Exposure of astrocytes to thrombin reduces levels of the metabotropic glutamate receptor mGLuR5

Journal of Neurochemistry

Volumn 67, Issue 4, 1996, Pages 1435-1447

  Miller, Stephan ^a,d   Sehati, Nouzhan ^a   Romano, Carmelo ^c   Cotman, Carl W ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Actin; Astrocytes; Metabotropic glutamate receptor; mGluR5; Phosphoinositide; Thrombin; Transforming growth factor

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; BETA ACTIN; GLUTAMATE RECEPTOR; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; THROMBIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN INJURY; CELL PROTECTION; NEUROTRANSMISSION; NONHUMAN; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL; RAT; RECEPTOR DENSITY; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0029790022     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1996.67041435.x     Document Type: Article

References (83)

1. 2+ signal transduction. J. Biol. Chem. 267, 13361-13368.
2. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., Shibuya M., and Fukami Y. (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262, 5592-5595.
3. 12 requirement for thrombin-stimulated gene expression and DNA synthesis in 1321N1 astrocytoma cells. J. Biol. Chem. 270, 20073-20077.
4. Baghdassarian D., Toru-Delbauffe D., Gavaret J. M., and Pierre M. (1993) Effects of transforming growth factor-beta 1 on the extracellular matrix and cytoskeleton of cultured astrocytes. Glia 7, 193-202.
5. Beecher K. L., Andersen T. T., Fenton J. N. 2nd, and Festoff B. W. (1994) Thrombin receptor peptides induce shape change in neonatal murine astrocytes in culture. J. Neurosci. Res. 37, 108-115.
6. Bokoch G. M., Katada T., Northup J. K., Hewlett E. L., and Gilman A. G. (1983) Identification of the predominant substrate for ADP-ribosylation by islet activating protein. J. Biol. Chem. 258, 2072-2075.
7. Burdick D., Soreghan B., Kwon M., Kosmoski J., Knauer M., Henschen A., Yates J., Cotman C., and Glabe C. (1992) Assembly and aggregation properties of synthetic Alzheimer's A4/beta amyloid peptide analogs. J. Biol. Chem. 267, 546-554.
8. Cavanaugh K. P., Gurwitz D., Cunningham D. D., and Bradshaw R. A. (1990) Reciprocal modulation of astrocyte stellation by thrombin and protease nexin-1. J. Neurochem. 54, 1735-1743.
9. Chen J., Ishii M., Wang L., Ishii K., and Coughlin S. R. (1994) Thrombin receptor activation. Confirmation of the intramolecular tethered liganding hypothesis and discovery of an alternative intermolecular liganding mode. J. Biol. Chem. 269, 16041-16045.
10. Chomczynski P. and Sacchi N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
11. Chuong C. M. (1990) Differential roles of multiple adhesion molecules in cell migration: granule cell migration in cerebellum. Experientia 46, 892-899.
12. Condorelli D. F., Dell'Albani P., Amico C., Casabona G., Genazzani A. A., Sortino M. A., and Nicoletti F. (1992) Development profile of metabotropic glutamate receptor mRNA in rat brain. Mol. Pharmacol. 41, 660-664.
13. Condorelli D. F., Dell'Albani P., Amico C., Kaczmarek L., Nicoletti F., Lukasiuk K., and Giuffrida Stella A. M. (1993) Induction of primary response genes by excitatory amino acid receptor agonists in primary astroglial cultures. J. Neurochem. 60, 877-885.
14. Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., and Smith S. J. (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470-473.
15. Coughlin S. R. (1994) Molecular mechanisms of thrombin signaling. Semin. Hematol. 31, 270-277.
16. Cunningham D. D., Pulliam L., and Vaughan P. J. (1993) Protease nexin-1 and thrombin: injury-related processes in the brain. Thromb. Haemost. 70, 168-171.
17. Dani J. W., Chernjavsky A., and Smith S. J. (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8, 429-440.
18. Dihanich M., Kaser M., Reinhard E., Cunningham D., and Monard D. (1991) Prothrombin mRNA is expressed by cells of the nervous system. Neuron 6, 575-581.
19. Ehrenreich H., Costa T., Clouse K. A., Pluta R. M., Ogino Y., Coligan J. E., and Burd P. R. (1993) Thrombin is a regulator of astrocytic endothelin-1. Brain Res. 600, 201-207.
