Chemokines in the balance: Maintenance of homeostasis and protection at CNS barriers

Frontiers in Cellular Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Williams, Jessica L ^a   Holman, David W ^b   Klein, Robyn S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Decision Resources Group   (United Kingdom)

Author keywords

Blood brain barrier; Central nervous system; Chemokines; Choroid plexus; Homeostasis; Meninges; Neurogenesis; Vasculature

Indexed keywords

BETA ARRESTIN 1; CHEMOKINE; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; CXCL14 CHEMOKINE; FRACTALKINE; G PROTEIN COUPLED RECEPTOR; GLYCOPROTEIN P 15095; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MATRIX PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; SCAVENGER RECEPTOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; STROMAL CELL DERIVED FACTOR 1; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN PERICYTE; CELL INFILTRATION; CELL INTERACTION; CELL MIGRATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CHOROID PLEXUS; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; MAP KINASE ASSAY; NEURAL STEM CELL; NEUROLOGIC DISEASE; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; WNT SIGNALING PATHWAY;

EID: 84901633386     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00154     Document Type: Review

References (130)

1. Alt, C., Laschinger, M., and Engelhardt, B. (2002). Functional expression of the lymphoid chemokines CCL19 (ELC) and CCL 21 (SLC) at the blood-brain barrier suggests their involvement in G-protein-dependent lymphocyte recruitment into the central nervous system during experimental autoimmune encephalomyelitis. Eur. J. Immunol. 32, 2133-2144. doi: 10.1002/1521-4141(200208)32:8<2133::aid-immu2133>3.0.co;2-w
2. Alvarez-Buylla, A., and Lim, D. A. (2004). For the long run: maintaining germinal niches in the adult brain. Neuron41, 683-686. doi: 10.1016/S0896-6273(04)00111-4
3. Arima, Y., Harada, M., Kamimura, D., Park, J. H., Kawano, F., Yull, F. E., et al. (2012). Regional neural activation defines a gateway for autoreactive T cells to cross the blood-brain barrier. Cell 148, 447-457. doi: 10.1016/j.cell.2012.01.022
4. Bachmann, M. F., Kopf, M., and Marsland, B. J. (2006). Chemokines: more than just road signs. Nat. Rev. Immunol.6, 159-164. doi: 10.1038/nri1776
5. Bachstetter, A. D., Morganti, J. M., Jernberg, J., Schlunk, A., Mitchell, S. H., Brewster, K. W., et al. (2011). Fractalkine and CX 3 CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol. Aging 32, 2030-2044. doi: 10.1016/j.neurobiolaging.2009.11.022
6. Balabanov, R., and Dore-Duffy, P. (1998). Role of the CNS microvascular pericyte in the blood-brain barrier. J. Neurosci. Res. 53, 637-644. doi: 10.1002/(sici)1097-4547(19980915)53:6<637::aid-jnr1>3.0.co;2-6
7. Banisadr, G., Bhattacharyya, B. J., Belmadani, A., Izen, S. C., Ren, D., Tran, P. B., et al. (2011). The chemokine BRAK/CXCL14 regulates synaptic transmission in the adult mouse dentate gyrus stem cell niche. J. Neurochem.119, 1173-1182. doi: 10.1111/j.1471-4159.2011.07509.x
8. Ben Abdallah, N. M., Slomianka, L., Vyssotski, A. L., and Lipp, H. P. (2010). Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol. Aging 31, 151-161. doi: 10.1016/j.neurobiolaging.2008.03.002
9. Bhattacharyya, B. J., Banisadr, G., Jung, H., Ren, D., Cronshaw, D. G., Zou, Y., et al. (2008). The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J. Neurosci.28, 6720-6730. doi: 10.1523/jneurosci.1677-08.2008
