Chronic treatment with selective I2-imidazoline receptor ligands decreases the content of pro-apoptotic markers in rat brain

Journal of Psychopharmacology

Volumn 27, Issue 2, 2013, Pages 123-134

  Garau, Celia ^a   Miralles, Antonio ^a   García Sevilla, Jesús A ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

Author keywords

2 BFI; Apoptotic signalling; BU 224; FADD adaptor; Fas receptor; I2 imidazoline receptor; LSL 61112; mitochondrial proteins (Bcl 2, Bax, cytochrome c); neuroprotection; rat brain

Indexed keywords

2 (2 BENZOFURANYL) 2 IMIDAZOLINE; 2 (2 BENZOFURANYL)IMIDAZOLE; 2 (2 IMIDAZOLIN 2 YL)QUINOLINE; ALPHA 2 ADRENERGIC RECEPTOR; BIOLOGICAL MARKER; CYTOCHROME C; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; IDAZOXAN; IMIDAZOLINE DERIVATIVE; IMIDAZOLINE I2 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; SERINE; TRACIZOLINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN MITOCHONDRION; CONTROLLED STUDY; DRUG RECEPTOR BINDING; DRUG STRUCTURE; MALE; MOLECULAR MECHANICS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RAT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; UPREGULATION;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL DEATH; CEREBRAL CORTEX; CYTOCHROMES C; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEINS; DOWN-REGULATION; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; IMIDAZOLINE RECEPTORS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIGANDS; MALE; MITOCHONDRIA; NEUROPROTECTIVE AGENTS; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; UP-REGULATION;

EID: 84872853911     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881112450785     Document Type: Article

References (77)

