The L-type voltage-gated calcium channel modulates microglial pro-inflammatory activity

Molecular and Cellular Neuroscience

Volumn 64, Issue , 2015, Pages 104-115

  Espinosa Parrilla, J F ^a   Martinez Moreno M ^a   Gasull, X ^a   Mahy, N ^a   Rodriguez M J ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Dihydropyridine receptor; Excitotoxicity; L type voltage gated calcium channel; Neurodegeneration; Neuroinflammation

Indexed keywords

CALCIUM CHANNEL CAV1.2; CALCIUM CHANNEL CAV1.3; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL STIMULATING AGENT; CYTOKINE; N METHYL DEXTRO ASPARTIC ACID; NIFEDIPINE; NITRIC OXIDE; POTASSIUM CHLORIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; L-TYPE CALCIUM CHANNEL ALPHA(1C);

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELL POLARITY; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE RELEASE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOLECULAR PATHOLOGY; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; CELL LINE; CYTOLOGY; GENETICS; METABOLISM; MOUSE; WISTAR RAT;

RATTUS;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CELL LINE; HIPPOCAMPUS; MALE; MICE; MICROGLIA; NITRIC OXIDE; PHAGOCYTOSIS; RATS; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84922770340     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.12.004     Document Type: Article

References (52)

1. Ashcroft F.M., Proks P., Smith P.A., Ammälä C., Bokvist K., Rorsman P. Stimulus-secretion coupling in pancreatic beta cells. J. Cell. Biochem. 1994, 55:54-65. (Suppl.).
2. Bading H., Ginty D.D., Greenberg M.E. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 1993, 260:181-186.
3. Bataller R., Gasull X., Ginès P., Hellemans K., Görbig M.N., Nicolás J.M., Sancho-Bru P., De Las Heras D., Gual A., Geerts A., Arroyo V., Rodés J. In vitro and in vivo activation of rat hepatic stellate cells results in de novo expression of L-type voltage-operated calcium channels. Hepatology 2001, 33:956-962.
4. Bean B.P. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 1989, 340:153-156.
5. Berg M., Bruhn T., Frandsen A., Schousboe A., Diemer N.H. Kainic acid-induced seizures and brain damage in the rat: role of calcium homeostasis. J. Neurosci. Res. 1995, 40:641-646.
6. Bernal F., Petegnief V., Rodríguez M.J., Ursu G., Pugliese M., Mahy N. Nimodipine inhibits TMB-8 potentiation of AMPA-induced hippocampal neurodegeneration. J. Neurosci. Res. 2009, 87:1240-1249.
7. Catterall W.A., Perez-Reyes E., Snutch T.P., Striessnig J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev. 2005, 57:411-425.
8. Colton C.A., Wilcock D.M. Assessing activation states in microglia. CNS Neurol. Disord. Drug Targets 2010, 9:174-191.
9. 2+ channels. Am. J. Physiol. 1994, 266:C1650-C1655.
10. Crabtree G.R., Olson E.N. NFAT signaling: choreographing the social lives of cells. Cell 2002, 109:S67-S79. (Suppl.).
11. Damani M.R., Zhao L., Fontainhas A.M., Amaral J., Fariss R.N., Wong W.T. Age-related alterations in the dynamic behavior of microglia. Aging Cell 2011, 10:263-276.
12. Domercq M., Vázquez-Villoldo N., Matute C. Neurotransmitter signaling in the pathophysiology of microglia. Front. Cell. Neurosci. 2013, 7:49.
13. Färber K., Kettenmann H. Purinergic signaling and microglia. Pflugers Arch. 2006, 452:615-621.
14. 2+ and cGMP concentrations of sulphur-containing excitatory amino acids in cultured cerebral cortical neurons. J. Neurosci. Res. 1993, 34:331-339.
