Integrins regulate neuronal neurotrophin gene expression through effects on voltage-sensitive calcium channels

Neuroscience

Volumn 118, Issue 4, 2003, Pages 925-940

  Gall, C M ^a,b   Pinkstaff, J K ^a,c   Lauterborn, J C ^a   Xie, Y ^a   Lynch, G ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Targeted Molecules   (United States)

Author keywords

Adhesion; Brain derived neurotrophic factor; c fos; Hippocampus; L type calcium channel; Nerve growth factor

Indexed keywords

ACTIN; AMYLOID PRECURSOR PROTEIN; ARGINYLGLYCYLASPARTIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; FIBROBLAST GROWTH FACTOR 1; GLYCYLARGINYLGLYCYLASPARTYLSERYLPROLINE; INTEGRIN; LIGAND; MESSENGER RNA; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; PROTEIN; PROTEIN 43; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM TRANSPORT; CELL ACTIVITY; CELL GROWTH; CELL MATURATION; CYTOSKELETON; ELECTRIC POTENTIAL; GENE CONTROL; GENE EXPRESSION; HIPPOCAMPUS; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; RNA ANALYSIS; SIGNAL TRANSDUCTION; SOLUBILITY;

EID: 0038404979     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00990-9     Document Type: Article

References (142)

1. Alpin A., Howe A., Alahari S., Juliano R. Signal transduction and signal modulation by cell adhesion receptors the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins . Pharmacol Rev. 50:1998;197-263.
2. Bahr B., Lynch G. Purification of an Arg-Gly-Asp selective matrix receptor from brain synaptic plasma membranes. Biochem J. 281:1992;137-142.
3. Bahr B.A. Long term hippocampal slices a model system for investigating synaptic mechanisms and pathologic processes . J Neurosci Res. 42:1995;294-305.
4. Bahr B.A. Integrin-type signaling has a distinct influence on NMDA-induced cytoskeletal disassembly. J Neurosci Res. 59:2000;827-832.
5. Bahr B.A., Staubli U., Xiao P., Chun D., Ji Z.-X., Esteban E.T., Lynch G. Arg-Gly-Asp-Ser-Selective adhesion and the stabilization of long-term potentiation pharmacological studies and the characterization of a candidate matrix receptor . J Neurosci. 17:1997;1320-1329.
6. Bence-Hanulec K., Marshall J., Blair L.A. Potentiation of neuronal L calcium channels by IGF-1 requires phosphorylation of the alpha 1 subunit on specific tyrosine residue. Neuron. 27:2000;121-131.
7. Bengzon J., Kokaia Z., Ernfors P., Kokaia M., Leanza G., Nilsson O.G., Persson H., Lindvall O. Regulation of neurotrophin and trkA, trkB and trkC tyrosine kinase receptor messenger RNA expression in kindling. Neuroscience. 53:1993;433-446.
8. Beumer K.J., Bohrbough J., Prokop A., Broadie K. A role for PS integrins in morphological growth and synaptic function at the postembryonic neuromuscular junction of Drosophila. Development. 126:1999;5833-5846.
9. ++ influx in pulmonary endothelial cells. Circ Res. 86:2000;456-462.
10. Bi X., Yong A.P., Zhou J., Ribak C.E., Lynch G. Rapid induction of intraneuronal neurofibrillary tangles in apolipoprotein E-deficient mice. Proc Natl Acad Sci USA. 98:2001;8832-8837.
11. Bi X., Zhou J., Lynch G., Gall C.M. Polarized distribution of α5 integrin in the dendrites of hippocampal and cortical neurons. J Comp Neurol. 435:2001;184-193.
12. Bishop J.F., Joahi G., Mueller G.P., Mouradian M.M. Localization of putative calcium-responsive regions in the rat BDNF gene. Mol Brain Res. 50:1997;154-164.
13. Bishop J.F., Mueller G.P., Mouradian M.M. Alternate 5′ exons in the rat brain-derived neurotrophic factor gene differential patterns of expression across brain regions . Mol Brain Res. 26:1994;225-232.
