Expression of protein phosphatase 2B (Calcineurin) subunit A isoforms in Rat hippocampus after traumatic brain injury

Journal of Neurotrauma

Volumn 27, Issue 1, 2010, Pages 109-120

  Bales, James W ^a,b   Ma, Xiecheng ^a,b   Yan, Hong Q ^a,b   Jenkins, Larry W ^a,b   Dixon, C Edward ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Calcineurin; Hippocampus; Traumatic brain injury

Indexed keywords

CALCINEURIN; CALCINEURIN A; CALCINEURIN A ALPHA; CALCINEURIN A BETA; ISOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DYSFUNCTION; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; ENZYME ACTIVATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN INJURIES; CA1 REGION, HIPPOCAMPAL; CALCINEURIN; CALCIUM; CALCIUM SIGNALING; DENTATE GYRUS; DOWN-REGULATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LONG-TERM POTENTIATION; MALE; NEURONAL PLASTICITY; NEURONS; PROTEIN ISOFORMS; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 76349104216     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2009.1072     Document Type: Article

References (59)

1. Albensi, B.C., Sullivan, P.G., Thompson, M.B., Scheff, S.W., and Mattson, M.P. (2000). Cyclosporin amerliorates traumatic brain injury induced alterations of hippocampal synaptic plasticity. Exp. Neurol. 162, 385-389.
2. Asai, A., Qiu, J., Narita, Y., Chi, S., Saito, N., Shinoura, N., Hamada, H., Kuchino, Y., and Kirino, T. (1999). High level calcineurin activity predisposes neuronal cells to apoptosis. J. Biol. Chem. 274, 34450-34458.
3. Banke, T.G., Bowie, D., Lee, H., Huganir, R.L., Schousboe, A., and Traynelis, S.F. (2000). Control of Glur1 AMPA receptor function by cAMP-dependent protein kinase. J. Neurosci. 20, 89-102.
4. Beattie, E.C., Carroll, R.C., Yu, X., Morishita, W., Yasuda, H., von Zastrow, M., Malenka, and R.C. (2000). Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 3, 1291-1300.
5. Butcher, S.P., Henshall, D.C., Teramura, Y., Iwasaki, K., and Sharkey, J. (1997). Neuroprotective actions of Fk506 in experimental stroke: in vivo evidence against an antiexeitotoxic mechanism. J. Neurosci. 17, 6939-6946.
6. Buzsaki, G. (1996). The hippocapmo-neocortical dialogue. Cereb. Cortex 6, 81-92.
7. D'Ambrosio, R., Maris, D.O., Grady, M.S., Winn, H.R., and Janigro, D. (1998). Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res. 786, 64-79.
8. Dell'Acqua, M.L., Smith, K.E., Gorski, J.A., Horne, E.A., Gibson, E.S., and Gomez, L.L. (2006). Regulation of neuronal PKA signaling through AKAP targeting dynamics. Eur. J. Cell Biol. 85, 627-633.
9. Deshpande, L.S., Sun, D.A., Sombati, S., Baranova, A., Wilson, M.S., Attkisson, E., Hamm, R.J., and DeLorenzo, R.J. (2008). Alterations in neuronal calcium levels are associated with cognitive deficits after traumatic brain injury. Neurosci. Lett. 441, 115-119.
10. Dixon, C.E., Bao, J., Long, D.A., and Hayes, R.L. (1996). Reduced evoked release of acetylcholine in the rodent hippocampus following traumatic brain injury. Pharmacol. Biochem. Behav. 53, 679-686.
11. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghmai, A.A., and Hayes, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262.
12. Dixon, C.E., Ma, X., and Marion, D.W. (1997). Effects of CDPcholine treatment on neurobehavioral deficits after TBI and on hippocampal and neocortical acetylcholine release. J. Neurotrauma 14, 161-169.
13. Eastwood, S.L., Salih, T., and Harrison, P.J. (2005). Differential expression of calcineurin a subunit mRNA isoforms during rat hippocampal and cerebellar development. Eur. J. Neurosci. 22, 3017-3024.
14. Fineman, I., Hovda, D.A., Smith, M., Yoshino, A., and Becker, D.P. (1993). Concussive brain injury is associated with a prolonged accumulation of calcium: A 45ca autoradiographic study. Brain Res. 624, 94-102.
15. Friberg, H., Ferrand-Drake, M., Bengtsoon, F., Halestrap, A.P., and Wieloch, T. (1998). Cyclosporin A, but not FK-506, protects mitochondria and neurons against hypoglycemic damage and implicates the mitochondrial permeability transition in cell death. J. Neurosci. 18, 5151-5159.
16. Groth, R.D., Dunbar, R.L., and Mermelstein, P.G. (2003). Calcineurin regulation of neuronal plasticity. Biochem. Biophys. Res. Commun. 311, 1159-1171.
