Mild in vitro trauma induces rapid Glur2 endocytosis, robustly augments calcium permeability and enhances susceptibility to secondary excitotoxic insult in cultured Purkinje cells

Brain

Volumn 130, Issue 10, 2007, Pages 2528-2542

  Bell, Joshua D ^a,b   Ai, Jinglu ^a   Chen, Yonghong ^a   Baker, Andrew J ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

AMPA; Calcium; Cerebellum; Endocytosis; GluR2; Purkinje cells; Stretch; Traumatic brain injury

Indexed keywords

1 NAPHTHYLACETYL SPERMINE; 12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCIUM; GLUTAMATE RECEPTOR 2; NIFEDIPINE; PROPIDIUM IODIDE; PROTEIN KINASE C; PROTEIN KINASE C ALPHA INHIBITOR; SPERMINE DERIVATIVE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CALCIUM TRANSPORT; CELL CULTURE; CELL LOSS; CELL MEMBRANE PERMEABILITY; CHANNEL GATING; CONTROLLED STUDY; DENDRITIC CELL; DISEASE MODEL; DISEASE PREDISPOSITION; DOWN REGULATION; ENDOCYTOSIS; FEMALE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; NEUROPROTECTION; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PURKINJE CELL; RAT; SPIKE WAVE; STATISTICAL SIGNIFICANCE; SYNAPTIC MEMBRANE;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CALCIUM; CARBAZOLES; CELL DEATH; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; ENDOCYTOSIS; ENZYME INHIBITORS; INDOLES; NEUROPROTECTIVE AGENTS; PROTEIN KINASE C; PURKINJE CELLS; RATS; RATS, WISTAR; RECEPTORS, AMPA; SPERMINE; STRESS, MECHANICAL;

EID: 34848869976     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm164     Document Type: Article

References (77)