1. Alemany R, Olmos G, Escribá PV, et al. LSL 60101, a selective ligand for imidazoline I2 receptors, on glial fibrillary acidic protein concentration. Eur J Pharmacol. 1995 ; 280: 205-210
2. Alemany R, Olmos G, García-Sevilla JA. Labelling of I2B-imidazoline receptors by [3H]2-(2-benzofuranyl)-2-imidazoline (2-BFI) in rat brain and liver: characterization, regulation and relation to monoamine oxidase enzymes. Naunyn Schmiedeberg's Arch Pharmacol. 1997 ; 356: 39-47
3. Álvaro-Bartolomé M, Esteban S, García- Gutiérrez MS, et al. Regulation of Fas receptor/Fas-associated protein with death domain apoptotic complex and associated signalling systems by cannabinoid receptors in the mouse brain. Br J Pharmacol. 2010 ; 160: 643-656
4. Álvaro-Bartolomé M, La Harpe R, Callado LF, et al. Molecular adaptations of apoptotic pathways and signaling partners in the cerebral cortex of human cocaine addicts and cocaine-treated rats. Neuroscience. 2011 ; 196: 1-15
5. Anderson NJ, Lupo PA, Nutt DJ, et al. Characterisation of imidazoline I2 binding sites in pig brain. Eur J Pharmacol. 2005 ; 519: 68-74
6. Boronat MA, Olmos G, García-Sevilla JA. Attenuation of tolerance to opioid-induced antinociception and protection against morphine-induced decrease of neurofilament proteins by idazoxan and other I2-imidazoline ligands. Br J Pharmacol. 1998 ; 125: 175-185
7. Boronat MA, García-Fuster MJ, García-Sevilla JA. Chronic morphine induces up-regulation of the pro-apoptotic Fas receptor and down-regulation of the anti-apoptotic Bcl-2 oncoprotein in rat brain. Br J Pharmacol. 2001 ; 134: 1263-1270
8. Casanovas A, Olmos G, Ribera J, et al. Induction of reactive astrocytosis and prevention of motoneuron cell death by the I2-imidazoline receptor ligand LSL60101. Br J Pharmacol. 2000 ; 130: 1767-1776
9. Chaitanya GV, Alexander JS, Babu PP. PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun Signal. 2010 ; 8: 31
10. Choi SH, Choi DH, Lee JJ, et al. Imidazoline drugs stabilize lysosomes and inhibit oxidative cytotoxicity in astrocytes. Free Rad. Biol Med. 2002 ; 32: 394-405
11. Dhanasekaran DN, Reddy EP. JNK signaling in apoptosis. Oncogene. 2008 ; 27: 6245-6251
12. Díaz A, Mayet S, Dickeson AH. BU-224 produces spinal antinociception as an agonist at imidazoline I2 receptors. Eur J Pharmacol. 1997 ; 333: 9-15
13. Dontenwill M, Piletz JE, Chen M, et al. IRAS is an anti-apoptotic protein. Ann NY Acad Sci. 2003 ; 1009: 400-412
14. Dupuy L, Urosevic D, Greney H, et al. I1 imidazoline receptor-mediated effects on apoptotic processes in PC12 cells. Cell Death Diff. 2004 ; 11: 1049-1052
15. Edwards L, Fishman D, Horowitz P, et al. The imidazoline-1 receptor in PC12 pheochromocytoma cells activates protein kinase C, extracellular signal-regulated kinsase (ERK) and c-jun N-terminal kinsase (JNK). J Neurochem. 2001 ; 79: 931-940
16. Eglen RM, Hudson AL, Kendall DA, et al. 'Seeing through a glass darkly': casting light on imidazoline 'I' sites. Trends Pharmacol Sci. 1998 ; 19: 381-390
17. Escribá PV, Ozaita A, Miralles A, et al. Molecular characterization and isolation of a 45-kilodalton imidazoline receptor protein from the rat brain. Brain Res Mol Brain Res. 1995 ; 32: 187-196
18. Escribá PV, Ozaita A, García-Sevilla JA. Pharmacologic characterization of imidazoline receptor proteins identified by immunologic techniques and other methods. Ann NY Acad Sci. 1999 ; 881: 8-25
19. Ferrari F, Fiorentino S, Mennuni L, et al. Analgesic efficacy of CR4056, a novel imidazoline-2 receptor ligand, in rat models of inflammatory and neuropathic pain. J Pain Res. 2011 ; 4: 111-125
20. Finn DP, Martí O, Harbuz MS, et al. Behavioral, neuroendocrine and neurochemical effects of the imidazoline I2 receptor selective ligand BU224 in naive rats and rats exposed to the stress of the forced swim test. Psychopharmacology (Berl.). 2003 ; 167: 195-202
21. Galluzzi L, Blomgren K, Kroemer G. Mitochondrial membrane permeabilization in neuronal injury. Nature Rev Neurosci. 2009 ; 10: 481-494
22. García-Fuster MJ, Ferrer-Alcón M, Miralles A, et al. Modulation of Fas receptor proteins and dynamin during opiate addiction and induction of opiate withdrawal in rat brain. Naunyn-Schmiedeberg's Arch Pharmacol. 2003 ; 368: 421-431
23. García-Fuster MJ, Miralles A, García-Sevilla JA. Effects of opiate drugs on Fas-associated protein with death domain (FADD) and effector caspases in the rat brain: regulation by the ERK 1/2 MAP kinase pathway. Neuropsychopharmacology. 2007 ; 32: 399-411
24. García-Fuster MJ, Ramos-Miguel A, Miralles A, et al. Opioid receptor agonists enhance the phosphorylation state of Fas-associated death domain (FADD) protein in the rat brain: functional interactions with casein kinase Iα, Gαi proteins, and ERK 1/2 signaling. Neuropharmacology. 2008a ; 55: 886-899
