Alterations of CXCR4 function in μ-opioid receptor-deficient glia

European Journal of Neuroscience

Volumn 32, Issue 8, 2010, Pages 1278-1288

  Burbassi, Silvia ^a   Sengupta, Rajarshi ^a   Meucci, Olimpia ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Chemokine; CXCR4; G protein coupled receptor; Glia; Opioid

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR ANTAGONIST; GUANINE NUCLEOTIDE BINDING PROTEIN; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE 3; MU OPIATE RECEPTOR; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN SLICE; BRAIN TISSUE; CELL CULTURE; CONTROLLED STUDY; GLIA CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MACROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TISSUE HOMOGENATE; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; BRAIN; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; NEUROGLIA; NEURONS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CXCR4; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77958487299     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07402.x     Document Type: Article

References (49)

1. Ananthan, S., Johnson, C.A., Carter, R.L., Clayton, S.D., Rice, K.C., Xu, H., Davis, P., Porreca, F. & Rothmand, R.B. (1998) Synthesis, opioid receptor binding, and bioassay of naltrindole analogues substituted in the indolic benzene moiety. J. Med. Chem., 41, 2872-2881.
2. Bell, J.E., Arango, J.C., Robertson, R., Brettle, R.P., Leen, C. & Simmonds, P. (2002) HIV and drug misuse in the Edinburgh cohort. J. Acquir. Immune Defic. Syndr., 31(Suppl 2), S35-S42.
3. Bezzi, P., Domercq, M., Brambilla, L., Galli, R., Schols, D. et al. (2001) CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci., 4, 702-710.
4. Burbassi, S., Aloyo, V.J., Simansky, K.J. & Meucci, O. (2008) GTPgammaS incorporation in the rat brain: a study on mu-opioid receptors and CXCR4. J. Neuroimmune Pharmacol., 3, 26-34.
5. Cahill, C.M., Morinville, A., Lee, M.C., Vincent, J.P., Collier, B. & Beaudet, A. (2001) Prolonged morphine treatment targets delta opioid receptors to neuronal plasma membranes and enhances delta-mediated antinociception. J. Neurosci., 21, 7598-7607.
6. Cali', C., Marchaland, J., Mirante, O. & Bezzi, P. (2010) Chemokines as neuromodulators: regulation of glutamatergic transmission by CXCR4-mediated glutamated release from astrocytes. In Meucci, O. (Ed.), Chemokine Receptors and NeuroAIDS. Springer, New York, pp. 271-300.
7. Commons, K.G. (2003) Translocation of presynaptic delta opioid receptors in the ventrolateral periaqueductal gray after swim stress. J. Comp. Neurol., 464, 197-207.
8. Cook, A., Hippensteel, R., Shimizu, S., Nicolai, J., Fatatis, A. & Meucci, O. (2010) Interactions between chemokines: regulation of fractalkine/CX3CL1 homeostasis by SDF/CXCL12 in cortical neurons. J. Biol. Chem., 285, 10563-10571.
9. Decaillot, F.M., Rozenfeld, R., Gupta, A. & Devi, L.A. (2008) Cell surface targeting of mu-delta opioid receptor heterodimers by RTP4. Proc. Natl Acad. Sci. USA, 105, 16045-16050.
10. Devi, L.A. (2001) Heterodimerization of G-protein-coupled receptors: pharmacology, signaling and trafficking. Trends Pharmacol. Sci., 22, 532-537.
11. Donahoe, R.M. & Vlahov, D. (1998) Opiates as potential cofactors in progression of HIV-1 infections to, AIDS. J. Neuroimmunol., 83, 77-87.
12. Forster, K., Kuno, A., Solenkova, N., Felix, S.B. & Krieg, T. (2007) The delta-opioid receptor agonist DADLE at reperfusion protects the heart through activation of pro-survival kinases via EGF receptor transactivation. Am. J. Physiol. Heart Circ. Physiol., 293, H1604-H1608.
