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Journal of Neuroimmune Pharmacology

, Volume 7, Issue 4, pp 820–834 | Cite as

CXCL12 Signaling in the Development of the Nervous System

  • Divakar S. Mithal
  • Ghazal Banisadr
  • Richard J. Miller
INVITED REVIEW

Abstract

Chemokines are small, secreted proteins that have been shown to be important regulators of leukocyte trafficking and inflammation. All the known effects of chemokines are transduced by action at a family of G protein coupled receptors. Two of these receptors, CCR5 and CXCR4, are also known to be the major cellular receptors for HIV-1. Consideration of the evolution of the chemokine family has demonstrated that the chemokine Stromal cell Derived Factor-1 or SDF1 (CXCL12) and its receptor CXCR4 are the most ancient members of the family and existed in animals prior to the development of a sophisticated immune system. Thus, it appears that the original function of chemokine signaling was in the regulation of stem cell trafficking and development. CXCR4 signaling is important in the development of many tissues including the nervous system. Here we discuss the manner in which CXCR4 signaling can regulate the development of different structures in the central and peripheral nervous systems and the different strategies employed to achieve these effects.

Keywords

Chemokine Chemokine receptor Development Nervous system 

References

  1. Alcendor DJ, Zong J, Dolan A, Gatherer D, Davison AJ, Hayward GS (2009) Patterns of divergence in the vCXCL and vGPCR gene clusters in primate cytomegalovirus genomes. Virology 395:21–32PubMedCrossRefGoogle Scholar
  2. Alonso E, Gomez-Santos L, Madrid JF, Saez F (2009) The expression of a novel cxcr4 gene in xenopus embryo. Histol Histopathol 24:1097–1103PubMedGoogle Scholar
  3. Ara T, Nakamura Y, Egawa T, Sugiyama T, Abe K, Kishimoto T, Matsui Y, Nagasawa T (2003) Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF1). Proc Natl Acad Sci U S A 100:5319–5323PubMedCrossRefGoogle Scholar
  4. Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M, Pleasure SJ (2002) The chemokine SDF regulates migration of dentate granule cells. Development 129:4249–4260PubMedGoogle Scholar
  5. Bajetto A, Barbero S, Bonavia R, Piccioli P, Pirani P, Florio T, Schettini G (2001a) Stromal cell-derived factor 1 alpha induces astrocyte proliferation through the activation of extracellular signal-regulated kinases 1/2 pathway. J Neurochem 77:1226–1236PubMedCrossRefGoogle Scholar
  6. Bajetto A, Bonavia R, Barbero S, Florio T, Schettini G (2001b) Chemokines and their receptors in the central nervous system. Front Neuroendocrinol 22:147–84PubMedCrossRefGoogle Scholar
  7. Barbero S, Bajetto A, Bonavia R, Porcile C, Piccioli P, Pirani P, Ravetti JL, Zona G, Spaziante R, Florio T, Schettini G (2002) Expression of the chemokine receptor CXCR4 and its ligand stromal cell-derived factor 1 in human brain tumors and their involvement in glial proliferation in vitro. Ann N Y Acad Sci 973:60–69PubMedCrossRefGoogle Scholar
  8. Belmadani A, Tran PB, Ren D, Assimacopoulos S, Grove EA, Miller RJ (2005) The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J Neurosci 25:3995–4003PubMedCrossRefGoogle Scholar
  9. Berger O, Li G, Han SM, Paredes M, Pleasure SJ (2007) Expression of SDF1 and cxcr4 during reorganization of the postnatal dentate gyrus. Dev Neurosci 29:48–58PubMedCrossRefGoogle Scholar
  10. Bhangoo S, Ren D, Miller RJ, Henry KJ, Lineswala J, Hamdouchi C, Li B, Monahan PE, Chan DM, Ripsch MS, White FA (2007a) Delayed functional expression of neuronal chemokine receptors following focal nerve demyelination in the rat: a mechanism for the development of chronic sensitization of peripheral nociceptors. Mol Pain 3:38PubMedCrossRefGoogle Scholar