15. Fryer H.J., Knox R.J., Strittmatter S.M., Kalb R.G. Excitotoxic death of a subset of embryonic rat motor neurons in vitro. J. Neurochem. 1999, 72:500-513.
16. Graeber M.B., Streit W.J. Microglia: biology and pathology. Acta Neuropathol. 2010, 119:89-105.
17. Hegg C.C., Hu S., Peterson P.K., Thayer S.A. Beta-chemokines and human immunodeficiency virus type-1 proteins evoke intracellular calcium increases in human microglia. Neuroscience 2000, 98:191-199.
18. Hoffmann A., Kann O., Ohlemeyer C., Hanisch U.-K., Kettenmann H. Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. J. Neurosci. 2003, 23:4410-4419.
19. Horn J., de Haan R.J., Vermeulen M., Limburg M. Very early nimodipine use in stroke (VENUS): a randomized, double-blind, placebo-controlled trial. Stroke 2001, 32:461-465.
20. Jaskolski F., Mulle C., Manzoni O.J. An automated method to quantify and visualize colocalized fluorescent signals. J. Neurosci. Methods 2005, 146:42-49.
21. Kettenmann H., Hanisch U.-K., Noda M., Verkhratsky A. Physiology of microglia. Physiol. Rev. 2011, 91:461-553.
22. Li Y., Hu X., Liu Y., Bao Y., An L. Nimodipine protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. Neuropharmacology 2009, 56:580-589.
23. Liao B., Zhao W., Beers D.R., Henkel J.S., Appel S.H. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp. Neurol. 2012, 237:147-152.
24. Lipscombe D., Helton T.D., Xu W. L-type calcium channels: the low down. J. Neurophysiol. 2004, 92:2633-2641.
25. Logan M.R., Odemuyiwa S.O., Moqbel R. Understanding exocytosis in immune and inflammatory cells: the molecular basis of mediator secretion. J. Allergy Clin. Immunol. 2003, 111:923-932. (quiz 933).
26. Maghazachi A.A. Intracellular signaling events at the leading edge of migrating cells. Int. J. Biochem. Cell Biol. 2000, 32:931-943.
27. Manders E.M.M., Verbeek F.J., Aten J.A. Measurement of co-localisation of objects in dual-colour confocal images. J. Microsc. 1993, 169:375-382.
28. Mattsson P., Aldskogius H., Svensson M. Nimodipine-induced improved survival rate of facial motor neurons following intracranial transection of the facial nerve in the adult rat. J. Neurosurg. 1999, 90:760-765.
29. 2+ mobilization and functional responses in microglia: effects of low levels of ATP. J. Neurosci. Res. 2005, 81:349-356.
30. Ortega F.J., Gimeno-Bayon J., Espinosa-Parrilla J.F., Carrasco J.L., Batlle M., Pugliese M., Mahy N., Rodríguez M.J. ATP-dependent potassium channel blockade strengthens microglial neuroprotection after hypoxia-ischemia in rats. Exp. Neurol. 2012, 235:282-296.
31. Ortega F.J., Vidal-Taboada J.M., Mahy N., Rodríguez M.J. Molecular mechanisms of acute brain injury and ensuing neurodegeneration. Brain Damage - Bridging Between Basic Research and Clinics 2012, 163-186. InTech, Rijeka. A. González-Quevedo (Ed.).
32. Ortega F.J., Jolkkonen J., Mahy N., Rodríguez M.J. Glibenclamide enhances neurogenesis and improves long-term functional recovery after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2013, 33:356-364.
33. Paxinos G., Watson J. The Rat Brain in Stereotaxic Coordinates 1986, Academic Press.
34. Petegnief V., Ursu G., Bernal F., Mahy N. Nimodipine and TMB-8 potentiate the AMPA-induced lesion in the basal ganglia. Neurochem. Int. 2004, 44:287-291.