13. Gomes, I., Jordan, B.A., Gupta, A., Trapaidze, N., Nagy, V. & Devi, L.A. (2000) Heterodimerization of mu and delta opioid receptors: a role in opiate synergy. J. Neurosci., 20, RC110.
14. Hack, S.P., Bagley, E.E., Chieng, B.C. & Christie, M.J. (2005) Induction of delta-opioid receptor function in the midbrain after chronic morphine treatment. J. Neurosci., 25, 3192-3198.
15. Hauser, K.F., El-Hage, N., Buch, S., Berger, J.R., Tyor, W.R. et al. (2005) Molecular targets of opiate drug abuse in neuroAIDS. Neurotox. Res., 8, 63-80.
16. Hauser, K.F., El-Hage, N., Buch, S., Nath, A., Tyor, W.R. et al. (2006) Impact of opiate-HIV-1 interactions on neurotoxic signaling. J. Neuroimmune Pharmacol., 1, 98-105.
17. Hauser, K.F., El-Hage, N., Stiene-Martin, A., Maragos, W.F., Nath, A. et al. (2007) HIV-1 neuropathogenesis: glial mechanisms revealed through substance abuse. J. Neurochem., 100, 567-586.
18. Heiss, A., Ammer, H. & Eisinger, D.A. (2009) delta-Opioid receptor-stimulated Akt signaling in neuroblastoma x glioma (NG108-15) hybrid cells involves receptor tyrosine kinase-mediated PI3K activation. Exp. Cell Res., 315, 2115-2125.
19. Hutchinson, A.C., Simpson, G.R., Randall, J.F., Zhang, X., Calderon, S.N. et al. (2000) Assessment of SNC 80 and naltrindole within a conditioned taste aversion design. Pharmacol. Biochem. Behav., 66, 779-787.
20. Jones, G.J., Barsby, N.L., Cohen, E.A., Holden, J., Harris, K. et al. (2007) HIV-1 Vpr causes neuronal apoptosis and in vivo neurodegeneration. J. Neurosci., 27, 3703-3711.
21. Jordan, B.A., Trapaidze, N., Gomes, I., Nivarthi, R. & Devi, L.A. (2001) Oligomerization of opioid receptors with beta 2-adrenergic receptors: a role in trafficking and mitogen-activated protein kinase activation. Proc. Natl Acad. Sci. USA, 98, 343-348.
22. Khan, M.Z., Brandimarti, R., Shimizu, S., Nicolai, J., Crowe, E. & Meucci, O. (2008) The chemokine CXCL12 promotes survival of postmitotic neurons by regulating Rb protein. Cell Death Differ., 15, 1663-1672.
23. Kitchen, I., Slowe, S.J., Matthes, H.W. & Kieffer, B. (1997) Quantitative autoradiographic mapping of mu-, delta- and kappa-opioid receptors in knockout mice lacking the mu-opioid receptor gene. Brain Res., 778, 73-88.
24. Lazarini, F., Tham, T.N., Casanova, P., Arenzana-Seisdedos, F. & Dubois-Dalcq, M. (2003) Role of the alpha-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia, 42, 139-148.
25. Levoye, A., Balabanian, K., Baleux, F., Bachelerie, F. & Lagane, B. (2009) CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood, 113, 6085-6093.
26. Li, M. & Ransohoff, R.M. (2008) Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog. Neurobiol., 84, 116-131.
27. Li, R., Luo, C., Mines, M., Zhang, J. & Fan, G.H. (2006) Chemokine CXCL12 induces binding of ferritin heavy chain to the chemokine receptor CXCR4, alters CXCR4 signaling, and induces phosphorylation and nuclear translocation of ferritin heavy chain. J. Biol. Chem., 281, 37616-37627.
28. Loh, H.H., Liu, H.C., Cavalli, A., Yang, W., Chen, Y.F. & Wei, L.N. (1998) mu Opioid receptor knockout in mice: effects on ligand-induced analgesia and morphine lethality. Brain Res. Mol. Brain Res., 54, 321-326.
29. Ma, Q., Jones, D., Borghesani, P.R., Segal, R.A., Nagasawa, T. et al. (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl Acad. Sci. USA, 95, 9448-9453.
30. Ma, J., Zhang, Y., Kalyuzhny, A.E. & Pan, Z.Z. (2006) Emergence of functional delta-opioid receptors induced by long-term treatment with morphine. Mol. Pharmacol., 69, 1137-1145.
31. Matthes, H.W., Smadja, C., Valverde, O., Vonesch, J.L., Foutz, A.S. et al. (1998) Activity of the delta-opioid receptor is partially reduced, whereas activity of the kappa-receptor is maintained in mice lacking the mu-receptor. J. Neurosci., 18, 7285-7295.
