Functions of the chemokine receptor CXCR4 in the central nervous system and its regulation by μ-Opioid receptors

International Review of Neurobiology

Volumn 118, Issue , 2014, Pages 105-128

  Nash, Bradley ^a   Meucci, Olimpia ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Chemokine receptors; CXCR4; Ferritin heavy chain; HIV associated neurocognitive disorders; Opioid receptors; Opioids

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; CXCL16 CHEMOKINE; FERRITIN; FRACTALKINE; MU OPIATE RECEPTOR; OPIATE; OPIATE RECEPTOR; STROMAL CELL DERIVED FACTOR 1; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CX3CR1; DELTA OPIATE RECEPTOR; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; EPIDERMAL GROWTH FACTOR; G PROTEIN COUPLED RECEPTOR; GLUTAMATE RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; JANUS KINASE; KAPPA OPIATE RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C; PROTEIN KINASE B; PROTEIN KINASE C; STAT PROTEIN; TOLL LIKE RECEPTOR 4;

ARTICLE; CENTRAL NERVOUS SYSTEM; DESENSITIZATION; DIMERIZATION; HIV ASSOCIATED DEMENTIA; HUMAN; NERVE CELL; NEUROMODULATION; NEUROPATHOLOGY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; METABOLISM; PHYSIOLOGY; CELL COMMUNICATION; CELL DENSITY; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMOTAXIS; COMPLEX FORMATION; DEGENERATIVE DISEASE; DENDRITIC SPINE; DOWN REGULATION; EXCITOTOXICITY; GLIA; IMMUNOCOMPETENT CELL; INTERNEURON; LIGAND BINDING; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROPROTECTION; NEUROTRANSMISSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SPINAL GANGLION; SYNAPTIC POTENTIAL; UPREGULATION;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; RECEPTORS, CXCR4; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION;

EID: 84906739336     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-801284-0.00005-1     Document Type: Chapter

References (103)

1. Bajetto A., Bonavia R., Barbero S., Piccioli P., Costa A., Florio T., et al. Glial and neuronal cells express functional chemokine receptor CXCR4 and its natural ligand stromal cell-derived factor 1. Journal of Neurochemistry 1999, 73(6):2348-2357.
2. Balabanian K., Lagane B., Infantino S., Chow K.Y., Harriague J., Moepps B., et al. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. Journal of Biological Chemistry 2005, 280(42):35760-35766. 10.1074/jbc.M508234200.
3. Bardi G., Sengupta R., Khan M.Z., Patel J.P., Meucci O. Human immunodeficiency virus gp120-induced apoptosis of human neuroblastoma cells in the absence of CXCR4 internalization. Journal of Neurovirology 2006, 12(3):211-218. 10.1080/13550280600848373.
4. Belcheva M.M., Tan Y., Heaton V.M., Clark A.L., Coscia C.J. Mu opioid transactivation and down-regulation of the epidermal growth factor receptor in astrocytes: Implications for mitogen-activated protein kinase signaling. Molecular Pharmacology 2003, 64(6):1391-1401. 10.1124/mol.64.6.1391.
5. Bezzi P., Domercq M., Brambilla L., Galli R., Schols D., De Clercq E., et al. CXCR4-activated astrocyte glutamate release via TNFalpha: Amplification by microglia triggers neurotoxicity. Nature Neuroscience 2001, 4(7):702-710. 10.1038/89490.
6. Bunn S.J., Hanley M.R., Wilkin G.P. Evidence for a kappa-opioid receptor on pituitary astrocytes: An autoradiographic study. Neuroscience Letters 1985, 55(3):317-323.
7. Burbassi S., Aloyo V.J., Simansky K.J., Meucci O. GTPgammaS incorporation in the rat brain: A study on mu-opioid receptors and CXCR4. Journal of Neuroimmune Pharmacology 2008, 3(1):26-34. 10.1007/s11481-007-9083-1.
8. Burbassi S., Sengupta R., Meucci O. Alterations of CXCR4 function in mu-opioid receptor-deficient glia. European Journal of Neuroscience 2010, 32(8):1278-1288. 10.1111/j.1460-9568.2010.07402.x.
