Cxcr7 Controls Neuronal Migration by Regulating Chemokine Responsiveness

Neuron

Volumn 69, Issue 1, 2011, Pages 77-90

  Sánchez Alcañiz, Juan Antonio ^a   Haege, Sammy ^b,c   Mueller, Wiebke ^b   Pla, Ramón ^a   Mackay, Fabienne ^d   Schulz, Stefan ^b   López Bendito, Guillermina ^a   Stumm, Ralf ^b,c   Marín, Oscar ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; INTERNEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CEREBRAL CORTEX; CHEMOKINE CXCL12; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, CXCR; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 78650929993     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.12.006     Document Type: Article

References (61)

1. Bagri A., Gurney T., He X., Zou Y.R., Littman D.R., Tessier-Lavigne M., Pleasure S.J. The chemokine SDF1 regulates migration of dentate granule cells. Development 2002, 129:4249-4260.
2. Balabanian K., Lagane B., Infantino S., Chow K.Y., Harriague J., Moepps B., Arenzana-Seisdedos F., Thelen M., Bachelerie F. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J. Biol. Chem. 2005, 280:35760-35766.
3. Balabanian K., Lagane B., Pablos J.L., Laurent L., Planchenault T., Verola O., Lebbe C., Kerob D., Dupuy A., Hermine O., et al. WHIM syndromes with different genetic anomalies are accounted for by impaired CXCR4 desensitization to CXCL12. Blood 2005, 105:2449-2457.
4. Batista-Brito R., Fishell G. The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 2009, 87:81-118.
5. Bleul C.C., Farzan M., Choe H., Parolin C., Clark-Lewis I., Sodroski J., Springer T.A. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 1996, 382:829-833.
6. Boldajipour B., Mahabaleshwar H., Kardash E., Reichman-Fried M., Blaser H., Minina S., Wilson D., Xu Q., Raz E. Control of chemokine-guided cell migration by ligand sequestration. Cell 2008, 132:463-473.
7. Borrell V., Marín O. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat. Neurosci. 2006, 9:1284-1293.
8. Burger J.A., Kipps T.J. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006, 107:1761-1767.
9. Burns J.M., Summers B.C., Wang Y., Melikian A., Berahovich R., Miao Z., Penfold M.E., Sunshine M.J., Littman D.R., Kuo C.J., et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 2006, 203:2201-2213.
10. Cubedo N., Cerdan E., Sapede D., Rossel M. CXCR4 and CXCR7 cooperate during tangential migration of facial motoneurons. Mol. Cell. Neurosci. 2009, 40:474-484.
11. Dambly-Chaudiere C., Cubedo N., Ghysen A. Control of cell migration in the development of the posterior lateral line: antagonistic interactions between the chemokine receptors CXCR4 and CXCR7/RDC1. BMC Dev. Biol. 2007, 7:23.
12. Fischer T., Nagel F., Jacobs S., Stumm R., Schulz S. Reassessment of CXCR4 chemokine receptor expression in human normal and neoplastic tissues using the novel rabbit monoclonal antibody UMB-2. PLoS ONE 2008, 3:e4069.
13. Flames N., Pla R., Gelman D.M., Rubenstein J.L., Puelles L., Marín O. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 2007, 27:9682-9695.
14. Fogarty M., Grist M., Gelman D., Marín O., Pachnis V., Kessaris N. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 2007, 27:10935-10946.
15. Fong A.M., Premont R.T., Richardson R.M., Yu Y.R., Lefkowitz R.J., Patel D.D. Defective lymphocyte chemotaxis in beta-arrestin2- and GRK6-deficient mice. Proc. Natl. Acad. Sci. USA 2002, 99:7478-7483.
16. Gong S., Zheng C., Doughty M.L., Losos K., Didkovsky N., Schambra U.B., Nowak N.J., Joyner A., Leblanc G., Hatten M.E., Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 2003, 425:917-925.
17. Graham G.J. D6 and the atypical chemokine receptor family: novel regulators of immune and inflammatory processes. Eur. J. Immunol. 2009, 39:342-351.