10. Boldajipour, B., Mahabaleshwar, H., Kardash, E., Reichman-Fried, M., Blaser, H., Minina, S., et al. (2008). Control of chemokine-guided cell migration by ligand sequestration. Cell 132, 463-473. doi: 10.1016/j.cell.2007.12.034
11. Bonacchi, A., Romagnani, P., Romanelli, R. G., Efsen, E., Annunziato, F., Lasagni, L., et al. (2001). Signal transduction by the chemokine receptor CXCR3: activation of Ras/ERK, Src and phosphatidylinositol 3-kinase/Akt controls cell migration and proliferation in human vascular pericytes. J. Biol. Chem. 276, 9945-9954. doi: 10.1074/jbc.m010303200
12. Burns, J. M., Summers, B. C., Wang, Y., Melikian, A., Berahovich, R., Miao, Z., et al. (2006). A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion and tumor development. J. Exp. Med. 203, 2201-2213. doi: 10.1084/jem.20052144
13. Carbajal, K. S., Miranda, J. L., Tsukamoto, M. R., and Lane, T. E. (2011). CXCR4 signaling regulates remyelination by endogenous oligodendrocyte progenitor cells in a viral model of demyelination. Glia 59, 1813-1821. doi: 10.1002/glia.21225
14. Carbajal, K. S., Schaumburg, C., Strieter, R., Kane, J., and Lane, T. E. (2010). Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viral model of multiple sclerosis. Proc. Natl. Acad. Sci. U S A 107, 11068-11073. doi: 10.1073/pnas.1006375107
15. Chapman, G. A., Moores, K., Harrison, D., Campbell, C. A., Stewart, B. R., and Strijbos, P. J. (2000). Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J. Neurosci. 20, 1-5, RC87.
16. Charles, J., Di Domizio, J., Salameire, D., Bendriss-Vermare, N., Aspord, C., Muhammad, R., et al. (2010). Characterization of circulating dendritic cells in melanoma: role of CCR6 in plasmacytoid dendritic cell recruitment to the tumor. J. Invest. Dermatol. 130, 1646-1656. doi: 10.1038/jid.2010.24
17. Chinnery, H. R., Ruitenberg, M. J., and Mcmenamin, P. G. (2010). Novel characterization of monocyte-derived cell populations in the meninges and choroid plexus and their rates of replenishment in bone marrow chimeric mice. J. Neuropathol. Exp. Neurol. 69, 896-909. doi: 10.1097/nen.0b013e3181edbc1a
18. Choe, Y., and Pleasure, S. J. (2012). Wnt signaling regulates intermediate precursor production in the postnatal dentate gyrus by regulating CXCR4 expression. Dev. Neurosci. 34, 502-514. doi: 10.1159/000345353
19. Clarkson, B. D., Héninger, E., Harris, M. G., Lee, J., Sandor, M., and Fabry, Z. (2012). Innate-adaptive crosstalk: how dendritic cells shape immune responses in the CNS. Adv. Exp. Med. Biol. 946, 309-333. doi: 10.1007/978-1-4614-0106-3_18
20. Conductier, G., Blondeau, N., Guyon, A., Nahon, J. L., and Rovère, C. (2010). The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J. Neuroimmunol. 224, 93-100. doi: 10.1016/j.jneuroim.2010.05.010
21. Cruz-Orengo, L., Holman, D. W., Dorsey, D., Zhou, L., Zhang, P., Wright, M., et al. (2011). CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J. Exp. Med. 208, 327-339. doi: 10.1084/jem.20102010
22. Cunningham, C. L., Martínez-Cerdeño, V., and Noctor, S. C. (2013). Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33, 4216-4233. doi: 10.1523/jneurosci.3441-12.2013
23. Danielyan, L., Schäfer, R., Von Ameln-Mayerhofer, A., Buadze, M., Geisler, J., Klopfer, T., et al. (2009). Intranasal delivery of cells to the brain. Eur. J. Cell Biol. 88, 315-324. doi: 10.1016/j.ejcb.2009.02.001
