Role of extracellular cGMP and of hyperammonemia in the impairment of learning in rats with chronic hepatic failure. Therapeutic implications

Neurochemistry International

Volumn 48, Issue 6-7, 2006, Pages 441-446

  Erceg, Slaven ^a   Monfort, Pilar ^a   Cauli, Omar ^a   Montoliu, Carmina ^b   Llansola, Marta ^a   Piedrafita, Blanca ^a   Felipo, Vicente ^a  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^b HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

Author keywords

Extracellular cGMP; Hepatic encephalopathy; Hyperammonemia; Learning; Phosphodiesterase

Indexed keywords

8 BROMO CYCLIC GMP; AMMONIA; CYCLIC GMP; CYCLIC GMP DERIVATIVE; GLUTAMIC ACID; NITRIC OXIDE; PHOSPHODIESTERASE INHIBITOR; SCOPOLAMINE; SILDENAFIL; ZAPRINAST;

ACUTE DISEASE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN FUNCTION; BRAIN LEVEL; CEREBELLUM; CHRONIC DISEASE; CHRONIC LIVER DISEASE; COGNITION; CONTINUOUS INFUSION; DISEASE MODEL; DRUG PENETRATION; HEPATIC ENCEPHALOPATHY; HUMAN; HYPERAMMONEMIA; IN VIVO STUDY; INTELLECTUAL IMPAIRMENT; LEARNING; LEARNING DISORDER; LIVER FAILURE; LONG TERM EXPOSURE; NEUROMODULATION; NEUROPATHOLOGY; NEUROPSYCHIATRY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNDROME;

ANIMALS; BRAIN; CHRONIC DISEASE; CYCLIC GMP; EXTRACELLULAR FLUID; GLUTAMIC ACID; HEPATIC ENCEPHALOPATHY; HUMANS; HYPERAMMONEMIA; LEARNING; LIVER FAILURE; NITRIC OXIDE; PHOSPHODIESTERASE INHIBITORS; PIPERAZINES; PURINONES; RATS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 33645867381     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2005.10.016     Document Type: Article

References (39)