  11. Bhangoo SK, Ren D, Miller RJ, Chan DM, Ripsch MS, Weiss C, McGinnis C, White FA (2007b) Cxcr4 chemokine receptor signaling mediates pain hypersensitivity in association with antiretroviral toxic neuropathy. Brain Behav Immun 21:581–591PubMedCrossRefGoogle Scholar
  12. Bhangoo SK, Ripsch MS, Buchanan DJ, Miller RJ, White FA (2009) Increased chemokine signaling in a model of HIV1-associated peripheral neuropathy. Mol Pain 5:48PubMedCrossRefGoogle Scholar
  13. Bhattacharyya BJ, Banisadr G, Jung H, Ren D, Cronshaw DG, Zou Y, Miller RJ (2008) The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J Neurosci 28:6720–6730PubMedCrossRefGoogle Scholar
  14. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S, Wilson D, Xu Q, Raz E (2008) Control of chemokine-guided cell migration by ligand sequestration. Cell 132:463–473PubMedCrossRefGoogle Scholar
  15. Bonecchi R, Galliera E, Borroni EM, Corsi MM, Locati M, Mantovani A (2009) Chemokines and chemokine receptors: an overview. Front Biosci 14:540–551PubMedCrossRefGoogle Scholar
  16. Bonecchi R, Savino B, Borroni EM, Mantovani A, Locati M (2010) Chemokine decoy receptors: structure-function and biological properties. Curr Top Microbiol Immunol 341:15–36PubMedCrossRefGoogle Scholar
  17. Borrell V, Marín O (2006) Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat Neurosci 9:1284–1293PubMedCrossRefGoogle Scholar
  18. Borroni EM, Bonecchi R, Buracchi C, Savino B, Mantovani A, Locati M (2008) Chemokine decoy receptors: new players in reproductive immunology. Immunol Invest 37:483–497PubMedCrossRefGoogle Scholar
  19. Borroni EM, Mantovani A, Locati M, Bonecchi R (2010) Chemokine receptors intracellular trafficking. Pharmacol Ther 127:1–8PubMedCrossRefGoogle Scholar
  20. Brenneman DE, Westbrook GL, Fitzgerald SP, Ennist DL, Elkins KL, Ruff MR, Pert CB (1988) Neuronal cell killing by the envelope protein of HIV and its prevention by vasoactive intestinal peptide. Nature 335:639–642PubMedCrossRefGoogle Scholar
  21. Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, Liles WC, Li X, Graham-Evans B, Campbell TB, Calandra G, Bridger G, Dale DC, Srour EF (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 201:1307–1318PubMedCrossRefGoogle Scholar
  22. Burbassi S, Sengupta R, Meucci O (2010) Alterations of CXCR4 function in μ-opioid receptor-deficient glia. Eur J Neurosci 32:1278–1288PubMedCrossRefGoogle Scholar
  23. Caviness VS Jr, Sidman RL (1973) Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J Comp Neurol 148:141–151PubMedCrossRefGoogle Scholar
  24. Caviness VS Jr, Rakic P (1978) Mechanisms of cortical development: a view from mutations in mice. Annu Rev Neurosci 1:297–326PubMedCrossRefGoogle Scholar
  25. Chalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA (2003) A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 23:1360–1371PubMedGoogle Scholar
  26. Chalasani SH, Sabol A, Xu H, Gyda MA, Rasband K, Granato M, Chien CB, Raper JA (2007) Stromal cell-derived factor-1 antagonizes slit/robo signaling in vivo. J Neurosci 27:973–980PubMedCrossRefGoogle Scholar
  27. Clapham PR, Reeves JD, Simmons G, Dejucq N, Hibbitts S, McKnight A (1999) HIV coreceptors, cell tropism and inhibition by chemokine receptor ligands. Mol Membr Biol 16:49–55PubMedCrossRefGoogle Scholar
  28. Clark-Lewis I, Kim KS, Rajarathnam K, Gong JH, Dewald B, Moser B, Baggiolini M, Sykes BD (1995) Structure-activity relationships of chemokines. J Leukoc Biol 57:703–711PubMedGoogle Scholar
  29. Cocchi F, DeVico AL, Garzino-Demo A, Cara A, Gallo RC, Lusso P (1996) The v3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection. Nat Med 2:1244–1247PubMedCrossRefGoogle Scholar