14. Bizon J.M., Lauterborn J.C., Isackson P.J., Gall C.M. Acidic fibroblast growth factor mRNA is expressed by basal forebrain and striatal cholinergic neurons. J Comp Neurol. 366:1996;379-389.
15. Buckley C.D., Pilling D., Henriquez N.V., Parsonage G., Threlfall K., Scheel-Toellner D., Simmons D.L., Akbar A.N., Lord J.M., Salmon M. RGD peptides induce apoptosis by direct caspase-3 activation. Nature. 397:1999;534-539.
16. Bugra K., Pollard H., Charton G., Moreau J., Ben-Ari Y., Khrestchatisky M. aFGF, bFGF and flg mRNAs show distinct patterns of induction in the hippocampus following kainate-induced seizures. Eur J Neurosci. 6:1994;58-66.
17. Burkin D.J., Gu M., Hodges B.L., Campanelli J.T., Kaufman S.J. A functional role for specific spliced variants of the alpha7beta1 integrin in acetylcholine receptor clustering. J Cell Biol. 143:1998;1067-1075.
18. Capaldi D., Rosario R., Esteban E.T., Bahr B.A. A 27-kDa matrix receptor from rat brain synaptosomes selective recognition of the Arg-Gly-Asp-Ser domain and unique resistance to calcium-dependent . Neurosci Res. 28:1997;275-279.
19. Castren E., Berninger B., Leingartner A., Lindholm D. Regulation of brain derived neurotrophic factor mRNA levels in hippocampus by neuronal activity. Prog Brain Res. 117:1998;57-64.
20. Castrén E., Pitkänen M., Sirviö J., Parsadanian A., Lindholm D., Thoenen H., Riekkinen P.J. The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport. 4:1993;895-898.
21. Chen G., Kolbeck R., Barde Y.A., Bonhoeffer T., Kossel A. Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation. J Neurosci. 19:1999;7983-7990.
22. Chun D., Gall C.M., Bi X., Lynch G. Evidence that integrins contribute to multiple stages in the consolidation of long term potentiation. Neuroscience. 105:2001;815-829.
23. Clark E., Brugge J. Integrins and signal transduction pathways. Science. 268:1995;233.
24. Collin C., Miyaguchi K., Segal M. Dendritic spine density and LTP induction in cultured hippocampal slices. J Neurophysiol. 77:1997;1614-1623.
25. Comelli M.C., Seren M.S., Guidolin D., Manev R.M., Favaron M., Rimland J.M., Canella R., Negro A., Manev H. Photochemical stroke and brain-derived neurotrophic factor (BDNF) mRNA expression. Neuroreport. 3:1992;473-476.
26. Cowie A., Ivanco T.L., Fahnestock M. Mouse NGF promoter upstream sequences do not affect gene expression in mouse fibroblasts. Mol Brain Res. 27:1994;58-62.
27. D'Mello S., Heinrich G. Nerve growth factor gene expression involvement of a downstream AP-1 element in basal and modulated transcription . Mol Cell Neurosci. 2:1991;157-167.
28. Damsky C.H., Werb Z. Signal transduction by integrin receptors for extracellular matrix cooperative processing of extracellular information . Curr Opin Cell Biol. 4:1992;772-781.
29. Davis M.J., Wu X., Nruiewicz T.R., Kawasaki J., Gui P., Hill M.A., Wilson E. Regulation of ion channels by integrins. Cell Biochem Biophys. 36:2002;41-66.
30. Dedhar S., Hannigan G. Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr Opin Cell Biol. 8:1996;657-669.
31. del Cerro S., Larson J., Oliver M., Lynch G. Development of hippocampal long-term potentiation is reduced by recently introduced calpain inhibitors. Brain Res. 530:1990;1-5.
32. Desmond N.L., Levy W.B. Synaptic correlates of associative potentiation/depression an ultrastructural study in the hippocampus . Brain Res. 265:1983;21-30.
33. Dixon J.E., McKinnon D. Expression of the trk gene family of neurotrophin receptors in prevertebral sympathetic ganglia. Dev Brain Res. 77:1994;177-182.
