Does the neuroprotective role of anandamide display diurnal variations?

International Journal of Molecular Sciences

Volumn 14, Issue 12, 2013, Pages 23341-23355

  Martinez Vargas, Marina ^a   Morales Gomez, Julio ^a   Gonzalez Rivera, Ruben ^a   Hernandez Enriquez, Carla ^a   Perez Arredondo, Adan ^a   Estrada Rojo, Francisco ^a   Navarro, Luz ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Anandamide; Cannabinoid receptor; Cerebral cortex; Circadian rhythms; Neuroprotection

Indexed keywords

ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; AMIDE; ARACHIDONIC ACID DERIVATIVE; CANNABINOID RECEPTOR ANTAGONIST; ENDOCANNABINOID; MESSENGER RNA; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; CIRCADIAN RHYTHM; CONTROLLED STUDY; FOOD INTAKE; LIGHT DARK CYCLE; MALE; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; RATING SCALE; REPERFUSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCORING SYSTEM; SURVIVAL RATE; TRAUMATIC BRAIN INJURY; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; BRAIN INJURIES; DISEASE MODEL; GENETICS; METABOLISM; MORTALITY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ARACHIDONIC ACIDS; BRAIN INJURIES; CANNABINOID RECEPTOR ANTAGONISTS; CEREBRAL CORTEX; CIRCADIAN RHYTHM; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; HEMORRHAGE; MALE; NEUROPROTECTIVE AGENTS; POLYUNSATURATED ALKAMIDES; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RNA, MESSENGER; SURVIVAL RATE;

EID: 84888411435     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141223341     Document Type: Article

References (61)