  30. Cruz-Orengo L, Holman DW, Dorsey D, Zhou L, Zhang P, Wright M, McCandless EE, Patel JR, Luker GD, Littman DR, Russell JH, Klein RS (2011) CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J Exp Med 208:327–339PubMedCrossRefGoogle Scholar
  31. Cubedo N, Cerdan E, Sapede D, Rossel M (2009) CXCR4 and CXCR7 cooperate during tangential migration of facial motoneurons. Mol Cell Neurosci 40:474–484PubMedCrossRefGoogle Scholar
  32. Dambly-Chaudiere C, Cubedo N, Ghysen A (2007) 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 29:7–23Google Scholar
  33. Dar A, Kollet O, Lapidot T (2006) Mutual, reciprocal SDF1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in nod/scid chimeric mice. Exp Hematol 34:967–975PubMedCrossRefGoogle Scholar
  34. Diotel N, Vaillant C, Gueguen MM, Mironov S, Anglade I, Servili A, Pellegrini E, Kah O (2010) CXCR4 and CXCL12 expression in radial glial cells of the brain of adult zebrafish. J Comp Neurol 518:4855–4876PubMedCrossRefGoogle Scholar
  35. Dittmar MT, McKnight A, Simmons G, Clapham PR, Weiss RA, Simmonds P (1997) Hiv-1 tropism and co-receptor use. Nature 385:495–496PubMedCrossRefGoogle Scholar
  36. Dominguez F, Galan A, Martin JJL, Remohi J, Pellicer A, Simón C (2003) Hormonal and embryonic regulation of chemokine receptors cxcr1, cxcr4, ccr5 and ccr2b in the human endometrium and the human blastocyst. Mol Hum Reprod 9:189–198PubMedCrossRefGoogle Scholar
  37. Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, Peiper SC, Parmentier M, Collman RG, Doms RW (1996) A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors ckr-5, ckr-3, and ckr-2b as fusion cofactors. Cell 85:1149–1158PubMedCrossRefGoogle Scholar
  38. Dreyer EB, Kaiser PK, Offermann JT, Lipton SA (1990) HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 248:364–367PubMedCrossRefGoogle Scholar
  39. Fernandez EJ, Lolis E (2002) Structure, function, and inhibition of chemokines. Annu Rev Pharmacol Toxicol 42:469–499PubMedCrossRefGoogle Scholar
  40. Göttle P, Kremer D, Jander S, Odemis V, Engele J, Hartung HP, Küry P (2010) Activation of CXCR7 receptor promotes oligodendroglial cell maturation. Ann Neurol 68:915–924PubMedCrossRefGoogle Scholar
  41. Halks-Miller M, Hesselgesser J, Miko IJ, Horuk R (1997) Chemokine receptors in developing human brain. Methods Enzymol 288:27–38PubMedCrossRefGoogle Scholar
  42. Heinisch S, Palma J, Kirby LG (2011) Interactions between chemokine and mu-opioid receptors: anatomical findings and electrophysiological studies in the rat periaqueductal grey. Brain Behav Immun 25:360–372PubMedCrossRefGoogle Scholar
  43. Hesselgesser J, Halks-Miller M, DelVecchio V, Peiper SC, Hoxie J, Kolson DL, Taub D, Horuk R (1997) Cd4-independent association between HIV-1 gp120 and CXCR4: functional chemokine receptors are expressed in human neurons. Curr Biol 7:112–121PubMedCrossRefGoogle Scholar
  44. 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 SDF1 alpha is mediated by the chemokine receptor CXCR4. Curr Biol 8:595–598PubMedCrossRefGoogle Scholar
  45. Hill JM, Mervis RF, Avidor R, Moody TW, Brenneman DE (1993) HIV envelope protein-induced neuronal damage and retardation of behavioral development in rat neonates. Brain Res 603:222–233PubMedCrossRefGoogle Scholar
  46. Horuk R, Martin AW, Wang Z, Schweitzer L, Gerassimides A, Guo H, Lu Z, Hesselgesser J, Perez HD, Kim J, Parker J, Hadley TJ, Peiper SC (1997) Expression of chemokine receptors by subsets of neurons in the central nervous system. J Immunol 158:2882–2890PubMedGoogle Scholar
  47. Huising MO, Stet RJM, Kruiswijk CP, Savelkoul HFJ, Lidy Verburg-van Kemenade BM (2003) Molecular evolution of CXC chemokines: extant CXC chemokines originate from the CNS. Trends Immunol 24:307–313PubMedGoogle Scholar
