Integrin regulation of cytoplasmic calcium in excitatory neurons depends upon glutamate receptors and release from intracellular stores

Molecular and Cellular Neuroscience

Volumn 37, Issue 4, 2008, Pages 770-780

  Lin, C Y ^a   Hilgenberg, L G W ^a   Smith, M A ^a   Lynch, G ^a   Gall, C M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

1 integrin; Adhesion; AMPA receptor; Calcium currents; Fibronectin; NMDA receptor; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR ANTAGONIST; CALCIUM; GENISTEIN; GLUTAMATE RECEPTOR; INTEGRIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; TETRODOTOXIN; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; BRAIN CELL; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPOLARIZATION; HUMAN; HUMAN CELL; MACROGLIA; NERVE CELL PLASTICITY; PRIORITY JOURNAL; PROTEIN SECRETION;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELLS, CULTURED; CYTOPLASM; EXCITATORY AMINO ACID ANTAGONISTS; INTEGRINS; INTRACELLULAR FLUID; MICE; MICE, INBRED ICR; NEURONS; RECEPTORS, GLUTAMATE;

EID: 41149130589     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.01.001     Document Type: Article

References (76)

1. Bardo S., Cavazzini M.G., and Emptage N. The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. Trends Pharmacol. Sci. 27 (2006) 78-84
2. Bernard-Trifilo J.A., Kramár E.A., Torp R., Lin C.Y., Pineda E.A., Lynch G., and Gall C.M. Integrin signaling cascades are operational in adult hippocampal synapses and modulate NMDA receptor physiology. J. Neurochem. 93 (2005) 834-849
3. ++ influx in pulmonary endothelial cells. Circ. Res. 86 (2000) 456-462
4. Bi X., Lynch G., Zhou J., and Gall C.M. Polarized distribution of α5 integrin in the dendrites of hippocampal and cortical neurons. J. Comp. Neurol. 435 (2001) 184-193
5. Blaschke M., Keller B.U., Rivosecchi R., Hollmann M., Heinemann S., and Konnerth A. A single amono acid determines the subunit-specific spider toxin block of α-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor channels. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 6528-6532
6. Chan C.-S., Weeber E.J., Kurup S., Sweatt J.D., and Davis R.L. Integrin requirement for hippocampal synaptic plasticity and spatial memory. J. Neurosci. 23 (2003) 7107-7116
7. Chan C.S., Weeber E.J., Zong L., Fuchs E., Sweatt J.D., and Davis R.L. Beta1-integrins are required for hippocampal AMPA receptor-dependent synaptic transmission, synaptic plasticity, and working memory. J. Neurosci. 26 (2006) 223-232
8. Chun D., Gall C.M., Bi X., and Lynch G. Evidence that integrins contribute to multiple stages in the consolidation of long-term potentiation. Neuroscience 105 (2001) 815-829
9. Cousin B., Leloup C., Penicaud L., and Price J. Developmental changes in integrin ß-subunits in rat cerebral cortex. Neurosci. Lett. 234 (1997) 161-165
10. Cull-Candy S., Kelly L., and Farrant M. Regulation of Ca2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16 (2006) 288-297
11. DeMali K.A., Wennerberg K., and Burridge K. Integrin signaling to the actin cytoskeleton. Curr. Opin. Cell Biol. 15 (2003) 572-582
12. Dong E., Caruncho H., Liu W.S., Smalheiser N.R., Grayson D.R., Costa E., and Guidotti A. A reelin-integrin receptor interaction regulates Arc mRNA translation in synaptoneurosomes. Proc. Natl. Acad. Sci. U. S. A. (2003) 5479-5484
13. Dulabon L., Olson E.C., Taglienti M.G., Eisenbuth S., McGrath B., Walsh C.A., Kreidberg J.A., and Anton E.S. Reelin binds α3ß1 integrin and inhibits neuronal migration. Neuron 27 (2000) 33-44