20. Fantus I. G., Kadota S., Deragon G., Foster B., and Posner B. I. (1989) Pervanadate [peroxide(s) of vanadate] mimics insulin action in rat adipocytes via activation of the insulin receptor tyrosine kinase. Biochemistry 28, 8864-8871.
21. Finkbeiner S. (1992) Calcium waves in astrocytes - filling in the gaps. Neuron 8, 1101-1108.
22. Flott B. and Seifert W. (1991) Characterization of glutamate uptake systems in astrocyte primary cultures from rat brain. Glia 4, 293-304.
23. Garcia-Morales P., Minami Y., Luong E., Klausner R. D., and Samelson L. E. (1990) Tyrosine phosphorylation in T cells is regulated by phosphatase activity: studies with phenylarsine oxide. Proc. Natl Acad. Sci. USA 87, 9255-9259.
24. 2+ influx into astrocytes. Proc. Natl. Acad. Sci. USA 87, 3454-3458.
25. Grabham P. and Cunningham D. D. (1995) Thrombin receptor activation stimulates astrocyte proliferation and reversal of stellation by distinct pathways: involvement of tyrosine phosphorylation. J. Neurochem. 64, 583-591.
26. Grand R. J., Grabham P. W., Gallimore M. J., and Gallimore P. H. (1989) Modulation of morphological differentiation of human neuroepithelial cells by serine proteases: independence from blood coagulation. EMBO J. 8, 2209-2215.
27. Gurwitz D. and Cunningham D. D. (1988) Thrombin modulates and reverses neuroblastoma neurite outgrowth. Proc. Natl. Acad. Sci. USA 85, 3440-3444.
28. Hidaka H., Inagaki M., Kawamoto S., and Sasaki Y. (1984) Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23, 5036-5041.
29. Honma Y., Okabe-Kado J., Hozumi M., Uehara Y., and Mizuno S. (1989) Induction of erythroid differentiation of K562 human leukemic cells by herbimycin A, an inhibitor of tyrosine kinase activity. Anticancer Res. 12, 189-192.
30. Ikeda T. and Puro D. G. (1995) Regulation of retinal glial cell proliferation by antiproliferative molecules. Exp. Eye Res. 60, 435-443.
31. Jalink K. and Moolenaar W. H. (1992) Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. J. Cell Biol. 118, 411-419.
32. Jalink K., Van Corven E. J., Hengeveld T., Morii N., Narumiya S., and Moolenaar W. H. (1994) Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801-810.
33. Joly C., Gomeza J., Brabet I., Curry K., Bockaert J., and Pin J. P. (1995) Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mG1uR1. J. Neurosci. 15, 3970-3981.
34. Joseph S. and MacDermot J. (1992) Thrombin promotes actin polymerization in U937 human monocyte-macrophage cells. Analysis of the signalling mechanisms mediating actin polymerization. Biochem. J. 286, 945-950.
35. Junier M. P., Ma Y. J., Costa M. E., Hoffman G., Hill D. F., and Ojeda S. R. (1991) Transforming growth factor-α contributes to the mechanism by which hypothalamic injury induces precocious puberty. Proc. Natl. Acad. Sci. USA 88, 9743-9747.
36. Junier M. P., Coulpier M., Le F. N., Cadusseau J., Suzuki F., Peschanski M., and Dreyfus P. A. (1994) Transforming growth factor-α (TGFα) expression in degenerating motoneurons of the murine mutant wobbler: a neuronal signal for astrogliosis? J. Neurosci. 14, 4206-4216.
37. Kornblum H. I., Chugani H. T., Tatsukawa K., and Gall C. M. (1994) Cerebral hemidecortication alters expression of transforming growth factor-α mRNA in the neostriatum of developing rats. Brain Res. Mol. Brain Res. 21, 107-114.
38. Lee R. K., Jimenez J., Cox A. J., and Wurtman R. J. (1996) Metabotropic glutamate receptors regulate APP processing in hippocampal neurons and cortical astrocytes derived from fetal rats. Ann. NY Acad. Sci. 777, 338-343.
39. Liotta L. A., Goldfarb R. H., Brundage R., Siegal G. P., Terranova V., and Garbisa S. (1981) Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res. 41, 4629-4636.
