The expression mechanism of the residual LTP in the CA1 region of BDNF k.o. mice is insensitive to NO synthase inhibition

Brain Research

Volumn 1391, Issue , 2011, Pages 14-23

  Leßmann, Volkmar ^a,b   Stroh Kaffei, Sigrid ^a   Steinbrecher, Violetta ^a   Edelmann, Elke ^b   Brigadski, Tanja ^a,b   Kilb, Werner ^a   Luhmann, Heiko J ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Neurotrophins; Nitric oxide; Retrograde messenger; Synaptic plasticity; TrkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTRIC POTENTIAL; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HIPPOCAMPAL CA1 REGION; INTRACELLULAR SIGNALING; LONG TERM POTENTIATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL;

ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CA1 REGION, HIPPOCAMPAL; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE;

ANIMALIA; MUS;

EID: 79955629734     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.03.061     Document Type: Article

References (57)

1. Abidin, I., Kohler, T., Weiler, E., Zoidl, G., Eysel, U.T., Lessmann, V., Mittmann, T., 2006. Reduced presynaptic efficiency of excitatory synaptic transmission impairs LTP in the visual cortex of BDNF-heterozygous mice. Eur. J. Neurosci. 24, 3519-3531.
2. Akaneya, Y., Tsumoto, T., Kinoshita, S., Hatanaka, H., 1997. Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J. Neurosci. 17, 6707-6716. (Pubitemid 27366623)
3. Arancio, O., Kiebler, M., Lee, C.J., Lev-Ram, V., Tsien, R.Y., Kandel, E.R., Hawkins, R.D., 1996a. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87, 1025-1035. (Pubitemid 26427986)
4. Arancio, O., Lev-Ram, V., Tsien, R.Y., Kandel, E.R., Hawkins, R.D., 1996b. Nitric oxide acts as a retrograde messenger during long-term potentiation in cultured hippocampal neurons. J. Physiol. Paris 90, 321-322. (Pubitemid 27113370)
5. Bohme, G.A., Bon, C., Stutzmann, J.M., Doble, A., Blanchard, J.C., 1991. Possible involvement of nitric oxide in long-term potentiation. Eur. J. Pharmacol. 199, 379-381.
6. Bon, C.L., Garthwaite, J., 2001. Nitric oxide-induced potentiation of CA1 hippocampal synaptic transmission during baseline stimulation is strictly frequency-dependent. Neuropharmacology 40, 501-507. (Pubitemid 32209035)
7. Bon, C.L., Garthwaite, J., 2003. On the role of nitric oxide in hippocampal long-term potentiation. J. Neurosci. 23, 1941-1948. (Pubitemid 36314749)
8. Burette, A., Zabel, U., Weinberg, R.J., Schmidt, H.H., Valtschanoff, J.G., 2002. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J. Neurosci. 22, 8961-8970. (Pubitemid 35379066)
9. Canossa, M., Giordano, E., Cappello, S., Guarnieri, C., Ferri, S., 2002. Nitric oxide down-regulates brain-derived neurotrophic factor secretion in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 99, 3282-3287.
10. Carmignoto, G., Pizzorusso, T., Tia, S., Vicini, S., 1997. Brain-derived neurotrophic factor and nerve growth factor potentiate excitatory synaptic transmission in the rat visual cortex. J. Physiol. 498 (Pt 1), 153-164. (Pubitemid 27056886)
11. Chetkovich, D.M., Klann, E., Sweatt, J.D., 1993. Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. Neuroreport 4, 919-922. (Pubitemid 23202249)
12. Drake, C.T., Milner, T.A., Patterson, S.L., 1999. Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity. J. Neurosci. 19, 8009-8026. (Pubitemid 30225797)
13. Ernst, A.F., Gallo, G., Letourneau, P.C., McLoon, S.C., 2000. Stabilization of growing retinal axons by the combined signaling of nitric oxide and brain-derived neurotrophic factor. J. Neurosci. 20, 1458-1469. (Pubitemid 30220425)
14. Gartner, A., Polnau, D.G., Staiger, V., Sciarretta, C., Minichiello, L., Thoenen, H., Bonhoeffer, T., Korte, M., 2006. Hippocampal long-term potentiation is supported by presynaptic and postsynaptic tyrosine receptor kinase B-mediated phospholipase Cgamma signaling. J. Neurosci. 26, 3496-3504.