  48. Jones MC, Caswell PT, Norman JC (2006) Endocytic recycling path-ways: emerging regulators of cell migration. Curr Opin Cell Biol 18:549–557PubMedCrossRefGoogle Scholar
  49. Kaiser PK, Offermann JT, Lipton SA (1990) Neuronal injury due to HIV-1 envelope protein is blocked by anti-gp120 antibodies but not by anti-cd4 antibodies. Neurology 40:1757–1761PubMedCrossRefGoogle Scholar
  50. Kasemeier-Kulesa JC, McLennan R, Romine MH, Kulesa PM, Lefcort F (2010) CXCR4 controls ventral migration of sympathetic precursor cells. J Neurosci 30:13078–13088PubMedCrossRefGoogle Scholar
  51. Khan MZ, Brandimarti R, Musser BJ, Resue DM, Fatatis A, Meucci O (2003) The chemokine receptor CXCR4 regulates cell-cycle proteins in neurons. J Neurovirol 9:300–314PubMedGoogle Scholar
  52. Klein RS, Rubin JB, Gibson HD, DeHaan EN, Alvarez-Hernandez X, Segal RA, Luster AD (2001) SDF1 alpha induces chemo-taxis and enhances sonic hedgehog-induced proliferation of cerebellar granule cells. Development 128:1971–1981PubMedGoogle Scholar
  53. Knaut H, Werz C, Geisler R, Tübingen 2000 Screen Consortium, Nüsslein-Volhard C (2003) A zebrafish homologue of the chemokine receptor CXCR4 is a germ-cell guidance receptor. Nature 421:279–282PubMedCrossRefGoogle Scholar
  54. Kolodziej A, Schulz S, Guyon A, Wu DF, Pfeiffer M, Odemis V, Höllt V, Stumm R (2008) Tonic activation of CXC chemokine receptor 4 in immature granule cells supports neurogenesis in the adult dentate gyrus. J Neurosci 28:4488–4500PubMedCrossRefGoogle Scholar
  55. Kramp BK, Sarabi A, Koenen RR, Weber C (2011) Heterophilic chemokine receptor interactions in chemokine signaling and biology. Exp Cell Res 317:655–663PubMedCrossRefGoogle Scholar
  56. Kreibich TA, Chalasani SH, Raper JA (2004) The neurotransmitter glutamate reduces axonal responsiveness to multiple repellents through the activation of metabotropic glutamate receptor 1. J Neurosci 24:7085–7095PubMedCrossRefGoogle Scholar
  57. Lagane B, Chow KYC, Balabanian K, Levoye A, Harriague J, Planchenault T, Baleux F, Gunera-Saad N, Arenzana-Seisdedos F, Bachelerie F (2008) CXCR4 dimerization and beta-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in whim syndrome. Blood 112:34–44PubMedCrossRefGoogle Scholar
  58. Lapham CK, Ouyang J, Chandrasekhar B, Nguyen NY, Dimitrov DS, Golding H (1996) Evidence for cell-surface association between fusin and the cd4-gp120 complex in human cell lines. Science 274:602–605PubMedCrossRefGoogle Scholar
  59. Lapidot T, Dar A, Kollet O (2005) How do stem cells find their way home? Blood 106:1901–1910PubMedCrossRefGoogle Scholar
  60. Lavi E, Kolson DL, Ulrich AM, Fu L, González-Scarano F (1998) Chemokine receptors in the human brain and their relationship to HIV infection. J Neurovirol 4:301–311PubMedCrossRefGoogle Scholar
  61. Lazarini F, Tham TN, Casanova P, Arenzana-Seisdedos F, Dubois-Dalcq M (2003) Role of the alpha-chemokine stromal cell-derived factor (SDF1) in the developing and mature central nervous system. Glia 42:139–148PubMedCrossRefGoogle Scholar
  62. Li G, Pleasure SJ (2005) Morphogenesis of the dentate gyrus: what we are learning from mouse mutants. Dev Neurosci 27:93–99PubMedCrossRefGoogle Scholar
  63. Li G, Kataoka H, Coughlin SR, Pleasure SJ (2009) Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by CXCL12 and reelin signaling. Development 136:327–335PubMedCrossRefGoogle Scholar
  64. Liapi A, Pritchett J, Jones O, Fujii N, Parnavelas JG, Nadarajah B (2008) Stromal-derived factor 1 signaling regulates radial and tangential migration in the developing cerebral cortex. Dev Neurosci 30:117–131PubMedCrossRefGoogle Scholar
  65. Lieberam I, Agalliu D, Nagasawa T, Ericson J, Jessell TM (2005) A CXCL12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47:667–679PubMedCrossRefGoogle Scholar