1. Mechoulam, R.; Panikashvili, D.; Shohami, E. Cannabinoids and brain injury: Therapeutic implications. Trends Mol. Med. 2002, 8, 58-61.
2. Panikashvili, D.; Mechoulam, R.; Beni, S.M.; Alexandrovich, A.; Shohami, E. CB1 cannabinoid receptors are involved in neuroprotection via NF-kappa B inhibition. J. Cereb. Blood Flow Metab. 2005,25, 477-484.
3. Panikashvili, D.; Shein, N.A.; Mechoulam, R.; Trembovler, V.; Kohen, R.; Alexandrovich, A.; Shohami, E. The endocannabinoid 2-AG protects the blood-brain barrier after closed head injury and inhibits mRNA expression of proinflammatory cytokines. Neurobiol. Dis. 2006, 22, 257-264.
4. Mechoulam, R.; Shohami, E. Endocannabinoids and traumatic brain injury. Mol. Neurobiol. 2007, 36, 68-74.
5. Leker, R.R.; Shohami, E. Cerebral ischemia and trauma different etiologies yet similar mechanisms: Neuroprotective opportunities. Brain Res. Rev. 2002, 39, 55-73.
6. Turner, W.M. Epidemiology of nocturnal asthma. Am. J. Med. 1988, 85, 6-8.
7. Solomon, G.D. Circadian rhythms and migraine. Cleve Clin. J. Med. 1992, 59, 326-329.
8. Muller, J.E.; Stone, P.H.; Turi, Z.G.; Rutherford, J.D.; Czeisler, C.A.; Parker, C.; Poole, W.K.; Passamani, E.; Roberts, R.; Robertson, T.; et al. Circadian variation in the frequency of onset of acute myocardial infarction. N. Engl. J. Med. 1985, 313, 1315-1322.
9. Marshall, J. Diurnal variation in occurrence of strokes. Stroke 1977, 8, 230-231.
10. Toni, D.; Argentino, C.; Gentile, M.; Sacchetti, M.L.; Girmenia, F.; Millefiorini, E.; Fieschi, C. Circadian variation in the onset of acute cerebral ischemia: Ethiopathogenetic correlates in 80 patients given angiography. Chronobiol. Int. 1991, 8, 321-326.
11. Vinall, P.E.; Kramer, M.S.; Heinel, L.A.; Rosenwasser, R.H. Temporal changes in sensitivity of rats to cerebral ischemic insult. J. Neurosurg. 2000, 93, 82-89.
12. Martinez-Vargas, M.; Gonzalez-Rivera, R.; Soto-Nuñez, M.; Cisneros Martinez. M.; Huerta Saquero, A.; Morales Gpmez, J.; Molina Guarneros, J.; Navarro, L. Recovery after a traumatic brain injury depends on diurnal variations. Effect of cystatin C. Neurosci. Lett. 2006, 400, 21-24.
13. Martínez-Vargas, M.; Murillo-Rodriguez, E.; González Rivera. R.; Landa, A.; Méndez Diaz, M.; Prospero-Garcia, O.; Navarro, L. Sleep modulates cannabinoid receptor 1 expression in the pons of rats. Neuroscience 2003, 117, 197-201.
14. Rueda-Orozco, P.E.; Soria-Gomez, E.; Montes-Rodriguez, C.J.; Martínez-Vargas, M.; Galicia, O.; Navarro, L.; Prospero-Garcia, O. A potential function of endocannabinoids in the selection of a navigation strategy by rats. Psychopharmacology 2008, 198, 565-576.
15. Valenti, M.; Vigano, D.; Cascico, M.G.; Rubino, T.; Steardo, L.; Parolaro, D.; Di Marzo V. Differential diurnal variations of anandamide and 2-arachidonoyl-glycerol levels in rat brain. Cell Mol. Life Sci. 2004, 61, 945-950.
16. Murillo-Rodriguez, E.; Désarnaud, F.; Prospéro-Garcia, O. Diurnal variation of arachidonoylethanolamine, palmitoylethanolamide and oleoylethanolamide in the brain of the rat. Life Sci. 2006, 79, 30-37.
17. Glaser, S.T.; Kaczocha, M. Temporal changes in mouse brain fatty acid amide hydrolase activity. Neuroscience 2009, 163, 594-600.
18. Wittmann, G.; Deli, L.; Kallo, I.; Hrabovszky, E.; Watanabe, M.; Lipozits, Z.; Fekete, C. Distribution of type I cannabinoid receptor (CB1)-immunoreactive axons in the mouse hypothalamous. J. Comp. Neurol. 2007, 503, 270-279.
19. Acuna, G.C.; Obrietan, K.V. Cannabinoids excite circadian clock neurons. J. Neurosci. 2010, 30, 10061-10066.
20. Sanford, A.E.; Castillo, E.; Gannon, R.L. Cannabinoids and hamster circadian activity rhythms. Brain Res. 2008, 1222, 141-148.
21. Montagnana, M.; Salvagno, G.L.; Lippi, G. Circadian variation within hemostasis: An underrecognized link between biology and disease? Semin. Thromb. Hemost. 2009, 35, 23-33.
22. Soulban, G.; Labrecque, G. Circadian rhythms of blood clotting time and coagulation factors II, VII, IX and X in rats. Life Sci. 1989, 45, 2485-2489.