34. 3 (platelet GPIIb-IIIa). Cell. 65:1991;409-416.
35. Einheber S., Schnapp L., Salzer J., Cappiello Z., Milner T.A. The regional and ultrastructural distribution of the α8 integrin subunit in the developing and adult rat brain suggests a role in synaptic plasticity. J Comp Neurol. 370:1996;105-134.
36. Elliott R.C., Gall C.M. Changes in activating protein 1 (AP-1) composition correspond with the biphasic profile of nerve growth factor mRNA expression in rat following hilus lesion-induced seizures. J Neurosci. 20:2000;2142-2149.
37. Ernfors P., Wetmore C., Olson L., Persson H. Identification of cells in the rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron. 5:1990;511-526.
38. 2+ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J Neurosci. 22:2002;7177-7194.
39. Finkbeiner S. Calcium regulation of the brain-derived neurotrophic factor gene. Call Mol Life Sci. 57:2000;394-401.
40. Frey U., Frey S., Schollmeier F., Krug M. Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol. 490:1996;703-711.
41. Gall C. Regulation of brain neurotrophin expression by physiological activity. Trends Pharmacol Sci. 13:1992;401-403.
42. Gall C. Seizure-induced changes in neurotrophin expression implications for epilepsy . Exp Neurol. 124:1993;150-166.
43. Gall C., Isackson P.J. Limbic seizures increase neuronal production of mRNA for nerve growth factor. Science. 245:1989;758-760.
44. Gall C., Lauterborn J., Bundman M., Murray K., Isackson P.J. Seizures and the regulation of growth factor and neuropeptide gene expression in brain. Anderson V.E., Hauser W.A., Leppik T.E., Noebels J.L., Rich S.S. Epilepsy research. 1991;219-239 Elsevier, Amsterdam. 4.
45. Gall C., Lauterborn J.C. Dentate gyrus as a model system for studies of neurotrophic factor regulation in the CNS: seizure studies. Ribak C.E., Gall C.M., Mody I. The dentate gyrus and its role in seizures. 1992;171-185 Elsevier, Amsterdam.
46. Gall C.M., Gold S.J., Isackson P.J., Seroogy S.B. Brain-derived neurotrophic factor and neurotrophin-3 mRNAs are expressed in ventral midbrain regions containing dopaminergic neurons. Mol Cell Neurosci. 3:1992;56-63.
47. Gall C.M., Lauterborn J.C. Regulation of BDNF expression: multifaceted, region-specific control of a neuronal survival factor in the adult CNS. Mocchetti I. Neurobiology of the neurotrophins. 2000;541-579 FP Graham Publishing Co, Johnson City, TN.
48. Gall C.M., Lauterborn J.C., Guthrie K.M., Stinis C.T. Seizures and the regulation of neurotrophic factor expression: associations with structural plasticity in epilepsy. Seil F.J. Advances in neurologyneuronal regeneration, reorganization, and repair. 1997;9-24 Lippincott-Raven Publishers, Philadelphia. 72.
49. Gall CM, Lynch G (2002) Integrins, synaptic plasticity, and epileptogenesis. In: Recent advances in epilepsy research: molecular mechanisms of epileptogenesis (Scharfman H, Binder D, eds). Georgetown, TX: Landes Bioscience, in press.
50. Gehlsen K.R., Agraves W.S., Pierschbacher M.D., Rouslahti E. Inhibition of in vitro tumor cell invasion by Arg-Gly-Asp-containing synthetic peptides. J Cell Biol. 106:1988;925-930.
51. Geiger B, Bershadsky A, Pankov R, Yamada KM (2001) Transmembrane extracellular matrix-cytoskeleton crosstalk. Nature Rev Mol Cell Biol 2:793-805.
52. Ghosh A., Greenberg M.E. Calcium signaling in neurons molecular mechanisms and cellular consequences . Science. 268:1995;239-247.
53. Giancotti F.G., Ruoslahti E. Integrin signaling. Science. 285:1999;1028-1032.
54. Gibbs R.B. Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Res. 787:1998;259-268.
55. Grooms S., Jones L. RGDS tetrapeptide and hippocampal in vitro kindling in rats evidence for integrin-mediated physiological stability . Neurosci Lett. 231:1997;139-142.