9. Cali C., Bezzi P. CXCR4-mediated glutamate exocytosis from astrocytes. Journal of Neuroimmunology 2010, 224(1-2):13-21. 10.1016/j.jneuroim.2010.05.004.
10. Rates of diagnoses of HIV infection among adults and adolescents, by area of residence, 2011-United States and 6 dependent areas 2013, Centers for Disease Control, HIV Surveillance Report, 23.
11. Chao D., Bazzy-Asaad A., Balboni G., Xia Y. delta-, but not mu-, opioid receptor stabilizes K(+) homeostasis by reducing Ca(2+) influx in the cortex during acute hypoxia. Journal of Cellular Physiology 2007, 212(1):60-67. 10.1002/jcp.21000.
12. Chen X., Geller E.B., Rogers T.J., Adler M.W. Rapid heterologous desensitization of antinociceptive activity between mu or delta opioid receptors and chemokine receptors in rats. Drug and Alcohol Dependence 2007, 88(1):36-41. 10.1016/j.drugalcdep.2006.09.010.
13. Clark A.K., Staniland A.A., Malcangio M. Fractalkine/CX3CR1 signalling in chronic pain and inflammation. Current Pharmaceutical Biotechnology 2011, 12(10):1707-1714.
14. Corbett A.D., Henderson G., McKnight A.T., Paterson S.J. 75 Years of opioid research: The exciting but vain quest for the Holy Grail. British Journal of Pharmacology 2006, 147(Suppl. 1):S153-S162. 10.1038/sj.bjp.0706435.
15. DeWire S.M., Yamashita D.S., Rominger D.H., Liu G., Cowan C.L., Graczyk T.M., et al. A G protein-biased ligand at the mu-opioid receptor is potently analgesic with reduced gastrointestinal and respiratory dysfunction compared with morphine. The Journal of Pharmacology and Experimental Therapeutics 2013, 344(3):708-717. 10.1124/jpet.112.201616.
16. Ellis R., Langford D., Masliah E. HIV and antiretroviral therapy in the brain: Neuronal injury and repair. Nature Reviews. Neuroscience 2007, 8(1):33-44. 10.1038/nrn2040.
17. Feng Y., He X., Yang Y., Chao D., Lazarus L.H., Xia Y. Current research on opioid receptor function. Current Drug Targets 2012, 13(2):230-246.
18. Festa L., Meucci O. Effects of opiates and HIV proteins on neurons: The role of ferritin heavy chain and a potential for synergism. Current HIV Research 2012, 10(5):453-462.
19. Finley M.J., Chen X., Bardi G., Davey P., Geller E.B., Zhang L., et al. Bi-directional heterologous desensitization between the major HIV-1 co-receptor CXCR4 and the kappa-opioid receptor. Journal of Neuroimmunology 2008, 197(2):114-123. 10.1016/j.jneuroim.2008.04.021.
20. Finley M.J., Steele A., Cornwell W.D., Rogers T.J. Transcriptional regulation of the major HIV-1 coreceptor, CXCR4, by the kappa opioid receptor. Journal of Leukocyte Biology 2011, 90(1):111-121. 10.1189/jlb.1010546.
21. Fitting S., Xu R., Bull C., Buch S.K., El-Hage N., Nath A., et al. Interactive comorbidity between opioid drug abuse and HIV-1 Tat: Chronic exposure augments spine loss and sublethal dendritic pathology in striatal neurons. American Journal of Pathology 2010, 177(3):1397-1410. 10.2353/ajpath.2010.090945.
22. Ganju R.K., Brubaker S.A., Meyer J., Dutt P., Yang Y., Qin S., et al. The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. Journal of Biological Chemistry 1998, 273(36):23169-23175.
23. Gelman J.S., Sironi J., Berezniuk I., Dasgupta S., Castro L.M., Gozzo F.C., et al. Alterations of the intracellular peptidome in response to the proteasome inhibitor bortezomib. PLoS One 2013, 8(1):e53263. 10.1371/journal.pone.0053263.
