Effects of disrupting calcium homeostasis on neuronal maturation: Early inhibition and later recovery

Cellular and Molecular Neurobiology

Volumn 28, Issue 3, 2008, Pages 389-409

  Ringler, Sarah L ^a   Aye, Jamie ^a   Byrne, Erica ^a   Anderson, Megan ^a   Turner, Christopher P ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Development; Glutamate; Growth cone; Morphology; Neurite

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); DIMETHYL SULFOXIDE; DIZOCILPINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; THAPSIGARGIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL CULTURE; CELL GROWTH; CELL MATURATION; IN VITRO STUDY; NEURITE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; CHELATING AGENTS; DIZOCILPINE MALEATE; EGTAZIC ACID; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; GROWTH CONES; HOMEOSTASIS; MODELS, BIOLOGICAL; NEURITES; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; THAPSIGARGIN;

RATTUS;

EID: 40349111629     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-007-9255-9     Document Type: Article

References (53)

1. Allen CN, Brady R, Swann J, Hori N, Carpenter DO (1988) N-methyl-d-aspartate (NMDA) receptors are inactivated by trypsin. Brain Res 458:147-150
2. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21
3. Bradke F, Dotti CG (1999) The role of local actin instability in axon formation. Science 283:1931-1934
4. Bradke F, Dotti CG (2000) Differentiated neurons retain the capacity to generate axons from dendrites. Curr Biol 10:1467-1470
5. Brewer GJ, Cotman CW (1989) NMDA receptor regulation of neuronal morphology in cultured hippocampal neurons. Neurosci Lett 99:268-273
6. Burgoyne RD, Pearce IA, Cambray-Deakin M (1988) N-methyl-d-aspartate raises cytosolic calcium concentration in rat cerebellar granule cells in culture. Neurosci Lett 91:47-52
7. 2+ and N-methyl-d-aspartate-stimulated neuritogenesis in rat cerebellar granule cell cultures. Brain Res Dev Brain Res 66:25-32
8. Chang S, De Camilli P (2001) Glutamate regulates actin-based motility in axonal filopodia. Nat Neurosci 4:787-793
9. Cheng C, Fass DM, Reynolds IJ (1999) Emergence of excitotoxicity in cultured forebrain neurons coincides with larger glutamate-stimulated [Ca(2+)](i) increases and NMDA receptor mRNA levels. Brain Res 849:97-108
10. Chilton JK, Gordon-Weeks PR (2006) Role of microtubules and MAPs during neuritogenesis. In: de Curtis I (ed) Intracellular mechanisms for neuritogenesis. Springer, Milan, pp 57-88
11. Cuppini R, Sartini S, Ambrogini P, Falcieri E, Maltarello MC, Gallo G (1999) Control of neuron outgrowth by NMDA receptors. J Submicrosc Cytol Pathol 31:31-40
12. Davenport RW, Dou P, Mills LR, Kater SB (1996) Distinct calcium signaling within neuronal growth cones and filopodia. J Neurobiol 31:1-15
13. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468
14. Fletcher TL, Banker GA (1989) The establishment of polarity by hippocampal neurons: the relationship between the stage of a cell's development in situ and its subsequent development in culture. Dev Biol 136:446-454
15. Fletcher TL, De Camilli P, Banker G (1994) Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development. J Neurosci 14:6695-6706
16. Gallo G, Letourneau PC (1999) Axon guidance: a balance of signals sets axons on the right track. Curr Biol 9:R490-R492
17. Gibney J, Zheng JQ (2003) Cytoskeletal dynamics underlying collateral membrane protrusions induced by neurotrophins in cultured Xenopus embryonic neurons. J Neurobiol 54:393-405
18. Gomez TM, Zheng JQ (2006) The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7:115-125
19. Harris LW, Sharp T, Gartlon J, Jones DN, Harrison PJ (2003) Long-term behavioural, molecular and morphological effects of neonatal NMDA receptor antagonism. Eur J Neurosci 18:1706-1710
20. Heng JE, Moscaritolo K, Dreyer EB (1995) NMDA sensitivity is neurite enhanced. Neuroreport 6:1890-1892
21. Heng JE, Zurakowski D, Vorwerk CK, Grosskreutz CL, Dreyer EB (1999) Cation channel control of neurite morphology. Brain Res Dev Brain Res 113:67-73
22. Herschkowitz N (1988) Brain development in the fetus, neonate and infant. Biol Neonate 54:1-19
23. Hoffmann H, Gremme T, Hatt H, Gottmann K (2000) Synaptic activity-dependent developmental regulation of NMDA receptor subunit expression in cultured neocortical neurons. J Neurochem 75:1590-1599
24. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283:70-74
25. Johnson EM Jr, Koike T, Franklin J (1992) A "calcium set-point hypothesis" of neuronal dependence on neurotrophic factor. Exp Neurol 115:163-166
26. Kater SB, Mattson MP, Cohan C, Connor J (1988) Calcium regulation of the neuronal growth cone. Trends Neurosci 11:315-321