56. Guthrie K.M., Nguyen T., Gall C.M. Insulin-like growth factor-1 mRNA is increased in deafferented hippocampus spatiotemporal correspondence of a trophic event with axon sprouting . J Comp Neurol. 352:1995;147-160.
57. Harris-White M.E., Zanotti S.A., Frautschy S.A., Charles A.C. Spiral intercellular calcium waves in hippocampal slice cultures. J Neurophysiol. 79:1998;1045-1052.
58. Hengerer B., Lindholm D., Heumann R., Ruther U., Wagner E.F., Thoenen H. Lesion-induced increase in nerve growth factor mRNA is mediated by c-fos. Proc Natl Acad Sci USA. 87:1990;3899-3903.
59. Hernandez R.M., Garza J.M., Graves M.E., Martinez J.L.J., LeBaron R.G. The process of reducing CA1 long-term potentiation by the integrin peptide GRGDSP occurs within the first few minutes following theta-burst stimulation. Biol Bull. 201:2001;236-237.
60. Hess U.S., Lynch G., Gall C.M. Changes in c-fos mRNA expression in rat brain during odor discrimination learning differential involvement of hippocampal subfields CA1 and CA3 . J Neurosci. 15:1995;4786-4795.
61. Howe A., Aplin A., Alahari S., Juliano R. Integrin signaling and cell growth control. Curr Opin Cell Biol. 10:1998;220-231.
62. Huttenlocher A., Palecek S.P., Lu Q., Zhang W., Mellgren R.L., Lauffenburger D.A., Ginsberg M.H., Horwitz A.F. Regulation of cell migration by the calcium-dependent protease calpain. J Biol Chem. 272:1997;32719-32722.
63. Hynes R. Integrins, versatility, modulation, and signaling in cell adhesion. Cell. 69:1992;11-25.
64. Isackson P.J., Murray K., Huntsman M., Gall C.M. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures temporal patterns of induction distinct from NGF . Neuron. 6:1991;937-948.
65. Juliano R. Cooperation between soluble factors and integrin-mediated cell anchorage in the control of cell growth and differentiation. Bioessays. 18:1998;911-917.
66. Kang H., Schuman E.M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science. 273:1996;1402-1406.
67. Kang H.J., Welcher A.A., Shelton D., Schuman E.M. Neurotrophins and time different roles for TrkB signaling in hippocampal long-term potentiation . Neuron. 19:1997;653-664.
68. Kramár E.A., Bernard J.A., Gall C.M., Lynch G. Alpha3 integrin receptors contribute to the consolidation of long term potentiation. Neuroscience. 110:2002;29-39.
69. Kulkarni S., Saido T.C., Suzuki K., Fox J.E. Calpain mediates integrin-induced signaling at a point upstream of Rho family members. J Biol Chem. 274:1999;21265-21275.
70. Kwon M.S., Park C.S., Choi K.-R., Park C.-S., Ahnn J., Kim J.I., Eom S.H., Kaufman S.J., Song W.K. Calreticulin couples calcium release and calcium influx in integrin-mediated calcium signaling. Mol Biol Cell. 11:2000;1433-1443.
71. Lauri S.E., Taira T., Rauvala H. High-frequency synaptic stimulation induces association of fyn and c-src to distinct phosphorylated components. Neuroreport. 11:2000;997-1000.
72. Lauterborn J.C., Berschauer R., Gall C.M. Cell-specific modulation of basal and seizure-induced neurotrophin expression by adrenalectomy. Neuroscience. 68:1995;363-378.
73. Lauterborn J.C., Isackson P.J., Gall C.M. Cellular localization of NGF and NT-3 mRNAs in postnatal rat forebrain. Mol Cell Neurosci. 5:1994;46-62.
74. Lauterborn J.C., Isackson P.J., Montalvo R., Gall C.M. In situ hybridization localization of choline acetyltransferase mRNA in adult rat brain and spinal cord. Mol Brain Res. 17:1993;59-69.
