In vitro findings of alterations in intracellular calcium homeostasis in schizophrenia

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 34, Issue 8, 2010, Pages 1367-1374

  Bojarski, Lukasz ^a   Debowska, Katarzyna ^b   Wojda, Urszula ^b  

^a Celon Pharma Ltd   (Poland)

^b INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

Author keywords

Ca2+ homeostasis; Ca2+ signaling; Calcium or Ca2+; Dopamine; Glutamate; NMDA; Schizophrenia

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; CALMODULIN; DOPAMINE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROMODULIN; PROTEIN S100B;

ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CALCIUM SIGNALING; DISEASE MODEL; DOPAMINERGIC TRANSMISSION; HUMAN; IN VITRO STUDY; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; SCHIZOPHRENIA;

ANIMALS; CALCIUM; CALCIUM SIGNALING; HOMEOSTASIS; HUMANS; NEURONS; SCHIZOPHRENIA;

EID: 78649520021     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2010.08.020     Document Type: Article

References (93)

1. Allan C.L., Cardno A.G., McGuffin P. Schizophrenia: from genes to phenes to disease. Curr Psychiatry Rep 2008, 10:339-343.
2. Amici M., Doherty A., Jo J., Jane D., Cho K., Collingridge G., et al. Neuronal calcium sensors and synaptic plasticity. Biochem Soc Trans 2009, 37:1359-1363.
3. Araneda R., Bustos G. Modulation of dendritic release of dopamine by N-methyl-D-aspartate receptors in rat substantia nigra. J Neurochem 1989, 52:962-970.
4. Arnold S.E., Talbot K., Hahn C.G. Neurodevelopment, neuroplasticity, and new genes for schizophrenia. Prog Brain Res 2005, 147:319-345.
5. Atlas D. Signaling role of the voltage-gated calcium channel as the molecular 'on/off' switch of secretion. Cell Signal 2010, 22:1597-1603.
6. Bai J., He F., Novikova S.I., Undie A.S., Dracheva S., Haroutunian V., et al. Abnormalities in the dopamine system in schizophrenia may lie in altered levels of dopamine receptor-interacting proteins. Biol Psychiatry 2004, 56:427-440.
7. Baier P.C., Koch J.M., Seeck-Hirschner M., Ohlmeyer K., Wilms S., Aldenhoff J.B., et al. A flow-cytometric method to investigate glutamate-receptor-sensitivity in whole blood platelets - results from healthy controls and patients with schizophrenia. J Psychiatr Res 2009, 43:585-591.
8. Barclay J.W., Morgan A., Burgoyne R.D. Calcium-dependent regulation of exocytosis. Cell Calcium 2005, 38:343-353.
9. Bergson C., Levenson R., Goldman-Rakic P.S., Lidow M.S. Dopamine receptor-interacting proteins: the Ca(2+) connection in dopamine signaling. Trends Pharmacol Sci 2003, 24:486-492.
10. Bernstein H.G., Braunewell K.H., Spilker C., Danos P., Baumann B., Funke S., et al. Hippocampal expression of the calcium sensor protein visinin-like protein-1 in schizophrenia. NeuroReport 2002, 13:393-396.
11. Bernstein H.G., Sahin J., Smalla K.H., Gundelfinger E.D., Bogerts B., Kreutz M.R. A reduced number of cortical neurons show increased Caldendrin protein levels in chronic schizophrenia. Schizophr Res 2007, 96:246-256.
12. Berridge M.J. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 2009, 1793:933-940.
13. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003, 4:517-529.
14. Bickel S., Javitt D.C. Neurophysiological and neurochemical animal models of schizophrenia: focus on glutamate. Behav Brain Res 2009, 204:352-362.