1. Aguilar M.A., Minarro J., and Felipo V. Chronic moderate hyperammonemia impairs active and passive avoidance behavior and conditional discrimination learning in rats. Exp. Neurol. 161 (2000) 704-713
2. Amodio P., Del Piccolo F., Marchetti, Angeli P., Iemmolo R., Caregaro L., Merkel C., Gerunda G., and Gatta A. Clinical features and survival of cirrhotic patients with subclinical cognitive alterations detected by the number connection test and computerized psychometric tests. Hepatology 29 (1999) 1662-1667
3. Amodio P., Montagnese S., Gatta A., and Morgan M.Y. Characteristics of minimal hepatic encephalopathy. Metab. Brain Dis. 19 (2004) 253-267
4. Azorin I., Minana M.D., Felipo V., and Grisolia S. A simple animal model of hyperammonemia. Hepatology 10 (1989) 311-314
5. Bernabeu R., Schmitz P., Faillace M., Izquierdo I., and Medina J.H. Hippocampal cGMP and cAMP are differentially involved in memory processing of inhibitor avoidance learning. Neuroreport 7 (1996) 585-588
6. Bernabeu R., Schroder N., Quevedo J., Cammarota M., Izquierdo I., and Medina J.H. Further evidence for the involvement of a hippocampal cGMP/cGMP-dependent protein kinase cascade in memory consolidation. Neuroreport 8 (1997) 2221-2224
7. Chen J., Zhang P., Zuo P., and Tang L. Memory-related changes of nitric oxide synthase activity and nitrite level in rat brain. Neuroreport 8 (1997) 1771-1774
8. Corbalan R., Chatauret N., Behrends S., Butterworth R.F., and Felipo V. Region selective alterations of soluble guanylate cyclase content and modulation in brain of cirrhotic patients. Hepatology 36 (2002) 1155-1162
9. Danysz W., Zajaczkowski W., and Parsons C.G. Modulation of learning processes by ionotropic glutamate receptor ligands. Behav. Pharmacol. 6 (1995) 455-474
10. Elithorn A., Lunzer M., and Weinman J. Cognitive deficit associated with chronic hepatic encephalopathy and their response to levodopa. J. Neurol. Neurosurg. Psych. 38 (1975) 794-798
11. Erceg S., Monfort P., Hernandez-Viadel M., Rodrigo R., Montoliu C., and Felipo V. Oral administration of sildenafil restores learning ability in rats with hyperammonemia and with portacaval shunts. Hepatology 41 (2005) 299-306
12. Erceg S., Monfort P., Hernandez-Viadel M., Llansola M., Montoliu C., and Felipo V. Restoration of learning ability in hyperammonemic rats by increasing extracellular cGMP in brain. Brain Res. 1036 (2005) 115-121
13. Felipo V., and Butterworth R.F. Neurobiology of ammonia. Prog. Neurobiol. 67 (2002) 259-279
14. Ferenci P., Lockwood A., Mullen K., Tarter R., Weissenborn K., and Blei A.T. Hepatic encephalopathy-definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna. Hepatology 35 (1998) 716-721
15. Garcia-Moreno L.M., Conejo N.M., Gonzalez-Pardo H., Aller M.A., Nava M.P., Arias J., and Arias J.L. Evaluation of two experimental models of hepatic encephalopathy in rats. Braz. J. Med. Biol. Res. 38 (2005) 127-132
16. Groeneweg M., Quero J.C., De Bruijn I., Hartmann I.J., Essink-bot M.L., Hop W.C., and Schalm S.W. Subclinical hepatic encephalopathy impairs daily functioning. Hepatology 28 (1998) 45-49
17. Hartmann I.J., Groeneweg M., Quero J.C., Beijeman S.J., de Man R.A., Hop W.C., and Schalm S.W. The prognostic significance of subclinical hepatic encephalopathy. Am. J. Gastroenterol. 95 (2000) 2029-2034
18. Hermenegildo C., Montoliu C., Llansola M., Muñoz M.D., Gaztelu J.M., Minana M.D., and Felipo V. Chronic hyperammonemia impairs glutamate-nitric oxide-cyclic GMP pathway in cerebellar neurons in culture and in the rat in vivo. Eur. J. Neurosci. 10 (1998) 3201-3209
19. Ingram D.K., Spangler E.L., Kametani H., Meyer R.C., and London E.D. Intraventricular injection of N-nitro-l-arginine in rats impairs learning in a 14-unit T-maze. Eur. J. Pharmacol. 341 (1998) 11-16
20. Ingram D.K., Spangler E.L., Meyer R.C., and London E.D. Learning in a 14-unit T-maze is impaired in rats following the systemic treatment with N-nitro-l-arginina. Eur. J. Pharmacol. 341 (1998) 1-9
21. McCrea M., Cordoba J., Vessey G., Blei A.T., and Randolph C. Neuropsychological characterization and detection of subclinical hepatic encephalopathy. Arch. Neurol. 53 (1996) 758-763
22. Marchesini G., Bianchi G., Amodio P., Salerno F., Merli M., Panella C., Loguercio C., Apolone G., Niero M., Abbiati R., and Italian Study Group for quality of life in cirrhosis. Factors associated with poor health-related quality of life of patients with cirrhosis. Gastroenterology 120 (2001) 170-178
23. Meyer R.C., Knox J., Purwin D.A., Spangler E.L., and Ingram D.K. Combined stimulation of the glycine and polyamine sites of the NMDA receptor attenuates NMDA blockade-induced learning deficits of rats in a 14-unit-T-maze. Psychopharmacology 135 (1998) 290-295
24. Monfort P., Corbalan R., Martinez L., Lopez-Talavera J., Cordoba J., and Felipo V. Altered content and modulation of soluble guanylate cyclase in the cerebellum of rats with portacaval anastomosis. Neuroscience 104 (2001) 1127-1139
25. Myslivecek J. Inhibitory learning and memory in new-born rats. Prog. Neurobiol. 53 (1997) 399-430
26. Prickaerts J., Steinbusch H.W., Smits J.F., and de Vente J. Possible role of nitric oxide-cyclic GMP pathway in object recognition memory: effects of 7-nitroindazole and zaprinast. Eur. J. Pharmacol. 337 (1997) 125-136
27. Prickaerts J., de Vente J., Honig W., Steinbusch H.W., and Blokland A. cGMP, but not cAMP, in rat hippocampus is involved in early stages of object memory consolidation. Eur. J. Pharmacol. 436 (2002) 83-87
28. Rikkers L., Jenko P., Rudman D., and Freides D. Subclinical hepatic encephalopathy: detection, prevalence, and relationship to nitrogen metabolism. Gastroenterology 75 (1978) 462-469
29. Romero-Gomez M., Boza F., Garcia-Valdecasas M.S., Garcia E., and Aguilar-Reina J. Subclinical hepatic encephalopathy predicts the development of overt hepatic encephalopathy. Am. J. Gastroenterol. 96 (2001) 2718-2723
30. Schomerus H., and Hamster W. Neuropsychological aspects of portal-systemic encephalopathy. Metab. Brain Dis. 13 (1998) 361-377
31. Schomerus H., and Hamster W. Quality of life in cirrhotics with minimal hepatic encephalopathy. Metab. Brain Dis. 16 (2001) 37-41
32. Schomerus H., Hamster W., Blunck H., Reinhard U., Mayer K., and Dolle W. Latent portasystemic encephalopathy. I. Nature of cerebral functional defects and their effect on fitness to drive. Dig. Dis. Sci. 26 (1981) 622-630
33. Smith S., Dringenberg H.C., Bennett B.M., Thatcher G.R., and Reynolds J.N. A novel nitrate ester reverses the cognitive impairment caused by scopolamine in the Morris water maze. Neuroreport 11 (2000) 3883-3886
34. Srivastava A., Mehta R., Rothke S.P., Rademaker A.W., and Blei A.T. Fitness to drive in patients with cirrhosis and portal-systemic shunting: a pilot study evaluating driving performance. J. Hepatol. 21 (1994) 1023-1028
35. Tarter R.E., Arria A.M., Carra J., and Van Thiel D.H. Memory impairments concomitant with nonalcoholic cirrhosis. Int. J. Neurosci. 32 (1987) 853-859
36. Tzathas C., Christidou A., and Ladas S.D. Sildenafil (viagra) is a risk factor for acute variceal bleeding. Am. J. Gastroenterol. 97 (2002) 1856
37. Weissenborn K., Heidenreich S., Giewekemeyer K., Ruckert N., and Hecker H. Memory function in early hepatic encephalopathy. J. Hepatol. 39 (2003) 320-325
38. Yamada K., Hiramatsu M., Noda Y., Mamiya T., Murai M., Kameyama T., Komori Y., Nikai T., Sugihara H., and Nabeshima T. Role of nitric oxide and cyclic GMP in the dizocilpine-induced impairment of spontaneous alternation behavior in mice. Neuroscience 74 (1996) 365-374
39. Zou L.B., Yamada K., Tanaka T., Kameyama T., and Nabeshima T. Nitric oxide synthase inhibitors impair reference memory formation in a radial arm maze task in rats. Neuropharmacology 37 (1998) 323-330