17. Hall, E.D., Bryant, Y.D., Cho, W., and Sullivan, P.G. (2008). Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de olmos silver and fluorojade staining methods. J. Neurotrauma 25, 235-247.
18. Hamm, R.J., Temple, M.D., Pike, B.R., O'Dell, D.M., Buck, D.L., and Lyeth, B.G. (1996). Working memory deficits following traumatic brain injury in the rat. J. Neurotrauma 13, 317-323.
19. Hashimoto, T., Kawamata, T., Saito, N., Sasaki, M., Nakai, M., Niu, S., Taniguchi, T., Terashima, A., Yasuda, M., Maeda, K., and Tanaka, C. (1998). Isoform-specific redistribution of calcineurin a alpha and a beta in the hippocampal ca1 region of gerbils after transient ischemia. J. Neurochem. 70, 1289-1298.
20. Hovda, D.A., Becker, D.P., and Katayama, Y. (1992). Secondary injury and acidosis. J. Neurotrauma 9(Suppl. 1), S47-S60.
21. Hovda, D.A., Yoshino, A., Kawamata, T., Katayama, Y., Fineman, I., and Becker, D.P. (1990). The increase in local cerebral glucose utilization following fluid percussion brain injury is prevented with kynurenic acid and is associated with an increase in calcium. Acta Neurochir. Suppl. 51, 331-333.
22. Huang, R.Q., and Dillon, G.H. (1998). Maintenance of recombinant type a gamma-aminobutyric acid receptor function: Role of protein tyrosine phosphorylation and calcineurin. J. Pharmacol. Exp. Ther. 286, 243-255.
23. Kayyali, U.S., Zhang, W., Yee, A.G., Seidman, J.G., and Potter, H. (1997). Cytoskeletal changes in the brains of mice lacking calcineurin a alpha. J. Neurochem. 68, 1668-1678.
24. Klee, C.B., Crouch, T.H., and Krinks, M.H. (1979). Calcineurin: A calcium-and calmodulin-binding protein of the nervous system. Proc. Natl. Acad. Sci. U.S.A. 76, 6270-6273.
25. Kline, A.E., Massucci, J.L., Marion, D.W., and Dixon, C.E. (2002). Attenuation of working memory and spatial acquisition deficits after a delayed and chronic bromocriptine treatment regimen in rats subjected to traumatic brain injury by controlled cortical impact. J. Neurotrauma 19, 415-425.
26. Kline, A.E., Yan, H.Q., Bao, J., Marion, D.W., and Dixon, C.E. (2000). Chronic methylphenidate treatment enhances water maze performance following traumatic brain injury in rats. Neurosci. Lett. 280, 163-166.
27. Kurz, J.E., Hamm, R.J., Singleton, R.H., Povlishock, J.T., and Churn, S.B. (2005a). A persistent change in subcellular distribution of calcineurin following fluid percussion injury in the rat. Brain Res. 1048, 153-160.
28. Kurz, J.E., Parsons, J.T., Rana, A., Gibson, C.J., Hamm, R.J., and Churn, S.B. (2005b). A significant increase in both basal and maximal calcineurin activity following fluid percussion injury in the rat. J. Neurotrauma 22, 476-490.
29. Lee, H.K., Takamiya, K., Han, J.S., Man, H., Kim, C.H., Rumbaugh, G., Yu, S., Ding, L., He, C., Petralia, R.S., Wenthold, R.J., Gallagher, M., and Huganir, R.L. (2003). Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112, 631-643.
30. Lee, S.H., Liu, L., Wang, Y.T., and Sheng, M. (2002). Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36, 661-674.
31. Lemon, N., Manahan-Vaughan, O. (2006). Dopamine D1=D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J. Neurosci. 26, 7723-7729.
32. Li, S., Cullen, W.K., Anwyl, R., and Rowan, M.J. (2003). Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat. Neurosci. 6, 526-531.
33. Liu, Y.L., Fann, C.S., Liu, C.M., Chang, C.C., Yang, W.C., Hung, S.I., Yu, S.L., Hwang, T.J., Hsieh, M.H., Liu, C.C., Tsuang, M.M., Wu, J.Y., Jou, Y.S., Faraone, S.V., Tsuang, M.T., Chen, W.J., and Hwu, H.G. (2007). More evidence supports the association of ppp3cc with schizophrenia. Mol. Psychiatry 12, 966-974.
34. Lu, Y.M., Mansuy, I.M., Kandel, E.R., and Roder, J. (2000). Calcineurin-mediated ltd of gabaergic inhibition underlies the increased excitability of ca1 neurons associated with ltp. Neuron 26, 197-205.
35. Manalan, A.S., and Klee, C.B. (1983). Activation of calcineurin by limited proteolysis. Proc. Natl. Acad. Sci. U.S.A. 80, 4291-4295.
36. Mbye, L.H., Singh, I.N., Carrico, K.M., Saatman, K.E., and Hall, E.D. (2009). Comparative neuroprotective effects of cyclosporin a and nim811, a nonimmunosuppressive cyclosporin a analog, following traumatic brain injury. J. Cereb. Blood Flow Metab. 29, 87-97.