1. Ai J, Baker A. Long-term potentiation of evoked presynaptic response at CA3-CA1 synapses by transient oxygen-glucose deprivation in rat brain slices. Exp Brain Res 2006; 169: 126-9.
2. Ai J, Liu E, Park E, Baker AJ. Structural and functional alterations of cerebellum following fluid percussion injury in rats. Exp Brain Res 2007; 177: 95-112.
3. Amar AP, Levy ML. Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury. Neurosurgery 1999; 44: 1027-39.
4. Arundine M, Tymianski M. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 2004; 61: 657-68.
5. Arundine M, Chopra GK, Wrong AW, Lei S, Aarts M, MacDonald JF, et al. Enhanced vulnerability to NMDA toxicity in sublethal traumatic neuronal injury in-vitro. J Neurotrauma 2003; 20: 1377-95.
6. Arundine M, Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 2003; 34: 325-37.
7. Arundine M, Aarts M, Lau A, Tymianski M. Vulnerability of central neurons to secondary insults after in vitro mechanical stretch. J Neurosci 2004; 24: 8106-23.
8. Audinat E, Knöpfel T, Gähwiler BH. Responses to excitatory amino acids of Purkinje cells and neurones of the deep nuclei in cerebellar slice cultures. J Physiol 1990; 430: 297-313.
9. Bartoletti DC, Harrison GI, Weaver JC. The number of molecules taken up by electroporated cells: quantitative determination. FEBS Lett 1989; 256: 4-10.
10. Blackman JA, Patrick PD, Buck ML, Rust RS Jr. Paroxysmal autonomic instability with dystonia after brain injury. Arch Neurol 2004; 61: 321-8.
11. Brorson JR, Bleakman D, Chard PS, Miller RJ. Calcium directly permeates kainate/α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors in cultured cerebellar Purkinje neurons. Mol Pharmacol 1992; 41: 603-8.
12. 2+ entry via AMPA/KA receptors and excitotoxicity in cultured cerebellar Purkinje cells. J Neurosci 1994; 14: 187-97.
13. Brorson JR, Manzolillo PA, Gibbons SJ, Miller RJ. AMPA receptor desensitization predicts the selective vulnerability of cerebellar Purkinje cells to excitotoxicity. J Neurosci 1995; 15: 4515-24.
14. Bruno VMG, Goldberg MP, Dugan LL, Giffard RG, Choi DW. Neuroprotective effect of hypothermia in cortical cultures exposed to oxygen-glucose deprivation or excitatory amino acids. J Neurochem 1994; 63: 1398-1406.
15. Burette A, Khatri L, Wyszynski M, Sheng M, Ziff EB, Weinberg RJ. Differential cellular and subcellular localization of AMPA receptor-binding protein and glutamate receptor-interacting protein. J Neurosci 2001; 21: 495-503.
16. Burnashev N, Monyer H, Seeburg PH, Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 1992; 8: 189-98.
17. David JC, Yamada KA, Bagwe MR, Goldberg MP. AMPA receptor activation is rapidly toxic to cortical astrocytes when desensitization is blocked. J Neurosci 1996; 16: 200-9.
18. Ellis EF, McKinney JS, Willoughby KA, Liang S, Povlishock JT. A New model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J Neurotrauma 1995; 12: 325-39.
19. Faden AI. Neuroprotection and traumatic brain injury: theoretical option or realistic proposition. Curr Opin Neurol 2002; 15: 707-12.
20. Fukuda K, Aihara N, Sagar SM, et al. Purkinje cell vulnerability to mild traumatic brain injury. J Neurotrauma 1996; 13: 255-66.
21. Fujimoto ST, Longhi L, Saatman KE, Conte V, Stocchetti N, McIntosh TK. Motor and cognitive function evaluation following experimental traumatic brain injury. Neurosci Biobehav Rev 2004; 28: 365-78.
22. Gale SD, Johnson SC, Bigler ED, Blatter DD. Trauma-induced degenerative changes in brain injury: a morphometric analysis of three patients with preinjury and postinjury MR scans. J Neurotrauma 1995; 12: 151-8.
23. Geddes DM, Cargill RS. An in vitro model of neurotrauma: device characterization and calcium response to mechanical stretch. J Biomech Eng 2001; 123: 247-55.
24. Geddes DM, Cargill RS, LaPlaca MC. Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability. J Neurotrauma 2003; 20: 1039-49.
25. Geddes-Klein DM, Schiffman KB, Meaney DF. Mechanisms and consequences of neuronal stretch injury in vitro differ with the model of trauma. J Neurotrauma 2006; 23: 193-204.
26. Gift EA, Weaver JC. Simultaneous quantitative determination of electroporated molecular uptake and subsequent cell survival using gel microdrops and flow cytometry. Cytometry 2000; 9: 243-9.
