Wnt signaling induces GLT-1 expression in rat C6 glioma cells

Journal of Neurochemistry

Volumn 73, Issue 3, 1999, Pages 1012-1023

  Palos, Teresa P ^a,b   Zheng, Shuang ^a   Howard, Bruce D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aberrant RNA processing; Glutamate transporter; Lef 1 Tcf

Indexed keywords

CARRIER PROTEIN; GLUTAMIC ACID;

AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; GLIOMA CELL; IMMUNOCYTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTO ONCOGENE; RAT; SIGNAL TRANSDUCTION;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BLOTTING, NORTHERN; BLOTTING, WESTERN; GLIOMA; IMMUNOHISTOCHEMISTRY; PROTO-ONCOGENE PROTEINS; RATS; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; WNT PROTEINS; WNT1 PROTEIN; ZEBRAFISH PROTEINS;

EID: 0032818544     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0731012.x     Document Type: Article

References (66)

1. Amara S. G. and Arriza J. L. (1993) Neurotransmitter transporters: three distinct gene families. Curr. Opin. Neurobiol. 3, 337-344.
2. Aoki M., Lin C. L. G., Rothstein J. D., Gellar B. A., Hosler B. A., Munsat T. L., Horvitz H. R., and Brown R. H. (1998) Mutations in the glutamate transporter EAAT2 gene do not cause abnormal EAAT2 transcripts in amyotrophic lateral sclerosis. Ann. Neurol. 43, 645-653.
3. Arriza J. L., Fairman W. A., Wadiche J. I., Murdoch G. H., Kavanaugh M. P., and Amara S. G. (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci. 14, 5559-5569.
4. Arriza J. L., Eliasof S., Kavanaugh M. P., and Amara S. G. (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc. Natl. Acad. Sci. USA 94, 4155-4160.
5. Bergles D. E. and Jahr C. E. (1997) Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19, 1297-1308.
6. Bristol L. A. and Rothstein J. D. (1996) Glutamate transporter gene expression in amyotrophic lateral sclerosis motor cortex. Ann. Neurol. 39, 676-679.
7. Brodie C. and Vernadakis A. (1991) Muscle-derived factors induce proliferation and astrocytic phenotypic expression in C6 glial cells. Glia 4, 269-275.
8. Cadigan K. M. and Nusse R. (1997) Wnt signaling: a common theme in animal development. Genes Dev. 11, 3286-3305.
9. Casado M., Bendahan A., Zafra F., Danbolt N. C., Aragon C., Giménez C., and Kanner B. I. (1993) Phosphorylation and modulation of brain glutamate transporters by protein kinase C. J. Biol. Chem. 268, 27313-27317.
10. Chabot B. (1996) Directing alternative splicing: cast and scenarios. Trends Genet. 12, 472-478.
11. Chaudhry F. A., Lehre K. P., Campagne M. V. L., Otterson O. P., Danbolt N. C., and Storm-Mathisen J. (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15, 711-720.
12. Chew S. L. (1997) Alternative splicing of mRNA as a mode of endocrine regulation. Trends Endocrinol. Metab. 8, 405-413.
13. Chirgwin J. M., Przybyla A. E., MacDonald R. J., and Rutter W. J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294-5299.
14. Dehnes Y., Chaudhry F. A., Ullensvang K., Lehre K. P., StormMathisen J., and Danbolt N. C. (1998) The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J. Neurosci. 18, 3606-3619.
15. +-dependent glutamate transport activity in synaptosomes, C6 glioma, and Xenopus oocytes expressing excitatory amino acid carrier 1 (EAAC1). Mol. Pharmacol. 49, 465-473.
16. Fairman W. A., Vandenberg R. J., Arriza J. L., Kavanaugh M. P., and Amara S. G. (1995) An excitatory amino acid transporter with properties of a ligand-gated chloride channel. Nature 375, 599-603.
17. Faivre-Bauman A., Rossier J., and Benda P. (1974) Glutamate accumulation by a clone of glial cells. Brain Res. 76, 371-375.
18. Gegelashvili G. and Schousboe A. (1997) High affinity glutamate transporters: regulation of expression and activity. Mol. Pharmacol. 52, 6-15.
19. Goya L., Peng P. T., Aliabadi S., and Timiras P. S. (1996) Effect of growth factors on the in vitro growth and differentiation of early and late passage C6 glioma cells. Int. J. Dev. Neurosci. 14, 409-417.
20. Harlow E. and Lane D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