24. Goldstein A., Tachibana S., Lowney L.I., Hunkapiller M., Hood L. Dynorphin-(1-13), an extraordinarily potent opioid peptide. Proceedings of the National Academy of Sciences of the United States of America 1979, 76(12):6666-6670.
25. Gonzalez-Scarano F., Martin-Garcia J. The neuropathogenesis of AIDS. Nature Reviews. Immunology 2005, 5(1):69-81. 10.1038/nri1527.
26. Gosnell B.A., Levine A.S. Reward systems and food intake: Role of opioids. International Journal of Obesity (London) 2009, 33(Suppl. 2):S54-S58. 10.1038/ijo.2009.73.
27. Graham G.J. D6 and the atypical chemokine receptor family: Novel regulators of immune and inflammatory processes. European Journal of Immunology 2009, 39(2):342-351. 10.1002/eji.200838858.
28. Hattermann K., Mentlein R. An infernal trio: The chemokine CXCL12 and its receptors CXCR4 and CXCR7 in tumor biology. Annals of Anatomy 2013, 195(2):103-110. 10.1016/j.aanat.2012.10.013.
29. Hauser K.F., Fitting S., Dever S.M., Podhaizer E.M., Knapp P.E. Opiate drug use and the pathophysiology of neuroAIDS. Current HIV Research 2012, 10(5):435-452.
30. Heaton R.K., Clifford D.B., Franklin D.R., Woods S.P., Ake C., Vaida F., et al. HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 2010, 75(23):2087-2096. 10.1212/WNL.0b013e318200d727.
31. Heinisch S., Palma J., Kirby L.G. Interactions between chemokine and mu-opioid receptors: Anatomical findings and electrophysiological studies in the rat periaqueductal grey. Brain, Behavior, and Immunity 2011, 25(2):360-372. 10.1016/j.bbi.2010.10.020.
32. Hesselgesser J., Taub D., Baskar P., Greenberg M., Hoxie J., Kolson D.L., et al. Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 alpha is mediated by the chemokine receptor CXCR4. Current Biology 1998, 8(10):595-598.
33. Hu S., Sheng W.S., Lokensgard J.R., Peterson P.K. Morphine induces apoptosis of human microglia and neurons. Neuropharmacology 2002, 42(6):829-836.
34. Hu G., Yao H., Chaudhuri A.D., Duan M., Yelamanchili S.V., Wen H., et al. Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death & Disease 2012, 3:e381. 10.1038/cddis.2012.114.
35. Hughes J., Smith T.W., Kosterlitz H.W., Fothergill L.A., Morgan B.A., Morris H.R. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 1975, 258(5536):577-580.
36. Huising M.O., Stet R.J., Kruiswijk C.P., Savelkoul H.F., Lidy Verburg-van Kemenade B.M. Molecular evolution of CXC chemokines: Extant CXC chemokines originate from the CNS. Trends in Immunology 2003, 24(6):307-313.
37. Hutchinson M.R., Shavit Y., Grace P.M., Rice K.C., Maier S.F., Watkins L.R. Exploring the neuroimmunopharmacology of opioids: An integrative review of mechanisms of central immune signaling and their implications for opioid analgesia. Pharmacological Reviews 2011, 63(3):772-810. 10.1124/pr.110.004135.
38. Iegorova O., Fisyunov A., Krishtal O. G-protein-independent modulation of P-type calcium channels by mu-opioids in Purkinje neurons of rat. Neuroscience Letters 2010, 480(2):106-111. 10.1016/j.neulet.2010.06.015.
39. Ketwaroo G.A., Cheng V., Lembo A. Opioid-induced bowel dysfunction. Current Gastroenterology Reports 2013, 15(9):344. 10.1007/s11894-013-0344-2.
40. Khan M.Z., Brandimarti R., Musser B.J., Resue D.M., Fatatis A., Meucci O. The chemokine receptor CXCR4 regulates cell-cycle proteins in neurons. Journal of Neurovirology 2003, 9(3):300-314. 10.1080/13550280390201010.
