A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: Isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia

Journal of Neuroscience

Volumn 22, Issue 14, 2002, Pages 5865-5878

  Stumm, Ralf K ^a   Rummel, Jutta ^a   Junker, Vera ^b   Culmsee, Carsten ^b   Pfeiffer, Manuela ^a   Krieglstein, Josef ^b   Höllt, Volker ^a   Schulz, Stefan ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Antibody; CXC chemokine; CXCR4; Focal cerebral ischemia; Immunocytochemistry; In situ hybridization; Lipopolysaccharide; Stromal cell derived factor 1

Indexed keywords

ALPHA CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR4; LIPOPOLYSACCHARIDE; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CELL COMPARTMENTALIZATION; CHEMOTAXIS; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; GENE TARGETING; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LEUKOCYTE ACTIVATION; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION;

EID: 0037101610     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-14-05865.2002     Document Type: Article

References (55)

1. Angerer LM, Cox KH, Angerer RC (1987) Demonstration of tissue-specific gene expression by in situ hybridization. Methods Enzymol 152:649-661.
2. Bajetto A, Bonavia R, Barbero S, Piccioli P, Costa A, Florio T, Schettini G (1999) Glial and neuronal cells express functional chemokine receptor CXCR4 and its natural ligand stromal cell-derived factor 1. J Neurochem 73:2348-2357.
3. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A (2001) CXCR4-activated astrocyte glutamate release via TNFalpha: Amplification by microglia triggers neurotoxicity. Nat Neurosci 4:702-710.
4. Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA (1996a) A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med 184:1101-1109.
5. Bleul CC, Farzan M, Choe H, Parolin C, Clark-Lewis I, Sodroski J, Springer TA (1996b) The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382:829-833.
6. Campbell JJ, Hedrick J, Zlotnik A, Siani MA, Thompson DA, Butcher EC (1998) Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 279:381-384.
7. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: An integrated view. Trends Neurosci 22:391-397.
8. Fedyk ER, Jones D, Critchley HO, Phipps RP, Blieden TM, Springer TA (2001) Expression of stromal-derived factor-1 is decreased by IL-1 and TNF and in dermal wound healing. J Immunol 166:5749-5754.
9. Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: Functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877.
10. Forster R, Kremmer E, Schubel A, Breitfeld D, Kleinschmidt A, Nerl C, Bernhardt G, Lipp M (1998) Intracellular and surface expression of the HIV-1 coreceptor CXCR4/fusin on various leukocyte subsets: Rapid internalization and recycling during activation. J Immunol 160:1522-1531.
11. Franklin KBJ, Paxinos G (1997) The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic.
12. Gleichmann M, Gillen C, Czardybon M, Bosse F, Greiner-Petter R, Auer J, Muller HW (2000) Cloning and characterization of SDF-1gamma, a novel SDF-1 chemokine transcript with developmentally regulated expression in the nervous system. Eur J Neurosci 12:1857-1866.
13. Goodman RH, Montminy MR, Low MJ, Habener JF (1985) Biosynthesis of rat preprosomatostatin. Adv Exp Med Biol 188:31-47.
14. Grabovsky V, Feigelson S, Chen C, Bleijs DA, Peled A, Cinamon G, Baleux F, Arenzana-Seisdedos F, Lapidot T, van Kooyk Y, Lobb RR, Alon R (2000) Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J Exp Med 192:495-506.
15. Heesen M, Berman MA, Benson JD, Gerard C, Dorf ME (1996) Cloning of the mouse fusin gene, homologue to a human HIV-1 co-factor. J Immunol 157:5455-5460.
16. Henninger DD, Panes J, Eppihimer M, Russell J, Gerritsen M, Anderson DC, Granger DN (1997) Cytokine-induced VCAM-1 and ICAM-1 expression in different organs of the mouse. J Immunol 158:1825-1832.
17. Hesselgesser J, Taub D, Baskar P, Greenberg M, Hoxie J, Kolson DL, Horuk R (1998) Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 alpha is mediated by the chemokine receptor CXCR4. Curr Biol 8:595-598.