75. Lauterborn J.C., Lynch G., Vanderklish P., Arai A., Gall C.M. Positive modulation of AMPA receptors increases neurotrophin expression by hippocampal and cortical neurons. J Neurosci. 20:2000;8-21.
76. Lauterborn J.C., Poulsen F.R., Stinis C.T., Isackson P.J., Gall C.M. Transcript-specific effects of adrenalectomy on seizure-induced BDNF expression in rat hippocampus. Mol Brain Res. 55:1998;81-91.
77. Lauterborn J.C., Rivera S., Stinis C.T., Hayes V.Y., Isackson P.J., Gall C.M. Differential effects of protein synthesis inhibition on the activity dependent expression of BDNF mRNA transcripts evidence for immediate-early gene responses from specific promotors . J Neurosci. 16:1996;7428-7436.
78. Lee K., Schottler F., Oliver M., Lynch G. Brief bursts of high-frequency stimulation produce two types of structural changes in rat hippocampus. J Neurophysiol. 44:1980;247-258.
79. Levine E.S., Dreyfus C.F., Black I.B., Plummer M.R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc Nat Acad Sci USA. 92:1995;8074-8077.
80. Lindvall O., Kokaia Z., Bengzon J., Elmér E., Kokaia M. Neurotrophins and brain insults. Trends Neurosci. 17:1994;490-496.
81. 2+ channels in neurons by increasing protein tyrosine phosphorylation. J Biol Chem. 27:2002;24368-24375.
82. Ludwig A., Flockerzi B., Hofmann F. Regional expression and cellular localization of the α1 and β subunit of high voltage-activated calcium channels in rat brain. J Neurosci. 17:1997;1339-1349.
83. Meberg P.J., Gall C.M., Routtenberg A. Induction of F1/GAP43 gene expression in hippocampal granule cells after seizures. Mol Brain Res. 17:1992;295-299.
84. Meberg P.J., Valcourt E.G., Routtenberg A. Protein F1/GAP-43 and PKC gene expression patterns in hippocampus are altered 1-2 h after LTP. Mol Brain Res. 34:1995;343-346.
85. Merlio J.-P., Ernfors P., Kokaia Z., Middlemas D.S., Bengzon J., Kokaia M., Smith M.-J., Siesjö B.K., Hunter T., Lindvall O., Persson H. Increased production of the TrkB protein tyrosine kinase receptor after brain insults. Neuron. 10:1993;151-164.
86. Metsis M., Timmusk T., Arenas E., Persson H. Differential usage of multiple brain-derived neurotrophic factor promoters in the rat brain following neuronal activation. Proc Natl Acad Sci USA. 90:1993;8802-8806.
87. Michael G.J., Averill S., Nitkunan A., Rattray M., Bennett D.L., Yan Q., Priestley J.V. Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root gangion cells and their central terminations within the spinal cord. J Neurosci. 17:1997;8476-8490.
88. Miranti C.K., Brugge J.S. Sensing the environment a historical perspective on integrin signal transduction . Nature Cell Biol. 4:2002;83-90.
89. Miyamoto S., Teramoto H., Gutkind J.S., Yamada K.M. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation roles of integrin aggregation and occupancy of receptors . J Cell Biol. 135:1996;1633-1642.
90. Mocchetti I., Spiga G., Hayes V.Y., Isackson P.J., Colangelo A. Glucocorticoids differentially increase nerve growth factor and basic fibroblast growth factor expression in the rat brain. J Neurosci. 16:1996;2141-2148.
91. Mogford J.E., Davis G.E., Meininger G.A. RGDN peptide interactions with endothelial α5β1 integrin causes sustained endothelin-dependent vasoconstriction of rat skeletal muscle arterioles. J Clin Invest. 100:1997;1647-1653.
92. Morgan J.I., Curran T. Stimulus-transcription coupling in neurons role of cellular immediate-early genes . Trends Neurosci. 12:1989;459-462.