  66. Lipton SA, Sucher NJ, Kaiser PK, Dreyer EB (1991) Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 7:111–118PubMedCrossRefGoogle Scholar
  67. Lu M, Grove EA, Miller RJ (2002) Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci U S A 99:7090–7095PubMedCrossRefGoogle Scholar
  68. 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 SDF1-deficient mice. Proc Natl Acad Sci U S A 95:9448–9453PubMedCrossRefGoogle Scholar
  69. Mackay CR (2001) Chemokines: immunology’s high impact factors. Nat Immunol 2:95–101PubMedCrossRefGoogle Scholar
  70. Marchionni I, Takács VT, Nunzi MG, Mugnaini E, Miller RJ, Maccaferri G (2010) Distinctive properties of CXC chemokine receptor 4-expressing Cajal-Retzius cells versus GABAergic interneurons of the postnatal hippocampus. J Physiol 588:2859–2878PubMedCrossRefGoogle Scholar
  71. McIntyre JC, Titlow WB, McClintock TS (2010) Axon growth and guidance genes identify nascent, immature, and mature olfactory sensory neurons. J Neurosci Res 88:3243–3256PubMedCrossRefGoogle Scholar
  72. Meucci O, Miller RJ (1996) gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: protective action of tgf-beta1. J Neurosci 16:4080–4088PubMedGoogle Scholar
  73. Meucci O, Fatatis A, Simen AA, Bushell TJ, Gray PW, Miller RJ (1998) Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc Natl Acad Sci U S A 95:14500–14505PubMedCrossRefGoogle Scholar
  74. Miller RJ (2008) Chemokine signaling in the central and peripheral nervous systems and its role in development and neuropathology in “Chemokine receptors and neuroAIDS; Beyond co-receptor function and links to other neuropathologies. (ed Meucci O) Springer-Verlag: 191–220Google Scholar
  75. Miller RJ, Meucci O (1999) AIDS and the brain: is there a chemokine connection? Trends Neurosci 22:471–479PubMedCrossRefGoogle Scholar
  76. Miller RJ, Banisadr G, Bhattacharyya BJ (2008) CXCR4 signaling in the regulation of stem cell migration and development. J Neuroimmunol 198:31–38PubMedCrossRefGoogle Scholar
  77. Mitra P, Shibuta K, Mathai J, Shimoda K, Banner BF, Mori M, Barnard GF (1999) CXCR4 mRNA expression in colon, esophageal and gastric cancers and hepatitis C infected liver. Int J Oncol 14:917–925PubMedGoogle Scholar
  78. Miyasaka N, Knaut H, Yoshihara Y (2007) CXCL12/CXCR4 chemokine signaling is required for placode assembly and sensory axon pathfinding in the zebrafish olfactory system. Development 134:2459–2468PubMedCrossRefGoogle Scholar
  79. Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verástegui E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410:50–56PubMedCrossRefGoogle Scholar
  80. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T (1996) Defects of b-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine pbsf/SDF1. Nature 382:635–638PubMedCrossRefGoogle Scholar
  81. Neel NF, Schutyser E, Sai J, Fan GH, Richmond A (2005) Chemokine receptor internalization and intracellular trafficking. Cytokine Growth Factor Rev 16:637–658PubMedCrossRefGoogle Scholar
  82. Nijmeijer S, Leurs R, Smit MJ, Vischer HF (2010) The Epstein-bar virus-encoded g protein-coupled receptor bilf1 hetero-oligomerizes with human CXCR4, scavenges Gi proteins, and constitutively impairs CXCR4 functioning. J Biol Chem 285:29632–29641PubMedCrossRefGoogle Scholar
  83. Odemis V, Lamp E, Pezeshki G, Moepps B, Schilling K, Gierschik P, Littman DR, Engele J (2005) Mice deficient in the chemokine receptor CXCR4 exhibit impaired limb innervation and myogenesis. Mol Cell Neurosci 30:494–505PubMedCrossRefGoogle Scholar
  84. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899–912PubMedCrossRefGoogle Scholar
  85. Oh SB, Tran PB, Gillard SE, Hurley RW, Hammond DL, Miller RJ (2001) Chemokines and glycoprotein120 produce pain hypersensitivity by directly exciting primary nociceptive neurons. J Neurosci 21:5027–5035PubMedGoogle Scholar