15. Gooney, M., Messaoudi, E., Maher, F.O., Bramham, C.R., Lynch, M.A., 2004. BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events. Neurobiol. Aging 25, 1323-1331. (Pubitemid 39299170)
16. Gottmann, K., Mittmann, T., Lessmann, V., 2009. BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp. Brain Res. 199, 203-234.
17. Hardingham, N., Fox, K., 2006. The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation. J. Neurosci. 26, 7395-7404. (Pubitemid 44315208)
18. Haul, S., Godecke, A., Schrader, J., Haas, H.L., Luhmann, H.J., 1999. Impairment of neocortical long-term potentiation in mice deficient of endothelial nitric oxide synthase. J. Neurophysiol. 81, 494-497. (Pubitemid 29264496)
19. Hawkins, R.D., Son, H., Arancio, O., 1998. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog. Brain Res. 118, 155-172.
20. Holscher, C., 1997. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 20, 298-303. (Pubitemid 27348739)
21. Hopper, R.A., Garthwaite, J., 2006. Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J. Neurosci. 26, 11513-11521. (Pubitemid 44772122)
22. Husi, H., Ward, M.A., Choudhary, J.S., Blackstock, W.P., Grant, S.G., 2000. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3, 661-669.
23. Itami, C., Kimura, F., Kohno, T., Matsuoka, M., Ichikawa, M., Tsumoto, T., Nakamura, S., 2003. Brain-derived neurotrophic factor-dependent unmasking of "silent" synapses in the developing mouse barrel cortex. Proc. Natl. Acad. Sci. USA 100, 13069-13074.
24. Ji, Y., Lu, Y., Yang, F., Shen, W., Tang, T.T., Feng, L., Duan, S., Lu, B., 2010. Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat. Neurosci. 13, 302-309.
25. Kang, H., Schuman, E.M., 1995. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662.
26. Klocker, N., Cellerino, A., Bahr, M., 1998. Free radical scavenging and inhibition of nitric oxide synthase potentiates the neurotrophic effects of brain-derived neurotrophic factor on axotomized retinal ganglion cells in vivo. J. Neurosci. 18, 1038-1046. (Pubitemid 28112925)
27. Koh, J.Y., Gwag, B.J., Lobner, D., Choi, D.W., 1995. Potentiated necrosis of cultured cortical neurons by neurotrophins. Science 268, 573-575.
28. Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H., Bonhoeffer, T., 1995. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92, 8856-8860.
29. Korte, M., Griesbeck, O., Gravel, C., Carroll, P., Staiger, V., Thoenen, H., Bonhoeffer, T., 1996. Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. USA 93, 12547-12552.
30. Lander, H.M., Jacovina, A.T., Davis, R.J., Tauras, J.M., 1996. Differential activation of mitogen-activated protein kinases by nitric oxide-related species. J. Biol. Chem. 271, 19705-19709.
31. Lessmann, V., Gottmann, K., Heumann, R., 1994. BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport 6, 21-25.
32. Lessmann, V., Heumann, R., 1998. Modulation of unitary glutamatergic synapses by neurotrophin-4/5 or brain-derived neurotrophic factor in hippocampal microcultures: presynaptic enhancement depends on pre-established paired-pulse facilitation. Neuroscience 86, 399-413. (Pubitemid 28293919)
33. Levine, E.S., Dreyfus, C.F., Black, I.B., Plummer, M.R., 1995. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Acad. Sci. USA 92, 8074-8077.
34. Levine, E.S., Crozier, R.A., Black, I.B., Plummer, M.R., 1998. Brain-derived neurotrophic factor modulates hippocampal synaptic transmission by increasing N-methyl-D-aspartic acid receptor activity. Proc. Natl. Acad. Sci. USA 95, 10235-10239.
35. Lewin, G.R., Barde, Y.A., 1996. Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
36. Li, Y.X., Xu, Y., Ju, D., Lester, H.A., Davidson, N., Schuman, E.M., 1998. Expression of a dominant negative TrkB receptor, T1, reveals a requirement for presynaptic signaling in BDNF-induced synaptic potentiation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 95, 10884-10889.