18. Kantele JM, Kurk S, Jutila MA (2000) Effects of continuous exposure to stromal cell-derived factor-1 alpha on T cell rolling and tight adhesion to monolayers of activated endothelial cells. J Immunol 164:5035-5040.
19. Kaul M, Lipton SA (1999) Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc Natl Acad Sci USA 96:8212-8216.
20. Klein RS, Williams KC, Alvarez-Hernandez X, Westmoreland S, Force T, Lackner AA, Luster AD (1999) Chemokine receptor expression and signaling in macaque and human fetal neurons and astrocytes: Implications for the neuropathogenesis of AIDS. J Immunol 163:1636-1646.
21. Klein RS, Rubin JB, Gibson HD, DeHaan EN, Alvarez-Hernandez X, Segal RA, Luster AD (2001) SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development 128:1971-1981.
22. Koch T, Schulz S, Pfeiffer M, Klutzny M, Schroder H, Kahl E, Hollt V (2001) C-terminal splice variants of the mouse mu-opioid receptor differ in morphine-induced internalization and receptor resensitization. J Biol Chem 276:31408-31414.
23. Kowalska MA, Ratajczak MZ, Majka M, Jin J, Kunapuli S, Brass L, Poncz M (2000) Stromal cell-derived factor-1 and macrophage-derived chemokine: 2 Chemokines that activate platelets. Blood 96:50-57.
24. Lazarini F, Casanova P, Tham TN, De Clercq E, Arenzana-Seisdedos F, Baleux F, Dubois-Dalcq M (2000) Differential signalling of the chemokine receptor CXCR4 by stromal cell-derived factor 1 and the HIV glycoprotein in rat neurons and astrocytes. Eur J Neurosci 12:117-125.
25. Lebel E, Vallieres L, Rivest S (2000) Selective involvement of interleukin-6 in the transcriptional activation of the suppressor of cytokine signaling-3 in the brain during systemic immune challenges. Endocrinology 141:3749-3763.
26. Lewis SA, Balcarek JM, Krek V, Shelanski M, Cowan NJ (1984) Sequence of a cDNA clone encoding mouse glial fibrillary acidic protein: Structural conservation of intermediate filaments. Proc Natl Acad Sci USA 81:2743-2746.
27. Limatola C, Giovannelli A, Maggi L, Ragozzino D, Castellani L, Ciotti MT, Vacca F, Mercanti D, Santoni A, Eusebi F (2000) SDF-1alpha-mediated modulation of synaptic transmission in rat cerebellum. Eur J Neurosci 12:2497-2504.
28. Lu Q, Sun EE, Klein RS, Flanagan JG (2001) Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction. Cell 105:69-79.
29. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA (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. Melton DA, Krieg PA, Rebagliati MR, Maniatis T, Zinn K, Green MR (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter, Nucleic Acids Res 12:7035-7056.
31. Nagasawa T, Kikutani H, Kishimoto T (1994) Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proc Natl Acad Sci USA 91:2305-2309.
32. Nagasawa T, Nakajima T, Tachibana K, Iizasa H, Bleul CC, Yoshie O, Matsushima K, Yoshida N, Springer TA, Kishimoto T (1996) Molecular cloning and characterization of a murine pre-B-cell growth-stimulating factor/stromal cell-derived factor 1 receptor, a murine homolog of the human immunodeficiency virus I entry coreceptor fusin. Proc Natl Acad Sci USA 93:14726-14729.
33. Nanki T, Hayashida K, El-Gabalawy HS, Suson S, Shi K, Girschick HJ, Yavuz S, Lipsky PE (2000) Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J Immunol 165:6590-6598.
34. Oberlin E, Amara A, Bachelerie F, Bessia C, Virelizier JL, Arenzana-Seisdedos F, Schwartz O, Heard JM, Clark-Lewis I, Legler DF, Loetscher M, Baggiolini M, Moser B (1996) The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell- line-adapted HIV-1. Nature 382:833-835.
35. Ohtani Y, Minami M, Kawaguchi N, Nishiyori A, Yamamoto J, Takami S, Satoh M (1998) Expression of stromal cell-derived factor-1 and CXCR4 chemokine receptor mRNAs in cultured rat glial and neuronal cells. Neurosci Lett 249:163-166.
36. Pablos JL, Amara A, Bouloc A, Santiago B, Caruz A, Galindo M, Delaunay T, Virelizier JL, Arenzana-Seisdedos F (1999) Stromal-cell derived factor is expressed by dendritic cells and endothelium in human skin. Am J Pathol 155:1577-1586.