25. García-Fuster MJ, Ramos-Miguel A, Rivero G, et al. Regulation of the extrinsic and intrinsic apoptotic pathways in the prefrontal cortex of short- and long-term human opiate abusers. Neuroscience. 2008b ; 157: 105-119
26. García-Fuster MJ, Clinton SM, Watson SJ, et al. Effect of cocaine on Fas-associated protein with death domain in the rat brain: Individual differences in a model of differential vulnerability to drug abuse. Neuropsychopharmacology. 2009 ; 34: 1123-1134
27. García-Sevilla JA, Meana JJ, Barturen F, et al. New 2-benzofuranyl-imidazole derivatives with imidazoline receptor affinity, used as appetite stimulants or anti-anorexics. UK patent GB2262739-A. 1993 ;: 1993-207864
28. García-Sevilla JA, Escribá PV, Guimón J. Imidazoline receptors and human brain disorders. Ann NY Acad Sci. 1999 ; 21: 392-409
29. García-Vallejo P, Barturen F, García-Sevilla JA. Modulation by central postsynaptic α2-adrenoceptors of the jaw-opening reflex induced by orofacial stimulation in rats. Br J Pharmacol. 1994 ; 111: 1140-1146
30. Gentili F, Cardinaletti C., Carrieri A, et al. Involvement of I2-imidazoline binding sites in positive and negative morphine analgesia modulatory effects. Eur J Pharmacol. 2006 ; 553: 73-81
31. Greney H, Ronde P, Magnier C, et al. Coupling of I1 imidazoline receptors to the cAMP pathway: studies with a highly selective ligand, benazoline. Mol Pharmacol. 2000 ; 57: 1142-1151
32. Han Z, Xiao MJ, Shao B, et al. Attenuation of ischemia-induced rat brain injury by 2-(-2-benzofuranyl)-2-imidazoline, a high selectivity ligand for imidazoline I-2 receptors. Neurol Res. 2009 ; 31: 390-395
33. Han Z, Zhang H-X, Tian J-S, et al. 2-(2-benzofuranyl)-2-imidazoline induces Bcl-2 expression and provides neuroprotection against transient cerebral ischemia in rats. Brain Res. 2010 ; 1361: 86-92
34. Head GA, Mayorov DN. Imidazoline receptors, novel agents and therapeutic potential. Cardiovasc Hematol Agents Med Chem. 2006 ; 4: 7-32
35. Hudson AL, Chapleo CB, Lewis JW, et al. Identification of ligands selective for central I2-imidazoline binding sites. Neurochem Int. 1997 ; 30: 47-53
36. Hudson AL, Gough RE, Tyacke R, et al. Novel selective compounds for the investigation of imidazoline receptors. Ann NY Acad Sci. 1999 ; 881: 81-91
37. Jiang S, Zheng R-Y, Zeng J-Q, et al. Reversible inhibition of intracellular calcium influx through NMDA receptors by imidazoline I2 receptor antagonists. Eur J Pharmacol. 2010 ; 629: 12-19
38. Kawamura K, Maeda J, Hatori A, et al. In vivo and in vitro imaging of I2 imidazoline receptors in the monkey brain. Synapse. 2011 ; 65: 452-455
39. Kimura A, Tyacke RJ, Robinson JJ, et al. Identification of an imidazoline binding protein: creatine kinase and an imidazoline-2 binding site. Brain Res. 2009 ; 1279: 21-28
40. Korsmeyer SJ, Shutter JR, Veis DJ, et al. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol. 1993 ; 4: 327-332
41. Kumar S. Caspase function in programmed cell death. Cell Death Differ. 2007 ; 14: 32-43
42. Li J-X, Zhang Y. Imidazoline I2 receptors: target for new analgesics?. Eur J Pharmacol. 2011 ; 658: 49-56
43. Li J-X, Zhang Y, Winter JC. Morphine-induced antinociception in the rat: supra-additive interactions with imidazoline I2 receptor ligands. Eur J Pharmacol. 2011 ; 669: 59-65
44. Lione LA, Nutt DJ, Hudson AL. Characterisation and localisation of [3H]2-(2-benzofuranyl)-2-imidazoline binding in rat brain: a selective ligand for imidazoline I2 receptors. Eur J Pharmacol. 1998 ; 353: 123-135
45. Lossi L, Merighi A. In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS. Progr Neurobiol. 2003 ; 69: 287-312
46. Lui T-N, Tsao C-W, Huang S-Y, et al. Activation of imidazoline I2B receptors is linked with AMP kinase pathway to increase glucose uptake in cultured C2C12 cells. Neurosci Lett. 2010 ; 474: 144-147
47. Meana JJ, Barturen F, García-Sevilla JA. Characterization and regional distribution of α2-adrenoceptors in postmortem human brain using the full agonist [3H]UK14304. J Neurochem. 1989 ; 52: 1210-1217
48. Menargues A, Obach R, García-Sevilla JA. Modulation by antidepressant drugs of CNS postsynaptic α2-adrenoceptors mediating mydriasis in the rat. Naunyn-Schmiedeberg's Arch Pharmacol. 1990 ; 341: 101-107
49. Milhaud D, Fagni L, Bockaert J, et al. Imidazoline-induced neuroprotective effects result from blockade of NMDA receptor channels in neuronal cultures. Neuropharmacology. 2000 ; 39: 2244-2254
50. Miralles A, Olmos G, Sastre M, et al. Discrimination and pharmacological characterization of I2-imidazoline sites with [3H]idazoxan and alpha-2 adrenoceptors with [3H]RX821002 (2-methoxy idazoxan) in the human and rat brains. J Pharmacol Exp Ther. 1993 ; 264: 1187-1197
51. Molderings GJ, Bönisch H, Bruss M, et al. S1P-receptors in PC12 and transfected HEK293 cells: molecular targets of hypotensive imidazoline I(1) receptor ligands. Neurochem Int. 2007 ; 51: 476-485