41. Khan M.Z., Brandimarti R., Patel J.P., Huynh N., Wang J., Huang Z., et al. Apoptotic and antiapoptotic effects of CXCR4: Is it a matter of intrinsic efficacy? Implications for HIV neuropathogenesis. AIDS Research and Human Retroviruses 2004, 20(10):1063-1071. 10.1089/aid.2004.20.1063.
42. Khan M.Z., Brandimarti R., Shimizu S., Nicolai J., Crowe E., Meucci O. The chemokine CXCL12 promotes survival of postmitotic neurons by regulating Rb protein. Cell Death and Differentiation 2008, 15(10):1663-1672. 10.1038/cdd.2008.95.
43. Knapp P.E., Maderspach K., Hauser K.F. Endogenous opioid system in developing normal and jimpy oligodendrocytes: Mu and kappa opioid receptors mediate differential mitogenic and growth responses. Glia 1998, 22(2):189-201.
44. Kraft-Terry S.D., Buch S.J., Fox H.S., Gendelman H.E. A coat of many colors: Neuroimmune crosstalk in human immunodeficiency virus infection. Neuron 2009, 64(1):133-145. 10.1016/j.neuron.2009.09.042.
45. La Porta C.A. CXCR6: The role of environment in tumor progression. Challenges for therapy. Stem Cell Reviews 2012, 8(4):1282-1285. 10.1007/s12015-012-9383-6.
46. Lazarini F., Tham T.N., Casanova P., Arenzana-Seisdedos F., Dubois-Dalcq M. Role of the alpha-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 2003, 42(2):139-148. 10.1002/glia.10139.
47. Leveille F., El Gaamouch F., Gouix E., Lecocq M., Lobner D., Nicole O., et al. Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB Journal 2008, 22(12):4258-4271. 10.1096/fj.08-107268.
48. Li C.H., Chung D., Doneen B.A. Isolation, characterization and opiate activity of beta-endorphin from human pituitary glands. Biochemical and Biophysical Research Communications 1976, 72(4):1542-1547.
49. Li R., Luo C., Mines M., Zhang J., Fan G.H. 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. Journal of Biological Chemistry 2006, 281(49):37616-37627. 10.1074/jbc.M607266200.
50. Li M., Ransohoff R.M. Multiple roles of chemokine CXCL12 in the central nervous system: A migration from immunology to neurobiology. Progress in Neurobiology 2008, 84(2):116-131. 10.1016/j.pneurobio.2007.11.003.
51. Lindl K.A., Marks D.R., Kolson D.L., Jordan-Sciutto K.L. HIV-associated neurocognitive disorder: Pathogenesis and therapeutic opportunities. Journal of Neuroimmune Pharmacology 2010, 5(3):294-309. 10.1007/s11481-010-9205-z.
52. Lipfert J., Odemis V., Wagner D.C., Boltze J., Engele J. CXCR4 and CXCR7 form a functional receptor unit for SDF-1/CXCL12 in primary rodent microglia. Neuropathology and Applied Neurobiology 2013, 39(6):667-680. 10.1111/nan.12015.
53. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T., et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(16):9448-9453.
54. Malik S., Khalique H., Buch S., Seth P. A growth factor attenuates HIV-1 Tat and morphine induced damage to human neurons: Implication in HIV/AIDS-drug abuse cases. PLoS One 2011, 6(3):e18116. 10.1371/journal.pone.0018116.
55. Mansour A., Fox C.A., Akil H., Watson S.J. Opioid-receptor mRNA expression in the rat CNS: Anatomical and functional implications. Trends in Neurosciences 1995, 18(1):22-29.
56. Maysami S., Nguyen D., Zobel F., Pitz C., Heine S., Hopfner M., et al. Modulation of rat oligodendrocyte precursor cells by the chemokine CXCL12. Neuroreport 2006, 17(11):1187-1190. 10.1097/01.wnr.0000227985.92551.9a.
57. McArthur J.C., Steiner J., Sacktor N., Nath A. Human immunodeficiency virus-associated neurocognitive disorders: Mind the gap. Annals of Neurology 2010, 67(6):699-714. 10.1002/ana.22053.
