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Chemokine Signaling in the Nervous System and Its Role in Development and Neuropathology

  • Richard J. Miller
Chapter

Abstract

Chemokines are small proteins that are well known as regulators of leukocyte migration. However, recent data have indicated that chemokines also play a number of roles in the nervous system. Here, we discuss the chemokine SDF-1/CXCL12, which has an important role in directing the migration of stem cells in the development of the nervous system. Deletion of the gene for SDF-1 or its receptor CXCR4 produces deficits in the development of numerous parts of the central and peripheral nervous systems. In the adult nervous system, SDF-1 takes on a role as a neurotransmitter and contributes to adult neurogenesis in the dentate gyrus. Other chemokines such as MCP-1/CCL2 are upregulated in the context of brain disease. In particular, we discuss the role of MCP-1 and its receptor CCR2 in the generation of chronic pain hypersensitivity. MCP-1 is upregulated by sensory nociceptors under these circumstances, and it plays a role in the control of nociceptor excitability. Overall, the data we discuss illustrate the extensive role of chemokines and their receptors in the control of neural development and disease.

Keywords

Dorsal Root Ganglion Dentate Gyrus Dorsal Root Ganglion Neuron Pain Hypersensitivity Chemokine Signaling 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ (2003) Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci USA 100:7947–7952PubMedCrossRefGoogle Scholar
  2. Agostini C, Gurrieri C (2006) Chemokine/cytokine cocktail in idiopathic pulmonary fibrosis. Proc Am Thorac Soc 3:357–363PubMedCrossRefGoogle Scholar
  3. Araujo DM, Cotman CW (1993) Trophic effects of interleukin-4, -7 and -8 on hippocampal neuronal cultures: potential involvement of glial-derived factors. Brain Res 600:49–55PubMedCrossRefGoogle Scholar
  4. Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M, Pleasure SJ (2002) The chemokine SDF1 regulates migration of dentate granule cells. Development 129:4249–4260PubMedGoogle Scholar
  5. Banisadr G, Skrzydelski D, Kitabgi P, Rostene W, Parsadaniantz SM (2003) Highly regionalized distribution of stromal cell-derived factor-1/CXCL12 in adult rat brain: constitutive expression in cholinergic, dopaminergic and vasopressinergic neurons. Eur J Neurosci 18:1593–1606PubMedCrossRefGoogle Scholar
  6. 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
  7. Belmadani A, Tran PB, Ren D, Miller RJ (2006) Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J Neurosci 26:3182–3191PubMedCrossRefGoogle Scholar
  8. Bensinger SJ, Tontonoz P (2008) Integration of metabolism and inflammation by lipid activated nuclear receptors. Nature 454:470–477PubMedCrossRefGoogle Scholar
  9. Berger O, Li G, Han SM, Paredes M, Pleasure SJ (2007) Expression of SDF-1 and CXCR4 during reorganization of the postnatal dentate gyrus. Dev Neurosci 29:48–58PubMedCrossRefGoogle Scholar
  10. Bhangoo SK, Ren D, Miller RJ, Chan DM, Ripsch MS, Weiss C, McGinnis C, White FA (2007a) CXCR4 chemokine receptor signaling mediates pain hypersensitivity in association with antiretroviral toxic neuropathy. Brain Behav Immun 21:581–591PubMedCrossRefGoogle Scholar
  11. Bhangoo S, Ren D, Miller RJ, Henry KJ, Lineswala J, Hamdouchi C, Li B, Monahan PE, Chan DM, Ripsch MS, White FA (2007b) 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 3:38–48PubMedCrossRefGoogle Scholar
