Role of calcineurin in activity-dependent pattern formation in the dorsal lateral geniculate nucleus of the ferret

Journal of Neurobiology

Volumn 56, Issue 2, 2003, Pages 153-162

  Leamey, Catherine A ^a,b   Ho Pao, Chrystal L ^a,c   Sur, Mriganka ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c TRINITY EVANGELICAL DIVINITY SCHOOL   (United States)

Author keywords

Development; FK506; Protein phosphatase 2B; Synaptic plasticity; Visual thalamus

Indexed keywords

AMOXICILLIN; ANTIBIOTIC AGENT; CALCINEURIN; CYCLIC GMP; HORSERADISH PEROXIDASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SYNTHETIC PEPTIDE; TACROLIMUS; TETRAMETHYLBENZIDINE; WHEAT GERM AGGLUTININ;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; FERRET; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LATERAL GENICULATE BODY; NERVE CELL PLASTICITY; NONHUMAN; OSMOTIC MINIPUMP; PRIORITY JOURNAL; RETINA GANGLION CELL; SYNAPSE; VISUAL NERVOUS SYSTEM;

AFFERENT PATHWAYS; ANIMALS; ANIMALS, NEWBORN; ANTIBODY SPECIFICITY; CALCINEURIN; FERRETS; GENICULATE BODIES; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE AGENTS; MOTOR ACTIVITY; NEUROPIL; RETINA; TACROLIMUS; UP-REGULATION;

EID: 0037490797     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10226     Document Type: Article

References (61)