58. Mellado M., Rodriguez-Frade J.M., Vila-Coro A.J., Fernandez S., Martin de Ana A., Jones D.R., et al. Chemokine receptor homo- or heterodimerization activates distinct signaling pathways. The EMBO Journal 2001, 20(10):2497-2507. 10.1093/emboj/20.10.2497.
59. Meucci O., Fatatis A., Simen A.A., Bushell T.J., Gray P.W., Miller R.J. Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(24):14500-14505.
60. Miller R.J., Rostene W., Apartis E., Banisadr G., Biber K., Milligan E.D., et al. Chemokine action in the nervous system. The Journal of Neuroscience 2008, 28(46):11792-11795. 10.1523/JNEUROSCI.3588-08.2008.
61. Molina P.E. Stress-specific opioid modulation of haemodynamic counter-regulation. Clinical and Experimental Pharmacology and Physiology 2002, 29(3):248-253.
62. Morrison J.H., Baxter M.G. The ageing cortical synapse: Hallmarks and implications for cognitive decline. Nature Reviews. Neuroscience 2012, 13(4):240-250. 10.1038/nrn3200.
63. Moser B., Wolf M., Walz A., Loetscher P. Chemokines: Multiple levels of leukocyte migration control. Trends in Immunology 2004, 25(2):75-84. 10.1016/j.it.2003.12.005.
64. Nath A. Human immunodeficiency virus-associated neurocognitive disorder: Pathophysiology in relation to drug addiction. Annals of the New York Academy of Sciences 2010, 1187:122-128. 10.1111/j.1749-6632.2009.05277.x.
65. Nicolai J., Burbassi S., Rubin J., Meucci O. CXCL12 inhibits expression of the NMDA receptor's NR2B subunit through a histone deacetylase-dependent pathway contributing to neuronal survival. Cell Death & Disease 2010, 1:e33. 10.1038/cddis.2010.10.
66. Nomiyama H., Osada N., Yoshie O. A family tree of vertebrate chemokine receptors for a unified nomenclature. Developmental and Comparative Immunology 2011, 35(7):705-715. 10.1016/j.dci.2011.01.019.
67. Ohtani Y., Minami M., Kawaguchi N., Nishiyori A., Yamamoto J., Takami S., et al. Expression of stromal cell-derived factor-1 and CXCR4 chemokine receptor mRNAs in cultured rat glial and neuronal cells. Neuroscience Letters 1998, 249(2-3):163-166.
68. Okamoto M., Wang X., Baba M. HIV-1-infected macrophages induce astrogliosis by SDF-1alpha and matrix metalloproteinases. Biochemical and Biophysical Research Communications 2005, 336(4):1214-1220. 10.1016/j.bbrc.2005.08.251.
69. Pandey V., Bolsover S.R. Immediate and neurotoxic effects of HIV protein gp120 act through CXCR4 receptor. Biochemical and Biophysical Research Communications 2000, 274(1):212-215. 10.1006/bbrc.2000.3113.
70. Parachikova A., Cotman C.W. Reduced CXCL12/CXCR4 results in impaired learning and is downregulated in a mouse model of Alzheimer disease. Neurobiology of Disease 2007, 28(2):143-153. 10.1016/j.nbd.2007.07.001.
71. Patel J.R., McCandless E.E., Dorsey D., Klein R.S. CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(24):11062-11067. 10.1073/pnas.1006301107.
72. Patel J.P., Sengupta R., Bardi G., Khan M.Z., Mullen-Przeworski A., Meucci O. Modulation of neuronal CXCR4 by the micro-opioid agonist DAMGO. Journal of Neurovirology 2006, 12(6):492-500. 10.1080/13550280601064798.
73. Pello O.M., Martinez-Munoz L., Parrillas V., Serrano A., Rodriguez-Frade J.M., Toro M.J., et al. Ligand stabilization of CXCR4/delta-opioid receptor heterodimers reveals a mechanism for immune response regulation. European Journal of Immunology 2008, 38(2):537-549. 10.1002/eji.200737630.
74. Persson P.A., Thorlin T., Ronnback L., Hansson E., Eriksson P.S. Differential expression of delta opioid receptors and mRNA in proliferating astrocytes during the cell cycle. Journal of Neuroscience Research 2000, 61(4):371-375.