  12. Bhattacharrya B, Banisadr G, Jung HS, Ren DJ, Cranshaw DG, Zou YR, Miller RJ (2008) The chemokine SDF-1 is a neurotransmitter that regulates neurotransmission in the adult dentate gyrus stem cell niche. J Neurosci 28:6720–6730CrossRefGoogle Scholar
  13. Bradley WG, Shapshak P, Delgado S, Nagano I, Stewart R, Rocha B (1998) Morphometric analysis of the peripheral neuropathy of AIDS. Muscle Nerve 21:1188–1195PubMedCrossRefGoogle Scholar
  14. 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
  15. Carroll SL, Frohnert PW (1998) Expression of JE (monocyte chemoattractant protein-1) is induced by sciatic axotomy in wild type rodents but not in C57BL/Wld(s) mice. J Neuropathol Exp Neurol 57:915–930PubMedCrossRefGoogle Scholar
  16. Cashen AF, Nervi B, DiPersio J (2007) AMD3100: CXCR4 antagonist and rapid stem cell-mobilizing agent. Future Oncol 3:19–27PubMedCrossRefGoogle Scholar
  17. Ceradini DJ, Gurtner GC (2005) Homing to hypoxia: HIF-1 as a mediator of progenitor cell recruitment to injured tissue. Trends Cardiovasc Med 15:57–63PubMedCrossRefGoogle Scholar
  18. 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
  19. 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
  20. Chen T, Bai H, Shao Y, Arzigian M, Janzen V, Attar E, Xie Y, Scadden DT, Wang ZZ (2007) Stromal cell-derived factor-1/CXCR4 signaling modifies the capillary-like organization of human embryonic stem cell-derived endothelium in vitro. Stem Cells 25:392–401PubMedCrossRefGoogle Scholar
  21. Chute JP (2006) Stem cell homing. Curr Opin Hematol 13:399–406PubMedCrossRefGoogle Scholar
  22. Conover JC, Notti RQ (2008) The neural stem cell niche. Cell Tissue Res 331:211–224PubMedCrossRefGoogle Scholar
  23. Cornblath DR, Hoke A (2006) Recent advances in HIV neuropathy. Curr Opin Neurol 19:446–450PubMedCrossRefGoogle Scholar
  24. D’Mello R, Dickenson AH (2008) Spinal cord mechanisms of pain. Br J Anaesth 101:8–16PubMedCrossRefGoogle Scholar
  25. Dar A, Kollet O, Lapidot T (2006) Mutual, reciprocal SDF-1/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
  26. de Jong EK, Dijkstra IM, Hensens M, Brouwer N, van Amerongen M, Liem RS, Boddeke HW, Biber K (2005) Vesicle-mediated transport and release of CCL21 in endangered neurons: a possible explanation for microglia activation remote from a primary lesion. J Neurosci 25:7548–7557PubMedCrossRefGoogle Scholar
  27. de Jong EK, Vinet J, Stanulovic VS, Meijer M, Wesseling E, Sjollema K, Boddeke HW, Biber K (2008) Expression, transport, and axonal sorting of neuronal CCL21 in large dense-core vesicles. FASEB J 22(12):4136–4145PubMedCrossRefGoogle Scholar
  28. Devor M (2006) Sodium channels and mechanisms of neuropathic pain. J Pain 7:S3–S12PubMedGoogle Scholar
  29. Duan X, Kang E, Liu CY, Ming GL, Song H (2008) Development of neural stem cell in the adult brain. Curr Opin Neurobiol 18:108–115PubMedCrossRefGoogle Scholar
  30. Dumstrei K, Mennecke R, Raz E (2004) Signaling pathways controlling primordial germ cell migration in zebrafish. J Cell Sci 117:4787–4795PubMedCrossRefGoogle Scholar
  31. Dunfee R, Thomas ER, Gorry PR, Wang J, Ancuta P, Gabuzda D (2006) Mechanisms of HIV-1 neurotropism. Curr HIV Res 4:267–279PubMedCrossRefGoogle Scholar
  32. Dziembowska M, Tham TN, Lau P, Vitry S, Lazarini F, Dubois-Dalcq M (2005) A role for CXCR4 signaling in survival and migration of neural and oligodendrocyte precursors. Glia 50:258–269PubMedCrossRefGoogle Scholar
  33. Epstein LG, Gelbard HA (1999) HIV-1-induced neuronal injury in the developing brain. J Leukoc Biol 65:453–457PubMedGoogle Scholar
