Cannabinoids ameliorate cerebral dysfunction following liver failure via AMP-activated protein kinase

FASEB Journal

Volumn 21, Issue 10, 2007, Pages 2431-2441

  Dagon, Yossi ^a   Avraham, Yosefa ^a   Ilan, Yaron ^b   Mechoulam, Raphael ^c   Berry, Elliot M ^a  

^a HEBREW UNIVERSITY   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

AMPK; Endocannabinoid receptor; Hepatic encephalopathy; Liver disease

Indexed keywords

CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; DRONABINOL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; RIMONABANT; THIOACETAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DYSFUNCTION; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; FEMALE; LIVER FAILURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; BILE DUCTS; BRAIN; CANNABINOIDS; FEMALE; HEPATIC ENCEPHALOPATHY; LIVER FAILURE; MICE; MICE, INBRED STRAINS; MULTIENZYME COMPLEXES; PROTEIN-SERINE-THREONINE KINASES; TETRAHYDROCANNABINOL;

MURINAE; MUS;

EID: 34547823575     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7705com     Document Type: Article

References (52)

1. Summerskill, W. H. J., Davidson, E. A., Sherlock, S., and Steiner, R. E. (1956) The neuropsychiatric syndrome associated with hepatic cirrhosis and an extensive portal collateral circulation. Q. J. Med. 25, 245-266
2. Ferenci, P., Lockwood, A., Mullen, K., Tarter, R., Weissenborn, K., and Blei, A. T. (2002) Hepatic encephalopathy - definition, nomenclature, diagnosis and quantification: final report of the Working Party at the 11th World Congress of Gastroenterology, Vienna, 1998. Hepatology 35, 716-721
3. Gerber, T., and Schomerus, H. (2000) Hepatic encephalopathy in liver cirrhosis: pathogenesis, diagnosis and management (review). Drugs 60, 1353-1370
4. Zwingmann, C., Chatauret, N., Leibfritz, D., and Butterworth, R. F. (2003) Selective increase of brain lactate synthesis in experimental acute liver failure: results of a [H-C] nuclear magnetic resonance study. Hepatology 37, 420-428
5. Butterworth, R. F., Giguere, J. F., Michaud, J., Lavoie, J., and Layrargues, G. P. (1987) Ammonia: key factor in the pathogenesis of hepatic encephalopathy (review). Neurochem. Pathol. 6, 1-12
6. Rose, C., and Felipo, V. (2005) Limited capacity for ammonia removal by brain in chronic liver failure: potential role of nitric oxide (review). Metab. Brain Dis. 20, 275-283
7. Felipo, V., and Butterworth, R. F. (2002) Neurobiology of ammonia (review). Prog. Neurobiol. 67, 259-279
8. Ott, P., Clemmesen, O., and Larsen, F. S. (2005) Cerebral metabolic disturbances in the brain during acute liver failure: from hyperammonemia to energy failure and proteolysis (review). Neurochem. Int. 47, 13-18
9. Hardie, D. G. (2004) The AMP-activated protein kinase pathway-new players upstream and downstream (review). J. Cell Sci. 117, 5479-5487
10. Hardie, D. G., and Carling, D. (1997) The AMP-activated protein kinase-fuel gauge of the mammalian cell? Review. Eur. J. Biochem. 246, 259-273
11. Campas, C., Lopez, J. M., Santidrian, A. F., Barragan, M., Bellosillo, B., Colomer, D., and Gil, J. (2003) Acadesine activates AMPK and induces apoptosis in B-cell chronic lymphocytic leukemia cells but not in T lymphocytes. Blood 101, 3674-3680
12. Meisse, D., Van de Casteele, M., Beauloye, C., Hainault, I., Kefas, B. A., Rider, M. H., Foufelle, F., and Hue, L. (2002) Sustained activation of AMP-activated protein kinase induces c-Jun N-terminal kinase activation and apoptosis in liver cells. FEBS Lett. 526, 38-42
13. Kahn, B. B., Alquier, T., Carling, D., and Hardie, D. G. (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism (review). Cell Metab. 1, 15-25
14. Andersson, U., Filipsson, K., Abbott, C. R., Woods, A., Smith, K., Bloom, S. R., Carling D., and Small, C. J. (2004) AMP-activated protein kinase plays a role in the control of food intake. J. Biol. Chem. 279, 12005-12008