15. Blennow K., Bogdanovic N., Gottfries C.G., Davidsson P. The growth-associated protein GAP-43 is increased in the hippocampus and in the gyrus cinguli in schizophrenia. J Mol Neurosci 1999, 13:101-109.
16. Bojarski L., Herms J., Kuznicki J. Calcium dysregulation in Alzheimer's disease. Neurochem Int 2008, 52:621-633.
17. Bozzi Y., Borrelli E. Dopamine in neurotoxicity and neuroprotection: what do D2 receptors have to do with it?. Trends Neurosci 2006, 29:167-174.
18. Broadbelt K., Jones L.B. Evidence of altered calmodulin immunoreactivity in areas 9 and 32 of schizophrenic prefrontal cortex. J Psychiatr Res 2008, 42:612-621.
19. Bubenikova-Valesova V., Horacek J., Vrajova M., Hoschl C. Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 2008, 32:1014-1023.
20. Burgoyne R.D. Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci 2007, 8:182-193.
21. Dalley J.W., Everitt B.J. Dopamine receptors in the learning, memory and drug reward circuitry. Semin Cell Dev Biol 2009, 20:403-410.
22. Das I., Khan N.S., Puri B.K., Sooranna S.R., de Belleroche J., Hirsch S.R. Elevated platelet calcium mobilization and nitric oxide synthase activity may reflect abnormalities in schizophrenic brain. Biochem Biophys Res Commun 1995, 212:375-380.
23. Dawe G.S., Hwang E.H., Tan C.H. Pathophysiology and animal models of schizophrenia. Ann Acad Med Singapore 2009, 38:425-426.
24. Den Boer J.A., van Megen H.J., Fleischhacker W.W., Louwerens J.W., Slaap B.R., Westenberg H.G., et al. Differential effects of the D1-DA receptor antagonist SCH39166 on positive and negative symptoms of schizophrenia. Psychopharmacology (Berl) 1995, 121:317-322.
25. Donato R., Sorci G., Riuzzi F., Arcuri C., Bianchi R., Brozzi F., et al. S100B's double life: intracellular regulator and extracellular signal. Biochim Biophys Acta 2009, 1793:1008-1022.
26. Eyles D.W., McGrath J.J., Reynolds G.P. Neuronal calcium-binding proteins and schizophrenia. Schizophr Res 2002, 57:27-34.
27. Fleckenstein A.E., Volz T.J., Riddle E.L., Gibb J.W., Hanson G.R. New insights into the mechanism of action of amphetamines. Annu Rev Pharmacol Toxicol 2007, 47:681-698.
28. Gerber U., Gee C.E., Benquet P. Metabotropic glutamate receptors: intracellular signaling pathways. Curr Opin Pharmacol 2007, 7:56-61.
29. Grace A.A. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 1991, 41:1-24.
30. Gunduz-Bruce H. The acute effects of NMDA antagonism: from the rodent to the human brain. Brain Res Rev 2009, 60:279-286.
31. Halberstadt A.L. The phencyclidine-glutamate model of schizophrenia. Clin Neuropharmacol 1995, 18:237-249.
32. Harnett M.T., Bernier B.E., Ahn K.C., Morikawa H. Burst-timing-dependent plasticity of NMDA receptor-mediated transmission in midbrain dopamine neurons. Neuron 2009, 62:826-838.
33. Harrison P.J., McLaughlin D., Kerwin R.W. Decreased hippocampal expression of a glutamate receptor gene in schizophrenia. Lancet 1991, 337:450-452.
34. Higley M.J., Sabatini B.L. Calcium signaling in dendrites and spines: practical and functional considerations. Neuron 2008, 59:902-913.
35. Howes O.D., Kapur S. The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr Bull 2009, 35:549-562.
36. Inada K., Ishigooka J., Anzai T., Suzuki E., Miyaoka H., Saji M. Antisense hippocampal knockdown of NMDA-NR1 by HVJ-liposome vector induces deficit of prepulse inhibition but not of spatial memory. Neurosci Res 2003, 45:473-481.
