CXCR4 and CXCR7 Have Distinct Functions in Regulating Interneuron Migration

Neuron

Volumn 69, Issue 1, 2011, Pages 61-76

  Wang, Yanling ^a   Li, Guangnan ^b   Stanco, Amelia ^a   Long, Jason E ^c   Crawford, Dianna ^d   Potter, Gregory B ^a   Pleasure, Samuel J ^b   Behrens, Timothy ^c   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GENENTECH INC   (United States)

^d AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MITOGEN ACTIVATED PROTEIN KINASE; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LHX6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IN VIVO STUDY; INHIBITION KINETICS; INTERNEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CEREBRAL CORTEX; CHEMOKINE CXCL12; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; RECEPTORS, CXCR; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 78650956554     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.12.005     Document Type: Article

References (64)

1. Albert P.R., Robillard L. G protein specificity: Traffic direction required. Cell. Signal. 2002, 14:407-418.
2. Alifragis P., Liapi A., Parnavelas J.G. Lhx6 regulates the migration of cortical interneurons from the ventral telencephalon but does not specify their GABA phenotype. J. Neurosci. 2004, 24:5643-5648.
3. Anderson S.A., Eisenstat D.D., Shi L., Rubenstein J.L. Interneuron migration from basal forebrain to neocortex: Dependence on Dlx genes. Science 1997, 278:474-476.
4. Anderson S.A., Qiu M., Bulfone A., Eisenstat D.D., Meneses J., Pedersen R., Rubenstein J.L. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 1997, 19:27-37.
5. Anderson S.A., Marin O., Horn C., Jennings K., Rubenstein J.L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 2001, 128:353-363.
6. Azim E., Jabaudon D., Fame R.M., Macklis J.D. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 2009, 12:1238-1247.
7. 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.
8. 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.
9. Batista-Brito R., Rossignol E., Hjerling-Leffler J., Denaxa M., Wegner M., Lefebvre V., Pachnis V., Fishell G. The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 2009, 63:466-481.
10. Baudoin J.P., Alvarez C., Gaspar P., Metin C. Nocodazole-induced changes in microtubule dynamics impair the morphology and directionality of migrating medial ganglionic eminence cells. Dev. Neurosci. 2008, 30:132-143.
11. Belmadani A., Tran P.B., Ren D., Assimacopoulos S., Grove E.A., Miller R.J. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J. Neurosci. 2005, 25:3995-4003.
12. 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.
13. Borrell V., Marin O. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat. Neurosci. 2006, 9:1284-1293.
14. Butt S.J., Fuccillo M., Nery S., Noctor S., Kriegstein A., Corbin J.G., Fishell G. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 2005, 48:591-604.
15. Casarosa S., Fode C., Guillemot F. Mash1 regulates neurogenesis in the ventral telencephalon. Development 1999, 126:525-534.
16. Cobos I., Calcagnotto M.E., Vilaythong A.J., Thwin M.T., Noebels J.L., Baraban S.C., Rubenstein J.L. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 2005, 8:1059-1068.
17. Cobos I., Long J.E., Thwin M.T., Rubenstein J.L. Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb. Cortex 2006, 16(Suppl 1):i82-i88.
18. Cobos I., Borello U., Rubenstein J.L. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 2007, 54:873-888.
19. Colasante G., Collombat P., Raimondi V., Bonanomi D., Ferrai C., Maira M., Yoshikawa K., Mansouri A., Valtorta F., Rubenstein J.L., Broccoli V. Arx is a direct target of Dlx2 and thereby contributes to the tangential migration of GABAergic interneurons. J. Neurosci. 2008, 28:10674-10686.
20. Cottrell G.S., Padilla B.E., Amadesi S., Poole D.P., Murphy J.E., Hardt M., Roosterman D., Steinhoff M., Bunnett N.W. Endosomal endothelin-converting enzyme-1: A regulator of beta-arrestin-dependent ERK signaling. J. Biol. Chem. 2009, 284:22411-22425.
21. 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.
22. D'Apuzzo M., Rolink A., Loetscher M., Hoxie J.A., Clark-Lewis I., Melchers F., Baggiolini M., Moser B. The chemokine SDF-1, stromal cell-derived factor 1, attracts early stage B cell precursors via the chemokine receptor CXCR4. Eur. J. Immunol. 1997, 27:1788-1793.
23. Donzella G.A., Schols D., Lin S.W., Este J.A., Nagashima K.A., Maddon P.J., Allaway G.P., Sakmar T.P., Henson G., De Clercq E., Moore J.P. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 1998, 4:72-77.
24. Etienne-Manneville S. Actin and microtubules in cell motility: Which one is in control? Traffic 2004, 5:470-477.
25. Fogarty M., Grist M., Gelman D., Marin 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.
26. Gerrits H., van Ingen Schenau D.S., Bakker N.E., van Disseldorp A.J., Strik A., Hermens L.S., Koenen T.B., Krajnc-Franken M.A., Gossen J.A. Early postnatal lethality and cardiovascular defects in CXCR7-deficient mice. Genesis 2008, 46:235-245.
27. Guo H., Hong S., Jin X.L., Chen R.S., Avasthi P.P., Tu Y.T., Ivanco T.L., Li Y. Specificity and efficiency of Cre-mediated recombination in Emx1-Cre knock-in mice. Biochem. Biophys. Res. Commun. 2000, 273:661-665.
28. Hamm H.E. The many faces of G protein signaling. J. Biol. Chem. 1998, 273:669-672.
29. Hesselgesser J., Liang M., Hoxie J., Greenberg M., Brass L.F., Orsini M.J., Taub D., Horuk R. Identification and characterization of the CXCR4 chemokine receptor in human T cell lines: Ligand binding, biological activity, and HIV-1 infectivity. J. Immunol. 1998, 160:877-883.