27. Goforth PB, Ellis EF, Satin LS. Enhancement of AMPA-mediated current after traumatic injury in cortical neurons. J Neurosci 1999; 19: 7367-74.
28. Gorrie C, Oakes S, Duflou J, Blumbergs P, Waite PM. Axonal injury in children after motor vehicle crashes: extent, distribution, and size of axonal swellings using beta-APP immunohistochemistry. J Neurotrauma 2002; 19: 1171-82.
29. Greger IH, Khatri L, Ziff EB. RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 2002; 34: 759-72.
30. Groc L, Choquet D. AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res 2006; 326: 423-38.
31. Hume RI, Dingledine R, Heinemann SF. Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 1991; 253: 1028-31.
32. Igarashi T, Potts MB, Noble-Haeusslein LJ. Injury severity determines Purkinje cell loss and microglial activation in the cerebellum after cortical contusion injury. Exp Neurol 2007; 203: 258-68.
33. Joels M, Yool AJ, Gruol DL. Unique properties of non-N-methyld-aspartate excitatory responses in cultured Purkinje cells. Proc Natl Acad Sci USA 1989; 86: 3404-8.
34. Joyal CC, Meyer C, Jacquart G, Mahler P, Caston J, Lalonde R. Effects of midline and lateral cerebellar lesions on motor coordination and spatial orientation. Brain Res 1996; 739: 1-11.
35. Keinenen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, et al. A family of AMPA-selective glutamate receptors. Science 1990; 249: 556-60.
36. Kersel DA, Marsh NV, Havill JH, Sleigh JW. Neuropsychological functioning during the year following severe traumatic brain injury. Brain Inj 2001a; 15: 283-96.
37. Kersel DA, Marsh NV, Havill JH, Sleigh JW. Psychosocial functioning during the year following severe traumatic brain injury. Brain Inj 2001b; 15: 683-96.
38. Kwak S, Weiss JH. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr Opin Neurobiol 2006; 16: 281-7.
39. Lalonde R, Strazielle C. The effects of cerebellar damage on maze learning in animals. Cerebellum 2003; 2: 300-9.
40. Lambolez B, Audinat E, Bochet P, Crtpel F, Rossier J. AMPA receptor subunits expressed by single Purkinje cells. Neuron 1992; 9: 247-58.
41. LaPlaca MC, Lee VM, Thibault LE. An in vitro model of traumatic neuronal injury: loading rate-dependent changes in acute cytosolic calcium and lactate dehydrogenase release. J Neurotrauma 1997; 14: 355-68.
42. Leggio MG, Molinari M, Neri P, Graziano A, Mandolesi L, Petrosini L. Representation of actions in rats: the role of cerebellum in learning spatial performances by observation. Proc Natl Acad Sci USA 2000; 97: 2320-5.
43. Linden DJ, Smeyne M, Connor JA. Induction of cerebellar long.term depression in culture requires postsynaptic action of sodium ions. Neuron 1993; 11: 1093-100.
44. Liu SQ, Cull-Candy SG. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 2000; 405: 454-8.
45. Liu B, Liao M, Mielke JG, Ning K, Chen Y, Li L, et al. Ischemic insults direct glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites. J Neurosci 2006; 26: 5309-19.
46. Llano I, Marty A, Johnson JW, Ascher P, Gahwiler BH. Patch-clamp recording of amino acid-activated responses in "organotypic" slice-cultures. Proc Natl Acad Sci USA 1988; 85: 3221-5.
47. Luchter S, Walz MC. Long-term consequences of head injury. J Neurotrauma 1995; 12: 517-26.
48. Lusardi TA, Wolf JA, Putt ME, Smith DH, Meaney DF. Effect of acute calcium influx after mechanical stretch injury in vitro on the viability of hippocampal neurons. J Neurotrauma 2004; 21: 61-72.
49. Manni E, Petrosini L. A century of cerebellar somatotopy: a debated representation. Nat Rev Neurosci 2004; 5: 241-9.
50. Mautes AE, Fukuda K, Noble LJ. Cellular response in the cerebellum after midline traumatic brain injury in the rat. Neurosci Lett 1996; 214: 95-8.
51. McKinney JS, Willoughby KA, Liang S, Ellis EF. Stretch-induced injury of cultured neuronal, glial, and endothelial cells. Effect of polyethylene glycol-conjugated superoxide dismutase. Stroke 1996; 27: 934-40.
52. Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci 2001; 15: 700-12.
53. Middleton FA, Strick PL. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 2000; 31: 236-50.