23. Maccarrone, M.; Bari, M.; Menichelli, A.; del Principe, D.; Agro, A.F. Anandamide activates human platelets through a pathway independent of the arachidonate cascade. FEBS Lett. 1999, 447, 277-282.
24. Braud, S.; Bon, C.; Touqui, L.; Mounier, C. Activation of rabbit blood platelets by anandamide through its cleavage into arachidonic acid. FEBS Lett. 2000, 471, 12-16.
25. Sritharan, K.; Thompson, H. Understanding the metabolic response to trauma. Br. J. Hosp. Med. 2009, 70, M156-M518.
26. Kazanis, I.; Bozas, E.; Philippidis, H.; Stylianopoulou, F. Neuroprotective effects of insulin-like growth factor-I (IGF-I) following a penetrating brain injury in rats. Brain Res. 2003, 991, 34-45.
27. Vickers, S.P.; Kennett, G.A. Cannabinoids and the regulation of ingestive behavior. Curr. Drug Targets 2005, 6, 215-223.
28. Schmid, P.C.; Krebsbach, R.J.; Perry, S.R.; Dettmer, T.M.; Maasson, J.L.; Schmid, H.H. Occurrence and postmortem generation of anandamide and other long-chain N-acylethanolamines in mammalian brain. FEBS Lett. 1995, 375, 143-147.
29. Shen, M.; Thayer, S.A.; Cannabinoid receptor agonists protect cultured rat hippocampal neurons from excitotoxicity. Mol. Pharmacol. 1998, 54, 459-462.
30. Nagayama, T.; Sinor, A.D.; Simon, R.P.; Chen, J.; Graham, S.H.; Jin, K.; Greenberg, D.A. Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J. Neuroci. 1999, 19, 2987-2995.
31. Schomacher, M.; Müller, H.D.; Sommer, C.; Schwab, S.; Schabitz, W.R. Endocannabinoids mediate neuroprotection after transient focal cerebral ischemia. Brain Res. 2008, 1240, 213-220.
32. Tominaga, K.; Shinohara, K.; Otori, Y.; Fukuhara, C.; Inouye, S.T. Circadian rhythms of vasopressin content in the suprachiasmatic nucleus of the rat. Neuroreport 1992, 3, 809-812.
33. Burbach, J.P.; Liu, B.; Voorhuis, T.A.; van Tol, H.H. Diurnal variation in vasopressin and oxytocin messenger RNAs in hypothalamic nuclei of the rat. Brain Res. 1988, 464, 157-160.
34. Bruinink, A.; Lichtensteiger, W.; Schlumpf, M. Ontogeny of diurnal rhythms of central dopamine, serotonin and spirodecanone bindings sites and of motor activity in the rat. Life Sci. 1983, 33, 31-38.
35. Naber, D.; Wirz, J.A.; Kafka, M.S.; Tobler, I.; Borbely, A.A. Seasonal variations in the endogenous rhythm of dopamine receptor binding in rat striatum. Biol. Psychiatry 1981, 16, 831-835.
36. Torner, C.; Sanchez, H.S.; Aguilar-Roblñero, R. Diurnal variations of striatal D2 dopaminergic receptors and its relation with haloperidol-induced catalepsy. Biol. Rhythm Res. 1998, 29, 538-545.
37. Stella, N.; Schweitzer, P.; Piomelli, D. A second endogenous cannabinoid that modulates long-term potentiation. Nature 1997, 388, 773-778.
38. Romero, J.; Berrendero, F.; Manzanares, J.; Perez, A.; Cochero, J.; Fuentes, J.A.; Fernandez Ruiz, J.J.; Ramos, J.A. Time-course of the cannabinoid receptor down-regulation in the adult rat brain caused by repeated exposure to delta-9-tethahydrocannabinol. Synapse 1998, 30, 298-308.
39. Zhuang, S.Y.; Kittler, J.; Grigorensko, E.V.; Kirby, M.T.; Sim, L.J.; Hapson, R.E.; Childers, S.R.; Deadwyler, S.A. Effects of long-term exposure to delta-9-THC on expression of cannabinoid receptor (CB1) mRNA in different brain regions. Mol. Brain Res. 1998, 62, 141-149.
40. Borner, C.; Hollt, V.; Sebald, W.; Kraus, J. Transcriptional regulation of the cannabinoid receptor type 1 gene in T cells by cannabinoids. J. Leukoc. Biol. 2007, 81, 336-343.
41. White, T.E.; Ford, G.D.; Surles-Zeigler, M.C.; Gates, A.S.; LaPlaca, M.C.; Ford, B.D. Gene expression patterns following unilateral traumatic brain injury reveals a local pro-inflammatory and remote anti-inflammatory response. Genomics 2013, 14, 282.
42. Garcia-Ovejero, D.; Arevalo-Martin, A.; Petrosino, S.; Docagne, F.; Hagen, C.; Bisogno, T.; Watanabe, M.; Guaza, C.; di Marzo, V.; Molina-Holgado, E. The endocannabinoid system is modulated in response to spinal cord injury in rats. Neurobiol. Dis. 2009, 33, 57-71.