40. Liu C. and Hermann T. E. (1978) Characterization of ionomycin as a calcium ionophore. J. Biol. Chem. 253, 5892-5894.
41. Masu M., Tanabe Y., Tsuchida K., Shigemoto R., and Nakanishi S. (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349, 760-765.
42. McCarthy K. D. and de Vellis J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral cultures. J. Cell Biol. 85, 890-902.
43. Miller S., Cotman C. W., and Bridges R. J. (1992) 1-Aminocyclo-pentane-trans-1,3-dicarboxylic acid induces glutamine synthetase activity in cultured astrocytes. J. Neurochem. 58, 1967-1970.
44. Miller S., Romano C., and Cotman C. W. (1995) Growth factor upregulation of a phosphoinositide-coupled metabotropic glutamate receptor in cortical astrocytes. J. Neurosci. 15, 6103-6109.
45. Minakami R., Katsuki F., and Sugiyama H. (1993) A variant of metabotropic glutamate receptor subtype 5: an evolutionally conserved insertion with no termination codon. Biochem. Biophys. Res. Commun. 194, 622-627.
46. Monard D. (1988) Cell-derived proteases and protease inhibitors as regulators of neurite outgrowth. Trends Neurosci. 11, 541-544.
47. Nakanishi S., and Masu M. (1994) Molecular diversity and functions of glutamate receptors. Annu. Rev. Biophys. Biomol. Struct. 23, 319-348.
48. Nelson R. B. and Siman R. (1990) Thrombin and its inhibitors regulate morphological and biochemical differentiation of astrocytes in vitro. Brain Res. Dev. Brain Res. 54, 93-104.
49. Neveu I., Jehan F., Jandrot-Perrus M., Wion D., and Brachet P. (1993) Enhancement of the synthesis and secretion of nerve growth factor in primary cultures of glial cells by proteases: a possible involvement of thrombin. J. Neurochem. 60, 858-867.
50. Niclou S., Suidan H. S., Brown-Luedi M., and Monard D. (1994) Expression of the thrombin receptor mRNA in rat brain. Cell. Mol. Biol. 40, 421-428.
51. Nicoletti F., Magrì G., Ingrao F., Bruno V., Catania M. V., Dell'Albani P., Condorelli D. F., and Avola R. (1990) Excitatory amino acids stimulate inositol phospholipid hydrolysis and reduce proliferation in cultured astrocytes. J. Neurochem. 54, 771-777.
52. Nishino A., Suzuki M., Ohtani H., Motohashi O., Umezawa K., Nagura H., and Yoshimoto T. (1993) Thrombin may contribute to the pathophysiology of central nervous system injury. J. Neurotrauma 10, 167-179.
53. Nudel U., Zakut R., Shani M., Neuman S., Levy Z., and Yaffe D. (1983) The nucleotide sequence of the rat cytoplasmic β-actin gene. Nucleic Acids Res. 11, 1759-1771.
54. Perraud F., Besnard F., Sensenbrenner M., and Labourdette G. (1987) Thrombin is a potent mitogen for rat astroblasts but not for oligodendroblasts and neuroblasts in primary culture. Int. J. Dev. Neurosci. 5, 181-188.
55. Phillips P. G. (1994) Thrombin-induced alterations in endothelial cell cytoarchitectural and functional properties. Semin. Thromb. Hemost. 20, 417-425.
56. Pike C. J., Vaughan P. J., Cunningham D. D., and Cotman C. W. (1996) Thrombin attenuates neuronal cell death and modulates astrocyte reactivity induced by β-amyloid in vitro. J. Neurochem. 66, 1374-1382.
57. Pin J. P. and Duvoisin R. (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34, 1-26.
58. Pin J. P., Waeber C., Prezeau L., Bockaert J., and Heinemann S. F. (1992) Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proc. Natl. Acad. Sci. USA 89, 10331-10335.
59. Plata-Salaman C. R. (1991) Epidermal growth factor and the nervous system. Peptides 12, 653-663.
60. Romano C., Sesma M. A., MacDonald C., O'Malley K., van den Pol A. N., and Olney J. W. (1995) Distribution of metabotropic glutamate receptor mG1uR5 immunoreactivity in the rat brain. J. Comp. Neurol. 355, 455-469.