  86. Olesnicky Killian EC, Birkholz DA, Artinger KB (2009) A role for chemokine signaling in neural crest cell migration and craniofacial development. Dev Biol 333:161–172PubMedCrossRefGoogle Scholar
  87. Palevitch O, Abraham E, Borodovsky N, Levkowitz G, Zohar Y, Gothilf Y (2010) CXCL12a-CXCR4b signaling is important for proper development of the forebrain GnRH system in zebrafish. Gen Comp Endocrinol 165:262–268PubMedCrossRefGoogle Scholar
  88. Paredes MF, Li G, Berger O, Baraban SC, Pleasure SJ (2006) Stromal-derived factor-1 (CXCL12) regulates laminar position of Cajal-Retzius cells in normal and dysplastic brains. J Neurosci 26:9404–9012PubMedCrossRefGoogle Scholar
  89. Pello OM, Martínez-Muñoz L, Parrillas V, Serrano A, Rodríguez-Frade JM, Toro MJ, Lucas P, Monterrubio M, Martínez AC, Mellado M (2008) Ligand stabilization of CXCR4/delta-opioid receptor heterodimers reveals a mechanism for immune response regulation. Eur J Immunol 38:537–549PubMedCrossRefGoogle Scholar
  90. Penfold ME, Dairaghi DJ, Duke GM, Saederup N, Mocarski ES, Kemble GW, Schall TJ (1999) Cytomegalovirus encodes a potent alpha chemokine. Proc Natl Acad Sci U S A 96:9839–9844PubMedCrossRefGoogle Scholar
  91. Rajagopal S, Kim J, Ahn S, Craig S, Lam CM, Gerard NP, Gerard C, Lefkowitz RJ (2010a) Beta-arrestin- but not G protein-mediated signaling by the “decoy” receptor CXCR7. Proc Natl Acad Sci U S A 107:628–632PubMedCrossRefGoogle Scholar
  92. Rajagopal S, Rajagopal K, Lefkowitz RJ (2010b) Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nat Rev Drug Discov 9:373–386PubMedCrossRefGoogle Scholar
  93. Rakic P, Caviness VS Jr (1995) Cortical development: view from neurological mutants two decades later. Neuron 14:1101–1104PubMedCrossRefGoogle Scholar
  94. Reiss K, Mentlein R, Sievers J, Hartmann D (2002) Stromal cell-derived factor 1 is secreted by meningeal cells and acts as chemotactic factor on neuronal stem cells of the cerebellar external granular layer. Neuroscience 115:295–305PubMedCrossRefGoogle Scholar
  95. Rubin JB, Kung AL, Klein RS, Chan JA, Sun Y, Schmidt K, Kieran MW, Luster AD, Segal RA (2003) A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci U S A 100:13513–13518PubMedCrossRefGoogle Scholar
  96. Saederup N, Lin YC, Dairaghi DJ, Schall TJ, Mocarski ES (1999) Cytomegalovirus-encoded beta chemokine promotes monocyte-associated viremia in the host. Proc Natl Acad Sci U S A 96:10881–10886PubMedCrossRefGoogle Scholar
  97. Saederup N, Mocarski ES Jr (2002) Fatal attraction: cytomegalovirus-encoded chemokine homologs. Curr Top Microbiol Immunol 269:235–256PubMedCrossRefGoogle Scholar
  98. Sánchez-Alcañiz JA, Haege S, Mueller W, Pla R, Mackay F, Schulz S, López-Bendito G, Stumm R, Marín O (2011) CXCR7 controls neuronal migration by regulating chemokine responsiveness. Neuron 69:77–90PubMedCrossRefGoogle Scholar
  99. Sapède D, Rossel M, Dambly-Chaudière C, Ghysen A (2005) Role of SDF1 chemokine in the development of lateral line efferent and facial motor neurons. Proc Natl Acad Sci U S A 102:1714–1718PubMedCrossRefGoogle Scholar
  100. Savio T, Levi G (1993) Neurotoxicity of HIV coat protein gp120, NMDA receptors, and protein kinase c: a study with rat cerebellar granule cell cultures. J Neurosci Res 34:265–272PubMedCrossRefGoogle Scholar
  101. Schönemeier B, Kolodziej A, Schulz S, Jacobs S, Hoellt V, Stumm R (2008) Regional and cellular localization of the CXCL12/SDF-1 chemokine receptor CXCR7 in the developing and adult rat brain. J Comp Neurol 510:207–220PubMedCrossRefGoogle Scholar
  102. Schwarting GA, Henion TR, Nugent JD, Caplan B, Tobet S (2006) Stromal cell-derived factor-1 (chemokine C-X-C motif ligand 12) and chemokine C-X-C motif receptor 4 are required for migration of gonadotropin-releasing hormone neurons to the forebrain. J Neurosci 26:6834–6840PubMedCrossRefGoogle Scholar