24. Deverman, B. E., and Patterson, P. H. (2009). Cytokines and CNS development. Neuron 64, 61-78. doi: 10.1016/j.neuron.2009.09.002
25. Doetsch, F., and Scharff, C. (2001). Challenges for brain repair: insights from adult neurogenesis in birds and mammals. Brain Behav. Evol. 58, 306-322. doi: 10.1159/000057572
26. Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., et al. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. doi: 10.1038/3305
27. Fernández-Arenas, E., Calleja, E., Martinez-Martin, N., Gharbi, S. I., Navajas, R., Garcia-Medel, N., et al. (2014). Beta-arrestin-1 mediates the TCR-triggered re-routing of distal receptors to the immunological synapse by a PKC-mediated mechanism. EMBO J. 33, 559-577. doi: 10.1002/embj.201386022
28. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438. doi: 10.1126/science.287.5457.1433
29. Galea, I., Bechmann, I., and Perry, V. H. (2007). What is immune privilege (not)? Trends Immunol. 28, 12-18. doi: 10.1016/j.it.2006.11.004
30. Ge, S., Pradhan, D. A., Ming, G. L., and Song, H. (2007). GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci. 30, 1-8. doi: 10.1016/j.tins.2006.11.001
31. Gemma, C., Bachstetter, A. D., Cole, M. J., Fister, M., Hudson, C., and Bickford, P. C. (2007). Blockade of caspase-1 increases neurogenesis in the aged hippocampus. Eur. J. Neurosci. 26, 2795-2803. doi: 10.1111/j.1460-9568.2007.05875.x
32. Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., et al. (2010). Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845. doi: 10.1126/science.1194637
33. Goldmann, J., Kwidzinski, E., Brandt, C., Mahlo, J., Richter, D., and Bechmann, I. (2006). T cells traffic from brain to cervical lymph nodes via the cribroid plate and the nasal mucosa. J. Leukoc. Biol. 80, 797-801. doi: 10.1189/jlb.0306176
34. Gunsolly, C., Nicholson, J. D., Listwak, S. J., Ledee, D., Zelenka, P., Verthelyi, D., et al. (2010). Expression and regulation in the brain of the chemokine CCL27 gene locus. J. Neuroimmunol. 225, 82-90. doi: 10.1016/j.jneuroim.2010.04.019
35. Hamel, D. J., Sielaff, I., Proudfoot, A. E., and Handel, T. M. (2009). Chapter 4. Interactions of chemokines with glycosaminoglycans. Methods Enzymol. 461, 71-102. doi: 10.1016/s0076-6879(09)05404-4
36. Harrison, J. K., Jiang, Y., Chen, S., Xia, Y., Maciejewski, D., Mcnamara, R. K., et al. (1998). Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. U S A 95, 10896-10901. doi: 10.1073/pnas.95.18.10896
37. Haskell, C. A., Cleary, M. D., and Charo, I. F. (1999). Molecular uncoupling of fractalkine-mediated cell adhesion and signal transduction. Rapid flow arrest of CX3CR1-expressing cells is independent of G-protein activation. J. Biol. Chem. 274, 10053-10058. doi: 10.1074/jbc.274.15.10053
38. Hatori, K., Nagai, A., Heisel, R., Ryu, J. K., and Kim, S. U. (2002). Fractalkine and fractalkine receptors in human neurons and glial cells. J. Neurosci. Res. 69, 418-426. doi: 10.1002/jnr.10304
39. Hermand, P., Pincet, F., Carvalho, S., Ansanay, H., Trinquet, E., Daoudi, M., et al. (2008). Functional adhesiveness of the CX3CL1 chemokine requires its aggregation. Role of the transmembrane domain. J. Biol. Chem. 283, 30225-30234. doi: 10.1074/jbc.m802638200
40. Hill, W. D., Hess, D. C., Martin-Studdard, A., Carothers, J. J., Zheng, J., Hale, D., et al. (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, 84-96.
