Expression of AMPA-type glutamate receptors in HEK cells and cerebellar granule neurons impairs CXCL2-mediated chemotaxis

Journal of Neuroimmunology

Volumn 134, Issue 1-2, 2003, Pages 61-71

  Limatola, Cristina ^a   Di Bartolomeo, Sabrina ^a   Trettel, Flavia ^a,b   Lauro, Clotilde ^a   Ciotti, Maria T ^c   Mercanti, Delio ^c   Castellani, Loriana ^d   Eusebi, Fabrizio ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Dipto di Scienze Internistiche   (Italy)

^c CNR   (Italy)

^d INFM   (Italy)

Author keywords

Chemokines; Chemotaxis; Glutamate; Rat cerebellar neurons

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; CHEMOKINE; CHEMOKINE RECEPTOR CXCR2; CXC CHEMOKINE LIGAND 2; GLUTAMATE RECEPTOR; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG;

ARTICLE; BRAIN NERVE CELL; CELL STRAIN; CEREBELLUM; CHEMOTAXIS; CONTROLLED STUDY; GRANULE CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELL MEMBRANE; CELL MOVEMENT; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CEREBELLAR CORTEX; CHEMOKINES; CHEMOKINES, CXC; CHEMOTACTIC FACTORS; CHEMOTAXIS; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEUROIMMUNOMODULATION; NEURONS; PRECIPITIN TESTS; RATS; RATS, WISTAR; RECEPTORS, AMPA; RECEPTORS, INTERLEUKIN-8B; SIGNAL TRANSDUCTION;

EID: 0037219095     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-5728(02)00401-0     Document Type: Article

References (61)

