Expression of the cGMP-specific phosphodiesterases 2 and 9 in normal and Alzheimer's disease human brains

European Journal of Neuroscience

Volumn 25, Issue 11, 2007, Pages 3332-3338

  Reyes Irisarri, Elisabet ^a   Markerink Van Ittersum, Marjanne ^b   Mengod, Guadalupe ^a   De Vente, Jan ^b  

^a INST D INVESTIGACIONS B   (Spain)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Alzheimer's disease; Entorhinal cortex; Hippocampus; In situ hybridization

Indexed keywords

CYCLIC GMP; MESSENGER RNA; PHOSPHODIESTERASE; PHOSPHODIESTERASE 2; PHOSPHODIESTERASE 9; UNCLASSIFIED DRUG;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CLAUSTRUM; CONTROLLED STUDY; ENTORHINAL CORTEX; FEMALE; GENE EXPRESSION; GLOBUS PALLIDUS; HIPPOCAMPUS; HISTOCHEMISTRY; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; INSULA; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; PUTAMEN; VISUAL CORTEX;

3',5'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASE; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN; CYCLIC GMP; FEMALE; GENE EXPRESSION; HUMANS; IN SITU HYBRIDIZATION; MALE; MIDDLE AGED; PHOSPHORIC DIESTER HYDROLASES; STATISTICS, NONPARAMETRIC;

EID: 34249871389     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05589.x     Document Type: Article

References (56)