41. Hoshiko, M., Arnoux, I., Avignone, E., Yamamoto, N., and Audinat, E. (2012). Deficiency of the microglial receptor CX3CR1 impairs postnatal functional development of thalamocortical synapses in the barrel cortex. J. Neurosci.32, 15106-15111. doi: 10.1523/jneurosci.1167-12.2012
42. Howell, O. W., Reeves, C. A., Nicholas, R., Carassiti, D., Radotra, B., Gentleman, S. M., et al. (2011). Meningeal inflammation is widespread and linked to cortical pathology in multiple sclerosis. Brain 134(Pt. 9), 2755-2771. doi: 10.1093/brain/awr182
43. Huang, V., Lonsdorf, A. S., Fang, L., Kakinuma, T., Lee, V. C., Cha, E., et al. (2008). Cutting edge: rapid accumulation of epidermal CCL27 in skin-draining lymph nodes following topical application of a contact sensitizer recruits CCR10-expressing T cells. J. Immunol. 180, 6462-6466. doi: 10.4049/jimmunol.180.10.6462
44. Huising, M. O., Van Der Meulen, T., Flik, G., and Verburg-Van Kemenade, B. M. (2004). Three novel carp CXC chemokines are expressed early in ontogeny and at nonimmune sites. Eur. J. Biochem. 271, 4094-4106. doi: 10.1111/j.1432-1033.2004.04347.x
45. Iosif, R. E., Ekdahl, C. T., Ahlenius, H., Pronk, C. J., Bonde, S., Kokaia, Z., et al. (2006). Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J. Neurosci. 26, 9703-9712. doi: 10.1523/jneurosci.2723-06.2006
46. Israelsson, C., Bengtsson, H., Kylberg, A., Kullander, K., Lewen, A., Hillered, L., et al. (2008). Distinct cellular patterns of upregulated chemokine expression supporting a prominent inflammatory role in traumatic brain injury. J. Neurotrauma 25, 959-974. doi: 10.1089/neu.2008.0562
47. Ito, T., Carson, W. F. T., Cavassani, K. A., Connett, J. M., and Kunkel, S. L. (2011). CCR6 as a mediator of immunity in the lung and gut. Exp. Cell Res. 317, 613-619. doi: 10.1016/j.yexcr.2010.12.018
48. Johnson, Z., Proudfoot, A. E., and Handel, T. M. (2005). Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev. 16, 625-636. doi: 10.1016/j.cytogfr.2005.04.006
49. Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E. G., et al. (2013). Microglia emerge from erythromyeloid precursors via Pu.1-and Irf8-dependent pathways. Nat. Neurosci. 16, 273-280. doi: 10.1038/nn.3318
50. Kivisäkk, P., Imitola, J., Rasmussen, S., Elyaman, W., Zhu, B., Ransohoff, R. M., et al. (2009). Localizing central nervous system immune surveillance: meningeal antigen-presenting cells activate T cells during experimental autoimmune encephalomyelitis. Ann. Neurol. 65, 457-469. doi: 10.1002/ana.21379
51. Kivisäkk, P., Mahad, D. J., Callahan, M. K., Sikora, K., Trebst, C., Tucky, B., et al. (2004). Expression of CCR7 in multiple sclerosis: implications for CNS immunity. Ann. Neurol. 55, 627-638. doi: 10.1002/ana.20049
52. Kivisäkk, P., Mahad, D. J., Callahan, M. K., Trebst, C., Tucky, B., Wei, T., et al. (2003). Human cerebrospinal fluid central memory CD4+ T cells: evidence for trafficking through choroid plexus and meninges via P-selectin. Proc. Natl. Acad. Sci. U S A 100, 8389-8394. doi: 10.1073/pnas.1433000100
53. Klein, R. S., Rubin, J. B., Gibson, H. D., Dehaan, E. N., Alvarez-Hernandez, X., Segal, R. A., et al. (2001). SDF-1 alpha induces chemotaxis and enhances sonic hedgehog-induced proliferation of cerebellar granule cells. Development128, 1971-1981.
54. Kokovay, E., Goderie, S., Wang, Y., Lotz, S., Lin, G., Sun, Y., et al. (2010). Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 7, 163-173. doi: 10.1016/j.stem.2010.05.019
55. Kolattukudy, P. E., and Niu, J. (2012). Inflammation, endoplasmic reticulum stress, autophagy and the monocyte chemoattractant protein-1/CCR2 pathway. Circ. Res. 110, 174-189. doi: 10.1161/CIRCRESAHA.111.243212
56. Koo, J. W., and Duman, R. S. (2008). IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. U S A 105, 751-756. doi: 10.1073/pnas.0708092105
57. Kovac, A., Erickson, M. A., and Banks, W. A. (2011). Brain microvascular pericytes are immunoactive in culture: cytokine, chemokine, nitric oxide and LRP-1 expression in response to lipopolysaccharide. J. Neuroinflammation8:139. doi: 10.1186/1742-2094-8-139
58. Kremer, K. N., Clift, I. C., Miamen, A. G., Bamidele, A. O., Qian, N. X., Humphreys, T. D., et al. (2011). Stromal cell-derived factor-1 signaling via the CXCR4-TCR heterodimer requires phospholipase C-beta3 and phospholipase C-gamma1 for distinct cellular responses. J. Immunol. 187, 1440-1447. doi: 10.4049/jimmunol.1100820
59. Krumbholz, M., Theil, D., Steinmeyer, F., Cepok, S., Hemmer, B., Hofbauer, M., et al. (2007). CCL19 is constitutively expressed in the CNS, up-regulated in neuroinflammation, active and also inactive multiple sclerosis lesions. J. Neuroimmunol. 190, 72-79. doi: 10.1016/j.jneuroim.2007.07.024