21. Harpold M. M., Evans R. M., Saiditt-Georgieff M., and Darnell J. E. (1979) Production of mRNA in Chinese hamster cells: relationship of the rate of synthesis to the cytoplasmic concentration of nine specific mRNA sequences. Cell 17, 1025-1035.
22. +-dependent glutamate uptake in rat hippocampal astrocyte cultures. J. Neurochem. 67, 277-286.
23. Haugeto Ø., Ullensvang K., Levy L. M., Chaudry F. A., Honoré T., Nielson M., Lehre K. P., and Danbolt N. C. (1996) Brain glutamate transporter proteins form homomultimers. J. Biol. Chem. 271, 27715-27722.
24. Henn F. A., Goldstein M. N., and Hamberger A. (1974) Uptake of the neurotransmitter candidate glutamate by glia. Nature 249, 663-664.
25. Hsu S. C., Galceran J., and Grosschedl R. (1998) Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with β-catenin. Mol. Cell. Biol. 18, 4807-4818.
26. Ikeya M., Lee S. M. K., Johnson J. E., McMahon A. P., and Takada S. (1997) Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966-970.
27. Kanai Y. and Hediger M. A. (1992) Primary structure and functional characterization of a high affinity glutamate transporter. Nature 360, 467-471.
28. Keller J. N., Pang Z., Geddes J. W., Begley J. G., Germeyer A., Waeg G., and Mattson M. P. (1997) Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 69, 273-284.
29. -/- colon carcinoma. Science 275, 1784-1787.
30. Lee K., Kentroti S., Billie H., Brace C., and Vernadakis A. (1992) Comparative biochemical, morphological, and immunocytochemical studies between C6 glial cells of early and late passages and advanced passages of glial cells derived from aged mouse cerebral hemispheres. Glia 6, 245-257.
31. Lehre K. P., Levy L. M., Ottersen O. P., Storm-Mathisen J., and Danbolt N. C. (1995) Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J. Neurosci. 15, 1835-1853.
32. Lin C. L. G., Bristol L. A., Jin L., Dykes-Hoberg M., Crawford T., Clawson L., and Rothstein J. D. (1998) Aberrant RNA processing in a neurodegenerative disease: the cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron 20, 589-602.
33. Mason J. O., Kitajewski J., and Varmus H. E. (1992) Mutational analysis of mouse Wnt-1 identifies two temperature-sensitive alleles and attributes of Wnt-1 protein essential for transformation of a mammary cell line. Mol. Biol. Cell 3, 521-533.
34. McMahon A. P. and Bradley A. (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62, 1073-1085.
35. Mennerick S. and Zorumski C. F. (1994) Glial contributions to excitatory neurotransmission in cultured hippocampal cells. Nature 368, 59-62.
36. Meyer T., Münch C., Knappenberger B., Liebau S., Völkel H., and Ludolph A. C. (1998) Alternative splicing of the glutamate transporter EAAT2 (GLT-1). Neurosci. Lett. 241, 68-70.
37. Muller A. J., Young J. C., Pendergast A. M., Pondel M., Landau N. R., Littman D. R., and Witte O. N. (1991) BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol. 11, 1785-1792.
38. Münch C., Schwalenstöcker B., Knappenberger B., Liebau S., Völkel H., Ludolph A. C., and Meyer T. (1998) 5′-Heterogeneity of the human excitatory amino acid transporter cDNA EAAT2 (GLT-1). Neuroreport 9, 1295-1297.
39. Novak A., Hsu S. C., Leung-Hagesteijn C., Radeva G., Papkoff J., Montesano R., Roskelley C., Grosschedl R., and Dedhar S. (1998) Cell adhesion and the integrin-linked kinase regulate the LEF-1 and β-catenin signaling pathways. Proc. Natl. Acad. Sci. USA 95, 4374-4379.
40. Palos T. P., Ramachandran B., Boado R., and Howard B. D. (1996) Rat C6 and human astrocytic tumor cells express a neuronal type of glutamate transporter. Brain Res. Mol. Brain Res. 37, 297-303.
41. Parker K. K., Norenberg M. D., and Vernadakis A. (1980) "Transdifferentiation" of C6 glial cells in culture. Science 208, 179-181.
42. Parr B. A., Shea M. J., Vassileva G., and McMahon A. P. (1993) Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247-261.
43. Pines G., Danbolt N. C., Bjørås M., Zhang Y., Bendahan A., Eide L., Koepsell H., Storm-Mathisen J., Seeberg E., and Kanner B. I. (1992) Cloning and expression of a rat brain L-glutamate transporter. Nature 360, 464-467. [Corrected sequence in Kanner B. I. (1993) Glutamate transporters from brain. FEBS Lett. 325, 95-99.]