75. Pitcher J., Abt A., Myers J., Han R., Snyder M., Graziano A., et al. Neuronal ferritin heavy chain and drug abuse affect HIV-associated cognitive dysfunction. Journal of Clinical Investigation 2014, 124(2):656-669. Epub 2014 Jan 9. 10.1172/JCI70090.
76. Réaux-Le Goazigo A., Van Steenwinckel J., Rostène W., Mélik Parsadaniantz S. Current status of chemokines in the adult CNS. Progress in Neurobiology 2013, 104:67-92. 10.1016/j.pneurobio.2013.02.001.
77. Rios C., Gomes I., Devi L.A. mu opioid and CB1 cannabinoid receptor interactions: Reciprocal inhibition of receptor signaling and neuritogenesis. British Journal of Pharmacology 2006, 148(4):387-395. 10.1038/sj.bjp.0706757.
78. Rostene W., Kitabgi P., Parsadaniantz S.M. Chemokines: A new class of neuromodulator?. Nature Reviews. Neuroscience 2007, 8(11):895-903. 10.1038/nrn2255.
79. Ruzicka B.B., Fox C.A., Thompson R.C., Meng F., Watson S.J., Akil H. Primary astroglial cultures derived from several rat brain regions differentially express mu, delta and kappa opioid receptor mRNA. Brain Research. Molecular Brain Research 1995, 34(2):209-220.
80. Sanchez-Alcaniz J.A., Haege S., Mueller W., Pla R., Mackay F., Schulz S., et al. Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron 2011, 69(1):77-90. 10.1016/j.neuron.2010.12.006.
81. Sengupta R., Burbassi S., Shimizu S., Cappello S., Vallee R.B., Rubin J.B., et al. Morphine increases brain levels of ferritin heavy chain leading to inhibition of CXCR4-mediated survival signaling in neurons. Journal of Neuroscience 2009, 29(8):2534-2544. 10.1523/JNEUROSCI.5865-08.2009.
82. Shepherd A.J., Loo L., Mohapatra D.P. Chemokine co-receptor CCR5/CXCR4-dependent modulation of Kv2 1 channel confers acute neuroprotection to HIV-1 glycoprotein gp120 exposure. PLoS One 2013, 8(9):e76698. 10.1371/journal.pone.0076698.
83. Sheridan G.K., Murphy K.J. Neuron-glia crosstalk in health and disease: Fractalkine and CX3CR1 take centre stage. Open Biology 2013, 3(12):130181. 10.1098/rsob.130181.
84. Strieter R.M., Burdick M.D., Gomperts B.N., Belperio J.A., Keane M.P. CXC chemokines in angiogenesis. Cytokine & Growth Factor Reviews 2005, 16(6):593-609. 10.1016/j.cytogfr.2005.04.007.
85. Stumm R.K., Zhou C., Ara T., Lazarini F., Dubois-Dalcq M., Nagasawa T., et al. CXCR4 regulates interneuron migration in the developing neocortex. Journal of Neuroscience 2003, 23(12):5123-5130.
86. Szabo I., Wetzel M.A., Zhang N., Steele A.D., Kaminsky D.E., Chen C., et al. Selective inactivation of CCR5 and decreased infectivity of R5 HIV-1 strains mediated by opioid-induced heterologous desensitization. Journal of Leukocyte Biology 2003, 74(6):1074-1082. 10.1189/jlb.0203067.
87. Toth P.T., Ren D., Miller R.J. Regulation of CXCR4 receptor dimerization by the chemokine SDF-1alpha and the HIV-1 coat protein gp120: A fluorescence resonance energy transfer (FRET) study. Journal of Pharmacology and Experimental Therapeutics 2004, 310(1):8-17. 10.1124/jpet.103.064956.
88. Turchan-Cholewo J., Dimayuga F.O., Ding Q., Keller J.N., Hauser K.F., Knapp P.E., et al. Cell-specific actions of HIV-Tat and morphine on opioid receptor expression in glia. Journal of Neuroscience Research 2008, 86(9):2100-2110. 10.1002/jnr.21653.