60. Kuhn, H. G., Dickinson-Anson, H., and Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033.
61. Laman, J. D., and Weller, R. O. (2013). Drainage of cells and soluble antigen from the CNS to regional lymph nodes.J. Neuroimmune Pharmacol. 8, 840-856. doi: 10.1007/s11481-013-9470-8
62. Lenz, K. M., Nugent, B. M., Haliyur, R., and Mccarthy, M. M. (2013). Microglia are essential to masculinization of brain and behavior. J. Neurosci. 33, 2761-2772. doi: 10.1523/JNEUROSCI.1268-12.2013
63. Lie, D. C., Colamarino, S. A., Song, H. J., Desire, L., Mira, H., Consiglio, A., et al. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375. doi: 10.1038/nature04108
64. Luker, K. E., Steele, J. M., Mihalko, L. A., Ray, P., and Luker, G. D. (2010). Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene 29, 4599-4610. doi: 10.1038/onc.2010.212
65. Ma, S., Olucha-Bordonau, F. E., Hossain, M. A., Lin, F., Kuei, C., Liu, C., et al. (2009). Modulation of hippocampal theta oscillations and spatial memory by relaxin-3 neurons of the nucleus incertus. Learn. Mem. 16, 730-742. doi: 10.1101/lm.1438109
66. Machold, R., Hayashi, S., Rutlin, M., Muzumdar, M. D., Nery, S., Corbin, J. G., et al. (2003). Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39, 937-950. doi: 10.1016/s0896-6273(03)00593-2
67. Mahabaleshwar, H., Tarbashevich, K., Nowak, M., Brand, M., and Raz, E. (2012). beta-arrestin control of late endosomal sorting facilitates decoy receptor function and chemokine gradient formation. Development 139, 2897-2902. doi: 10.1242/dev.080408
68. Matyszak, M. K., and Perry, V. H. (1996). The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system. Neuroscience 74, 599-608. doi: 10.1016/0306-4522(96)00160-1
69. McCandless, E. E., Wang, Q., Woerner, B. M., Harper, J. M., and Klein, R. S. (2006). CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis.J. Immunol. 177, 8053-8064. doi: 10.4049/jimmunol.177.11.8053
70. McMenamin, P. G. (1999). Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges and choroid plexus of the rat brain as demonstrated in wholemount preparations. J. Comp. Neurol. 405, 553-562. doi: 10.1002/(sici)1096-9861(19990322)405:4<553::aid-cne8>3.3.co;2-y
71. Mirzadeh, Z., Merkle, F. T., Soriano-Navarro, M., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3, 265-278. doi: 10.1016/j.stem.2008.07.004
72. Monje, M. L., Toda, H., and Palmer, T. D. (2003). Inflammatory blockade restores adult hippocampal neurogenesis. Science 302, 1760-1765. doi: 10.1126/science.1088417
73. Morales, J., Homey, B., Vicari, A. P., Hudak, S., Oldham, E., Hedrick, J., et al. (1999). CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc. Natl. Acad. Sci. U S A 96, 14470-14475. doi: 10.1073/pnas.96.25.14470
74. Naumann, U., Cameroni, E., Pruenster, M., Mahabaleshwar, H., Raz, E., Zerwes, H. G., et al. (2010). CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS One 5:e9175. doi: 10.1371/journal.pone.0009175
75. Neumann, H., and Wekerle, H. (2013). Brain microglia: watchdogs with pedigree. Nat. Neurosci. 16, 253-255. doi: 10.1038/nn.3338
76. Nimmerjahn, A., Kirchhoff, F., and Helmchen, F. (2005). Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318. doi: 10.1126/science.1110647