44. Porfiri E., Rubinfeld B., Albert I., Hovanes K., Waterman M., and Polakis P. (1997) Induction of a β-catenin-LEF-1 complex by Wnt-1 and transforming mutants of β-catenin. Oncogene 15, 2833-2839.
45. Prince Miller H., Levey A. I., Rothstein J. D., Tzingounis A. V., and Conn P. J. (1997) Alterations in glutamate transporter protein levels in kindling-induced epilepsy. J. Neurochem. 68, 1564-1570.
46. Ramachandran B., Houben K., Rozenberg Y. Y., Haigh J. R., Varpetian A., and Howard B. D. (1993) Differential expression of transporters for norepinephrine and glutamate in wild type, variant, and Wnt-1-expressing PC12 cells. J. Biol. Chem. 268, 23891-23897.
47. Rao V. L. R., Başkaya M. K., Doǧan A., Rothstein J. D., and Dempsey R. J. (1998) Traumatic brain injury down-regulates glial glutamate transporter (GLT-1 and GLAST) proteins in rat brain. J. Neurochem. 70, 2020-2027.
48. Rothstein J. D. (1996) Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin. Neurosci. 3, 348-359.
49. Rothstein J. D., Martin L. J., and Kuncl R. W. (1992) Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N. Engl. J. Med. 326, 1464-1468.
50. Rothstein J. D., Martin L., Levey A. I., Dykes-Hoberg M., Jin L., Wu D., Nash N., and Kuncl R. W. (1994) Localization of neuronal and glial glutamate transporters. Neuron 13, 713-725.
51. Rothstein J. D., van Kammen M., Levey A. I., Martin L. J., and Kuncl R. W. (1995) Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann. Neurol. 38, 73-84.
52. Rothstein J. D., Dykes-Hoberg M., Pardo C. A., Bristol L. A., Jin L., Kuncle R. W., Kanai Y., Hediger M. A., Wang Y., Schielke J. P., and Welty D. F. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675-686.
53. Sarantis M., Ballerini L., Miller B., Silver R. A., Edwards M., and Attwell D. (1993) Glutamate uptake from the synaptic cleft does not shape the decay of the non-NMDA component of the synaptic current. Neuron 11, 541-549.
54. Shackleford G. M. and Varmus H. E. (1987) Expression of the proto-oncogene int-1 is restricted to postmeiotic male germ cells and the neural tube of mid-gestational embryos. Cell 50, 89-95.
55. Silbert S. W. and Goldstein M. N. (1972) Drug-induced differentiation of a rat glioma in vitro. Cancer Res. 32, 1422-1427.
56. +-dependent glutamate/aspartate transporter from rat brain. Proc. Natl. Acad. Sci. USA 89, 10955-10959.
57. Tanaka K., Watase K., Manabe T., Yamada K., Watanabe M., Takahashi K., Iwama H., Nishikawa T., Ichihara N., Kikuchi T., Okuyama S., Kawashima N., Hori S., Takimoto M., and Wada K. (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276, 1699-1702.
58. Thomas K. R. and Capecchi M. R. (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346, 847-850.
59. Thomas P. S. (1980) Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. USA 77, 5201-5205.
60. Tong G. and Jahr C. E. (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13, 1195-1203.
61. Torp R., Lekieffre D., Levy L. M., Haug F. M., Danbolt N. C., Meldrum B. S., and Ottersen O. P. (1995) Reduced postischemic expression of a glial glutamate transporter, GLT-1, in the rat hippocampus. Exp. Brain Res. 103, 51-58.
62. Utsunomiya-Tate N., Endou H., and Kanai Y. (1997) Tissue specific variants of glutamate transporter GLT-1. FEBS Lett. 416, 312-316.
63. Wang J. and Manley J. L. (1997) Regulation of pre-mRNA splicing in metazoa. Curr. Opin. Genet. Dev. 7, 205-211.
64. Wilkinson D. G., Bailes J. A., and McMahon A. P. (1987) Expression of the proto-oncogene int-1 is restricted to specific neural cells in the developing mouse embryo. Cell 50, 79-88.
65. Young C. S., Kitamura M., Hardy S., and Kitajewski J. (1998) Wnt-1 induces growth, cytosolic β-catenin, and Tcf/Lef transcriptional activation in Rat-1 fibroblasts. Mol. Cell. Biol. 18, 2474-2485.
66. Zheng S., Ramachandran B., Haigh J. R., Palos T. P., Steger K., and Howard B. D. (1996) The induction of ret by Wnt-1 in PC12 cells is atypically dependent on continual Wnt-1 expression. Oncogene 12, 555-562.