., and SCHARFMANN, R. (1996). Neurotrophin-3 increases intracellular calcium in a rat insulin-secreting cell line through its action on a functional TrkC receptor. J. Biol. Chem. 271:10154-10160.
58. TORAN-ALLERAND, C. D. (1990). The brain slicer: anatomical precision for organotypic explant culture. Brain Res. Bull. 24:565-568.
59. TREANOR, J. J. S., GOODMAN, L., DE SAUVAGE, F., STONE, D. M., POULSEN, K. T., BECK, C. D., GRAY, C., ARMANINI, M. P., POLLOCK, R. A., HEFTI, F., PHILLIPS, H. S., GODDARD, A., MOORE, M. W., BUJ-BELLO, A., DAVIES, A. M., ASAI, N., TAKAHASHI, M., VANDLEN, R., HENDERSON, C. E., and ROSENTHAL, A. (1996). Characterization of a multicomponent receptor for GDNF. Nature 382:80-83.
60. TRUPP, M., ARENAS, E., FAINZILBER, M., NILSSON, A.-S., SIEBER, B.-A., GRIGORIOU, M., KILKENNY, C., SALAZAR-GRUESO, E., PACHNIS, V., ARUMAE, U., SARIOLA, H., SAARMA, M., and IBANEZ, C. F. (1996). Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature 381:785-793.
61. TRUPP, M., BELLUARDO, N., FUNAKOSHI, H., and IBANEZ, C. F. (1997). Complementary and overlapping expression of glial cell line-derived neurotrophic factor (GDNF), c-ret proto-oncogene, and GDNF receptor-a indicates multiple mechanisms of trophic actions in the adult rat CNS. J. Neurosci. 17:3554-3567.
62. VAN ELDIK, L. J., ZENDEGUI, J. G., MARSHAK, D. R., and WATTERSON, D. M. (1982). Calcium binding proteins and the molecular basis of calcium action. Int. Rev. Cytol. 77:1-10.
63. VAN WEERING, D. H., MEDEMA, J. P., VAN PUIJENBROEK, A., BURGERING, B. M., BAAS, P. D., and BOS, J. L. (1995). Ret receptor tyrosine kinase activates extracellular signal-regulated kinase 2 in SK-N-MC cells. Oncogene 11:2207-2214.
64. WEST, J. R., CHEN, W.-J. A., and PANTAZIS, N. J. (1994). Fetal alcohol syndrome: the vulnerability of the developing brain and possible mechanisms of damage. Metab. Brain Dis. 9:291-322.