15. Minokoshi, Y., Alquier, T., Furukawa, N., Kim, Y. B., Lee, A., Xue, B., Mu, J., Foufelle, F., Ferre, P., Birnabaum, M. J., et al. (2004) AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428, 569-574
16. Dagon, Y., Avraham, Y., Magen, I., Gertler, A., Ben-Hur, T., and Berry, E. M. (2005) Nutritional status, cognition, and survival: a new role for leptin and AMP kinase. J. Biol. Chem. 280, 42142-42148
17. Pagotto, U., Vicennati, V., and Pasquali, R. (2005) The endocannabinoid system and the treatment of obesity (review). Ann. Med. 37, 270-275
18. Devane, W. A., Hanus, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., and Mechoulam, R. (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949
19. Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., and Bonner, T. I. (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346, 561-564
20. Iversen, L. L. (2000) The Science of Marijuana, p. 36, Oxford University Press, New York
21. Berry, E. M., and Mechoulam, R. (2002) Tetrahydrocannabinol and endocannabinoids in feeding and appetite (review). Pharmacol. Ther. 95, 185-190
22. Baker, D., Pryce, G., Giovannoni, G., and Thompson, A. J. (2003) The therapeutic potential of cannabis (review). Lancet Neurol. 2, 291-298
23. Avraham, Y., Israeli, E., Gabbay, E., Okun, A., Zolotarev, O., Silberman, I., Ganzburg, V., Dagon, Y., Magen, I., Vorobia, L., et al. (2006) Endocannabinoids affect neurological and cognitive function in thioacetamide-induced hepatic encephalopathy in mice. Neurobiol. Dis. 21, 237-245
24. Teixeira-Clerc, F., Julien, B., Grenard, P., Tran Van Nhieu, J., Deveaux, V., Li, L., Serriere-Lanneau, V., Ledent, C., Mallat, A., and Lotersztajn, S. (2006) CB1 cannabinoid receptor antagonism: a new strategy for the treatment of liver fibrosis. Nat. Med. 12, 671-676
25. Julien, B., Grenard, P., Teixeira-Clerc, F., Van Nhieu, J. T., Li, L., Karsak, M., Zimmer, A., Mallat, A., and Lotersztajn, S. (2005) Antifibrogenic role of the cannabinoid receptor CB2 in the liver. Gastroenterology 128, 742-755
26. Avraham, Y., Bonne, O., and Berry, E. M. (1996) Behavioral and neurochemical alterations caused by diet restriction - the effect of tyrosine administration in mice. Brain Res. 732, 133-144
27. Chen, Y., Constantini, S., Trembovler, V., Weinstock, M., and Shohami, E. (1996) An experimental model of closed head injury in mice: pathophysiology, histopathology and cognitive deficits. J. Neurotrauma 13, 557-568
28. Fride, E., and Mechoulam, R. (1993) Pharmacological activity of the cannabinoid receptor agonist, anandamide, a brain constituent. Eur. J. Pharmacol. 231, 313-314
29. Olton, D. S., and Samuelson, R. J. (1976) Remembrance of places passed: Spatial memory in rats. J. Exp. Psychol. Anim. Behav. Process 2, 97-116
30. Pick, C. G., and Yanai, J. (1983) Eight arm maze for mice. Int. J. Neurosci. 21, 63-66
31. Barbiroli, B., Gaiani, S., Lodi, R., Iotti, S., Tonon, C., Clementi, V., Donati, G., and Bolondi, L. (2002) Abnormal brain energy metabolism shown by in vivo phosphorus magnetic resonance spectroscopy in patients with chronic liver disease. Brain Res. Bull. 59, 75-82
32. Zimmermann, C., Ferenci, P., Pifl, C., Yurdaydin, C., Ebner, J., Lassmann, H., Roth, E., and Hortangl, H. (1989) Hepatic encephalopathy in thioacetamide-induced acute liver failure in rats: characterization of an improved model and study of amino acid-ergic neurotransmission. Hepatology 9, 594-601
33. Kola, B., Hubina, E., Tucci, S. A., Kirkham, T. C., Garcia, E. A., Mitchell, S. E., Williams, L. M., Hawley, S. A., Hardie, D. G., Grossman, A. B., and Korbonits, M. (2005) Cannabinoids and ghrelin have both central and peripheral metabolic and cardiac effects via AMP-activated protein kinase. J. Biol. Chem. 280, 25196-25201
34. Sulcova, E., Mechoulam, R., and Fride, E. (1998) Biphasic effects of anandamide. Pharmacol. Biochem. Behav. 59, 347-353