1. Altman J. Postnatal development of the cerebellar cortex in the rat: I. The external germinal layer and the transitional molecular layer. J. Comp. Neurol. 145:1972;353-398.
2. Altman J. Postnatal development of the cerebellar cortex in the rat: II. Maturation of the components of the granular layer. J. Comp. Neurol. 145:1972;465-514.
3. Araujo D.M., Cotman C.W. Trophic effect of interleukin-4 and -7 and -8 on hippocampal neuronal cultures: potential involvement of glial derived factor. Brain Res. 600:1993;49-55.
4. Asensio V.C., Campbell I.L. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci. 22:1999;504-512.
5. Becher A., White J.H., McIlhinney J. The γ-aminobutyric acid receptor B, but not the metabotropic glutamate receptor type-1, associates with lipid rafts in the rat cerebellum. J. Neurochem. 79:2001;787-795.
6. Ben-Baruch A., Grimm M., Bengali K., Evans G.A., Chertov O., Wang J.M., Howard O.M.Z., Mukaida K., Matsushima K., Oppenheim J.J. The differential ability of IL-8 and neutrophils-activating peptide-2 to induce attenuation of chemotaxis is mediated by their divergent capabilities to phosphorylate CXCR2 (IL-8 receptor B). J. Immunol. 158:1997;5927-5933.
7. Bigge C.F. Ionotropic glutamate receptors. Curr. Opin. Chem. Biol. 3:1999;441-447.
8. Bottestein J., Hayashi I., Hutchings S., Masui H., Mather J., McClure D.B., Ohasa S., Rizzino A., Sato G., Serrero G., Wolfe R., Wu R. The growth of cells in serum-free hormone-supplemented media. Methods Enzymol. 58:1979;94-109.
9. Bruno V., Copani A., Besong G., Scoto G., Nicoletti F. Neuroprotective activity of chemokines against N-methyl-D-aspartate or beta-amyloid-induced toxicity in culture. Eur. J. Pharmacol. 399:2000;117-121.
10. Cacalano G., Lee J., Kikly K., Ryan A.M., Pitts-Meek S., Hultgren B., Wood W.I., Moore M.W. Neutrophil B-cell expansion in mice that lack the murine IL-8 receptor homologue. Science. 265:1994;682-684.
11. Carroll R.C., Beattle E.C., von Zastrow M., Malenka R.C. Role of AMPA receptor endocytosis in synaptic plasticity. Nat. Rev., Neurosci. 2:2001;315-324.
12. Devalaraja R., Nanney L.B., Du J., Quian Q., Yu Y., Devalaraja M.N., Richmond A. Delayed wound healing in CXCR2 knock-out mice. J. Invest. Dermatol. 115:2000;234-244.
13. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51:1999;7-61.
14. Dong H., O'Brien R.J., Fung E.T., Lanahan A.A., Worley P.F., Huganir R.L. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature. 386:1997;279-284.
15. Dorf M.E., Berman M.A., Tanabe S., Heesen M., Luo Y. Astrocytes express functional chemokine receptors. J. Neuroimmunol. 111:2000;109-121.
16. Fan G.H., Yang W., Wang X.-J., Qian Q., Richmond A. Identification of a motif in the carboxyl terminus of CXCR2 that is involved in adaptin 2 binding and receptor internalization. Biochem. 40:2001;791-800.
17. Fan G.H., Yang W., Sai J., Richmond A. Phosphorylation-independent association of CXCR2 with the protein phosphatase 2A core enzyme. J. Biol. Chem. 276:2001;16960-16968.
18. Fan G.H., Yang W., Sai J., Richmond A. Hsc/Hsp70 interacting protein (Hip) associates with CXCR2 and regulates the receptor signaling and trafficking. J. Biol. Chem. 277:2002;6590-6597.
19. Fernandes H., Cohen S., Bishayee S. Glycosylation-induced conformational modification positively regulates receptor-receptor association: a study with an aberrant epidermal growth factor receptor (EGFRvIII/DeltaEGFR) expressed in cancer cells. J. Biol. Chem. 276:2001;5375-5383.
20. Giovannelli A., Limatola C., Ragozzino D., Mileo A.M., Ruggeri A., Ciotti M.T., Mercanti D., Santoni A., Eusebi F. CXC chemokine interleukin-8 (IL-8) and growth-related gene product a (GROα) modulate Purkinje neuron activity in mouse cerebellum. J. Neuroimmunol. 92:1998;122-132.
21. Glabinski A.R., Ransohoff R.M. Chemokines and chemokine receptors in CNS pathology. J. Neurovirology. 5:1999;3-12.