  34. Esiri MM, Morris CS, Millard PR (1993) Sensory and sympathetic ganglia in HIV-1 infection: immunocytochemical demonstration of HIV-1 viral antigens, increased MHC class II antigen expression and mild reactive inflammation. J Neurol Sci 114:178–187PubMedCrossRefGoogle Scholar
  35. Flugel A, Hager G, Horvat A, Spitzer C, Singer GM, Graeber MB, Kreutzberg GW, Schwaiger FW (2001) Neuronal MCP-1 expression in response to remote nerve injury. J Cereb Blood Flow Metab 21:69–76PubMedCrossRefGoogle Scholar
  36. Fox JM, Chamberlain G, Ashton BA, Middleton J (2007) Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol 137:491–502PubMedCrossRefGoogle Scholar
  37. Fryer AD, Stein LH, Nie Z, Curtis DE, Evans CM, Hodgson ST, Jose PJ, Belmonte KE, Fitch E, Jacoby DB (2006) Neuronal eotaxin and the effects of CCR3 antagonist on airway hyperreactivity and M2 receptor dysfunction. J Clin Invest 116:228–236PubMedCrossRefGoogle Scholar
  38. Giovannelli A, Limatola C, Ragozzino D, Mileo AM, Ruggieri A, Ciotti MT, Mercanti D, Santoni A, Eusebi F (1998) CXC chemokines interleukin-8 (IL-8) and growth-related gene product alpha (GROalpha) modulate Purkinje neuron activity in mouse cerebellum. J Neuroimmunol 92:122–132PubMedCrossRefGoogle Scholar
  39. Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5:69–81PubMedCrossRefGoogle Scholar
  40. Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481–488PubMedCrossRefGoogle Scholar
  41. Guo LH, Schluesener HJ (2007) The innate immunity of the central nervous system in chronic pain: the role of Toll-like receptors. Cell Mol Life Sci 64:1128–1136PubMedCrossRefGoogle Scholar
  42. Guo Y, Hangoc G, Bian H, Pelus LM, Broxmeyer HE (2005) SDF-1/CXCL12 enhances survival and chemotaxis of murine embryonic stem cells and production of primitive and definitive hematopoietic progenitor cells. Stem Cells 23:1324–1332PubMedCrossRefGoogle Scholar
  43. Hahn H, Robinson B, Anderson C, Li W, Pardo A, Morgello S, Simpson H, Nath A (2008) Differential effects of HIV infected macrophages on DRG neurons and axons. Exp Neurol 210:30–40PubMedCrossRefGoogle Scholar
  44. 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
  45. 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 8:595–598PubMedCrossRefGoogle Scholar
  46. Hill WD, Hess DC, Martin-Studdard A, Carothers JJ, Zheng J, Hale D, Maeda M, Fagan SC, Carroll JE, Conway SJ (2004) SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 63:84–96PubMedGoogle Scholar
  47. 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
  48. Hristov M, Zernecke A, Liehn EA, Weber C (2007) Regulation of endothelial progenitor cell homing after arterial injury. Thromb Haemost 98:274–277PubMedGoogle Scholar
  49. Huising MO, Stet RJ, Kruiswijk CP, Savelkoul HF, Lidy Verburg-van Kemenade BM (2003) Molecular evolution of CXC chemokines: extant CXC chemokines originate from the CNS. Trends Immunol 24:307–313PubMedGoogle Scholar
  50. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153–1161PubMedCrossRefGoogle Scholar
  51. Imitola J (2007) Prospects for neural stem cell-based therapies for neurological diseases. Neurotherapeutics 4:701–714PubMedCrossRefGoogle Scholar
  52. Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cardiac neural crest. Development 127:1607–1616PubMedGoogle Scholar
  53. Jung H, Toth PT, White FA, Miller RJ (2008) Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurochem 104:254–263PubMedGoogle Scholar
