Effect of δ-opioid receptor activation on BDNF-TrkB vs. TNF-α in the mouse cortex exposed to prolonged hypoxia

International Journal of Molecular Sciences

Volumn 14, Issue 8, 2013, Pages 15959-15976

  Tian, Xuesong ^a   Hua, Fei ^b   Sandhu, Harleen K ^a   Chao, Dongman ^a   Balboni, Gianfranco ^c   Salvadori, Severo ^d   He, Xiaozhou ^b   Xia, Ying ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b THE THIRD AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^c UNIVERSITY OF CAGLIARI   (Italy)

^d UNIVERSITY OF FERRARA   (Italy)

Author keywords

opioid receptor; Brain derived neurotrophic factor (BDNF); Hypoxia; Neuroprotection; TNF

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CD11B ANTIGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DELTA OPIATE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN HYPOXIA; CONTROLLED STUDY; DISEASE DURATION; DOWN REGULATION; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 1; ANIMALS; ANOXIA; ANTIGENS, CD11B; BENZIMIDAZOLES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBELLAR CORTEX; CEREBRAL CORTEX; CREB-BINDING PROTEIN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOWN-REGULATION; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; NEURONS; OLIGOPEPTIDES; RECEPTOR, TRKB; RECEPTORS, OPIOID, DELTA; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84881121091     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140815959     Document Type: Article

References (48)