22. Grimm M.C., Ben-Baruch A., Taub D.D., Howard O.M., Resau J.H., Wang J.M., Ali H., Richardson R., Snyderman R., Oppenheim J.J. Opiates transdeactivate chemokine receptors: delta and mu opiate receptor-mediated heterologous desensitization. J. Exp. Med. 188:1998;317-325.
23. Hesselgesser J., Halks-Miller M., Del Vecchio V., Peiper S.C., Hoxie J., Kolson D.L., Taub D., Horuk R. CD4-independent association between HIV-1 gp120 and CXCR4: functional chemokine receptors are expressed in human neurons. Curr. Biol. 7:1997;112-121.
24. Horuk R. Chemokine receptors. Cytokine Growth Factor Rev. 12:2001;313-335.
25. Horuk R., Martin A.W., Wang Z., Schweitzer L., Gerassimides A., Guo H., Lu Q., Hesselgesser J., Perez H.D., Kim J., Parker J., Hadley T.J., Peiper S.C. Expression of chemokine receptors by subsets of neurons in the central nervous system. J. Immunol. 158:1997;2882-2890.
26. Klein R.S., Rubin J.B., Gibson H.D., DeHaan E.N., Alvarez-Hernandez X., Segal R.A., Luster A.D. SDF-1α induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development. 128:2001;1971-1981.
27. Komuro H., Rakic P. Modulation of neuronal migration by NMDA receptors. Science. 260:1993;95-97.
28. Lax P., Limatola C., Fucile S., Trettel F., Di Bartolomeo S., Renzi M., Ragozzino D., Eusebi F. Chemokine receptor CXCR2 regulates the functional properties of AMPA-type glutamate receptor GluR1 in HEK cells. J. Neuroimmunol. 129:2002;66-73.
29. Leonard A.S., Davare M.A., Horne M.C., Garner C.C., Hell J.W. SAP97 is associated with the α-amino-3-hydroxy-5-methylisoxole-4-propionic acid receptor GluR1 subunit. J. Biol. Chem. 273:1998;19518-19524.
30. Li Q., Santini R., Rosenspire A.R. Glycosylated extracellular domains of membrane immunoglobulin M contribute to its association with mb-1/B29 gene products and the B cell receptor complex. Immunol. Invest. 27:1998;57-72.
31. Limatola C., Ciotti M.T., Mercanti D., Vacca F., Ragozzino D., Giovannelli A., Santoni A., Eusebi F., Miledi R. The chemokine growth-related gene product β protects rat cerebellar granule cells from apoptotic death through α-amino-3-hydroxy-5-methyl-4-isoxasolepropiate receptors. Proc. Natl. Acad. Sci. U. S. A. 97:2000;6197-6201.
32. Limatola C., Ciotti M.T., Mercanti F., Santoni A., Eusebi F. Signaling pathways activated by chemokine receptor CXCR2 and AMPA-type glutamate receptors and involvement in granule cells survival. J. Neuroimmunol. 123:2002;9-17.
33. Liu F., Wan Q., Pristupa Z.B., Yu X.-M., Wang Y.T., Niznik H.B. Direct protein-protein coupling enables cross-talk between dopamine D5 and γ-aminobutyric acid A receptors. Nature. 403:2000;274-280.
34. Lu M., Grove E.A., Miller R.J. Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc. Natl. Acad. Sci. U. S. A. 99:2002;7090-7095.
35. Luan J., Furuta Y., Du J., Richmond A. Developmental expression of two CXC chemokines, MIP-2 and KC, and their receptors. Cytokine. 14:2001;253-263.
36. Ludwig A., Ehlert J.E., Flad H.D., Brandt E. Identification of distinct surface-expressed and intracellular CXC-chemokine receptor 2 glycoforms in neutrophils: N-glycosylation is essential for maintenance of receptor surface expression. J. Immunol. 165:2000;1044-1052.
37. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T., Bronson R.T., Springer T.A. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 95:1998;9448-9453.
38. Mack V., Burnashev N., Kaiser K.M.M., Rozov A., Jensen V., Hvalby Ø., Seeburg P.H., Sakmann B., Sprengel R. Conditional restoration of hippocampal synaptic potentiation in GluR-A-deficient mice. Science. 292:2001;2501-2504.
39. Martin L.J., Furuta A., Blackstone C.D. AMPA receptor protein in developing rat brain: glutamate receptor-1 expression and localization change at regional, cellular, and subcellular levels with maturation. Neuroscience. 83:1998;917-928.
40. Masserini M., Palestini P., Pitto M. Glicolipid-enriched caveolae and caveolae-like domains in the nervous system. J. Neurochem. 73:1999;1-11.
41. Mellado M., Rodriguez-Frade J.M., Vila-Coro A.J., Fernandez S., de Ana A.M., Jones D.R., Toran J.L., Martinez A.C. Chemokine receptor homo- or heterodimerization activates distinct signalling pathways. EMBO J. 20:2001;2497-2507.