  54. Kadi L, Selvaraju R, de Lys P, Proudfoot AE, Wells TN, Boschert U (2006) Differential effects of chemokines on oligodendrocyte precursor proliferation and myelin formation in vitro. J Neuroimmunol 174:133–146PubMedCrossRefGoogle Scholar
  55. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K, Kasuga M (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116:1494–1505PubMedCrossRefGoogle Scholar
  56. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988–994PubMedCrossRefGoogle Scholar
  57. Klein RS, Rubin JB (2004) Immune and nervous system CXCL12 and CXCR4: parallel roles in patterning and plasticity. Trends Immunol 25:306–314PubMedCrossRefGoogle Scholar
  58. 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 128:1971–1981PubMedGoogle Scholar
  59. Knaut H, Werz C, Geisler R, Nusslein-Volhard C (2003) A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421:279–282PubMedCrossRefGoogle Scholar
  60. Knaut H, Blader P, Strahle U, Schier AF (2005) Assembly of trigeminal sensory ganglia by chemokine signaling. Neuron 47:653–666PubMedCrossRefGoogle Scholar
  61. 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
  62. Krathwohl MD, Kaiser JL (2004a) Chemokines promote quiescence and survival of human neural progenitor cells. Stem Cells 22:109–118PubMedCrossRefGoogle Scholar
  63. Krathwohl MD, Kaiser JL (2004b) HIV-1 promotes quiescence in human neural progenitor cells. J Infect Dis 190:216–226PubMedCrossRefGoogle Scholar
  64. Kucia M, Reca R, Jala VR, Dawn B, Ratajczak J, Ratajczak MZ (2005a) Bone marrow as a home of heterogenous populations of nonhematopoietic stem cells. Leukemia 19:1118–1127PubMedCrossRefGoogle Scholar
  65. Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, Ratajczak J, Ratajczak MZ (2005b) Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells 23:879–894PubMedCrossRefGoogle Scholar
  66. Kucia M, Wojakowski W, Reca R, Machalinski B, Gozdzik J, Majka M, Baran J, Ratajczak J, Ratajczak MZ (2006) The migration of bone marrow-derived non-hematopoietic tissue-committed stem cells is regulated in an SDF-1-, HGF-, and LIF-dependent manner. Arch Immunol Ther Exp (Warsz) 54:121–135CrossRefGoogle Scholar
  67. Lapidot T, Dar A, Kollet O (2005) How do stem cells find their way home? Blood 106:1901–1910PubMedCrossRefGoogle Scholar
  68. Li Q, Shirabe K, Kuwada JY (2004) Chemokine signaling regulates sensory cell migration in zebrafish. Dev Biol 269:123–136PubMedCrossRefGoogle Scholar
  69. 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
  70. Lipton SA, Yeh M, Dreyer EB (1994) Update on current models of HIV-related neuronal injury: platelet-activating factor, arachidonic acid and nitric oxide. Adv Neuroimmunol 4:181–188PubMedCrossRefGoogle Scholar
  71. Liu XS, Zhang ZG, Zhang RL, Gregg SR, Wang L, Yier T, Chopp M (2007) Chemokine ligand 2 (CCL2) induces migration and differentiation of subventricular zone cells after stroke. J Neurosci Res 85:2120–2125PubMedCrossRefGoogle Scholar
  72. 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 USA 99:7090–7095PubMedCrossRefGoogle Scholar
  73. 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 95:9448–9453PubMedCrossRefGoogle Scholar
  74. Maysami S, Nguyen D, Zobel F, Pitz C, Heine S, Hopfner M, Stangel M (2006) Modulation of rat oligodendrocyte precursor cells by the chemokine CXCL12. Neuroreport 17:1187–1190PubMedCrossRefGoogle Scholar
  75. McArthur JC, Haughey N, Gartner S, Conant K, Pardo C, Nath A, Sacktor N (2003) Human immunodeficiency virus-associated dementia: an evolving disease. J Neurovirol 9:205–221PubMedGoogle Scholar