18. Hartmann T.N., Grabovsky V., Pasvolsky R., Shulman Z., Buss E.C., Spiegel A., Nagler A., Lapidot T., Thelen M., Alon R. A crosstalk between intracellular CXCR7 and CXCR4 involved in rapid CXCL12-triggered integrin activation but not in chemokine-triggered motility of human T lymphocytes and CD34+ cells. J. Leukoc. Biol. 2008, 84:1130-1140.
19. Hevner R.F., Daza R.A., Englund C., Kohtz J., Fink A. Postnatal shifts of interneuron position in the neocortex of normal and reeler mice: evidence for inward radial migration. Neuroscience 2004, 124:605-618.
20. Kalatskaya I., Berchiche Y.A., Gravel S., Limberg B.J., Rosenbaum J.S., Heveker N. AMD3100 is a CXCR7 ligand with allosteric agonist properties. Mol. Pharmacol. 2009, 75:1240-1247.
21. Kawai T., Malech H.L. WHIM syndrome: congenital immune deficiency disease. Curr. Opin. Hematol. 2009, 16:20-26.
22. Kolodziej A., Schulz S., Guyon A., Wu D.F., Pfeiffer M., Odemis V., Hollt V., Stumm R. Tonic activation of CXC chemokine receptor 4 in immature granule cells supports neurogenesis in the adult dentate gyrus. J. Neurosci. 2008, 28:4488-4500.
23. Lavdas A.A., Grigoriou M., Pachnis V., Parnavelas J.G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 1999, 19:7881-7888.
24. Levoye A., Balabanian K., Baleux F., Bachelerie F., Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009, 113:6085-6093.
25. Li M., Ransohoff R.M. Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog. Neurobiol. 2008, 84:116-131.
26. Li G., Adesnik H., Li J., Long J., Nicoll R.A., Rubenstein J.L.R., Pleasure S.J. Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J. Neurosci. 2008, 28:1085-1098.
27. López-Bendito G., Sánchez-Alcaniz J.A., Pla R., Borrell V., Pico E., Valdeolmillos M., Marín O. Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J. Neurosci. 2008, 28:1613-1624.
28. Luker K.E., Gupta M., Steele J.M., Foerster B.R., Luker G.D. Imaging ligand-dependent activation of CXCR7. Neoplasia 2009, 11:1022-1035.
29. Luker K.E., Steele J.M., Mihalko L.A., Ray P., Luker G.D. Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene 2010, in press. Published online June 7, 2010. 2010.1038/onc.2010.2212.
30. 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. USA 1998, 95:9448-9453.
31. Marchese A., Benovic J.L. Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J. Biol. Chem. 2001, 276:45509-45512.
32. Marchese A., Chen C., Kim Y.M., Benovic J.L. The ins and outs of G protein-coupled receptor trafficking. Trends Biochem. Sci. 2003, 28:369-376.
33. Marín O., Valiente M., Ge X., Tsai L.H. Guiding neuronal cell migrations. Cold Spring Harb. Perspect. Biol. 2010, 2:a001834.
34. Métin C., Baudoin J.P., Rakic S., Parnavelas J.G. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur. J. Neurosci. 2006, 23:894-900.
35. Miao Z., Luker K.E., Summers B.C., Berahovich R., Bhojani M.S., Rehemtulla A., Kleer C.G., Essner J.J., Nasevicius A., Luker G.D., et al. CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc. Natl. Acad. Sci. USA 2007, 104:15735-15740.
36. Murphy P.M. Chemokines and the molecular basis of cancer metastasis. N. Engl. J. Med. 2001, 345:833-835.
37. Naumann U., Cameroni E., Pruenster M., Mahabaleshwar H., Raz E., Zerwes H.G., Rot A., Thelen M. CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS ONE 2010, 5:e9175.
38. Oberlin E., Amara A., Bachelerie F., Bessia C., Virelizier J.L., Arenzana-Seisdedos F., Schwartz O., Heard J.M., Clark-Lewis I., Legler D.F., et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 1996, 382:833-835.
39. Paredes M.F., Li G., Berger O., Baraban S.C., Pleasure S.J. Stromal-derived factor-1 (CXCL12) regulates laminar position of Cajal-Retzius cells in normal and dysplastic brains. J. Neurosci. 2006, 26:9404-9412.