89. van der Meer P., Ulrich A.M., Gonzalez-Scarano F., Lavi E. Immunohistochemical analysis of CCR2, CCR3, CCR5, and CXCR4 in the human brain: Potential mechanisms for HIV dementia. Experimental and Molecular Pathology 2000, 69(3):192-201. 10.1006/exmp.2000.2336.
90. van Dorp E.L., Kest B., Kowalczyk W.J., Morariu A.M., Waxman A.R., Arout C.A., et al. Morphine-6beta-glucuronide rapidly increases pain sensitivity independently of opioid receptor activity in mice and humans. Anesthesiology 2009, 110(6):1356-1363. 10.1097/ALN.0b013e3181a105de.
91. Vergote D., Butler G.S., Ooms M., Cox J.H., Silva C., Hollenberg M.D., et al. Proteolytic processing of SDF-1alpha reveals a change in receptor specificity mediating HIV-associated neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(50):19182-19187. 10.1073/pnas.0604678103.
92. Waldhoer M., Bartlett S.E., Whistler J.L. Opioid receptors. Annual Review of Biochemistry 2004, 73:953-990. 10.1146/annurev.biochem.73.011303.073940.
93. Wang W., Knovich M.A., Coffman L.G., Torti F.M., Torti S.V. Serum ferritin: Past, present and future. Biochimica et Biophysica Acta 2010, 1800(8):760-769. 10.1016/j.bbagen.2010.03.011.
94. Watkins L.R., Hutchinson M.R., Rice K.C., Maier S.F. The "toll" of opioid-induced glial activation: Improving the clinical efficacy of opioids by targeting glia. Trends in Pharmacological Sciences 2009, 30(11):581-591. 10.1016/j.tips.2009.08.002.
95. Williams J.T., Ingram S.L., Henderson G., Chavkin C., von Zastrow M., Schulz S., et al. Regulation of mu-opioid receptors: Desensitization, phosphorylation, internalization, and tolerance. Pharmacological Reviews 2013, 65(1):223-254. 10.1124/pr.112.005942.
96. Wilson N.M., Jung H., Ripsch M.S., Miller R.J., White F.A. CXCR4 signaling mediates morphine-induced tactile hyperalgesia. Brain, Behavior, and Immunity 2011, 25(3):565-573. 10.1016/j.bbi.2010.12.014.
97. Wittert G., Hope P., Pyle D. Tissue distribution of opioid receptor gene expression in the rat. Biochemical and Biophysical Research Communications 1996, 218(3):877-881. 10.1006/bbrc.1996.0156.
98. Xu M., Bruchas M.R., Ippolito D.L., Gendron L., Chavkin C. Sciatic nerve ligation-induced proliferation of spinal cord astrocytes is mediated by kappa opioid activation of p38 mitogen-activated protein kinase. Journal of Neuroscience 2007, 27(10):2570-2581. 10.1523/JNEUROSCI.3728-06.2007.
99. Zhang K., McQuibban G.A., Silva C., Butler G.S., Johnston J.B., Holden J., et al. HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration. Nature Neuroscience 2003, 6(10):1064-1071. 10.1038/nn1127.
100. Zhang N., Rogers T.J., Caterina M., Oppenheim J.J. Proinflammatory chemokines, such as C-C chemokine ligand 3, desensitize mu-opioid receptors on dorsal root ganglia neurons. Journal of Immunology 2004, 173(1):594-599.
101. Zheng J., Thylin M.R., Ghorpade A., Xiong H., Persidsky Y., Cotter R., et al. Intracellular CXCR4 signaling, neuronal apoptosis and neuropathogenic mechanisms of HIV-1-associated dementia. Journal of Neuroimmunology 1999, 98(2):185-200.
102. Zlotnik A., Yoshie O. Chemokines: A new classification system and their role in immunity. Immunity 2000, 12(2):121-127.
103. Zlotnik A., Yoshie O. The chemokine superfamily revisited. Immunity 2012, 36(5):705-716. 10.1016/j.immuni.2012.05.008.