93. Moro L., Dolce L., Cabodi S., Bergato E., Erba E.B., Smeriglio M., Turco E., Retta S.F., Giufridda M.G., Venturino M., Godovac-Zimmermann J., Conti A., Schaefer E., Berguino L., Tacchetti C., Gaggini P., Silengo L., Tarone G., Defilippi P. Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J Biol Chem. 277:2002;9405-9414.
94. MotulskyH (1995) Intuitive Biostatistics. New York: Oxford University Press.
95. Murase S.-I., Hayashi Y. Integrin α1 localization in murine central and peripheral nervous system. J Comp Neurol. 395:1998;161-176.
96. Nguyen P.V., Abel T., Kandel E.R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science. 265:1994;1104-1107.
97. Nibuya M., Norinobu S., Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci. 15:1995;7539-7547.
98. Nishimura S.L., Boylen K.P., Einheber S., Milner T.A., Ramos D.M., Pytela R. Synaptic and glial localization of the integrin αvβ8 in mouse and rat brain. Brain Res. 791:1998;271-282.
99. Patterson S.L., Grover L.M., Schwartzkroin P.A., Bothwell M. Neurotrophin expression in rat hippocampal slices a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 messenger RNAs . Neuron. 9:1992;1081-1088.
100. Pfaff M., Du X., Ginsberg M.H. Calpain cleavage of integrin beta cytoplasmic domains. FEBS Lett. 460:1999;17-22.
101. Pierschbacher M., Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 304:1984;30-33.
102. Pierschbacher M.D., Ruoslahti E. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesions. J Biol Chem. 262:1987;17294-17298.
103. Pinkstaff J.K., Detterich J., Lynch G., Gall C. Integrin subunit gene expression is regionally differentiated in adult brain. J Neurosci. 19:1999;1541-1556.
104. Pinkstaff J.K., Lynch G., Gall C.M. Localization and seizure regulation of integrin β1 mRNA in adult rat brain. Mol Brain Res. 19:1997;1541-1556.
105. + channels in arteriolar vasodilation mediated by integrin interaction with RGD-containing peptide. Am J Physiol. 275:1998;H1449-H1454.
106. Plow E.F., Haas T.A., Zhang L., Loftus J., Smith J.W. Ligand binding to integrins. J Biol Chem. 275:2000;21785-21788.
107. Porter J.C., Hogg N. Integrins take partners cross-talk between integrins and other membrane receptors . Trends Cell Biol. 8:1998;390-396.
108. Previtali S.C., Feltri M.L., Archelos J.J., Quattrini A., Wrabetz L., Hartung H.-P. Role of integrins in the peripheral nervous system. Prog Neurobiol. 64:2001;35-49.
109. Rivera S., Gold S., Gall C.M. Interleukin-1β increases basic fibroblast growth factor mRNA expression in adult rat brain and organotypic hippocampal cultures. Mol Brain Res. 27:1994;12-26.
110. Rodriquez M.A., Pesold C., Liu W.S., Kriho V., Guidotti A., Pappas G.D., Costa E. Colocalization of integrin receptors and reelin in dendritic spine postsynaptic densities of adult nonhuman primate cortex. Proc Natl Acad Sci USA. 97:2000;3550-3555.
111. Rohrbough J., Grotewiel M.S., Davis R.L., Broadie K. Integrin-mediated regulation of synaptic morphology, transmission and plasticity. J Neurosci. 20:2000;6868-6878.
112. Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol. 12:1996;697-715.
113. Ruoslahti E., Pierschbacher M. New perspectives in cell adhesion RGD and integrins . Science. 238:1987;491-497.
114. Ruoslahti E., Pierschbacher M.D. Arg-Gly-Asp a versatile cell recognition signal . Cell. 44:1986;517-518.
115. Schottelndreier H., Potter B.V.L., Mayr G.W., Guse A.H. Mechanisms involved in α6β1-integrin mediated Ca+2 signalling. Cell Signal. 13:2001;895-899.
116. Schuster T., Krug M., Stalder M., Hackel N., Gerardy-Schahn R., Schachner M. Immunoelectron microscopic localization of the neural recognition molecules L1, NCAM, and its isoform NCAM180, the NCAM-associated polysialic acid, beta1 integrin and the extracellular matrix molecule tenascin-R in synapses of the adult rat hippocampus. J Neurobiol. 49:2001;142-158.