  76. McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J (1999) Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol 213:442–456PubMedCrossRefGoogle Scholar
  77. McLeod DS, Hasegawa T, Prow T, Merges C, Lutty G (2006) The initial fetal human retinal vasculature develops by vasculogenesis. Dev Dyn 235:3336–3347PubMedCrossRefGoogle Scholar
  78. Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454:428–435PubMedCrossRefGoogle Scholar
  79. Mefford ME, Gorry PR, Kuntsman K, Wolinsky SM, Gabuzda D (2008) Bioinformatic prediction programs underestimate the frequency of CXCR4 usage by R5X4 HIV type 1 in brain and other tissues. AIDS Res Hum Retroviruses 24:1215–1220PubMedCrossRefGoogle Scholar
  80. Melli G, Keswani SC, Fischer A, Chen W, Hoke A (2006) Spatially distinct and functionally independent mechanisms of axonal degeneration in a model of HIV-associated sensory neuropathy. Brain 129:1330–1338PubMedCrossRefGoogle Scholar
  81. Menetski J, Mistry S, Lu M, Mudgett JS, Ransohoff RM, Demartino JA, Macintyre DE, Abbadie C (2007) Mice overexpressing chemokine ligand 2 (CCL2) in astrocytes display enhanced nociceptive responses. Neuroscience 149:706–714PubMedCrossRefGoogle Scholar
  82. 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 USA 95:14500–14505PubMedCrossRefGoogle Scholar
  83. Miao Z, Luker KE, Summers BC, Berahovich R, Bhojani MS, Rehemtulla A, Kleer CG, Essner JJ, Nasevicius A, Luker GD, Howard MC, Schall TJ (2007) CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc Natl Acad Sci USA 104:15735–15740PubMedCrossRefGoogle Scholar
  84. Miller RJ, Meucci O (1999) AIDS and the brain: is there a chemokine connection? Trends Neurosci 22:471–479PubMedCrossRefGoogle Scholar
  85. Miller JT, Bartley JH, Wimborne HJ, Walker AL, Hess DC, Hill WD, Carroll JE (2005) The neuroblast and angioblast chemotaxic factor SDF-1 (CXCL12) expression is briefly up regulated by reactive astrocytes in brain following neonatal hypoxic-ischemic injury. BMC Neurosci 6:63PubMedCrossRefGoogle Scholar
  86. Moepps B, Braun M, Knopfle K, Dillinger K, Knochel W, Gierschik P (2000) Characterization of a Xenopus laevis CXC chemokine receptor 4: implications for hematopoietic cell development in the vertebrate embryo. Eur J Immunol 30:2924–2934PubMedCrossRefGoogle Scholar
  87. Morgello S, Estanislao L, Simpson D, Geraci A, DiRocco A, Gerits P, Ryan E, Yakoushina T, Khan S, Mahboob R, Naseer M, Dorfman D, Sharp V (2004) HIV-associated distal sensory polyneuropathy in the era of highly active antiretroviral therapy: the Manhattan HIV Brain Bank. Arch Neurol 61:546–551PubMedCrossRefGoogle Scholar
  88. Nagasawa T (2007) The chemokine CXCL12 and regulation of HSC and B lymphocyte development in the bone marrow niche. Adv Exp Med Biol 602:69–75PubMedCrossRefGoogle Scholar
  89. 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 1 entry coreceptor fusin. Proc Natl Acad Sci USA 93:14726–14729PubMedCrossRefGoogle Scholar
  90. Nair S, Schilling TF (2008) Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 322:89–92PubMedCrossRefGoogle Scholar
  91. Nie Y, Waite J, Brewer F, Sunshine MJ, Littman DR, Zou YR (2004) The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J Exp Med 200:1145–1156PubMedCrossRefGoogle Scholar
  92. 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
  93. 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