  103. Schwarting GA, Wierman ME, Tobet SA (2007) Gonadotropin-releasing hormone neuronal migration. Semin Reprod Med 25:305–312PubMedCrossRefGoogle Scholar
  104. Sehgal A, Keener C, Boynton AL, Warrick J, Murphy GP (1998a) CXCR-4, a chemokine receptor, is overexpressed in and required for proliferation of glioblastoma tumor cells. J Surg Oncol 69:99–104PubMedCrossRefGoogle Scholar
  105. Sehgal A, Ricks S, Boynton AL, Warrick J, Murphy GP (1998b) Molecular characterization of cxcr-4: a potential brain tumor-associated gene. J Surg Oncol 69:239–248PubMedCrossRefGoogle Scholar
  106. Simmons G, Reeves JD, McKnight A, Dejucq N, Hibbitts S, Power CA, Aarons E, Schols D, De Clercq E, Proudfoot AE, Clapham PR (1998) CXCR4 as a functional coreceptor for human immunodeficiency virus type 1 infection of primary macrophages. J Virol 72:8453–8457PubMedGoogle Scholar
  107. Sloan EKI, Anderson RL (2002) Genes involved in breast cancer metastasis to bone. Cell Mol Life Sci 59:1491–1502PubMedCrossRefGoogle Scholar
  108. Sohy D, Yano H, de Nadai P, Urizar E, Guillabert A, Javitch JA, Parmentier M, Springael JY (2009) Hetero-oligomerization of CCR2, CCR5, and CXCR4 and the protean effects of “selective” antagonists. J Biol Chem 284:31270–31279PubMedCrossRefGoogle Scholar
  109. Springael JY, Urizar E, Parmentier M (2005) Dimerization of chemokine receptors and its functional consequences. Cytokine Growth Factor Rev 16:611–623PubMedCrossRefGoogle Scholar
  110. Springael JY, Le Minh PN, Urizar E, Costagliola S, Vassart G, Parmentier M (2006) Allosteric modulation of binding properties between units of chemokine receptor homo- and hetero-oligomers. Mol Pharmacol 69:1652–1661PubMedCrossRefGoogle Scholar
  111. Stumm R, Höllt V (2007) CXC chemokine receptor 4 regulates neuronal migration and axonal pathfinding in the developing nervous system: implications for neuronal regeneration in the adult brain. J Mol Endocrinol 38:377–382PubMedCrossRefGoogle Scholar
  112. Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Höllt V, Schulz S (2003) CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 23:5123–5130PubMedGoogle Scholar
  113. Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25:977–988PubMedCrossRefGoogle Scholar
  114. Suratt BT, Petty JM, Young SK, Malcolm KC, Lieber JG, Nick JA, Gonzalo JA, Henson PM, Worthen GS (2004) Role of the CXCR4/SDF1 chemokine axis in circulating neutrophil homeostasis. Blood 104:565–571PubMedCrossRefGoogle Scholar
  115. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591–594PubMedCrossRefGoogle Scholar
  116. Tanaka DH, Mikami S, Nagasawa T, Miyazaki JI, Nakajima K, Murakami F (2010) CXCR4 is required for proper regional and laminar distribution of cortical somatostatin-, calretinin-, and neuropeptide y-expressing GABAergic interneurons. Cereb Cortex 20:2810–2817PubMedCrossRefGoogle Scholar
  117. Thelen M (2001) Dancing to the tune of chemokines. Nat Immunol 2:129–34PubMedCrossRefGoogle Scholar
  118. Tiveron MC, Rossel M, Moepps B, Zhang YL, Seidenfaden R, Favor J, König N, Cremer H (2006) 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 26:13273–13278PubMedCrossRefGoogle Scholar
  119. Toba Y, Tiong JD, Ma Q, Wray S (2008) CXCR4/SDF-1 system modulates development of GnRH-1 neurons and the olfactory system. Dev Neurobiol 68:487–503PubMedCrossRefGoogle Scholar
  120. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188–193PubMedCrossRefGoogle Scholar
  121. Toth PB, Ren DJ, Miller RJ (2003) Regulation of CXCR4 receptor dimerization by the chemokine SDF-1α and the HIV-1 coat protein gp120; a fluorescence resonance energy transfer study. J Pharm Exp Ther 310:8–17CrossRefGoogle Scholar