35. Rami A., Krieglstein J. Neuronal protective effects of calcium antagonists in cerebral ischemia. Life Sci. 1994, 55:2105-2113.
36. Rodríguez M.J., Ursu G., Bernal F., Cusí V., Mahy N. Perinatal human hypoxia-ischemia vulnerability correlates with brain calcification. Neurobiol. Dis. 2001, 8:59-68.
37. Rodríguez M.J., Prats A., Malpesa Y., Andrés N., Pugliese M., Batlle M., Mahy N. Pattern of injury with a graded excitotoxic insult and ensuing chronic medial septal damage in the rat brain. J. Neurotrauma 2009, 26:1823-1834.
38. Rodríguez M.J., Pugliese M., Mahy N. Drug abuse, brain calcification and glutamate-induced neurodegeneration. Curr. Drug Abuse Rev. 2009, 2:99-112.
39. ATP channels to treat neurodegenerative diseases: a mitochondrial issue. Oxid. Med. Cell. Longev. 2013, 2013:194546.
40. Schurr A. Neuroprotection against ischemic/hypoxic brain damage: blockers of ionotropic glutamate receptor and voltage sensitive calcium channels. Curr. Drug Targets 2004, 5:603-618.
41. Shideman C.R., Hu S., Peterson P.K., Thayer S.A. CCL5 evokes calcium signals in microglia through a kinase-, phosphoinositide-, and nucleotide-dependent mechanism. J. Neurosci. Res. 2006, 83:1471-1484.
42. Silei V., Fabrizi C., Venturini G., Salmona M., Bugiani O., Tagliavini F., Lauro G.M. Activation of microglial cells by PrP and beta-amyloid fragments raises intracellular calcium through L-type voltage sensitive calcium channels. Brain Res. 1999, 818:168-170.
43. Small D.L., Monette R., Buchan A.M., Morley P. Identification of calcium channels involved in neuronal injury in rat hippocampal slices subjected to oxygen and glucose deprivation. Brain Res. 1997, 753:209-218.
44. Soto D., Comes N., Ferrer E., Morales M., Escalada A., Palés J., Solsona C., Gual A., Gasull X. Modulation of aqueous humor outflow by ionic mechanisms involved in trabecular meshwork cell volume regulation. Investig. Ophthalmol. Vis. Sci. 2004, 45:3650-3661.
45. Strober W. Trypan blue exclusion test of cell viability. Curr. Protoc. Immunol. 2001, 21:3B. A.3B.1-A.3B.2.
46. Toba Y., Pakiam J.G., Wray S. Voltage-gated calcium channels in developing GnRH-1 neuronal system in the mouse. Eur. J. Neurosci. 2005, 22:79-92.
47. Tokuhara N., Namiki K., Uesugi M., Miyamoto C., Ohgoh M., Ido K., Yoshinaga T., Yamauchi T., Kuromitsu J., Kimura S., Miyamoto N., Kasuya Y. N-type calcium channel in the pathogenesis of experimental autoimmune encephalomyelitis. J. Biol. Chem. 2010, 285:33294-33306.
48. ATP channel opener diazoxide ameliorates disease progression in a murine model of multiple sclerosis. J. Neuroinflammation 2011, 8:149.
49. Virgili N., Mancera P., Chanvillard C., Wegner A., Wappenhans B., Rodríguez M.J., Infante-Duarte C., Espinosa-Parrilla J.F., Pugliese M. Diazoxide attenuates autoimmune encephalomyelitis and modulates lymphocyte proliferation and dendritic cell functionality. J. Neuroimmune Pharmacol. 2014, 9:558-568.
50. Zamponi G.W., Snutch T.P. Advances in voltage-gated calcium channel structure, function and physiology. Biochim. Biophys. Acta 2013, 1828:1521.
51. Zhang H., Wang F.W., Yao L.L., Hao A.J. Microglia-friend or foe. Front. Biosci. (Schol. Ed.) 2011, 3:869-883.
52. Zhu D., Li R., Liu G., Hua W. Nimodipine inhibits calcium-independent nitric oxide synthase activity in transient focal cerebral ischemia rats and cultured mouse astroglial cells. Life Sci. 1999, 65:PL221-PL231.