117. Sheng M., Greenberg M.E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron. 4:2001;477-485.
118. Shieh P.B., Hu S.-C., Bobb K., Timmusk T., Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron. 20:1998;727-740.
119. ++ signaling. Proc Natl Acad Sci USA. 91:1994;8214-8218.
120. Smith M.A., Makina S., Kvetnansky R., Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophin factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci. 15:1995;1768-1777.
121. Sohrabji F., Miranda R.C., Toran-Allerand C.D. Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc Natl Acad Sci USA. 92:1995;11110-11114.
122. Staubli U., Chun D., Lynch G. Time-dependent reversal of long-term potentiation by an integrin antagonist. J Neurosci. 18:1998;3460-3469.
123. Staubli U., Vanderklish P.W., Lynch G. An inhibitor of integrin receptors blocks LTP. Behav Neural Biol. 53:1990;1-5.
124. Stoppini S., Buchs P.A., Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 37:1991;173-182.
125. Streuli C.H., Edwards G.M. Control of normal mammary epithelial phenotype by integrins. J Mammary Gland Biol Neoplasia. 3:1998;151-163.
126. +2 channels. J Biol Chem. 275:2000;17269-17275.
127. Tanaka J., Maeda N. Microglial ramification requires nondiffusible factors derived from astrocytes. Exp Neurol. 137:1996;367-375.
128. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron. 20:1998;709-726.
129. Timmusk T., Belluardo N., Persson H., Metsis M. Developmental regulaiton of brain-derived neurotrophic factor messenger RNAs transcribed from different promoters in the rat brain. Neuroscience. 60:1994;287-291.
130. Timmusk T., Palm K., Metsis M., Reintam T., Paalme V., Saarma M., Persson H. Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron. 10:1993;475-489.
131. Toni N., Buchs P.A., Nikonenko I., Bron C.R., Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature. 402:1999;421-425.
132. Tsao P.W., Mousa S.A. Thrombospondin mediates calcium mobilization in fibroblasts via its Arg-Gly-Asp and carboxyl-terminal domains. J Biol Chem. 270:1995;23747-23753.
133. Wang J.F., Zhang X.F., Groupman J.E. Stimulation of beta 1 integrin induces tyrosine phosphorylation of vascular endothelial growth factor receptor-3 and modulates cell migration. J Biol Chem. 276:2001;41950-41957.
134. West A.E., Chen W.G., Balva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., Greenberg M.E. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA. 98:2001;11024-11031.
135. Wildering W.C., Herman P.M., Bulloch A.G.M. Rapid neuromodulatory actions of integrin ligands. J Neurosci. 22:2002;2419-2426.
136. Wu X., Davis G.E., Meininger G.A., Wilson E., Davis M.J. Regulation of the L-type calcium channel by α5β1 integrin requires signaling between focal adhesion proteins. J Biol Chem. 276:2001;30285-30292.
137. Wu X., Mogford J.E., Platts S.H., Davis G.E., Meininger G.A., Davis M.J. Modulation of calcium current in arteriolar smooth muscle by alphav beta3 and alpha5 beta1 integrin ligands. J Cell Biol. 143:1998;241-252.
138. Xiao P., Bahr B., Staubli U., Vanderklish P., Lynch G. Evidence that matrix recognition contributes to stabilization but not induction of LTP. Neuroreport. 2:1991;461-464.
139. 2+]) and tyrosine phosphorylation in adhesion of cultured vascular smooth muscle cells to fibrinogen. Cardiovas Res. 39:1998;475-484.
140. Yamada K., Miyamoto S. Integrin transmembrane signaling and cytoskeletal control. Curr Opin Cell Biol. 7:1995;681-689.
141. Yamada K.M., Even-Ram S. Integrin regulation of growth factor receptors. Nat Cell Biol. 4:2002;E75-E76.
142. Zhu X., Assoian R.K. Integrin-dependent activation of MAP kinase a link to shape-dependent cell proliferation . Mol Biol Cell. 6:1995;273-282.