  94. Ohab JJ, Fleming S, Blesch A, Carmichael ST (2006) A neurovascular niche for neurogenesis after stroke. J Neurosci 26:13007–13016PubMedCrossRefGoogle Scholar
  95. 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 249:163–166PubMedCrossRefGoogle Scholar
  96. Okamoto S, Kang YJ, Brechtel CW, Siviglia E, Russo R, Clemente A, Harrop A, McKercher S, Kaul M, Lipton SA (2007) HIV/gp120 decreases adult neural progenitor cell proliferation via checkpoint kinase-mediated cell-cycle withdrawal and G1 arrest. Cell Stem Cell 1:230–236PubMedCrossRefGoogle Scholar
  97. Orimo A, Weinberg RA (2006) Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 5:1597–1601PubMedCrossRefGoogle Scholar
  98. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA (2005) Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121:335–348PubMedCrossRefGoogle Scholar
  99. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479–494PubMedCrossRefGoogle Scholar
  100. Pardo CA, McArthur JC, Griffin JW (2001) HIV neuropathy: insights in the pathology of HIV peripheral nerve disease. J Peripher Nerv Syst 6:21–27PubMedCrossRefGoogle Scholar
  101. 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 26:9404–9412PubMedCrossRefGoogle Scholar
  102. Qin X, Wan Y, Wang X (2005) CCL2 and CXCL1 trigger calcitonin gene-related peptide release by exciting primary nociceptive neurons. J. Neurosci Res 82(1):51–62PubMedCrossRefGoogle Scholar
  103. Rance NE, McArthur JC, Cornblath DR, Landstrom DL, Griffin JW, Price DL (1988) Gracile tract degeneration in patients with sensory neuropathy and AIDS. Neurology 38:265–271PubMedCrossRefGoogle Scholar
  104. Ratajczak MZ, Zuba-Surma E, Kucia M, Reca R, Wojakowski W, Ratajczak J (2006) The pleiotropic effects of the SDF-1-CXCR4 axis in organogenesis, regeneration and tumorigenesis. Leukemia 20:1915–1924PubMedCrossRefGoogle Scholar
  105. Raz E (2003) Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet 4:690–700PubMedCrossRefGoogle Scholar
  106. Rehimi R, Khalida N, Yusuf F, Dai F, Morosan-Puopolo G, Brand-Saberi B (2008) Stromal-derived factor-1 (SDF-1) expression during early chick development. Int J Dev Biol 52:87–92PubMedCrossRefGoogle Scholar
  107. Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M (2006) Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 26:125–134PubMedCrossRefGoogle Scholar
  108. Romero-Sandoval EA, Horvath RJ, DeLeo JA (2008) Neuroimmune interactions and pain: focus on glial-modulating targets. Curr Opin Investig Drugs 9:726–734PubMedGoogle Scholar
  109. Sacktor N, McDermott MP, Marder K, Schifitto G, Selnes OA, McArthur JC, Stern Y, Albert S, Palumbo D, Kieburtz K, De Marcaida JA, Cohen B, Epstein L (2002) HIV-associated cognitive impairment before and after the advent of combination therapy. J Neurovirol 8:136–142PubMedCrossRefGoogle Scholar
  110. Sano R, Tessitore A, Ingrassia A, d’Azzo A (2005) Chemokine-induced recruitment of genetically modified bone marrow cells into the CNS of GM1-gangliosidosis mice corrects neuronal pathology. Blood 106:2259–2268PubMedCrossRefGoogle Scholar
  111. Schifitto G, McDermott MP, McArthur JC, Marder K, Sacktor N, Epstein L, Kieburtz K (2002) Incidence of and risk factors for HIV-associated distal sensory polyneuropathy. Neurology 58:1764–1768PubMedCrossRefGoogle Scholar
  112. 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
  113. Schreiber RC, Krivacic K, Kirby B, Vaccariello SA, Wei T, Ransohoff RM, Zigmond RE (2001) Monocyte chemoattractant protein (MCP)-1 is rapidly expressed by sympathetic ganglion neurons following axonal injury. Neuroreport 12:601–606PubMedCrossRefGoogle Scholar