30. Kohwi M., Petryniak M.A., Long J.E., Ekker M., Obata K., Yanagawa Y., Rubenstein J.L., Alvarez-Buylla A. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J. Neurosci. 2007, 27:6878-6891.
31. Lazarini F., Casanova P., Tham T.N., De Clercq E., Arenzana-Seisdedos F., Baleux F., Dubois-Dalcq M. 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. 2000, 12:117-125.
32. 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.
33. Li G., Adesnik H., Li J., Long J., Nicoll R.A., Rubenstein J.L., 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.
34. Libert F., Passage E., Parmentier M., Simons M.J., Vassart G., Mattei M.G. Chromosomal mapping of A1 and A2 adenosine receptors, VIP receptor, and a new subtype of serotonin receptor. Genomics 1991, 11:225-227.
35. Liodis P., Denaxa M., Grigoriou M., Akufo-Addo C., Yanagawa Y., Pachnis V. Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J. Neurosci. 2007, 27:3078-3089.
36. Long J.E., Garel S., Alvarez-Dolado M., Yoshikawa K., Osumi N., Alvarez-Buylla A., Rubenstein J.L. Dlx-dependent and -independent regulation of olfactory bulb interneuron differentiation. J. Neurosci. 2007, 27:3230-3243.
37. Long J.E., Cobos I., Potter G.B., Rubenstein J.L. Dlx1 and Mash1 transcription factors control MGE and CGE patterning and differentiation through parallel and overlapping pathways. Cereb. Cortex 2009, 19:i96-i106.
38. Long J.E., Swan C., Liang W.S., Cobos I., Potter G.B., Rubenstein J.L. Dlx1&2 and Mash1 transcription factors control striatal patterning and differentiation through parallel and overlapping pathways. J. Comp. Neurol. 2009, 512:556-572.
39. Lopez-Bendito G., Sanchez-Alcaniz J.A., Pla R., Borrell V., Pico E., Valdeolmillos M., Marin O. Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J. Neurosci. 2008, 28:1613-1624.
40. Luttrell L.M., Ferguson S.S., Daaka Y., Miller W.E., Maudsley S., Della Rocca G.J., Lin F., Kawakatsu H., Owada K., Luttrell D.K., et al. Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes. Science 1999, 283:655-661.
41. 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.
42. Marin O., Rubenstein J.L. Cell migration in the forebrain. Annu. Rev. Neurosci. 2003, 26:441-483.
43. Marin O., Anderson S.A., Rubenstein J.L. Origin and molecular specification of striatal interneurons. J. Neurosci. 2000, 20:6063-6076.
44. Nobrega-Pereira S., Kessaris N., Du T., Kimura S., Anderson S.A., Marin O. Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 2008, 59:733-745.
45. 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.
46. Patrussi L., Baldari C.T. Intracellular mediators of CXCR4-dependent signaling in T cells. Immunol. Lett. 2008, 115:75-82.
47. Pleasure S.J., Anderson S., Hevner R., Bagri A., Marin O., Lowenstein D.H., Rubenstein J.L. Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 2000, 28:727-740.
48. Potter G.B., Petryniak M.A., Shevchenko E., McKinsey G.L., Ekker M., Rubenstein J.L. Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol. Cell. Neurosci. 2009, 40:167-186.
49. 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.
50. Regard J.B., Kataoka H., Cano D.A., Camerer E., Yin L., Zheng Y.W., Scanlan T.S., Hebrok M., Coughlin S.R. Probing cell type-specific functions of Gi in vivo identifies GPCR regulators of insulin secretion. J. Clin. Invest. 2007, 117:4034-4043.
51. Reiner O., Sapir T. Polarity regulation in migrating neurons in the cortex. Mol. Neurobiol. 2009, 40:1-14.
52. 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.
53. 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.
54. 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.
55. Sussel L., Marin O., Kimura S., Rubenstein J.L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: Evidence for a transformation of the pallidum into the striatum. Development 1999, 126:3359-3370.
56. Teicher B.A., Fricker S.P. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin. Cancer Res. 2010, 16:2927-2931.
57. 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.
58. Tohgo A., Pierce K.L., Choy E.W., Lefkowitz R.J., Luttrell L.M. beta-Arrestin scaffolding of the ERK cascade enhances cytosolic ERK activity but inhibits ERK-mediated transcription following angiotensin AT1a receptor stimulation. J. Biol. Chem. 2002, 277:9429-9436.
59. 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.
60. Valenzuela-Fernandez A., Planchenault T., Baleux F., Staropoli I., Le-Barillec K., Leduc D., Delaunay T., Lazarini F., Virelizier J.L., Chignard M., et al. Leukocyte elastase negatively regulates Stromal cell-derived factor-1 (SDF-1)/CXCR4 binding and functions by amino-terminal processing of SDF-1 and CXCR4. J. Biol. Chem. 2002, 277:15677-15689.
61. Wang Y., Dye C., Sohal V., Long J., Estrada R., Roztocil T., Lufkin T., Deisseroth K., Baraban S., Rubenstein J.L. Dlx5 and Dlx6 regulate the development of parvalbumin-expressing cortical interneurons. J. Neurosci. 2010, 30:5334-5345.
62. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
63. Xiao K., Sun J., Kim J., Rajagopal S., Zhai B., Villen J., Haas W., Kovacs J.J., Shukla A.K., Hara M.R., et al. Global phosphorylation analysis of {beta}-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc. Natl. Acad. Sci. USA 2010, 107:15299-15304.
64. Zhao Y., Flandin P., Long J.E., Cuesta M.D., Westphal H., Rubenstein J.L. Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J. Comp. Neurol. 2008, 510:79-99.