14. Einheber S., Schnapp L.M., Salzer J.L., Cappiello Z.B., and Milner T.A. Regional and ultrastructural distribution of the α8 integrin subunit in developing and adult rat brain suggests a role in synaptic function. J. Comp. Neurol. 370 (1996) 105-134
15. Fleming I., Fisslthaler B., and Busse R. Calcium signaling in endothelial cells involves activation of tyrosine kinases and leads to activation of mitogen-activated protein kinases. Circ. Res. 76 (1995) 522-529
16. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260 (1985) 3440-3450
17. Gui P., Wu X., Ling S., Stotz S.C., Winkfein R.J., Wilson E., Davis G.E., Braun A.P., Zamponi G.W., and Davis M.J. Integrin receptor activation triggers converging regulation of Cav1.2 calcium channels by c-Src and protein kinase A pathways. J. Biol. Chem. 281 (2006) 14015-14025
18. Hilgenberg L.G.W., and Smith M.A. Agrin signaling in cortical neurons is mediated by a tyrosine kinase-dependent increase in intracellular Ca2+ that engages both CaMKII and MAPK signal pathways. J. Neurobiol. 61 (2004) 289-300
19. Hoffman K.B., Pinkstaff J.K., Gall C.M., and Lynch G. Seizure induced synthesis of fibronectin is rapid and age dependent: implications for long-term potentiation and sprouting. Brain Res. 812 (1998) 209-215
20. Huang Z., Shimazu K., Woo N.H., Zang K., Muller U., Lu B., and Reichardt L.F. Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. J. Neurosci. 26 (2006) 11208-11219
21. Kang M.G., Chen C.C., Wakamori M., Hara Y., Mori Y., and Campbell K.P. A functional AMPA receptor-calcium channel complex in the postsynaptic membrane. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 5561-5566
22. Kelleher III R.J., Govindarajan A., and Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44 (2004) 59-73
23. Kramár E.A., and Lynch G. Developmental and regional differences in the consolidation of long-term potentiation. Neuroscience 118 (2003) 387-398
24. Kramár E.A., Bernard J.A., Gall C.M., and Lynch G. Alpha3 integrin receptors contribute to the consolidation of long-term potentiation. Neuroscience 110 (2002) 29-39
25. Kramár E.A., Bernard J.A., Gall C.M., and Lynch G. Integrins modulate fast excitatory transmission at hippocampal synapses. J. Biol. Chem. 278 (2003) 10722-10730
26. Kramár E.A., Lin B., Rex C.S., Gall C.M., and Lynch G. Integrin-driven actin polymerization consolidates long-term potentiation. Proc. Natl. Acad. Sci. USA 103 (2006) 5579-5584
27. Krause T., Gerbershagen M.U., Fiege M., Weibhorn R., and Wappler F. Dantrolene-A review of its pharmacology, therapeutic use and new developments. Anaesthesia 59 (2004) 364-373
28. Kwon M.S., Park C.S., Choi K.-R., Park C.-S., Ahnn J., Kim J.I., Eom S.H., Kaufman S.J., and Song W.K. Calreticulin couples calcium release and calcium influx in integrin-mediated calcium signaling. Mol. Biol. Cell 11 (2000) 1433-1443
29. Lin C.-Y., Lynch G., and Gall C. AMPA receptor stimulation increases α5ß1 integrin surface expression, adhesive function and signaling. J. Neurochem. 94 (2005) 531-546
30. Lynch G., Rex C.S., and Gall C.M. LTP consolidation: substrates, explanatory power, and functional significance. Neuropharm. 52 (2007) 12-23
31. Lynch G., Larson J., Kelso S., Barrionuevo G., and Schottler F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305 (1983) 719-721
32. Lynch G., Kessler M., Arai A., and Larson J. The nature and causes of hippocampal long-term potentiation. Prog. Brain Res. 83 (1990) 233-250
33. Maher B.J., Mackinnon II R.L., Bai J., Chapman E.R., and Kelly P.T. Activation of postsynaptic Ca(2+) stores modulates glutamate receptor cycling in hippocampal neurons. J. Neurophysiol. 93 (2005) 178-188