37. Ingason A., Giegling I., Cichon S., Hansen T., Rasmussen H.B., Nielsen J., et al. A large replication study and meta-analysis in European samples provides further support for association of AHI1 markers with schizophrenia. Hum Mol Genet 2010, 19:1379-1386.
38. Inta D., Monyer H., Sprengel R., Meyer-Lindenberg A., Gass P. Mice with genetically altered glutamate receptors as models of schizophrenia: a comprehensive review. Neurosci Biobehav Rev 2010, 34:285-294.
39. Jann M.W. Implications for atypical antipsychotics in the treatment of schizophrenia: neurocognition effects and a neuroprotective hypothesis. Pharmacotherapy 2004, 24:1759-1783.
40. Jimerson D.C., Post R.M., Carman J.S., van Kammen D.P., Wood J.H., Goodwin F.K., et al. CSF calcium: clinical correlates in affective illness and schizophrenia. Biol Psychiatry 1979, 14:37-51.
41. Kabbani N., Negyessy L., Lin R., Goldman-Rakic P., Levenson R. Interaction with neuronal calcium sensor NCS-1 mediates desensitization of the D2 dopamine receptor. J Neurosci 2002, 22:8476-8486.
42. Karlsson P., Smith L., Farde L., Harnryd C., Sedvall G., Wiesel F.A. Lack of apparent antipsychotic effect of the D1-dopamine receptor antagonist SCH39166 in acutely ill schizophrenic patients. Psychopharmacology (Berl) 1995, 121:309-316.
43. Kessels H.W., Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 2009, 61:340-350.
44. Klejman M.E., Gruszczynska-Biegala J., Skibinska-Kijek A., Wisniewska M.B., Misztal K., Blazejczyk M., et al. Expression of STIM1 in brain and puncta-like co-localization of STIM1 and ORAI1 upon depletion of Ca(2+) store in neurons. Neurochem Int 2009, 54:49-55.
45. Koh P.O., Undie A.S., Kabbani N., Levenson R., Goldman-Rakic P.S., Lidow M.S. Up-regulation of neuronal calcium sensor-1 (NCS-1) in the prefrontal cortex of schizophrenic and bipolar patients. Proc Natl Acad Sci USA 2003, 100:313-317.
46. Kotecha S.A., Oak J.N., Jackson M.F., Perez Y., Orser B.A., Van Tol H.H., et al. A D2 class dopamine receptor transactivates a receptor tyrosine kinase to inhibit NMDA receptor transmission. Neuron 2002, 35:1111-1122.
47. Krupp J.J., Vissel B., Thomas C.G., Heinemann S.F., Westbrook G.L. Interactions of calmodulin and alpha-actinin with the NR1 subunit modulate Ca2+-dependent inactivation of NMDA receptors. J Neurosci 1999, 19:1165-1178.
48. Leclerc E., Fritz G., Vetter S.W., Heizmann C.W. Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta 2009, 1793:993-1007.
49. Lewis D.A., Moghaddam B. Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Arch Neurol 2006, 63:1372-1376.
50. Lidow M.S. Calcium signaling dysfunction in schizophrenia: a unifying approach. Brain Res Brain Res Rev 2003, 43:70-84.
51. Lieberman J.A., Kane J.M., Alvir J. Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology (Berl) 1987, 91:415-433.
52. Lipska B.K., Weinberger D.R. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 2000, 23:223-239.
53. Marambaud P., Dreses-Werringloer U., Vingtdeux V. Calcium signaling in neurodegeneration. Mol Neurodegener 2009, 4:20.
54. Marcotte E.R., Pearson D.M., Srivastava L.K. Animal models of schizophrenia: a critical review. J Psychiatry Neurosci 2001, 26:395-410.
55. Martins-de-Souza D., Gattaz W.F., Schmitt A., Rewerts C., Maccarrone G., Dias-Neto E., et al. Prefrontal cortex shotgun proteome analysis reveals altered calcium homeostasis and immune system imbalance in schizophrenia. Eur Arch Psychiatry Clin Neurosci 2009, 259:151-163.