35. Folbergrova, J., Zhao, Q., Katsura, K., and Siesjo, B. K. (1995) N-tert-butyl-alpha-phenylnitrone improves recovery of brain energy state in rats following transient focal ischemia. Proc. Natl. Acad. Sci. U. S. A. 92, 5057-5061
36. Xiong, Y., Peterson, P. L., and Lee, C. P. (2001) Alterations in cerebral energy metabolism induced by traumatic brain injury (review). Neurol. Res. 23, 129-138
37. Mizuno, Y., Ikebe, S., Hattori, N., Nakagawa-Hattori, Y., Mochizuki, H., and Tanaka, M. (1995) Role of mitochondria in the etiology and pathogenesis of Parkinson's disease (review). Biochim. Biophys. Acta 1271, 265-274
38. Hoyer, S. (1993) Abnormalities in brain glucose utilization and its impact on cellular and molecular mechanisms in sporadic dementia of Alzheimer type. Ann. N. Y. Acad. Sci. 695, 77-80
39. 31P spectroscopic imaging shows energy deficit of thalamus in chronic hepatic encephalopathy. Annual Meeting of the Society of Magnetic Resonance in Medicine, Amsterdam, p. 465
40. Fitzhugh, O. G., and Nelson, A. A. (1984) Liver tumor in rats fed thiourea or thioacetamide. Science 108, 626-628
41. Zimmermann, T., Gardemann, A., Machnik, G., Dargel, R., and Jungermann, K. (1992) Metabolic and hemodynamic responses of bivascularly perfused rat liver to nerve stimulation, noradrenaline, acetylcholine and glucagon in thioacetamide induced micronodular cirrhosis. Hepatology 15, 467-470
42. Dagon, Y., Avraham, Y., and Berry, E. M. (2006) AMPK activation regulates apoptosis, adipogenesis, and lipolysis by eIF2alpha in adipocytes. Biochem. Biophys. Res. Commun. 340, 43-47
43. Bernard, A., Roger, D., Luigi, C., and Ramon, L. (1967) Actinomycin D blocks formation of memory of shock-avoidance in goldfish. Science 158, 1600-1601
44. Bergold, P. J., Sweatt, J. D., Winicov, I., Weiss, K. R., Kandel, E. R., and Schwartz, J. H. (1990) Protein synthesis during acquisition of long-term facilitation is needed for the persistent loss of regulatory subunits of the Aplysia cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U. S. A. 87, 3788-3791
45. Costa-Mattioli, M., Gobert, D., Harding, H., Herdy, B., Azzi, M., Bruno, M., Bidinosti, M., Ben Mamou, C., Marcinkiewicz, E., Yoshida, M., et al. (2005) Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 436, 1166-1173
46. Mishima, K., Egashira, N., Hirosawa, N., Fujii, M., Matsumoto, Y., Iwasaki, K., and Fujiwara, M. (2001) Characteristics of learning and memory impairment induced by delta9-tetrahydrocannabinol in rats. Jpn. J. Pharmacol. 87, 297-308
47. Martin, B. R. (2005) Role of lipids and lipid signaling in the development of cannabinoid tolerance (review). Life Sci. 77, 1543-1558
48. Molina-Holgado, F., Pinteaux, E., Heenan, L., Moore, J. D., Rothwell, N. J., and Gibson, R. M. (2005) Neuroprotective effects of the synthetic cannabinoid HU-210 in primary cortical neurons are mediated by phosphatidylinositol 3-kinase/AKT signaling. Mol. Cell Neurosci. 28, 189-194
49. Cheer, J. F., Wassum, K. M., Heien, M. L., Phillips, P. E., and Wightman, R. M. (2004) Cannabinoids enhance subsecond dopamine release in the nucleus accumbens of awake rats. J. Neurosci. 24, 4393-4400
50. Gerdeman, G. L., Partridge, J. G., Lupica, C. R., and Lovinger, D. M. (2003) It could be habit forming: drugs of abuse and striatal synaptic plasticity (review). Trends Neurosci. 26, 184-192
51. Bisogno, T., Melck, D., Bobrov, M. Y., Gretskaya, N. M., Bezuglov, V. V., De Petrocellis, L., and Di Marzo, V. (2000) N-Acyldopamines: novel synthetic CB(1) cannabinoid-receptor ligands and inhibitors of anandamide inactivation with cannabimimetic activity in vitro and in vivo. Biochem. J. 351, 817-824
52. Bezuglov, V., Bobrov, M., Gretskaya, N., Gonchar, A., Zinchenko, G., Melck, D., Bisogno, T., Di Marzo, V., Kuklev, D., Rossi, J. C., et al. (2001) Synthesis and biological evaluation of novel amides of polyunsaturated fatty acids with dopamine. Bioorg. Med. Chem. Lett. 11, 447-449