  114. 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
  115. Scotton CJ, Chambers RC (2007) Molecular targets in pulmonary fibrosis: the myofibroblast in focus. Chest 132:1311–1321PubMedCrossRefGoogle Scholar
  116. Sierro F, Biben C, Martinez-Munoz L, Mellado M, Ransohoff RM, Li M, Woehl B, Leung H, Groom J, Batten M, Harvey RP, Martinez AC, Mackay CR, Mackay F (2007) Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci USA 104:14759–14764PubMedCrossRefGoogle Scholar
  117. Snider P, Olaopa M, Firulli AB, Conway SJ (2007) Cardiovascular development and the colonizing cardiac neural crest lineage. ScientificWorldJournal 7:1090–1113PubMedCrossRefGoogle Scholar
  118. Sohy D, Parmentier M, Springael JY (2007) Allosteric transinhibition by specific antagonists in CCR2/CXCR4 heterodimers. J Biol Chem 282:30062–30069PubMedCrossRefGoogle Scholar
  119. Steiner B, Wolf S, Kempermann G (2006) Adult neurogenesis and neurodegenerative disease. Regen Med 1:15–28PubMedCrossRefGoogle Scholar
  120. Stumm RK, Rummel J, Junker V, Culmsee C, Pfeiffer M, Krieglstein J, Hollt V, Schulz S (2002) 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 22:5865–5878PubMedGoogle Scholar
  121. Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Hollt V, Schulz S (2003) CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 23:5123–5130PubMedGoogle Scholar
  122. Stumm R, Kolodziej A, Schulz S, Kohtz JD, Hollt V (2007) Patterns of SDF-1alpha and SDF-1gamma mRNAs, migration pathways, and phenotypes of CXCR4-expressing neurons in the developing rat telencephalon. J Comp Neurol 502:382–399PubMedCrossRefGoogle Scholar
  123. Sun JH, Yang B, Donnelly DF, Ma C, LaMotte RH (2006) MCP-1 enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia. J Neurophysiol 96:2189–2199PubMedCrossRefGoogle Scholar
  124. 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
  125. Tanaka T, Minami M, Nakagawa T, Satoh M (2004) Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: possible involvement in the development of neuropathic pain. Neurosci Res 48:463–469PubMedCrossRefGoogle Scholar
  126. Thacker MA, Clark AK, Bishop T, Grist J, Yip PK, Moon LD, Thompson SW, Marchand F, McMahon SB (2008) CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 13(3):263–272PubMedCrossRefGoogle Scholar
  127. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z, Lindvall O (2006) Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24:739–747PubMedCrossRefGoogle Scholar
  128. Tissir F, Wang CE, Goffinet AM (2004) Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res Dev Brain Res 149:63–71PubMedCrossRefGoogle Scholar
  129. Tiveron MC, Rossel M, Moepps B, Zhang YL, Seidenfaden R, Favor J, Konig 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
  130. Toews AD, Barrett C, Morell P (1998) Monocyte chemoattractant protein 1 is responsible for macrophage recruitment following injury to sciatic nerve. J Neurosci Res 53:260–267PubMedCrossRefGoogle Scholar
  131. 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 367:188–189PubMedCrossRefGoogle Scholar
  132. Tran PB, Miller RJ (2003) Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci 4:444–455PubMedCrossRefGoogle Scholar
  133. Tran PB, Ren D, Veldhouse TJ, Miller RJ (2004) Chemokine receptors are expressed widely by embryonic and adult neural progenitor cells. J Neurosci Res 76:20–34PubMedCrossRefGoogle Scholar
  134. 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 500:1007–1033PubMedCrossRefGoogle Scholar