37. Morioka, M., Hamada, J., Ushio, Y., and Miyamoto, E. (1999). Potential role of calcineurin for brain ischemia and traumatic injury. Prog. Neurobiol. 58, 1-30.
38. Muller, R.U., Stead, M., and Pach, J. (1996). The hippocampus as a cognitive graph. J. Gen. Physiol. 107, 663-694.
39. Okonkwo, D.O., Buki, A., Siman, R., and Povlishock, J.T. (1999). Cyclosporin a limits calcium-induced axonal damage following traumatic brain injury. Neuroreport 10, 353-358.
40. Okonkwo, D.O., Melon, D.E., Pellicane, A.J., Mutlu, L.K., Rubin, D.G., Stone, J.R., and Helm, G.A. (2003). Dose-response of cyclosporin a in attenuating traumatic axonal injury in rat. Neuroreport 14, 463-466.
41. Reeves, T.M., Lyeth, B.G., and Povlishock, J.T. (1995). Long-term potentiation deficits and excitability changes following traumatic brain injury. Exp. Brain Res. 106, 248-256.
42. Rusnak, F., and Mertz, P. (2000). Calcineurin: Form and function. Physiol. Rev. 80, 1483-1521.
43. Sanders, M.J., Sick, T.J., Perez-Pinzon, M.A., Dietrich, W.D., and Green, E.J. (2000). Chronic failure in the maintenance of longterm potentiation following fluid percussion injury in the rat. Brain Res. 861, 69-76.
44. Scheff, S.W., Baldwin, S.A., Brown, R.W., and Kraemer, P.J. (1997). Morris water maze deficits in rats following traumatic brain injury: Lateral controlled cortical impact. J. Neurotrauma 14, 615-627.
45. Shapira, Y., Yadid, G., Cotev, S., and Shohami, E. (1989). Accumulation of calcium in the brain following head trauma. Neurol. Res. 11, 169-172.
46. Sick, T.J., Perez-Pinzon, M.A., and Feng, Z.Z. (1998). Impaired expression of long-term potentiation in hippocampal slices 4 and 48 h following mild fluid-percussion brain injury in vivo. Brain Res. 785, 287-292.
47. Sun, D.A., Deshpande, L.S., Sombati, S., Baranova, A., Wilson, M.S., Hamm, R.J. and DeLorenzo, R.J. (2008). Traumatic brain injury causes a long-lasting calcium (ca2+)-plateau of elevated intracellular ca levels and altered ca2+ homeostatic mechanisms in hippocampal neurons surviving brain injury. Eur. J. Neurosci. 27, 1659-1672.
48. Tong, G., Shepherd D., and Jahr, C.E. (1995). Synaptic desensitization of nmda receptors by calcineurin. Science 267, 1510-1512.
49. Uchino, H., Kuroda, Y., Morota, S., Hirabayashi, G., Ishii, N., Shibasaki, F., Ikeda, Y., Hansson, M.J., and Elmer, E. (2008). Probing the molecular mechanisms of neuronal degeneration: Importance of mitochondrial dysfunction and calcineurin activation. J. Anesth. 22, 253-262.
50. Victor, R.G., Thomas, G.D., Marban, E., and O'Rourke, B. (1995). Presynaptic modulation of cortical synaptic activity by calcineurin. Proc. Natl. Acad. Sci. U.S.A. 92, 6269-6273.
51. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284, 339-343.
52. Wang, J.H., and Kelly, P.T. (1996). The balance between postsynaptic ca(2+)-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn. Mem. 3, 170-181.
53. Winder, D.G., and Sweatt, J.D. (2001). Roles of serine=threonine phosphatases in hippocampal synaptic plasticity. Nat. Rev. Neurosci. 2, 461-474.
54. Wu, H.Y., Tomizawa, K., Oda, Y., Wei, F.Y., Lu, Y.F., Matsushita, M., Li, S.T., Moriwaki, A., and Matsui, H. (2004). Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J. Biol. Chem. 279, 4929-4940.
55. Yakel, J.L. (1997). Calcineurin regulation of synaptic function: From ion channels to transmitter release and gene transcription. Trends Pharmacol. Sci. 18, 124-134.
56. Yan, A.Q., Yu, J., Kline, A.E., Letart, P., Jenkins, L.W., Marion, D.W., and Dixon, C.E. (2000). Evaluation of combined fibroblast growth factor-2 and moderate hypothermia in traumatically brain injured rats. Brain Res. 887, 134-143.
57. Yang, S.A., and Klee, C.B. (2000). Low affinity ca2+-binding sites of calcineurin b mediate conformational changes in calcineurin a. Biochemistry (Mosc.) 39, 16147-16154.
58. Zeng, H., Chattarji, S., Barbarosie, M., Rondi-Reig, L., Philpot, B.D., Miyakawa, T., Bear, M.F., and Tonegawa, S. (2001). Forebrain-specific calcineurin knockout selectively impairs bidirectional synaptic plasticity and working=episodic-like memory. Cell 107, 617-629.
59. Zhuo, M., Zhang, W., Son, H., Mansuy, I., Sobel, R.A., Seidman, J., and Kandel, E.R. (1999). A selective role of calcineurin a alpha in synaptic depotentiation in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 96, 4650-4655.