1. Zhang, J.; Haddad, G.G.; Xia, Y. Delta-, but not mu- and kappa-, opioid receptor activation protects neocortical neurons from glutamate-induced excitotoxic injury. Brain Res. 2000, 885, 143-153.
2. Tian, X.S.; Zhou, F.; Yang, R.; Xia, Y.; Wu, G.C.; Guo, J.C. Effects of intracerebroventricular injection of delta-opioid receptor agonist TAN-67 or antagonist naltrindole on acute cerebral ischemia in rat. Sheng Li Xue Bao 2008, 60, 475-484.
3. He, X.; Sandhu, H.K.; Yang, Y.; Hua, F.; Belser, N.; Kim, D.H.; Xia, Y. Neuroprotection against hypoxia/ischemia: Delta-opioid receptor-mediated cellular/molecular events. Cell Mol. Life Sci. 2013, 70, 2291-2303.
4. Zhao, P.; Huang, Y.; Zuo, Z. Opioid preconditioning induces opioid receptor-dependent delayed neuroprotection against ischemia in rats. J. Neuropathol. Exp. Neurol. 2006, 65, 945-952.
5. Gwak, M.S.; Li, L.; Zuo, Z. Morphine preconditioning reduces lipopolysaccharide and interferon-gamma-induced mouse microglial cell injury via delta 1 opioid receptor activation. Neuroscience 2010, 167, 256-260.
6. Borlongan, C.V.; Wang, Y.; Su, T.P. Delta opioid peptide (D-Ala 2, D-Leu 5) enkephalin: Linking hibernation and neuroprotection. Front. Biosci. 2004, 9, 3392-3398.
7. Borlongan, C.V.; Hayashi, T.; Oeltgen, P.R.; Su, T.P.; Wang, Y. Hibernation-like state induced by an opioid peptide protects against experimental stroke. BMC Biol. 2009, 7, 31.
8. Sun, X.; Zhou, H.; Luo, X.; Li, S.; Yu, D.; Hua, J.; Mu, D.; Mao, M. Neuroprotection of brain-derived neurotrophic factor against hypoxic injury in vitro requires activation of extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. Int. J. Dev. Neurosci. 2008, 26, 363-370.
9. Narumiya, S.; Ohno, M.; Tanaka, N.; Yamano, T.; Shimada, M. Enhanced expression of full-length TrkB receptors in young rat brain with hypoxic/ischemic injury. Brain Res. 1998, 797, 278-286.
10. Huang, E.J.; Reichardt, L.F. Neurotrophins: Roles in neuronal development and function. Annu. Rev. Neurosci. 2001, 24, 677-736.
11. Frisen, J.; Verge, V.M.; Fried, K.; Risling, M.; Persson, H.; Trotter, J.; Hökfelt, T.; Lindholm, D. Characterization of glial trkB receptors: Differential response to injury in the central and peripheral nervous systems. Proc. Natl. Acad. Sci. USA 1993, 90, 4971-4975.
12. Wong, J.; Higgins, M.; Halliday, G.; Garner, B. Amyloid beta selectively modulates neuronal TrkB alternative transcript expression with implications for Alzheimer's disease. Neuroscience 2012, 210, 363-374.
13. Wong, J.; Rothmond, D.A.; Webster, M.J.; Weickert, C.S. Increases in two truncated TrkB isoforms in the prefrontal cortex of people with schizophrenia. Schizophr. Bull. 2013, 39, 130-140.
14. Torregrossa, M.M.; Folk, J.E.; Rice, K.C.; Watson, S.J.; Woods, J.H. Chronic administration of the delta opioid receptor agonist (+)BW373U86 and antidepressants on behavior in the forced swim test and BDNF mRNA expression in rats. Psychopharmacology (Berl.) 2005, 183, 31-40.
15. Torregrossa, M.M.; Isgor, C.; Folk, J.E.; Rice, K.C.; Watson, S.J.; Woods, J.H. The delta-opioid receptor agonist (+)BW373U86 regulates BDNF mRNA expression in rats. Neuropsychopharmacology 2004, 29, 649-659.
16. Torregrossa, M.M.; Jutkiewicz, E.M.; Mosberg, H.I.; Balboni, G.; Watson, S.J.; Woods, J.H. Peptidic delta opioid receptor agonists produce antidepressant-like effects in the forced swim test and regulate BDNF mRNA expression in rats. Brain Res. 2006, 1069, 172-181.
17. Zhang, H.; Torregrossa, M.M.; Jutkiewicz, E.M.; Shi, Y.G.; Rice, K.C.; Woods, J.H.; Watson, S.J.; Ko, M.C. Endogenous opioids upregulate brain-derived neurotrophic factor mRNA through delta-and micro-opioid receptors independent of antidepressant-like effects. Eur. J. Neurosci. 2006, 23, 984-994.
18. McCoy, M.K.; Tansey, M.G. TNF signaling inhibition in the CNS: Implications for normal brain function and neurodegenerative disease. J. Neuroinflamm. 2008, 5, 45.
19. Makar, T.K.; Bever, C.T.; Singh, I.S.; Royal, W.; Sahu, S.N.; Sura, T.P.; Sultana, S.; Sura, K.T.; Patel, N.; Dhib-Jalbut, S.; et al. Brain-derived neurotrophic factor gene delivery in an animal model of multiple sclerosis using bone marrow stem cells as a vehicle. J. Neuroimmunol. 2009, 210, 40-51.
20. Fujino, H.; Kitaoka, Y.; Hayashi, Y.; Munemasa, Y.; Takeda, H.; Kumai, T.; Kobayashi, S.; Ueno, S. Axonal protection by brain-derived neurotrophic factor associated with CREB phosphorylation in tumor necrosis factor-alpha-induced optic nerve degeneration. Acta Neuropathol. 2009, 117, 75-84.
21. Bonni, A.; Brunet, A.; West, A.E.; Datta, S.R.; Takasu, M.A.; Greenberg, M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 1999, 286, 1358-1362.
22. Finkbeiner, S.; Tavazoie, S.F.; Maloratsky, A.; Jacobs, K.M.; Harris, K.M.; Greenberg, M.E. CREB: A major mediator of neuronal neurotrophin responses. Neuron 1997, 19, 1031-1047.
23. Bilecki, W.; Hollt, V.; Przewlocki, R. Acute delta-opioid receptor activation induces CREB phosphorylation in NG108-15 cells. Eur. J. Pharmacol. 2000, 390, 1-6.