43. Jin, K.L.; Mao, X.O.; Godsmith, P.C; Greenberg, D.A. CB1 cannabinoid receptor induction in experimental stroke. Ann. Neurol. 2000, 48, 257-261.
44. Schomacher, M.; Müller, H.D.; Sommer, C. Short-term ischemia usually used for ischemic preconditioning down-regulates central cannabinoid receptors in the gerbil hippocampus. Acta Neuropathol. 2006, 111, 8-14.
45. Zhang, M.; Martin, B.R.; Adler, M.W.; Razdan, R.K.; Ganea, D.; Tuma, R.F. Modulation of the balance between cannabinoid CB(1) and CB(2) receptor activation during cerebral ischemic/reperfusion injury. Neuroscience 2008, 152, 753-760.
46. Paul, T.; Lemmer, B. Disturbance of circadian rhythms in analgosedated intensive care unit patients with and without craniocerebral injury. Chronobiol. Int. 2007, 24, 45-61.
47. Llompart-Pou, J.; Perez, G.; Raurich, J.M.; Riesco, M.; Brell, M.; Ibañez, J.; Perez-Barcena, J.; Abadal, J.M.; Homar, J.; Burguera, B. Loss of cortisol circadian rhythm in patients with traumatic brain injury: A microdialysis evaluation. Neurocrit. Care 2010, 13, 211-216.
48. Ayalon, L.; Borodkin, K.; Dishon, L.; Kanety, H.; Dagan, Y. Circadian rhythm sleep disorders following mild traumatic brain injury. Neurology 2007, 68, 1136-1140.
49. Castriotta, R.J.; Murthy, J.N. Sleep disorders in patients with traumatic brain injury: A review. CNS Drugs 2010, 25, 175-185.
50. Boone, D.R.; Sell, S.L.; Micci, M.A.; Crookshanks, J.M.; Parsley, M.; Uchida, T.; Prough, D.S.; DeWitt, D.S.; Hellmich, H.L. Traumatic brain injury-induced dysregulation of the circadian clock. PLoS One 2012, 7, e46204.
51. Perron, R.R.; Tyson, R.L.; Sutherland, G.R. Delta-9-tetrahydrocannabinol increases brain temperature and inverts circadian Neuroreport 2001, 12, 3791-3794.
52. Oviedo, A.; Glowa, J.; Herkenham, M. Chronic cannabinoid administration alters cannabinoid receptor binding in rat brain: A quantitative autoradiographic study. Brain Res. 1993, 616, 293-302.
53. Rodríguez de Fonseca, F.; Gorriti M.A.; Fernández-Ruiz, J.J.; Palomo, T.; Ramos, J.A. Down-regulation of rat brain cannabinoid binding sites after chronic delta 9-tetrahydrocannabinol. Pharmacol. Biochem. Behav. 1994, 47, 33-34.
54. Marco, E.M.; Rubino, T.; Adriani, W.; Viveros, M.P.; Parolaro, D.; Laviola, G. Long-term consequences of URB597 administration during adolescence on cannabinoid CB1 receptor binding in brain areas. Brain Res. 2009, 1257, 25-31.
55. Coutts, A.A.; Anavi-Goffer, S.; Ross, R.A.; MacEwan, D.J.; Mackie, K.; Pertwee, R.G.; Irving, A.J. Agonist-induced internalization and trafficking of cannabinoid CB1 receptors in hippocampal neurons. J. Neurosci. 2001, 21, 2425-2433.
56. Romero, J.; García, L.; Fernández-Ruiz, J.J.; Cebeira, M.; Ramos, J.A. Changes in rat brain cannabinoid binding sites after acute or chronic exposure to their endogenous agonist, anandamide, or to delta 9-tetrahydrocannabinol. Pharmacol. Biochem. Behav. 1995, 51, 731-737.
57. Heller, J.E.; Baty, D.E.; Zhang, M.; Li, H.; Adler, M.; Ganea, D.; Gaughan, J.; Loftus, C.M.; Jallo, J.I.; Tuma, R.F. The combination of selective inhibition of the cannabinoid CB1 receptor and activation of the cannabinoid CB2 receptor yields improved attenuation of motor and autonomic deficits in a mouse model of spinal cord injury. Clin. Neurosurg. 2009, 56, 84-92.
58. Paxinos, G.; Watson, C. The Rat Brain in Stereotaxic Coordinates, 4th ed.; Academic Press: San Diego, CA, USA, 1998.
59. Murillo-Rodríguez, E.; Sánchez-Alavez, M.; Navarro, L.; Martínez-Gonzalez, D.; Drucker-Colin, R.; Prospero-Garcia, O. Anandamida modulates sleep and memory in rats. Brain Res. 1998, 812, 270-274.
60. Hunter, A.J.; Hatcher, J.; Virley, D.; Nelson, P.; Irving, E.; Hadingham, S.J.; Parsons, A.A. Functional assessments in mice and rats after focal stroke. Neuropharmacology 2000, 39, 806-816.
61. Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680-685.