  135. Uçeyler N, Sommer C (2008) Cytokine regulation in animal models of neuropathic pain and in human diseases. Neurosci Lett 437:194–198PubMedCrossRefGoogle Scholar
  136. Valentin G, Haas P, Gilmour D (2007) The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr Biol 17:1026–1031PubMedCrossRefGoogle Scholar
  137. Wallace VC, Blackbeard J, Segerdahl AR, Hasnie F, Pheby T, McMahon SB, Rice AS (2007) Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain. Brain 130(Pt 10):2688–2702PubMedCrossRefGoogle Scholar
  138. Wang JG, Strong JA, Xie W, Yang RH, Coyle DE, Wick DM, Dorsey ED, Zhang JM (2008) The chemokine CXCL1/growth related oncogene increases sodium currents and neuronal excitability in small diameter sensory neurons. Mol Pain 4:38PubMedCrossRefGoogle Scholar
  139. Watkins LR, Hutchinson MR, Ledeboer A, Wieseler-Frank J, Milligan ED, Maier SF (2007a) Norman Cousins Lecture. Glia as the “bad guys”: implications for improving clinical pain control and the clinical utility of opioids. Brain Behav Immun 21:131–146PubMedCrossRefGoogle Scholar
  140. Watkins LR, Hutchinson MR, Milligan ED, Maier SF (2007b) “Listening” and “talking” to neurons: implications of immune activation for pain control and increasing the efficacy of opioids. Brain Res Rev 56:148–169PubMedCrossRefGoogle Scholar
  141. Welner RS, Kincade PW (2007) Stem cells on patrol. Cell 131:842–844PubMedCrossRefGoogle Scholar
  142. Westmoreland SV, Rottman JB, Williams KC, Lackner AA, Sasseville VG (1998) Chemokine receptor expression on resident and inflammatory cells in the brain of macaques with simian immunodeficiency virus encephalitis. Am J Pathol 152:659–665PubMedGoogle Scholar
  143. White FA, Sun J, Waters SM, Ma C, Ren D, Ripsch M, Steflik J, Cortright DN, Lamotte RH, Miller RJ (2005) Excitatory monocyte chemoattractant protein-1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci USA 102:14092–14097PubMedCrossRefGoogle Scholar
  144. White FA, Jung H, Miller RJ (2007) Chemokines and the pathophysiology of neuropathic pain. Proc Natl Acad Sci USA 104:20151–20158PubMedCrossRefGoogle Scholar
  145. Williams KC, Hickey WF (2002) Central nervous system damage, monocytes and macrophages, and neurological disorders in AIDS. Annu Rev Neurosci 25:537–562PubMedCrossRefGoogle Scholar
  146. Xia M, Qin S, McNamara M, Mackay C, Hyman BT (1997) Interleukin-8 receptor B immunoreactivity in brain and neuritic plaques of Alzheimer’s disease. Am J Pathol 150:1267–1274PubMedGoogle Scholar
  147. Xu J, Mora A, Shim H, Stecenko A, Brigham KL, Rojas M (2007) Role of the SDF-1/CXCR4 axis in the pathogenesis of lung injury and fibrosis. Am J Respir Cell Mol Biol 37:291–299PubMedCrossRefGoogle Scholar
  148. Yusuf F, Rehimi R, Dai F, Brand-Saberi B (2005) Expression of chemokine receptor CXCR4 during chick embryo development. Anat Embryol (Berl) 210:35–41CrossRefGoogle Scholar
  149. Zhang J, De Koninck Y (2006) Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury. J Neurochem 97:772–783PubMedCrossRefGoogle Scholar
  150. Zhang J, Shi XQ, Echeverry S, Mogil JS, De Koninck Y, Rivest S (2007) Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J Neurosci 27:12396–12406PubMedCrossRefGoogle Scholar
  151. 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

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Molecular Pharmacology and Biological ChemistryNorthwestern University School of MedicineChicagoUSA

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