27. Lema Tomé CM, Miller R, Bauer C, Nottingham C, Smith C, Blackstone K, Brown L, Bryan R, Leigh A, Brady M, Busch J, Turner CP (2007) Decline in age-dependent MK801-induced injury coincides with developmental surge in parvalbumin expression: cingulate and retrosplenial cortex. Dev Psychobiol 49:606-618
28. Lema Tomé CM, Bauer C, Nottingham C, Smith C, Blackstone K, Brown L, Hlavaty C, Nelson C, Daker R, Sola R, Miller R, Bryan R, Turner CP (2006) MK801-induced caspase-3 in the postnatal brain: Inverse relationship with calcium binding proteins. Neuroscience 141:1351-1363
29. Levitt P (2003) Structural and functional maturation of the developing primate brain. J Pediatr 143:S35-S45
30. Li JH, Wang YH, Wolfe BB, Krueger KE, Corsi L, Stocca G, Vicini S (1998) Developmental changes in localization of NMDA receptor subunits in primary cultures of cortical neurons. Eur J Neurosci 10:1704-1715
31. Lin WW, Wang CW, Chuang DM (1997) Effects of depolarization and NMDA antagonists on the role survival of cerebellar granule cells: a pivotal role for protein kinase C isoforms. J Neurochem 68:2577-2586
32. Mattson MP (1992) Calcium as sculptor and destroyer of neural circuitry. Exp Gerontol 27:29-49
33. Mattson MP, Kater SB (1987) Calcium regulation of neurite elongation and growth cone motility. J Neurosci 7:4034-4043
34. Ming Z, Griffith BL, Breese GR, Mueller RA, Criswell HE (2002) Changes in the effect of isoflurane on N-methyl-d-aspartic acid-gated currents in cultured cerebral cortical neurons with time in culture: evidence for subunit specificity. Anesthesiology 97:856-867
35. Murphy TH, Baraban JM (1990) Glutamate toxicity in immature cortical neurons precedes development of glutamate receptor currents. Brain Res Dev Brain Res 57:146-150
36. Pearce IA, Cambray-Deakin MA, Burgoyne RD (1987) Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells. FEBS Lett 223:143-147
37. Portera-Cailliau C, Pan DT, Yuste R (2003) Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J Neurosci 23:7129-7142
38. Ramoa AS, Alkondon M, Aracava Y, Irons J, Lunt GG, Deshpande SS, Wonnacott S, Aronstam RS, Albuquerque EX (1990) The anticonvulsant MK-801 interacts with peripheral and central nicotinic acetylcholine receptor ion channels. J Pharmacol Exp Ther 254:71-82
39. Rashid NA, Cambray-Deakin MA (1992) N-methyl-d-aspartate effects on the growth, morphology and cytoskeleton of individual neurons in vitro. Brain Res Dev Brain Res 67:301-308
40. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511-533
41. Santama N, Dotti CG, Lamond AI (1996) Neuronal differentiation in the rat hippocampus involves a stage-specific reorganization of subnuclear structure both in vivo and in vitro. Eur J Neurosci 8:892-905
42. Suarez-Isla BA, Pelto DJ, Thompson JM, Rapoport SI (1984) Blockers of calcium permeability inhibit neurite extension and formation of neuromuscular synapses in cell culture. Brain Res 316:263-270
43. Takashima S, Iida K, Deguchi K (1995) Periventricular leukomalacia, glial development and myelination. Early Hum Dev 43:177-184
44. Tang F, Dent EW, Kalil K (2003) Spontaneous calcium transients in developing cortical neurons regulate axon outgrowth. J Neurosci 23:927-936
45. Tucker LM, Morton AJ (1995) A simple method for quantifying changes in neuronal populations in primary cultures of dissociated rat brain. J Neurosci Methods 59:217-223
46. Turner CP, Pulciani D, Rivkees SA (2002) Reduction in intracellular calcium levels induces injury in developing neurons. Exp Neurol 178:21-32
47. Turner CP, Connell J, Blackstone K, Ringler SL (2007a) Loss of calcium and increased apoptosis within the same neuron. Brain Res 1128:50-60
48. Turner CP, Miller R, Smith C, Brown L, Blackstone K, Dunham SR, Strehlow R, Manfredi M, Slocum P, Iverson K, West M, Ringler SL, Berry ZC (2007b) Widespread neonatal brain damage following calcium channel blockade. Dev Neurosci 29:213-231
49. Ujihara H, Albuquerque EX (1992) Ontogeny of N-methyl-d-aspartate-induced current in cultured hippocampal neurons. J Pharmacol Exp Ther 263:859-867
50. Williams CV, Davenport RW, Dou P, Kater SB (1995) Developmental regulation of plasticity along neurite shafts. J Neurobiol 27:127-140
51. Zheng JQ, Wan JJ, Poo MM (1996) Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16:1140-1149
52. Zhong J, Russell SL, Pritchett DB, Molinoff PB, Williams K (1994) Expression of mRNAs encoding subunits of the N-methyl-d-aspartate receptor in cultured cortical neurons. Mol Pharmacol 45:846-853
53. Zhong J, Carrozza DP, Williams K, Pritchett DB, Molinoff PB (1995) Expression of mRNAs encoding subunits of the NMDA receptor in developing rat brain. J Neurochem 64:531-539