37. Lu, Y., Christian, K., Lu, B., 2008. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol. Learn. Mem. 89, 312-323.
38. Luhmann, H.J., Raabe, K., Qu, M., Zilles, K., 1998. Characterization of neuronal migration disorders in neocortical structures: extracellular in vitro recordings. Eur. J. Neurosci. 10, 3085-3094.
39. Malenka, R.C., Nicoll, R.A., 1999. Long-term potentiation - a decade of progress? Science 285, 1870-1874.
40. Messaoudi, E., Bardsen, K., Srebro, B., Bramham, C.R., 1998. Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J. Neurophysiol. 79, 496-499. (Pubitemid 28133842)
41. Mizuno, M., Yamada, K., Olariu, A., Nawa, H., Nabeshima, T., 2000. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J. Neurosci. 20, 7116-7121.
42. O'Dell, T.J., Huang, P.L., Dawson, T.M., Dinerman, J.L., Snyder, S.H., Kandel, E.R., Fishman, M.C., 1994. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 265, 542-546. (Pubitemid 24265004)
43. Patterson, S.L., Abel, T., Deuel, T.A., Martin, K.C., Rose, J.C., Kandel, E.R., 1996. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 1137-1145. (Pubitemid 26227235)
44. Pozzo-Miller, L.D., Gottschalk, W., Zhang, L., McDermott, K., Du, J., Gopalakrishnan, R., Oho, C., Sheng, Z.H., Lu, B., 1999. Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci. 19, 4972-4983. (Pubitemid 29270132)
45. Samdani, A.F., Newcamp, C., Resink, A., Facchinetti, F., Hoffman, B.E., Dawson, V.L., Dawson, T.M., 1997. Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J. Neurosci. 17, 4633-4641. (Pubitemid 27246921)
46. Schuman, E.M., Madison, D.V., 1991. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254, 1503-1506. (Pubitemid 21917489)
47. Schuman, E.M., Madison, D.V., 1994. Locally distributed synaptic potentiation in the hippocampus. Science 263, 532-536. (Pubitemid 24082755)
48. Selig, D.K., Segal, M.R., Liao, D., Malenka, R.C., Malinow, R., Nicoll, R.A., Lisman, J.E., 1996. Examination of the role of cGMP in long-term potentiation in the CA1 region of the hippocampus. Learn. Mem. 3, 42-48.
49. Son, H., Hawkins, R.D., Martin, K., Kiebler, M., Huang, P.L., Fishman, M.C., Kandel, E.R., 1996. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87, 1015-1023. (Pubitemid 26427985)
50. Son, H., Lu, Y.F., Zhuo, M., Arancio, O., Kandel, E.R., Hawkins, R.D., 1998. The specific role of cGMP in hippocampal LTP. Learn. Mem. 5, 231-245.
51. Williams, J.H., Li, Y.G., Nayak, A., Errington, M.L., Murphy, K.P., Bliss, T.V., 1993. The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent. Neuron 11, 877-884. (Pubitemid 23347472)
52. Wilson, R.I., Yanovsky, J., Godecke, A., Stevens, D.R., Schrader, J., Haas, H.L., 1997. Endothelial nitric oxide synthase and LTP. Nature 386, 338. (Pubitemid 27154468)
53. Xiong, H., Yamada, K., Han, D., Nabeshima, T., Enikolopov, G., Carnahan, J., Nawa, H., 1999. Mutual regulation between the intercellular messengers nitric oxide and brain-derived neurotrophic factor in rodent neocortical neurons. Eur. J. Neurosci. 11, 1567-1576.
54. Xu, B., Gottschalk, W., Chow, A., Wilson, R.I., Schnell, E., Zang, K., Wang, D., Nicoll, R.A., Lu, B., Reichardt, L.F., 2000. The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J. Neurosci. 20, 6888-6897.
55. Yuen, E.C., Gunther, E.C., Bothwell, M., 2000. Nitric oxide activation of TrkB through peroxynitrite. Neuroreport 11, 3593-3597.
56. Zakharenko, S.S., Patterson, S.L., Dragatsis, I., Zeitlin, S.O., Siegelbaum, S.A., Kandel, E.R., Morozov, A., 2003. Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39, 975-990. (Pubitemid 37130213)
57. Zhuo, M., Small, S.A., Kandel, E.R., Hawkins, R.D., 1993. Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science 260, 1946-1950. (Pubitemid 23258276)