24. Zhang, J.; Xia, Y.; Haddad, G.G. Activation of δ-opioid receptors protects cortical neurons from glutamate excitotoxic injury. Soc. Neurosci. 1999, 28, 736.
25. Gao, C.J.; Niu, L.; Ren, P.C.; Wang, W.; Zhu, C.; Li, Y.Q.; Chai, W.; Sun, X.D. Hypoxic preconditioning attenuates global cerebral ischemic injury following asphyxial cardiac arrest through regulation of delta opioid receptor system. Neuroscience 2011, 202, 352-362.
26. Nagahara, A.H.; Tuszynski, M.H. Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat. Rev. Drug Discov. 2011, 10, 209-219.
27. Xie, Z. Neuronal vulnerability to anesthesia neurotoxicity depends on age of neurons. Ann. Neurol. 2013, 73, 686-687.
28. Chao, D.; Xia, Y. Ionic storm in hypoxic/ischemic stress: Can opioid receptors subside it? Prog. Neurobiol. 2010, 90, 439-470.
29. Yan, Q.; Rosenfeld, R.D.; Matheson, C.R.; Hawkins, N.; Lopez, O.T.; Bennett, L.; Welcher, A.A. Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 1997, 78, 431-448.
30. Dieni, S.; Rees, S. BDNF and TrkB protein expression is altered in the fetal hippocampus but not cerebellum after chronic prenatal compromise. Exp. Neurol. 2005, 192, 265-273.
31. Altar, C.A.; Cai, N.; Bliven, T.; Juhasz, M.; Conner, J.M.; Acheson, A.L.; Lindsay, R.M.; Wiegand, S.J. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 1997, 389, 856-860.
32. Zuccato, C.; Cattaneo, E. Role of brain-derived neurotrophic factor in Huntington's disease. Prog. Neurobiol. 2007, 81, 294-330.
33. Narantuya, D.; Nagai, A.; Sheikh, A.M.; Masuda, J.; Kobayashi, S.; Yamaguchi, S.; Kim, S.U. Human microglia transplanted in rat focal ischemia brain induce neuroprotection and behavioral improvement. PLoS One 2010, 5, e11746.
34. Nolan, S.M.; Mathew, E.C.; Scarth, S.L.; Al-Shamkhani, A.; Law, S.K. The effects of cysteine to alanine mutations of CD18 on the expression and adhesion of the CD11/CD18 integrins. FEBS Lett. 2000, 486, 89-92.
35. Fan, L.W.; Lin, S.; Pang, Y.; Rhodes, P.G.; Cai, Z. Minocycline attenuates hypoxia-ischemia-induced neurological dysfunction and brain injury in the juvenile rat. Eur. J. Neurosci. 2006, 24, 341-350.
36. Choi, B.R.; Kwon, K.J.; Park, S.H.; Jeon, W.K.; Han, S.H.; Kim, H.Y.; Han, J.S. Alternations of septal-hippocampal system in the adult wistar rat with spatial memory impairments induced by chronic cerebral hypoperfusion. Exp. Neurobiol. 2011, 20, 92-99.
37. Zhang, J.; Geula, C.; Lu, C.; Koziel, H.; Hatcher, L.M.; Roisen, F.J. Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp. Neurol. 2003, 183, 469-481.
38. Hallenbeck, J.M. The many faces of tumor necrosis factor in stroke. Nat. Med. 2002, 8, 1363-1368.
39. Kaur, C.; Rathnasamy, G.; Ling, E.A. Roles of activated microglia in hypoxia induced neuroinflammation in the developing brain and the retina. J. Neuroimmune. Pharmacol. 2013, 8, 66-78.
40. Wang, Y.; Cao, M.; Liu, A.; Di, W.; Zhao, F.; Tian, Y.; Jia, J. Changes of inflammatory cytokines and neurotrophins emphasized their roles in hypoxic-ischemic brain damage. Int. J. Neurosci. 2013, 123, 191-195.
41. Jiang, Y.; Wei, N.; Lu, T.; Zhu, J.; Xu, G.; Liu, X. Intranasal brain-derived neurotrophic factor protects brain from ischemic insult via modulating local inflammation in rats. Neuroscience 2011, 172, 398-405.
42. Lu, B. Pro-region of neurotrophins: role in synaptic modulation. Neuron 2003, 39, 735-738.
43. Ginty, D.D.; Kornhauser, J.M.; Thompson, M.A.; Bading, H.; Mayo, K.E.; Takahashi, J.S.; Greenberg, M.E. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 1993, 260, 238-241.
44. Balboni, G.; Salvadori, S.; Guerrini, R.; Negri, L.; Giannini, E.; Jinsmaa, Y.; Bryant, S.D.; Lazarus, L.H. Potent delta-opioid receptor agonists containing the Dmt-Tic pharmacophore. J. Med. Chem. 2002, 45, 5556-5563.
45. Vergura, R.; Balboni, G.; Spagnolo, B.; Gavioli, E.; Lambert, D.G.; McDonald, J.; Trapella, C.; Lazarus, L.H.; Regoli, D.; Guerrini, R.; et al. Anxiolytic- and antidepressant-like activities of H-Dmt-Tic-NH-CH(CH2-COOH)-Bid (UFP-512), a novel selective delta opioid receptor agonist. Peptides 2008, 29, 93-103.
46. Aguila, B.; Coulbault, L.; Boulouard, M.; Léveillé, F.; Davis, A.; Tóth, G.; Borsodi, A.; Balboni, G.; Salvadori, S.; Jauzac, P.; et al. In vitro and in vivo pharmacological profile of UFP-512, a novel selective delta-opioid receptor agonist; correlations between desensitization and tolerance. Br. J. Pharmacol. 2007, 152, 1312-1324.
47. Yang, Y.; Zhi, F.; He, X.; Moore, M.L.; Kang, X.; Chao, D.; Wang, R.; Kim, D.H.; Xia, Y. Delta-opioid receptor activation and microRNA expression of the rat cortex in hypoxia. PLoS One 2012, 7, e51524.
48. He, X.; Yang, Y.; Zhi, F.; Moore, M.L.; Kang, X.; Chao, D.; Wang, R.; Balboni, G.; Salvadori, S.; Kim, D.H.; et al. Delta-Opioid receptor activation modified microRNA expression in the rat kidney under prolonged hypoxia. PLoS One 2013, 8, e61080.