34. McDonald A.J., Muller J.F., and Mascagni R. GABaergic innervation of alpha type I calcium/calmodulin-dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala. J. Comp. Neurol. 446 (2002) 199-218
35. Meighan P.C., Meighan S.E., Davis C.J., Wright J.W., and Harding J.W. Effects of matrix metalloproteinase inhibition on short- and long-term plasticity of Schaffer collateral/CA1 synapses. J. Neurochem. 102 (2007) 2085-2096
36. Milner R., and Campbell I.L. The integrin family of cell adhesion molecules has multiple functions within the CNS. J. Neurosci. Res. 69 (2002) 286-291
37. 2+ transport by the sarcoplasmic reticulum ATPase. Biochim. Biophysi. Acta 1318 (1997) 52-70
38. Miranti C.K., and Brugge J.S. Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4 (2002) 83-90
39. Morris R.G. Long term potentiation and memory. Philos. Trans. R. Soc. Lond., Biol. Sci. 358 (2003) 643-647
40. Nagy V., Bozdagi O., Matynia A., Balcerzyk M., Okulski P., Dzwonek J., Costa R.M., Silva A.J., Kaczmarek L., and Huntley G.W. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J. Neurosci. 26 (2006) 1923-1934
41. Neher E. The use of Fura-2 for estimating Ca buffers and Ca fluxes. Neuropharm. 34 (1995) 1423-1442
42. Nishimura S.L., Boylen K.P., Einheber S., Milner T.A., Ramos D.M., and Pytela R. Synaptic and glial localization of the integrin αvß8 in mouse and rat brain. Brain Res. 791 (1998) 271-282
43. Numakawa T., Yamagishi S., Adachi N., Matsumoto T., Yokomaku D., Yamada M., and Hatanaka H. Brain-derived neurotrophic factor-induced potentiation of Ca(2+) oscillations in developing cortical neurons. J. Biol. Chem. 277 (2002) 6520-6529
44. Ogoshi F., Yinb H.Z., Kuppumbattia Y., Songa B., Amindarib S., and Weiss J.H. Tumor necrosis-factor-alpha (TNF-alpha) induces rapid insertion of Ca2+-permeable α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate (AMPA) kainate (Ca-A/K) channels in a subset of hippocampal pyramidal neurons. Exp. Neurol. 193 (2005) 384-393
45. Pinkstaff J.K., Lynch G., and Gall C.M. Localization and seizure regulation of integrin ß1 mRNA in adult rat brain. Mol. Brain Res. 19 (1997) 1541-1556
46. Pinkstaff J.K., Detterich J., Lynch G., and Gall C. Integrin subunit gene expression is regionally differentiated in adult brain. J. Neurosci. 19 (1999) 1514-1556
47. Plow E.F., Haas T.A., Zhang L., Loftus J., and Smith J.W. Ligand binding to integrins. J. Biol. Chem. 275 (2000) 21785-21788
48. Raymond C.R., and Redman S.J. Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus. J. Physiol. 570 (2006) 97-111
49. Rizzuto R. Intracellular Ca(2+) pools in neuronal signalling. Curr. Opin. Neurobiol. 11 (2001) 306-311
50. Roche K.W., O'Brien R.J., Mammen A.L., Bernhardt J., and Huganir R.L. Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16 (1996) 1179-1188
51. Rose C.R., and Konnerth A. Stores not just for storage. intracellular calcium release and synaptic plasticity. Neuron 31 (2001) 519-522
52. Schottelndreier H., Mayr G.W., and Guse A.H. Beta1-integrins mediate Ca2+-signalling and T cell spreading via divergent pathways. Cell. Signal. 11 (1999) 611-619
53. Schottelndreier H., Potter B.V.L., Mayr G.W., and Guse A.H. Mechanisms involved in α6ß1-integrin mediated Ca+2 signalling. Cell. Signal. 13 (2001) 895-899
54. Schwartz M.A., and Ginsberg M.H. Network and crosstalk: integrin signalling spreads. Nat. Cell. Biol. 4 (2002) E65-E68
55. Shi Y., and Ethell I.M. Integrins control dendritic spine plasticity in hippocampal neurons through NMDA receptor and Ca2+/calmodulin-dependent protein kinase II-mediated actin reorganization. J. Neurosci. 26 (2006) 1813-1822