1. Alderton, W.K., Cooper, C.E. Knowles, R.G. (2001) Nitric oxide synthases: structure, function and inhibition. Biochem. J., 357, 593 615.
2. Ando, H., Shi, Q., Kusakabe, T., Ohya, T., Suzuki, N. Urano, A. (2004) Localization of mRNAs encoding alpha and beta subunits of soluble guanylyl cyclase in the brain of rainbow trout: comparison with the distribution of neuronal nitric oxide synthase. Brain Res., 1013, 13 29.
3. Andreeva, S.G., Dikkes, P., Epstein, P.M. Rosenberg, P.A. (2001) Expression of cGMP-specific phosphodiesterase 9A mRNA in the rat brain. J. Neurosci., 21, 9068 9076.
4. Beavo, J.A. (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev., 75, 725 748.
5. Beavo, J.A. Brunton, L.L. (2002) Cyclic nucleotide research - still expanding after half a century. Nat. Rev. Mol. Cell Biol., 3, 710 718.
6. Benzing, W.C. Mufson, E.J. (1995) Increased number of NADPH-d-positive neurons within the substantia innominata in Alzheimer's disease. Brain Res., 670, 351 355.
7. Bicker, G. (1998) NO news from insect brains. Trends Neurosci., 21, 349 355.
8. Blusztajn, J.K. Berse, B. (2000) The cholinergic neuronal phenotype in Alzheimer's disease. Metab. Brain Dis., 15, 45 64.
9. Boess, F.G., Hendrix, M., van der Staay, F.J., Erb, C., Schreiber, R., van Staveren, W., de Vente, J., Prickaerts, J., Blokland, A. Koenig, G. (2004) Inhibition of phosphodiesterase 2 increases neuronal cGMP, synaptic plasticity and memory performance. Neuropharmacology, 47, 1081 1092.
10. Bonkale, W.L., Winblad, B., Ravid, R. Cowburn, R.F. (1995) Reduced nitric oxide responsive soluble guanylyl cyclase activity in the superior temporal cortex of patients with Alzheimer's disease. Neurosci. Lett., 187, 5 8.
11. Buchholzer, M.L. Klein, J. (2002) NMDA-induced acetylcholine release in mouse striatum: role of NO synthase isoforms. J. Neurochem., 82, 1558 1560.
12. Budworth, J., Meillerais, S., Charles, I. Powell, K. (1999) Tissue distribution of the human soluble guanylate cyclases. Biochem. Biophys. Res. Commun., 263, 696 701.
13. Conti, M. Jin, S.L. (1999) The molecular biology of cyclic nucleotide phosphodiesterases. Prog. Nucl. Acid Res. Mol. Biol., 63, 1 38.
14. Cummings, J.L., Vinters, H.V., Cole, G.M. Khachaturian, Z.S. (1998) Alzheimer's disease: etiologies, pathophysiology, cognitive reserve, and treatment opportunities. Neurology, 51, S2 S17.
15. Dawson, V.L. Dawson, T.M. (1998) Nitric oxide in neurodegeneration. Prog. Brain Res., 118, 215 229.
16. Ding, J.D., Burette, A., Nedvetsky, P.I., Schmidt, H.H. Weinberg, R.J. (2004) Distribution of soluble guanylyl cyclase in the rat brain. J. Comp. Neurol., 472, 437 448.
17. Domek-Lopacinska, K., Markerink-Van Ittersum, M., Steinbusch, H.W. de Vente, J. (2005a) Changes in expression of cGMP selective phosphodiesterases 2, 5 and 9 in the rat brain during aging. BMC Pharmacol., 5 (Suppl. 1 15.
18. Domek-Lopacinska, K.W.M., Markerink-Van Ittersum, M., Steinbusch, H.W. de Vente, J. (2005b) Nitric oxide-induced cGMP synthesis in the cholinergic system during the development and aging of the rat brain. Brain Res. Dev. Brain Res., 158, 72 81.
19. Fisher, D.A., Smith, J.F., Pillar, J.S., St Denis, S.H. Cheng, J.B. (1998) Isolation and characterization of PDE9A, a novel human cGMP-specific phosphodiesterase. J. Biol. Chem., 273, 15 559 15 564.
20. Fujishige, K., Kotera, J. Omori, K. (1999) Striatum- and testis-specific phosphodiesterase PDE10A isolation and characterization of a rat PDE10A [in process citation]. Eur. J. Biochem., 266, 1118 1127.
21. Garthwaite, G., Bartus, K., Malcolm, D., Goodwin, D., Kollb-Sielecka, M., Dooldeniya, C. Garthwaite, J. (2006) Signaling from blood vessels to CNS axons through nitric oxide. J. Neurosci., 26, 7730 7740.
22. Gibb, B.J. Garthwaite, J. (2001) Subunits of the nitric oxide receptor, soluble guanylyl cyclase, expressed in rat brain. Eur. J. Neurosci., 13, 539 544.
23. Guevara-Guzman, R., Emson, P.C. Kendrick, K.M. (1994) Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J. Neurochem., 62, 807 810.
24. Guipponi, M., Scott, H.S., Kudoh, J., Kawasaki, K., Shibuya, K., Shintani, A., Asakawa, S., Chen, H., Lalioti, M.D., Rossier, C., Minoshima, S., Shimizu, N. Antonarakis, S.E. (1998) Identification and characterization of a novel cyclic nucleotide phosphodiesterase gene (PDE9A) that maps to 21q22.3: alternative splicing of mRNA transcripts, genomic structure and sequence. Hum. Genet., 103, 386 392.
25. Hendrix, M. (2005) Selective inhibitors of cGMP phosphodiesterases as procognitive agents. BMC Pharmacol., 5 (Suppl. I S5.
26. Hyman, B.T., Marzloff, K., Wenniger, J.J., Dawson, T.M., Bredt, D.S. Snyder, S.H. (1992) Relative sparing of nitric oxide synthase-containing neurons in the hippocampal formation in Alzheimer's disease. Ann. Neurol., 32, 818 820.
27. Ikarashi, Y., Takahashi, A., Ishimaru, H., Shiobara, T. Maruyama, Y. (1998) The role of nitric oxide in striatal acetylcholine release induced by N-methyl-D-aspartate. Neurochem. Int., 33, 255 261.
28. Kendrick, K.M., Guevara-Guzman, R.R.C., Christensen, J., Ostergaard, K. Emson, P.C. (1996) NMDA and kainate-evoked release of nitric oxide and classical transmitters in the rat striatum: in vivo evidence that nitric oxide may play a neuroprotective role. Eur. J. Neurosci., 8, 2619 2634.
29. Koesling, D., Russwurm, M., Mergia, E., Mullershausen, F. Friebe, A. (2004) Nitric oxide-sensitive guanylyl cyclase: structure and regulation. Neurochem. Int., 45, 813 819.