32. Meucci, O. & Miller, R.J. (1996) gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: protective action of TGF-beta1. J. Neurosci., 16, 4080-4088.
33. Meucci, O., Fatatis, A., Simen, A.A., Bushell, T.J., Gray, P.W. & Miller, R.J. (1998) Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc. Natl Acad. Sci. USA, 95, 14500-14505.
34. Morinville, A., Cahill, C.M., Esdaile, M.J., Aibak, H., Collier, B. et al. (2003) Regulation of delta-opioid receptor trafficking via mu-opioid receptor stimulation: evidence from mu-opioid receptor knock-out mice. J. Neurosci., 23, 4888-4898.
35. Nicolai, J., Burbassi, S., Rubin, J. & Meucci, O. (2010) CXCL12 inhibits expression of the NMDA receptor's NR2B subunit through a histone deacetylase-dependent pathway contributing to neuronal survival. Cell Death Dis., 1, 1-11, e33; doi:.
36. Patel, J.P., Sengupta, R., Bardi, G., Khan, M.Z., Mullen-Przeworski, A. & Meucci, O. (2006) Modulation of neuronal CXCR4 by the micro-opioid agonist, DAMGO. J. Neurovirol., 12, 492-500.
37. Pello, O.M., Martinez-Munoz, L., Parrillas, V., Serrano, A., Rodriguez-Frade, J.M. et al. (2008) Ligand stabilization of CXCR4/delta-opioid receptor heterodimers reveals a mechanism for immune response regulation. Eur. J. Immunol., 38, 537-549.
38. Rogers, T.J., Steele, A.D., Howard, O.M. & Oppenheim, J.J. (2000) Bidirectional heterologous desensitization of opioid and chemokine receptors. Ann. N.Y. Acad. Sci., 917, 19-28.
39. Rozenfeld, R. & Devi, L.A. (2007) Receptor heterodimerization leads to a switch in signaling: beta-arrestin2-mediated ERK activation by mu-delta opioid receptor heterodimers. FASEB J., 21, 2455-2465.
40. Sengupta, R., Burbassi, S., Shimizu, S., Cappello, S., Vallee, R.B. et al. (2009) Morphine increases brain levels of ferritin heavy chain leading to inhibition of CXCR4-mediated survival signaling in neurons. J. Neurosci., 29, 2534-2544.
41. Sharp, B.M. (2006) Multiple opioid receptors on immune cells modulate intracellular signaling. Brain Behav. Immun., 20, 9-14.
42. Shimizu, S., Khan, M.Z., Hippensteel, R.L., Parkar, A., Raghupathi, R. & Meucci, O. (2007) Role of the transcription factor E2F1 in CXCR4-mediated neurotoxicity and HIV neuropathology. Neurobiol. Dis., 25, 17-26.
43. Sim, L.J., Selley, D.E., Dworkin, S.I. & Childers, S.R. (1996) Effects of chronic morphine administration on mu opioid receptor-stimulated [35S]GTPgammaS autoradiography in rat brain. J. Neurosci., 16, 2684-2692.
44. Steele, A.D., Szabo, I., Bednar, F. & Rogers, T.J. (2002) Interactions between opioid and chemokine receptors: heterologous desensitization. Cytokine Growth Factor Rev., 13, 209-222.
45. Tien, L.T., Ho, I.K., Loh, H.H. & Ma, T. (2007) Role of mu-opioid receptor in modulation of preproenkephalin mRNA expression and opioid and dopamine receptor binding in methamphetamine-sensitized mice. J. Neurosci. Res., 85, 673-680.
46. Traynor, J.R. & Elliott, J. (1993) delta-Opioid receptor subtypes and cross-talk with mu-receptors. Trends Pharmacol. Sci., 14, 84-86.
47. Vergote, D., Butler, G.S., Ooms, M., Cox, J.H., Silva, C. et al. (2006) Proteolytic processing of SDF-1alpha reveals a change in receptor specificity mediating HIV-associated neurodegeneration. Proc. Natl Acad. Sci. USA, 103, 19182-19187.
48. Zabel, B.A., Wang, Y., Lewen, S., Berahovich, R.D., Penfold, M.E. et al. (2009) Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J. Immunol., 183, 3204-3211.
49. Zou, Y.R., Kottmann, A.H., Kuroda, M., Taniuchi, I. & Littman, D.R. (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature, 393, 595-599.