56. ++ signaling. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 8214-8218
57. Smart F.M., Edelman G.M., and Vanderklish P.W. BDNF induces translocation of initiation factor 4E to mRNA granules: evidence for a role of synaptic microfilaments and integrins. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 14403-14408
58. Soderling T.R., and Derkach V.A. Postsynaptic protein phosphorylation and LTP. Trends Neurosci. 23 (2000) 75-80
59. Staubli U., Vanderklish P.W., and Lynch G. An inhibitor of integrin receptors blocks LTP. Behav. Neural Biol. 53 (1990) 1-5
60. Staubli U., Chun D., and Lynch G. Time-dependent reversal of long-term potentiation by an integrin antagonist. J. Neurosci. 18 (1998) 3460-3469
61. Tomita S., Stein V., Stocker T.J., Nicoll R.A., and Bredt D.S. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45 (2005) 269-277
62. Tomita S., Sekiguchi M., Wada K., Nicoll R.A., and Bredt D.S. Stargazin controls the pharmacology of AMPA receptor potentiators. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 10064-10067
63. Tsao P.W., and 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
64. Vandenberghe W., Nicoll R.A., and Bredt D.S. Stargazin is an AMPA receptor auxiliary subunit. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 485-490
65. Verkhratsky A., and Shmigol A. Calcium-induced calcium release in neurones. Cell Calcium 19 (1996) 1-14
66. Wang J.Q., Arora A., Yang L., Parelkar N.K., Zhang G., Liu X., Choe E.S., and Mao L. Phosphorylation of AMPA receptors: mechanisms and synaptic plasticity. Mol. Neurobiol. 32 (2005) 237-249
67. Wang Q., Klyubin I., Wright S., Griswold-Prenner I., Rowan M.J., and Anwyl R. alphav integrins mediate beta-amyloid induced inhibition of long-term potentiation. Neurobiol. Aging (2007) (Electronic publication ahead of print)
68. Watson P.M., Humphries M.J., Relton J., Rothwell N.J., Verkhratsky A., and Gibson R.M. Integrin-binding RGD peptides induce rapid intracellular calcium increases and MAPK signaling in cortical neurons. Mol. Cell. Neurosci. 34 (2007) 147-154
69. Webb D.J., Zhang H., Majumdar D., and Horwitz A.F. α5 integrin signaling regulates the formation of spines and synapses in hippocampal neurons. J. Biol. Chem. 282 (2007) 6929-6935
70. Wei J.Y., Jin X., Cohen E.D., Daw N.W., and Barnstable C.J. cGMP-induced presynaptic depression and postsynaptic facilitation at glutamatergic synapses in visual cortex. Brain Res. 927 (2002) 42-54
71. Weiss J.H., and Sensi S.L. Ca2+-Zn2+ permeable AMPA or kainate receptors: possible key factors in selective neurodegeneration. Trends Neurosci. 23 (2000) 365-371
72. Wildering W.C., Herman P.M., and Bulloch A.G.M. Rapid neuromodulatory actions of integrin ligands. J. Neurosci. 22 (2002) 2419-2426
73. Wu X., Mogford J.E., Platts S.H., Davis G.E., Meininger G.A., and Davis M.J. Modulation of calcium current in arteriolar smooth muscle by α5β3 and α5β1 integrin ligands. J. Cell. Biol. 143 (1998) 241-252
74. Wu X., Davis G.E., Meininger G.A., Wilson E., and Davis M.J. Regulation of the L-type calcium channel by α5ß1 integrin requires signaling between focal adhesion proteins. J. Biol. Chem. 276 (2001) 30285-30292
75. 2+]) and tyrosine phosphorylation in adhesion of cultured vascular smooth muscle cells to fibrinogen. Cardiovas. Res. 39 (1998) 475-484
76. Zhang Q., Kohler M., Yang S.N., Zhang F., Larsson O., and Berggren P.O. Growth hormone promotes Ca(2+)-induced Ca2+ release in insulin-secreting cells by ryanodine receptor tyrosine phosphorylation. Mol. Endocrinol. 18 (2004) 1658-1669