42. Meucci O., Fatatis A., Simen A.A., Bushell T.J., Gray P.W., Miller R.J. Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc. Natl. Acad. Sci. U. S. A. 95:1998;14500-14505.
43. Pelchen-Matthews A., Signoret N., Klasse P.J., Fraile-Ramos A., Marsh M. Chemokine receptor trafficking and viral replication. Immunol. Rev. 168:1999;33-49.
44. 2+ currents in identified cholinergic septal neurons expressing CXCR1 and CXCR2 receptor mRNAs. J. Neurochem. 78:2001;960-971.
45. Ragozzino D., Giovannelli A., Mileo A.M., Limatola C., Santoni A., Eusebi F. Modulation of the neurotransmitter release in rat cerebellar neurons by GROβ NeuroReport. 16:1998;3601-3606.
46. Ramanathan V.K., Hall Z.W. Altered glycosylation sites of the delta subunit of the acetylcholine receptor (AChR) reduce alpha delta association and receptor assembly. J. Biol. Chem. 274:1999;20513-20520.
47. Robinson S., Tani M., Strieter R.M., Ransohoff R.M., Miller R.H. The chemokine growth-related oncogene-α promotes spinal cord oligodendrocytes precursor proliferation. J. Neurosci. 18:1998;10457-10463.
48. Rocheville M., Lange D.C., Kumar U., Patel S.C., Patel R.C., Patel Y.C. Receptors for dopamine and somatostatin: formation of heteroligomers with enhanced functional activity. Science. 288:2000;154-157.
49. Saas P., Boucrat J., Quiquerez A.L., Schnuriger V., Perrin G., Desplat-Jego S., Bernard D., Walker P.R., Dietrich P.Y. CD95 (Fas/Apo-1) as a receptor governing astrocyte apoptotic or inflammatory responses: a key role in brain inflammation? J. Immunol. 162:1999;2326-2333.
50. Smith T.C., Wang L.-W., Howe J.R. Distinct kainate receptors phenotypes in immature and mature mouse cerebellar granule cells. J. Physiol. (Lond.). 517:1999;51-58.
51. Smith T.C., Wang L.-W., Howe J.R. Heterogeneous conductance levels of native AMPA receptors. J. Neurosci. 15:2000;2073-2085.
52. Snow B.E., Hall R.A., Krumins A.M., Brothers G.M., Bouchard D., Brothers C.A., Chung S., Mangion J., Gilman A.G., Lefkowitz R.J., Siderovski D.P. GTPase activating specificity of RGS12 and binding specificity of an alternatively spliced PDZ (PSD-95/Dlg/ZO-1) domain. J. Biol. Chem. 273:1998;17749-17755.
53. Srivastava S., Osten P., Vilim F.S., Khatri L., Inman G., States B., Daly C., DeSouza S., Abayan R., Valtschanoff J.G., Weinberg R.J., Ziff E.B. Novel anchorage of GluR2/3 to the postsynaptic density by the AMPA receptor binding protein ABP. Neuron. 21:1998;581-591.
54. Suzuki T., Ito J., Takagi H., Saitoh F., Nawa H., Shimizu H. Biochemical evidence for localization of AMPA-type glutamate receptor subunits in dendritic raft. Mol. Brain Res. 89:2001;20-28.
55. Swanson G.T., Kamboj S.K., Cull-Candy S.G. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J. Neurosci. 17:1997;58-69.
56. Wu Q., Miller R.H., Ransohoff R.M., Robinson S., Bu J., Nishiyama A. Elevated levels of the chemokine GRO-1 correlate with elevated oligodendrocyte progenitor proliferation in the jimpy mutant. J. Neurosci. 20:2000;2609-2617.
57. Wyszynski M., Valtschanoff J.G., Naisbitt S., Dunah A.W., Kim E., Standaert D.G., Weinberg R., Sheng M. Association of AMPA receptors with a subset of glutamate receptor-interacting protein in vivo. J. Neurosci. 19:1999;6528-6537.
58. Wyszynski M., Kim E., Dunah A.W., Passafaro M., Valtschanoff J.G., Serra-Pages C., Streuli M., Weinberg R.J., Sheng M. Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron. 34:2002;39-52.
59. Xia J., Zhang X., Staudinger J., Huganir R.L. Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron. 19:1999;179-187.
60. Zaslaver A., Feninger-Barish R., Ben-Baruch A. Actin filaments are involved in the regulation of trafficking of two closely related chemokine receptors, CXCR1 and CXCR2. J. Immunol. 166:2001;1272-1284.
61. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., Littman D.R. Function of the chemokines receptor CXCR4 in haematopoiesis and in cerebellar development. Nature. 393:1998;595-599.