52. Morgan NG, Chan SL. Imidazoline binding sites in the endocrine pancreas: can they fulfil their potential as targets for the development of new insulin secretagogues?. Curr Pharm Des. 2001 ; 7: 1413-1431
53. Nutt DJ, French N, Handley S, et al. Functional studies of specific imidazoline-2 receptor ligands. Ann NY Acad Sci. 1995 ; 763: 125-139
54. Olmos G, Miralles A, Barturen F, et al. Characterization of brain imidazoline receptors in normotensive and hypertensive rats: differential regulation by chronic imidazoline drug treatment. J Pharmacol Exp Ther. 1992 ; 260: 1000-1007
55. Olmos G, Alemany R, Escribá PV, et al. The effects of chronic imidazoline drug treatment on glial fibrillary acidic protein concentrations in rat brain. Br J Pharmacol. 1994 ; 111: 997-1002
56. Olmos G, Ribera J, García-Sevilla JA. Imidazoli(di)ne compounds interact with the phencyclidine site of NMDA receptors in the rat brain. Eur J Pharmacol. 1996 ; 310: 273-276
57. Olmos G, DeGregorio-Rocasolano N, Regalado PM, et al. Protection by imidazol(ine) drugs and agmatine of glutamate-induced neurotoxicity in cultured cerebellar granule cells through blockade of NMDA receptor. Br J Pharmacol. 1999 ; 127: 1317-1326
58. Ozaita A, Olmos G, Boronat MA, et al. Inhibition of monoamine oxidase A and B activities by imidazol(ine)/guanidine drugs, nature of the interaction and distinction from I2-imidazoline receptors in rat liver. Br J Pharmacol. 1997 ; 121: 901-912
59. Pigini M, Bousquet P, Carotti A, et al. Imidazoline receptors: qualitative structure-activity relationships and discovery of tracizoline and benazoline. Two ligands with high affinity and unprecedented selectivity. Bioorg Med Chem. 1997 ; 5: 833-841
60. Piletz JE, Ivanov TR, Sharp JD, et al. Imidazoline receptor antisera-selected (IRAS) cDNA: cloning and characterization. DNA Cell Biol. 2000 ; 19: 319-329
61. Qiu W-W, Zheng R-Y. Neuroprotective effects of receptor imidazoline 2 and its endogenous ligand agmatine. Neurosci Bull. 2006 ; 22: 187-191
62. Raddatz R, Parini A, Lanier SM. Imidazoline/guanidium binding domains on monoamine oxidases. J Biol Chem. 1995 ; 270: 27961-27968
63. Raddatz R, Parini A, Lanier SM. Localization of the imidazolinbe binding domain on monoamine oxidase B. Mol Pharmacol. 1997 ; 52: 549-553
64. Ramos-Miguel A, Miralles A, García-Sevilla JA. Correlation of rat cortical Fas-associated death domain (FADD) protein phosphorylation with the severity of spontaneous morphine abstinence syndrome: role of α2-adrenoceptors and extracellular signal-regulated kinases. J Psychopharmacol. 2011 ; 25: 1690-1701
65. Regunathan S, Feinstein DL, Reis DJ. Expression of non-adrenergic imidazoline sites in rat cerebral cortical astrocytes. J Neurosci Res. 1993 ; 34: 681-688
66. Regunathan S, Reis DJ. Imidazoline receptors and their endogenous ligands. Annu Rev Pharmacol Toxicol. 1996 ; 36: 511-544
67. Ruggiero DA, Reguhathan S, Wang H, et al. Immunocytochemical localization of an imidazoline receptor protein in the central nervous system. Brain Res. 1998 ; 780: 270-293
68. Sánchez-Blázquez P, Boronat MA, Olmos G, et al. Activation of I2-imidazoline receptors enhances supraspinal morphine analgesia in mice: a model to detect agonist and antagonist activities at these receptors. Br J Pharmacol. 2000 ; 130: 146-152
69. Sastre-Coll A, Esteban S, Miralles A, et al. The imidazoline receptor ligand 2-(2-benzofuranyl)-2-imidazoline is a dopamine-releasing agent in the rat stiatum in vivo. Neurosci Lett. 2001 ; 301: 29-32
70. Separovic D, Kester M, Ernsberger P. Coupling of I1-imidazoline receptors to diacylglyceride accumulation in PC12 rat pheochromocytoma cells. Mol Pharmacol. 1996 ; 49: 668-675
71. Smith KL, Jessop DS, Finn DP. Modulation of stress by imidazoline binding sites: implications for psychiatric disorders. Stress. 2009 ; 12: 97-114
72. Stabile AM, Aceros H, Stockmeyer K, et al. Functional and molecular effects of imidazoline receptor activation in heart failure. Life Sci. 2011 ; 88: 493-503
73. Thorn DA, Zhang Y, Peng B-W, et al. Effects of imidazoline I2 receptor ligands on morphine- and tramadol-induced antinociception in rats. Eur J Pharmacol. 2011 ; 670: 435-440
74. Tonello R, Villarinho JG, da Silva Sant'anna G, et al. The potential antidepressant-like effect of imidazoline I2 ligand 2-BFI in mice. Prog Neuro-Psychopharmacol Biol Psychiatry. 2012 ; 37: 15-21
75. Tourneur L, Chiocchia G. FADD: a regulator of life and death. Trends Immunol. 2010 ; 31: 260-269
76. Uzbay TI. The pharmacological importance of agmatine in the brain. Neurosci Biobehav Rev. 2012 ; 36: 502-519
77. Wang P, Wang ZW, Lin FH, et al. 2-BFI attenuates experimental autoimmune encephalomyelitis-induced spinal cord injury with enhanced B-CK, CaATPase, but reduced calpain activity. Biochem Biophys Res Commun. 2011 ; 406: 152-157