1. Arancio O, Antonova I, Gambaryan S, Lohmann SM, Wood JS, Lawrence DS, Hawkins RD. 2001. Presynaptic Role of cGMP-Dependent Protein Kinase during Long-Lasting Potentiation. J Neurosci 21:143-149.
2. Arancio O, Kiebler M, Lee CJ, Lev-Ram V, Tsien RY, Kandel ER, Hawkins RD. 1996. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87:1025-1035.
3. Bear MF. 1996. NMDA-receptor-dependent synaptic plasticity in the visual cortex. Prog Brain Res 108:205-218.
4. Bear MF, Malenka RC. 1994. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
5. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
6. Bredt DS, Ferris CD, Snyder SH. 1992. Nitric oxide synthase regulatory sites. Phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J Biol Chem 267:10976-10981.
7. Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasova E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, Marks AR. 1994. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77:513-523.
8. Burley JR, Sihra TS. 2000. A modulatory role for protein phosphatase 2B (calcineurin) in the regulation of Ca2+ entry. Eur J Neurosci 12:2881-2891.
9. Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M, Pisani A, Bernardi G. 1999. A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci 19:2489-2499.
10. Cameron AM, Steiner JP, Roskams AJ, Ali SM, Ronnett GV, Snyder SH. 1995. Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell 83:463-472.
11. Cramer KS, Angelucci A, Hahm JO, Bogdanov MB, Sur M. 1996. A role for nitric oxide in the development of the ferret retinogeniculate projection. J Neurosci 16:7995-8004.
12. Cramer KS, Moore CI, Sur M. 1995. Transient expression of NADPH-diaphorase in the lateral geniculate nucleus of the ferret during early postnatal development. J Comp Neurol 353:306-316.
13. Cramer KS, Sur M. 1996. The role of NMDA receptors and nitric oxide in retinogeniculate development. Prog Brain Res 108:235-244.
14. Cramer KS, Sur M. 1997. Blockade of afferent impulse activity disrupts on/off sublamination in the ferret lateral geniculate nucleus. Brain Res Dev Brain Res 98:287-290.
15. Cramer KS, Sur M. 1999. The neuronal form of nitric oxide synthase is required for pattern formation by retinal afferents in the ferret lateral geniculate nucleus. Brain Res Dev Brain Res 116:79-86.
16. Dawson TM, Steiner JP, Dawson VL, Dinerman JL, Uhl GR, Snyder SH. 1993. Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc Natl Acad Sci USA 90:9808-9812.
17. Funauchi M, Haruta H, Tsumoto T. 1994. Effects of an inhibitor for calcium/calmodulin-dependent protein phosphatase, calcineurin, on induction of long-term potentiation in rat visual cortex. Neurosci Res 19:269-278.
18. Genazzani AA, Carafoli E, Guerini D. 1999. Calcineurin controls inositol 1,4,5-trisphosphate type 1 receptor expression in neurons. Proc Natl Acad Sci USA 96:5797-5801.
19. Hahm JO, Cramer KS, Sur M. 1999. Pattern formation by retinal afferents in the ferret lateral geniculate nucleus: developmental segregation and the role of N-methyl-D-aspartate receptors. J Comp Neurol 411:327-345.
20. Hahm JO, Langdon RB, Sur M. 1991. Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351:568-570.
21. Halpain S, Greengard P. 1990. Activation of NMDA receptors induces rapid dephosphorylation of the cytoskeletal protein MAP2. Neuron 5:237-246.
22. Hodgkiss JP, Kelly JS. 1995. Only 'de novo' long-term depression (LTD) in the rat hippocampus in vitro is blocked by the same low concentration of FK506 that blocks LTD in the visual cortex. Brain Res 705:241-246.
23. Ikegami S, Inokuchi K. 2000. Antisense DNA against calcineurin facilitates memory in contextual fear conditioning by lowering the threshold for hippocampal long-term potentiation induction. Neuroscience 98:637-646.
24. Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P, Marks AR. 1992. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 267:9474-9477.
25. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
26. Lai MM, Hong JJ, Ruggiero AM, Burnett PE, Slepnev VI, De Camilli P, Snyder SH. 1999. The calcineurin-dynamin 1 complex as a calcium sensor for synaptic vesicle endocytosis. J Biol Chem 274:25963-25966.
27. Leamey CA, Ho-Pao CL, Sur M. 2001. Disruption of retinogeniculate pattem formation by inhibition of soluble guanylyl cyclase. J Neurosci 21:3871-3880.
28. Lieberman DN, Mody I. 1994. Regulation of NMDA channel function by endogenous Ca(2+)-dependent phosphatase. Nature 369:235-239.
29. Linden DC, Guillery RW, Cucchiaro J. 1981. The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J Comp Neurol 203:189-211.
30. Liu JP, Sim AT, Robinson PJ. 1994. Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science 265:970-973.
31. Lu YF, Hayashi Y, Moriwaki A, Tomizawa K, Matsui H. 1996. FK506, a Ca2+/calmodulin-dependent phosphatase inhibitor, inhibits the induction of long-term potentiation in the rat hippocampus. Neurosci Lett 205:103-106.
32. Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose AM, Weitlauf C, Kandel ER, Winder DG, Mansuy IM. 2001. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 104:675-686.
33. Marks B, McMahon HT. 1998. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr Biol 8:740-749.
34. Mesulam MM. 1978. Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106-117.
35. Morales M, Fifkova E. 1989. Distribution of MAP2 in dendritic spines and its colocalization with actin. An immunogold electron-microscope study. Cell Tissue Res 256:447-456.
36. Mulkey RM, Endo S, Shenolikar S, Malenka RC. 1994. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486-488.
37. Mulkey RM, Herron CE, Malenka RC. 1993. An essential role for protein phosphatases in hippocampal long-term depression. Science 261:1051-1055.
38. Nichols RA, Suplick GR, Brown JM. 1994. Calcineurin-mediated protein dephosphorylation in brain nerve terminals regulates the release of glutamate. J Biol Chem 269:23817-23823.
39. Nishio K, Arioka H, Ishida T, Fukumoto H, Kurokawa H, Sata M, Ohata M, Saijo N. 1995. Enhanced interaction between tubulin and microtubule-associated protein 2 via inhibition of MAP kinase and CDC2 kinase by paclitaxel. Int J Cancer 63:688-693.
40. Penn AA, Riquelme PA, Feller MB, Shatz CJ. 1998. Competition in retinogeniculate patterning driven by spontaneous activity. Science 279:2108-2112.
41. Quinlan EM, Halpain S. 1996. Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors. Neuron 16:357-368.
42. Rocha M, Sur M. 1995. Rapid acquisition of dendritic spines by visual thalamic neurons after blockade of N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 92:8026-8030.
43. Roe AW, Garraghty PE, Sur M. 1989. Terminal arbors of single ON-center and OFF-center X and Y retinal ganglion cell axons within the ferret's lateral geniculate nucleus. J Comp Neurol 288:208-242.
44. Sharkey J, Butcher SP. 1994. Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature 371:336-339.
45. Shatz CJ, Stryker MP. 1988. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87-89.
46. Shi J, Townsend M, Constantine-Paton M. 2000. Activity-dependent induction of tonic calcineurin activity mediates a rapid developmental downregulation of NMDA receptor currents. Neuron 28:103-114.
47. Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER. 1996. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015-1023.
48. Steiner JP, Dawson TM, Fotuhi M, Glatt CE, Snowman AM, Cohen N, Snyder SH. 1992. High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature 358:584-587.
49. Steiner JP, Dawson TM, Fotuhi M, Snyder SH. 1996. Immunophilin regulation of neurotransmitter release. Mol Med 2:325-333.
50. Stryker MP, Zahs KR. 1983. On and off sublaminae in the lateral geniculate nucleus of the ferret. J Neurosci 3:1943-1951.
51. Sutton JK, Brunso-Bechtold JK. 1991. A Golgi study of dendritic development in the dorsal lateral geniculate nucleus of normal ferrets. J Comp Neurol 309:71-85.
52. Tong G, Shepherd D, Jahr CE. 1995. Synaptic desensitization of NMDA receptors by calcineurin. Science 267:1510-1512.
53. Torii N, Kamishita T, Otsu Y, Tsumoto T. 1995. An inhibitor for calcineurin, FK506, blocks induction of long-term depression in rat visual cortex. Neurosci Lett 185:1-4.
54. Wang JH, Kelly PT. 1996. The balance between postsynaptic Ca(2+)-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn Mem 3:170-181.
55. Wang JH, Kelly PT. 1997. Postsynaptic calcineurin activity downregulates synaptic transmission by weakening intracellular Ca2+ signaling mechanisms in hippocampal CA1 neurons. J Neurosci 17:4600-4611.
56. Winder DG, Sweatt JD. 2001. Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Nat Rev Neurosci 2:461-474.
57. Wu J, Wang Y, Rowan MJ, Anwyl R. 1997. Evidence for involvement of the neuronal isoform of nitric oxide synthase during induction of long-term potentiation and long-term depression in the rat dentate gyrus in vitro. Neuroscience 78:393-398.
58. Wu J, Wang Y, Rowan MJ, Anwyl R. 1998. Evidence for involvement of the cGMP-protein kinase G signaling system in the induction of long-term depression, but not long-term potentiation, in the dentate gyrus in vitro. J Neurosci 18:3589-3596.
59. Wu LG, Saggau P. 1995. Block of multiple presynaptic calcium channel types by omega-conotoxin- MVIIC at hippocampal CA3 to CA1 synapses. J Neurophysiol 73:1965-1972.
60. Zeng H, Chattarji S, Barbarosie M, Rondi-Reig L, Philpot BD, Miyakawa T, Bear MF, Tonegawa S. 2001. Forebrain-specific calcineurin knockout selectively impairs bidirectional synaptic plasticity and working/episodic-like memory. Cell 107:617-629.
61. Zucker RS. 1993. Calcium and transmitter release. J Physiol Paris 87:25-36.