  122. Tran PB, Miller RJ (2003a) Chemokine receptors in the brain: a developing story. J Comp Neurol 457:1–6PubMedCrossRefGoogle Scholar
  123. Tran PB, Miller RJ (2003b) Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci 4:444–455PubMedCrossRefGoogle Scholar
  124. Tran PB, Banisadr G, Ren D, Chenn A, Miller RJ (2007) Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. J Comp Neurol 500:1007–1033Google Scholar
  125. Valles CS, Domínguez F (2006) Embryo-endometrial interaction. Chang Gung Med J 29:9–14PubMedGoogle Scholar
  126. Vilz TO, Moepps B, Engele J, Molly S, Littman DR, Schilling K (2005) The SDF1/CXCR4 pathway and the development of the cerebellar system. Eur J Neurosci 22:1831–1839PubMedCrossRefGoogle Scholar
  127. Vink C, Smit MJ, Leurs R, Bruggeman CA (2001) The role of cytomegalovirus-encoded homologs of g protein-coupled receptors and chemokines in manipulation of and evasion from the immune system. J Clin Virol 23:43–55PubMedCrossRefGoogle Scholar
  128. Vischer HF, Nijmeijer S, Smit MJ, Leurs R (2008) Viral hijacking of human receptors through heterodimerization. Biochem Biophys Res Commun 377:93–97PubMedCrossRefGoogle Scholar
  129. Wang Y, Li G, Stanco A, Long JE, Crawford D, Potter GB, Pleasure SJ, Behrens T, Rubenstein JLR (2011) CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 69:61–76PubMedCrossRefGoogle Scholar
  130. Wells TN, Proudfoot AE, Power CA, Marsh M (1996) Chemokine receptors-the new frontier for aids research. Chem Biol 3:603–609PubMedCrossRefGoogle Scholar
  131. Westmoreland SV, Kolson D, González-Scarano F (1996) Toxicity of TNF alpha and platelet activating factor for human nt2n neurons: a tissue culture model for human immunodeficiency virus dementia. J Neurovirol 2:118–126PubMedCrossRefGoogle Scholar
  132. Wilson NM, Jung H, Ripsch MS, Miller RJ, White FA (2011) CXCR4 signaling mediates morphine-induced tactile hyperalgesia. Brain Behav Immun 25:565–673PubMedCrossRefGoogle Scholar
  133. Wong ML, Xin WW, Duman RS (1996) Rat lcr1: cloning and cellular distribution of a putative chemokine receptor in brain. Mol Psychiatry 1:133–140PubMedGoogle Scholar
  134. Yang L, Jackson E, Woerner BM, Perry A, Piwnica-Worms D, Rubin JB (2007) Blocking CXCR4-mediated cyclic AMP suppression inhibits brain tumor growth in vivo. Cancer Res 67:651–658PubMedCrossRefGoogle Scholar
  135. Yeung MC, Pulliam L, Lau AS (1995) The HIV envelope protein gp120 is toxic to human brain-cell cultures through the induction of interleukin-6 and tumor necrosis factor-alpha. AIDS 9:137–143PubMedGoogle Scholar
  136. Zeelenberg IS, Ruuls-Van Stalle L, Roos E (2003) The chemokine receptor cxcr4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res 63:3833–3839PubMedGoogle Scholar
  137. Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL (2008) Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol 510:79–99PubMedCrossRefGoogle Scholar
  138. Zhu Y, Matsumoto T, Mikami S, Nagasawa T, Murakami F (2009) SDF1/CXCR4 signaling regulates two distinct processes of precerebellar neuronal migration and its depletion leads to abnormal pontine nuclei formation. Development 136:1919–1928PubMedCrossRefGoogle Scholar
  139. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393:595–599PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Divakar S. Mithal
    • 1
  • Ghazal Banisadr
    • 1
  • Richard J. Miller
    • 1
    • 2
  1. 1.Department of Molecular Pharmacology and Biological ChemistryNorthwestern University Feinberg School of MedicineChicagoUSA
  2. 2.Department of Molecular Pharmacology and Biological ChemistryNorthwestern University Medical SchoolChicagoUSA

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