37. Pfeiffer M, Koch T, Schroder H, Klutzny M, Kirscht S, Kreienkamp HJ, Hollt V, Schulz S (2001) Homo- and heterodimerization of somatostatin receptor subtypes. Inactivation of sst(3) receptor function by heterodimerization with sst(2A). J Biol Chem 276:14027-14036.
38. Quan N, Whiteside M, Kim L, Herkenham M (1997) Induction of inhibitory factor kappaBalpha mRNA in the central nervous system after peripheral lipopolysaccharide administration: An in situ hybridization histochemistry study in the rat. Proc Natl Acad Sci USA 94: 10985-10990.
39. Rivest S, Lacroix S, Vallieres L, Nadeau S, Zhang J, Laflamme N (2000) How the blood talks to the brain parenchyma and the paraventricular nucleus of the hypothalamus during systemic inflammatory and infectious stimuli. Proc Soc Exp Biol Med 223:22-38.
40. Schafer MK, Schwaeble WJ, Post C, Salvati P, Calabresi M, Sito RB, Petry F, Loos M, Weihe E (2000) Complement Clq is dramatically up-regulated in brain microglia in response to transient global cerebral ischemia. J Immunol 164:5446-5452,
41. Schreff M, Schulz S, Handel M, Keilhoff G, Braun H, Pereira G, Klutzny M, Schmidt H, Wolf G, Hollt V (2000) Distribution, targeting, and internalization of the sst4 somatostatin receptor in rat brain, J Neurosci 20:3785-3797.
42. Schulz S, Schreff M, Schmidt H, Handel M, Przewlocki R, Hoilt V (1998) Immunocytochemical localization of somatostatin receptor sst2A in the rat spinal cord and dorsal root ganglia. Eur J Neurosci 10:3700-3708.
43. Schwaeble W, Schafer MK, Petry F, Fink T, Knebel D, Weihe E, Loos M (1995) Follicular dendritic cells, interdigitating cells, and cells of the monocyte-macrophage lineage are the Clq-producing sources in the spleen. Identification of specific cell types by in situ hybridization and immunohistochemical analysis. J Immunol 155:4971-4978.
44. Shirozu M, Nakano T, Inazawa J, Tashiro K, Tada H, Shinohara T, Honjo T (1995) Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene. Genomics 28:495-500.
45. Stoll G, Jander S, Schroeter M (1998) Inflammation and glial responses in ischemic brain lesions, Prog Neurobiol 56:149-171.
46. Stumm R, Culmsee C, Schafer MK, Krieglstein J, Weihe E (2001) Adaptive plasticity in tachykinin and tachykinin receptor expression after focal cerebral ischemia is differentially linked to GABAergic and glutamatergic cerebrocortical circuits and cerebrovenular endothelium, J Neurosci 21:798-811.
47. Tashiro K, Tada H, Heilker R, Shirozu M, Nakano T, Honjo T (1993) Signal sequence trap: A cloning strategy for secreted proteins and type 1 membrane proteins. Science 261:600-603.
48. Telford JL, Macchia G, Massone A, Carinci V, Palla E, Melli M (1986) The murine interleukin 1 beta gene: Structure and evolution. Nucleic Acids Res 14:9955-9963.
49. Tham TN, Lazarini F, Franceschini IA, Lachapelle F, Amara A, Dubois-Dalcq M (2001) Developmental pattern of expression of the alpha chemokine stromal cell-derived factor 1 in the rat central nervous system, Eur J Neurosci 13:845-856.
50. Thibeault I, Laflamme N, Rivest S (2001) Regulation of the gene encoding the monocyte chemoattractant protein 1 (MCP-1) in the mouse and rat brain in response to circulating LPS and proinflammatory cytokines, J Comp Neurol 434:461-477.
51. Welsh FA, Sakamoto T, McKee AE, Sims RE (1987) Effect of lactacidosis on pyridine nucleotide stability during ischemia in mouse brain. J Neurochem 49:846-851.
52. Wong ML, Xin WW, Duman RS (1996) Rat LCRI: Cloning and cellular distribution of a putative chemokine receptor in brain. Mol Psychiatry 1:133-140.
53. Wood L, Pulaski S, Vogeli G (1988) cDNA clones coding for the complete murine B chain of complement Clq: Nucleotide and derived amino acid sequences. Immunol Lett 17:115-119.
54. Yamamoto K, de Waard V, Fearns C, Loskutoff DJ (1998) Tissue distribution and regulation of murine von Willebrand factor gene expression in vivo. Blood 92:2791-2801.
55. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development, Nature 393:595-599.