54. Middleton FA, Strick PL. The cerebellum: an overview. Trends Neurosci 1998; 21: 367-9.
55. Middleton FA, Strick PL. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science 1994; 266: 458-61.
56. Momiyama A, Feldmeyer D, Cull-Candy SG. Identification of a native low-conductance NMDA channel with reduced sensitivity to Mg2+ in rat central neurones. J Physiol 1996; 494: 479-92.
57. Momiyama A, Silver RA, Hausser M, Notomi T, Wu Y, Shigemoto R, et al. The density of AMPA receptors activated by a transmitter quantum at the climbing fibre-Purkinje cell synapse in immature rats. J Physiol 2003; 549: 75-92.
58. Monyer H, Seeburg PH, Wisden W. Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 1991; 6: 799-810.
59. Ogoshi F, Weiss JH. Heterogeneity of Ca2+-permeable AMPA/kainate channel expression in hippocampal pyramidal neurons: fluorescence imaging and immunocytochemical assessment. J Neurosci 2003; 23: 10521-30.
60. Park E, McKnight S, Ai J, Baker AJ. Purkinje cell vulnerability to mild and severe forebrain head trauma. J Neuropathol Exp Neurol 2006; 65: 226-34.
61. Petrosini L, Leggio MG, Molinari M. The cerebellum in the spatial problem solving: a co-star or a guest star? Prog Neurobiol 1998; 56: 191-210.
62. Pike BR, Zhao X, Newcomb JK, Glenn CC, Anderson DK, Hayes RL. Stretch injury causes calpain and caspase-3 activation and necrotic and apoptotic cell death in septo-hippocampal cell cultures. J Neurotrauma 2000; 17: 283-98.
63. Sattler R, Charlton MP, Hafner M, Tymianski M. Determination of the time-course and extent of neurotoxicity at defined temperatures in cultured neurons using a modified multi-well plate fluorescence scanner. J Cereb Blood Flow Metab 1997; 17: 455-63.
64. Schmahmann JD. An emerging concept. The cerebellar contribution to higher function. Arch Neurol 1991; 48: 1178-87.
65. Slemmer JE, Matser EJ, De Zeeuw CI, Weber JT. Repeated mild injury causes cumulative damage to hippocampal cells. Brain 2002; 125: 2699-709.
66. Slemmer JE, Weber JT, De Zeeuw CI. Cell death, glial protein alterations and elevated S-100 beta release in cerebellar cell cultures following mechanically induced trauma. Neurobiol Dis 2004; 15: 563-72.
67. Sommer B, Keinanen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, et al. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 1990; 249: 1580-5.
68. Sorimachi M. Calcium permeability of non-N-methyl-D-aspartate receptor channels in immature Purkinje cells: studies using Fura- microfluorometry. J Neurochem 1993; 60: 1236-43.
69. Soto-Ares G, Vinchon M, Delmaire C, Abeciden E, Dhellemes P, Pruvo JP. Cerebellar atrophy after severe traumatic head injury in children. Childs Nerv Syst 2001; 17: 263-69.
70. Tanaka J, Matsuzaki M, Tarusawa E, Momiyama A, Molnar E, Kasai H, et al. Number and density of AMPA receptors in single synapses in immature cerebellum. J Neurosci 2005; 25: 799-807.
71. Teasdale GM, Graham DI. Craniocerebral trauma: protection and retrieval of the neuronal population after injury. Neurosurgery 1998; 43: 723-37.
72. Tempia F, Kano M, Schneggenburger R, Schirra C, Garaschuk O, Plant T, et al. Fractional calcium current through neuronal AMPA-receptor channels with a low calcium permeability. J Neurosci 1996; 16: 456-66.
73. Weber JT, Rzigalinski BA, Willoughby KA, Moore SF, Ellis EF. Alterations in calcium-mediated signal transduction after traumatic injury of cortical neurons. Cell Calcium 1999; 26: 289-99.
74. 2+ permeable AMPA or kainate receptors: possible key factors in selective neurodegeneration. Trends Neurosci 2000; 23: 365-71.
75. Yuzaki M, Forrest D, Verselis LM, Sun SC, Curran T, Connor JA. Functional NMDA receptors are transiently active and support the survival of Purkinje cells in culture. J Neurosci 1996; 16: 4651-61.
76. Zhang L, Rzigalinski BA, Ellis EF, Satin LS. Reduction of voltage-dependent Mg2+ blockade of NMDA current in mechanically injured neurons. Science 1996; 274: 1921-3.
77. Zhao X, Newcomb JK, Pike BR, Wang KK, d'Avella D, Hayes RL. Novel characteristics of glutamate-induced cell death in primary septohippocampal cultures: relationship to calpain and caspase-3 protease activation. J Cereb Blood Flow Metab 2000; 20: 550-62.