61. Romano C., van den Pol A. N., and O'Malley K. L. (1996) Enhanced early developmental expression of the metabotropic glutamate receptor mG1uR5 in rat brain: protein, mRNA splice variants, and regional distribution. J. Comp. Neurol. 367, 403-412.
62. Ruegg U. T. and Burgess G. M. (1989) Staurosporine, K252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends Biochem. Sci. 10, 218-220.
63. Sakamoto T., Hinton D. R., Sakamoto H., Gopalakrishna R., Ryan S. J., and McDonnell P. J. (1995) Thrombin induced cytoskeletal change in cultured bovine corneal endothelial cells mediated via protein kinase C pathway. Curr. Eye Res. 14, 35-45.
64. Sawada M., Suzumura A., Ohno K., and Marunouchi T. (1993) Regulation of astrocyte proliferation by prostaglandin E2 and the alpha subtype of protein kinase C. Brain Res. 613, 67-73.
65. Schoepp D. D. (1994) Novel functions for subtypes of the metabotropic glutamate receptors. Neurochem. Int. 24, 439-449.
66. Schousboe A. and Hertz L. (1981) Role of astroglial cells in glutamate homeostasis. Adv. Biochem. Psychopharmacol. 27, 103-113.
67. Shen T. Y. and Winter C. A. (1977) Chemical and biological studies on indomethacin, sulindac and their analogs. Adv. Drug Res. 12, 90-245.
68. Shigemoto R., Nakanishi S., and Mizuno N. (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mG1uR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J. Comp. Neurol. 322, 121-135.
69. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., and Klenk D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
70. 2+ homeostasis and sensitivity to glucose deprivation-induced injury. J. Neurosci. 15, 5840-5850.
71. Soifer S. J., Peters K. G., O'Keefe J., and Coughlin S. R. (1994) Disparate temporal expression of the prothrombin and thrombin receptor genes during mouse development. Am. J. Pathol. 144, 60-69.
72. Staddon J. M., Herrenknecht K., Smales C., and Rubin L. L. (1995) Evidence that tyrosine phosphorylation may increase tight junction permeability. J. Cell Sci. 108, 609-619.
73. Suidan H. S., Stone S. R., Hemmings B. A., and Monard D. (1992) Thrombin causes neurite retraction in neuronal cells through activation of cell surface receptors. Neuron 8, 363-375.
74. Tanabe Y., Masu M., Ishii T., Shigemoto R., and Nakanishi S. (1992) A family of metabotropic glutamate receptors. Neuron 8, 169-179.
75. Thurston G. and Turner D. (1994) Thrombin-induced increase of F-actin in human umbilical vein endothelial cells. Microvasc. Res. 47, 1-20.
76. 2+/calmodulin protein kinase II. J. Biol. Chem. 265, 4315-4320.
77. van den Pol A. N., Romano C., and Ghosh P. (1995) Metabotropic glutamate receptor mG1uR5 subcellular distribution and developmental expression in hypothalamus. J. Comp. Neurol. 362, 134-150.
78. Van Obberghen-Schilling E. and Pouyssegur J. (1993) Signaling pathways of the thrombin receptor. Thromb. Haemost. 70, 163-167.
79. Vaughan P. J., Pike C. J., Cotman C. W., and Cunningham D. D. (1995) Thrombin receptor activation protects neurons and astrocytes from cell death produced by environmental insults. J. Neurosci. 15, 5389-5401.
80. Vouret-Craviari V., Auberger P., Pouyssegur J., and Van Obberghen-Schilling E. (1995) Distinct mechanisms regulate 5-HT2 and thrombin receptor desensitization. J. Biol. Chem. 270, 4813-4821.
81. Vu T. K., Hung D. T., Wheaton V. I., and Coughlin S. R. (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64, 1057-1068.
82. Weinstein J. R., Gold S. J., Cunningham D. D., and Gall C. M. (1995) Cellular localization of thrombin receptor mRNA in rat brain: expression by mesencephalic dopaminergic neurons and codistribution with prothrombin mRNA. J. Neurosci. 15, 2906-2919.
83. Wu H., Qu P., Friedman W. J., Black I. B., and Dreyfus C. F. (1995) The regulation of basal forebrain (BF) astrocyte trophic function by depolarizing signals. Soc. Neurosci. Abstr. 21, 304.