56. Martins-de-Souza D., Gattaz W.F., Schmitt A., Rewerts C., Marangoni S., Novello J.C., et al. Alterations in oligodendrocyte proteins, calcium homeostasis and new potential markers in schizophrenia anterior temporal lobe are revealed by shotgun proteome analysis. J Neural Transm 2009, 116:275-289.
57. Mirnics K., Middleton F.A., Stanwood G.D., Lewis D.A., Levitt P. Disease-specific changes in regulator of G-protein signaling 4 (RGS4) expression in schizophrenia. Mol Psychiatry 2001, 6:293-301.
58. Namkung Y., Dipace C., Javitch J.A., Sibley D.R. G protein-coupled receptor kinase-mediated phosphorylation regulates post-endocytic trafficking of the D2 dopamine receptor. J Biol Chem 2009, 284:15038-15051.
59. Namkung Y., Dipace C., Urizar E., Javitch J.A., Sibley D.R. G protein-coupled receptor kinase-2 constitutively regulates D2 dopamine receptor expression and signaling independently of receptor phosphorylation. J Biol Chem 2009, 284:34103-34115.
60. Neve K.A., Seamans J.K., Trantham-Davidson H. Dopamine receptor signaling. J Recept Signal Transduct Res 2004, 24:165-205.
61. Nguyen T., Di Giovanni S. NFAT signaling in neural development and axon growth. Int J Dev Neurosci 2008, 26:141-145.
62. Olney J.W., Farber N.B. Glutamate receptor dysfunction and schizophrenia. Arch Gen Psychiatry 1995, 52:998-1007.
63. Patel J.C., Witkovsky P., Avshalumov M.V., Rice M.E. Mobilization of calcium from intracellular stores facilitates somatodendritic dopamine release. J Neurosci 2009, 29:6568-6579.
64. Perrone-Bizzozero N.I., Sower A.C., Bird E.D., Benowitz L.I., Ivins K.J., Neve R.L. Levels of the growth-associated protein GAP-43 are selectively increased in association cortices in schizophrenia. Proc Natl Acad Sci USA 1996, 93:14182-14187.
65. Putney J.W. New molecular players in capacitative Ca2+ entry. J Cell Sci 2007, 120:1959-1965.
66. Rao V.R., Finkbeiner S. NMDA and AMPA receptors: old channels, new tricks. Trends Neurosci 2007, 30:284-291.
67. Rebola N., Srikumar B.N., Mulle C. Activity-dependent synaptic plasticity of NMDA receptors. J Physiol 2010, 588:93-99.
68. Reed G.L., Fitzgerald M.L., Polgar J. Molecular mechanisms of platelet exocytosis: insights into the "secrete" life of thrombocytes. Blood 2000, 96:3334-3342.
69. Ripova D., Strunecka A., Nemcova V., Farska I. Phospholipids and calcium alterations in platelets of schizophrenic patients. Physiol Res 1997, 46:59-68.
70. Rushlow W.J., Seah C., Sutton L.P., Bjelica A., Rajakumar N. Antipsychotics affect multiple calcium calmodulin dependent proteins. Neuroscience 2009, 161:877-886.
71. Schroeter M.L., Abdul-Khaliq H., Krebs M., Diefenbacher A., Blasig I.E. Neuron-specific enolase is unaltered whereas S100B is elevated in serum of patients with schizophrenia-original research and meta-analysis. Psychiatry Res 2009, 167:66-72.
72. Scott L., Aperia A. Interaction between N-methyl-D-aspartic acid receptors and D1 dopamine receptors: an important mechanism for brain plasticity. Neuroscience 2009, 158:62-66.
73. Scott L., Kruse M.S., Forssberg H., Brismar H., Greengard P., Aperia A. Selective up-regulation of dopamine D1 receptors in dendritic spines by NMDA receptor activation. Proc Natl Acad Sci USA 2002, 99:1661-1664.