40. Pla R., Borrell V., Flames N., Marín O. Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J. Neurosci. 2006, 26:6924-6934.
41. Raggo C., Ruhl R., McAllister S., Koon H., Dezube B.J., Fruh K., Moses A.V. Novel cellular genes essential for transformation of endothelial cells by Kaposi's sarcoma-associated herpesvirus. Cancer Res. 2005, 65:5084-5095.
42. Rajagopal S., Kim J., Ahn S., Craig S., Lam C.M., Gerard N.P., Gerard C., Lefkowitz R.J. Beta-arrestin- but not G protein-mediated signaling by the " decoy" receptor CXCR7. Proc. Natl. Acad. Sci. USA 2010, 107:628-632.
43. Sasado T., Yasuoka A., Abe K., Mitani H., Furutani-Seiki M., Tanaka M., Kondoh H. Distinct contributions of CXCR4b and CXCR7/RDC1 receptor systems in regulation of PGC migration revealed by medaka mutants kazura and yanagi. Dev. Biol. 2008, 320:328-339.
44. Schonemeier B., Kolodziej A., Schulz S., Jacobs S., Hoellt V., Stumm R. Regional and cellular localization of the CXCl12/SDF-1 chemokine receptor CXCR7 in the developing and adult rat brain. J. Comp. Neurol. 2008, 510:207-220.
45. Schwenk F., Baron U., Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 1995, 23:5080-5081.
46. Sierro F., Biben C., Martinez-Munoz L., Mellado M., Ransohoff R.M., Li M., Woehl B., Leung H., Groom J., Batten M., et al. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. USA 2007, 104:14759-14764.
47. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
48. Stenman J., Toresson H., Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 2003, 23:167-174.
49. Stumm R.K., Rummel J., Junker V., Culmsee C., Pfeiffer M., Krieglstein J., Hollt V., Schulz S. 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. J. Neurosci. 2002, 22:5865-5878.
50. Stumm R.K., Zhou C., Ara T., Lazarini F., Dubois-Dalcq M., Nagasawa T., Hollt V., Schulz S. CXCR4 regulates interneuron migration in the developing neocortex. J. Neurosci. 2003, 23:5123-5130.
51. Stumm R., Kolodziej A., Schulz S., Kohtz J.D., Hollt V. Patterns of SDF-1alpha and SDF-1gamma mRNAs, migration pathways, and phenotypes of CXCR4-expressing neurons in the developing rat telencephalon. J. Comp. Neurol. 2007, 502:382-399.
52. Sun Y., Cheng Z., Ma L., Pei G. Beta-arrestin2 is critically involved in CXCR4-mediated chemotaxis, and this is mediated by its enhancement of p38 MAPK activation. J. Biol. Chem. 2002, 277:49212-49219.
53. Tarasova N.I., Stauber R.H., Michejda C.J. Spontaneous and ligand-induced trafficking of CXC-chemokine receptor 4. J. Biol. Chem. 1998, 273:15883-15886.
54. Tiveron M.C., Rossel M., Moepps B., Zhang Y.L., Seidenfaden R., Favor J., Konig N., Cremer H. Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. J. Neurosci. 2006, 26:13273-13278.
55. Valentin G., Haas P., Gilmour D. The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr. Biol. 2007, 17:1026-1031.
56. Wang J., Shiozawa Y., Wang Y., Jung Y., Pienta K.J., Mehra R., Loberg R., Taichman R.S. The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J. Biol. Chem. 2008, 283:4283-4294.
57. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
58. Zabel B.A., Wang Y., Lewen S., Berahovich R.D., Penfold M.E., Zhang P., Powers J., Summers B.C., Miao Z., Zhao B., et al. Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J. Immunol. 2009, 183:3204-3211.
59. Zhu Y., Yu T., Zhang X.C., Nagasawa T., Wu J.Y., Rao Y. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat. Neurosci. 2002, 5:719-720.
60. Zhu Y., Matsumoto T., Mikami S., Nagasawa T., Murakami F. SDF1/CXCR4 signalling regulates two distinct processes of precerebellar neuronal migration and its depletion leads to abnormal pontine nuclei formation. Development 2009, 136:1919-1928.
61. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998, 393:595-599.