30. Kraus, M.M. Prast, H. (2001) The nitric oxide system modulates the in vivo release of acetylcholine in the nucleus accumbens induced by stimulation of the hippocampal fornix/fimbria-projection. Eur. J. Neurosci., 14, 1105 1112.
31. Mo, E., Amin, H., Bianco, I.H. Garthwaite, J. (2004) Kinetics of a cellular nitric oxide/cGMP/phosphodiesterase-5 pathway. J. Biol. Chem., 279, 26 149 26 158.
32. Norris, P.J., Faull, R.L. Emson, P.C. (1996) Neuronal nitric oxide synthase (nNOS) mRNA expression and NADPH-diaphorase staining in the frontal cortex, visual cortex and hippocampus of control and Alzheimer's disease brains. Brain Res. Mol. Brain Res., 41, 36 49.
33. Paxinos, G. (1990) The Human Nervous System. Academic Press, Inc., San Diego.
34. Pifarre, P., Garcia, A. Mengod, G. (2007) Species differences in the localization of soluble guanylyl cyclase subunits in monkey and rat brain. J. Comp. Neurol., 500, 942 957.
35. Prast, H., Tran, M.H., Fischer, H. Philippu, A. (1998) Nitric oxide-induced release of acetylcholine in the nucleus accumbens: role of cyclic GMP, glutamate, and GABA. J. Neurochem., 71, 266 273.
36. Rebeck, G.W., Marzloff, K. Hyman, B.T. (1993) The pattern of NADPH-diaphorase staining, a marker of nitric oxide synthase activity, is altered in the perforant pathway terminal zone in Alzheimer's disease. Neurosci. Lett., 152, 165 168.
37. Repaske, D.R., Corbin, J.G., Conti, M. Goy, M.F. (1993) A cyclic GMP-stimulated cyclic nucleotide phosphodiesterase gene is highly expressed in the limbic system of the rat brain. Neuroscience, 56, 673 686.
38. Rosman, G.J., Martins, T.J., Sonnenburg, W.K., Beavo, J.A., Ferguson, K. Loughney, K. (1997) Isolation and characterization of human cDNAs encoding a cGMP-stimulated 3′,5′-cyclic nucleotide phosphodiesterase. Gene, 191, 89 95.
39. Russwurm, M. Koesling, D. (2004) NO activation of guanylyl cyclase. EMBO J., 23, 4443 4450.
40. Schmidt, K., Schrammel, A., Koesling, D. Mayer, B. (2001) Molecular mechanisms involved in the synergistic activation of soluble guanylyl cyclase by YC-1 and nitric oxide in endothelial cells. Mol. Pharmacol., 59, 220 224.
41. Scholz, N.L. Truman, J.W. (2000) Invertebrate models for studying NO-mediated signaling. In Steinbusch, H.W., de Vente, J. Vincent, S.R. (Eds), Handbook of Chemical Neuroanatomy, Vol. 20. Elsevier, Amsterdam, pp. 417 441.
42. Seeger, T.F., Bartlett, B., Coskran, T.M., Culp, J.S., James, L.C., Krull, D.L., Lanfear, J., Ryan, A.M., Schmidt, C.J., Strick, C.A., Varghese, A.H., Williams, R.D., Wylie, P.G. Menniti, F.S. (2003) Immunohistochemical localization of PDE10A in the rat brain. Brain Res., 985, 113 126.
43. Soderling, S.H., Bayuga, S.J. Beavo, J.A. (1998) Identification and characterization of a novel family of cyclic nucleotide phosphodiesterases. J. Biol. Chem., 273, 15 553 15 558.
44. Southam, E. Garthwaite, J. (1993) The nitric oxide-cyclic GMP signalling pathway in rat brain. Neuropharmacology, 32, 1267 1277.
45. Stamler, J.S. Hausladen, A. (1998) Oxidative modifications in nitrosative stress. Nat. Struct. Biol., 5, 247 249.
46. Stasch, J.P., Becker, E.M., Alonso-Alija, C., Apeler, H., Dembowsky, K., Feurer, A., Gerzer, R., Minuth, T., Perzborn, E., Pleiss, U., Schroder, H., Schroeder, W., Stahl, E., Steinke, W., Straub, A. Schramm, M. (2001) NO-independent regulatory site on soluble guanylate cyclase. Nature, 410, 212 215.
47. van Staveren, W.C., Steinbusch, H.W., Markerink-Van Ittersum, M., Repaske, D.R., Goy, M.F., Kotera, J., Omori, K., Beavo, J.A. de Vente, J. (2003) mRNA expression patterns of the cGMP-hydrolyzing phosphodiesterases types 2, 5, and 9 during development of the rat brain. J. Comp. Neurol., 467, 566 580.
48. Thorns, V., Hansen, L. Masliah, E. (1998) nNOS expressing neurons in the entorhinal cortex and hippocampus are affected in patients with Alzheimer's disease. Exp. Neurol., 150, 14 20.
49. Trabace, L. Kendrick, K.M. (2000) Nitric oxide can differentially modulate striatal neurotransmitter concentrations via soluble guanylate cyclase and peroxynitrite formation. J. Neurochem., 75, 1664 1674.
50. de Vente, J. (2004) cGMP: a second messenger for acetylcholine in the brain? Neurochem. Int., 45, 799 812.
51. de Vente, J., Hopkins, D.A., Markerink-Van Ittersum, M., Emson, P.C., Schmidt, H.H. Steinbusch, H.W. (1998) Distribution of nitric oxide synthase and nitric oxide-receptive, cyclic GMP-producing structures in the rat brain. Neuroscience, 87, 207 241.
52. de Vente, J., Markerink-Van Ittersum, M., van Abeelen, J., Emson, P.C., Axer, H. Steinbusch, H.W. (2000) NO-mediated cGMP synthesis in cholinergic neurons in the rat forebrain: effects of lesioning dopaminergic or serotonergic pathways on nNOS and cGMP synthesis. Eur. J. Neurosci., 12, 507 519.
53. de Vente, J., Markerink-Van Ittersum, M., Axer, H. Steinbusch, H.W. (2001) Nitric-oxide-induced cGMP synthesis in cholinergic neurons in the rat brain. Exp. Brain Res., 136, 480 491.
54. Vincent, S.R. (2000) Histochemistry of the nitric oxyde synthase in the central nervous system. Handbook of Chemical Neuroanatomy, Vol. 17. Elsevier, Amsterdam, pp. 19 49.
55. Vincent, S.R. Kimura, H. (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience, 46, 755 784.
56. Yew, D.T., Wong, H.W., Li, W.P., Lai, H.W. W.H. (1999) Nitric oxide synthase neurons in different areas of normal aged and Alzheimer's brains. Neuroscience, 89, 675 686.