74. Seeman P. Glutamate and dopamine components in schizophrenia. J Psychiatry Neurosci 2009, 34:143-149.
75. Seeman P., Lee T. Antipsychotic drugs: direct correlation between clinical potency and presynaptic action on dopamine neurons. Science 1975, 188:1217-1219.
76. Sherman A.D., Hegwood T.S., Baruah S., Waziri R. Deficient NMDA-mediated glutamate release from synaptosomes of schizophrenics. Biol Psychiatry 1991, 30:1191-1198.
77. Steiner J., Bernstein H.G., Bielau H., Farkas N., Winter J., Dobrowolny H., et al. S100B-immunopositive glia is elevated in paranoid as compared to residual schizophrenia: a morphometric study. J Psychiatr Res 2008, 42:868-876.
78. Steiner J., Walter M., Wunderlich M.T., Bernstein H.G., Panteli B., Brauner M., et al. A new pathophysiological aspect of S100B in schizophrenia: potential regulation of S100B by its scavenger soluble RAGE. Biol Psychiatry 2009, 65:1107-1110.
79. Stone J.M., Morrison P.D., Pilowsky L.S. Glutamate and dopamine dysregulation in schizophrenia-a synthesis and selective review. J Psychopharmacol 2007, 21:440-452.
80. Tajima K., Fernandez H., Lopez-Ibor J.L., Carrasco J.L., Diaz-Marsa M. Schizophrenia treatment. Critical review on the drugs and mechanisms of action of antipsychotics. Actas Esp Psiquiatr 2009, 37:330-342.
81. Tamminga C.A., Holcomb H.H. Phenotype of schizophrenia: a review and formulation. Mol Psychiatry 2005, 10:27-39.
82. Tan Y., Luo X., Yang F., Zhang W., Wang Z., Zou Y., et al. Elevated serum S100B protein in first-episode drug-naive Chinese patients with schizophrenia. Schizophr Res 2010, 119:40-46.
83. Turner T.J. Nicotine enhancement of dopamine release by a calcium-dependent increase in the size of the readily releasable pool of synaptic vesicles. J Neurosci 2004, 24:11328-11336.
84. Vicente Miranda H., Outeiro T.F. The sour side of neurodegenerative disorders: the effects of protein glycation. J Pathol 2010, 221:13-25.
85. Vissel B., Krupp J.J., Heinemann S.F., Westbrook G.L. Intracellular domains of NR2 alter calcium-dependent inactivation of N-methyl-D-aspartate receptors. Mol Pharmacol 2002, 61:595-605.
86. Wang M., Lee F.J., Liu F. Dopamine receptor interacting proteins (DRIPs) of dopamine D1-like receptors in the central nervous system. Mol Cells 2008, 25:149-157.
87. Wayman G.A., Lee Y.S., Tokumitsu H., Silva A.J., Soderling T.R. Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 2008, 59:914-931.
88. Wojda U., Salinska E., Kuznicki J. Calcium ions in neuronal degeneration. IUBMB Life 2008, 60:575-590.
89. Wong A.H., Van Tol H.H. Schizophrenia: from phenomenology to neurobiology. Neurosci Biobehav Rev 2003, 27:269-306.
90. Yan S.D., Chen X., Fu J., Chen M., Zhu H., Roher A., et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996, 382:685-691.
91. Yarlagadda A. Role of calcium regulation in pathophysiology model of schizophrenia and possible interventions. Med Hypotheses 2002, 58:182-186.
92. Zhang X.Y., Xiu M.H., Chen da C., Zhu F.Y., Wu G.Y., Haile C.N., et al. Increased S100B serum levels in schizophrenic patients with tardive dyskinesia: association with dyskinetic movements. J Psychiatr Res 2010, 44:429-433.
93. Zhao C., Anand R., Braunewell K.H. Nicotine-induced Ca2+-myristoyl switch of neuronal Ca2+ sensor VILIP-1 in hippocampal neurons: a possible crosstalk mechanism for nicotinic receptors. Cell Mol Neurobiol 2009, 29:273-286.