77. Noda, M., Doi, Y., Liang, J., Kawanokuchi, J., Sonobe, Y., Takeuchi, H., et al. (2011). Fractalkine attenuates excito-neurotoxicity via microglial clearance of damaged neurons and antioxidant enzyme heme oxygenase-1 expression.J. Biol. Chem. 286, 2308-2319. doi: 10.1074/jbc.m110.169839
78. Odemis, V., Lipfert, J., Kraft, R., Hajek, P., Abraham, G., Hattermann, K., et al. (2012). The presumed atypical chemokine receptor CXCR7 signals through G(i/o) proteins in primary rodent astrocytes and human glioma cells. Glia 60, 372-381. doi: 10.1002/glia.22271
79. Parachikova, A., and Cotman, C. W. (2007). Reduced CXCL12/CXCR4 results in impaired learning and is downregulated in a mouse model of Alzheimer disease. Neurobiol. Dis. 28, 143-153. doi: 10.1016/j.nbd.2007.07.001
80. Parish, C. R. (2006). The role of heparan sulphate in inflammation. Nat. Rev. Immunol. 6, 633-643. doi: 10.1038/nri1918
81. Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R. 3rd, Lafaille, J. J., et al. (2013). Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155, 1596-1609. doi: 10.1016/j.cell.2013.11.030
82. Pastrana, E., Cheng, L. C., and Doetsch, F. (2009). Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc. Natl. Acad. Sci. U S A 106, 6387-6392. doi: 10.1073/pnas.0810407106
83. Patel, J. R., Mccandless, E. E., Dorsey, D., and Klein, R. S. (2010). CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination. Proc. Natl. Acad. Sci. U S A 107, 11062-11067. doi: 10.1073/pnas.1006301107
84. Patel, J. R., Williams, J. L., Muccigrosso, M. M., Liu, L., Sun, T., Rubin, J. B., et al. (2012). Astrocyte TNFR2 is required for CXCL12-mediated regulation of oligodendrocyte progenitor proliferation and differentiation within the adult CNS. Acta Neuropathol. 124, 847-860. doi: 10.1007/s00401-012-1034-0
85. Prodinger, C., Bunse, J., Kruger, M., Schiefenhovel, F., Brandt, C., Laman, J. D., et al. (2011). CD11c-expressing cells reside in the juxtavascular parenchyma and extend processes into the glia limitans of the mouse nervous system. Acta Neuropathol. 121, 445-458. doi: 10.1007/s00401-010-0774-y
86. Rajagopal, S., Kim, J., Ahn, S., Craig, S., Lam, C. M., Gerard, N. P., et al. (2010). Beta-arrestin-but not G protein-mediated signaling by the "decoy" receptor CXCR7. Proc. Natl. Acad. Sci. U S A 107, 628-632. doi: 10.1073/pnas.0912852107
87. Rao, M. S., Hattiangady, B., and Shetty, A. K. (2006). The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5, 545-558. doi: 10.1111/j.1474-9726.2006.00243.x
88. Réaux-Le Goazigo, A., Van Steenwinckel, J., Rostene, W., and Melik Parsadaniantz, S. (2013). Current status of chemokines in the adult CNS. Prog. Neurobiol. 104, 67-92. doi: 10.1016/j.pneurobio.2013.02.001
89. Reboldi, A., Coisne, C., Baumjohann, D., Benvenuto, F., Bottinelli, D., Lira, S., et al. (2009). C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10, 514-523. doi: 10.1038/ni.1716
90. Rogers, J. T., Morganti, J. M., Bachstetter, A. D., Hudson, C. E., Peters, M. M., Grimmig, B. A., et al. (2011). CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J. Neurosci. 31, 16241-16250. doi: 10.1523/JNEUROSCI.3667-11.2011
91. Sallusto, F., Schaerli, P., Loetscher, P., Schaniel, C., Lenig, D., Mackay, C. R., et al. (1998). Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28, 2760-2769. doi: 10.1002/(sici)1521-4141(199809)28:09<2760::aid-immu2760>3.0.co;2-n
92. Sanai, N., Nguyen, T., Ihrie, R. A., Mirzadeh, Z., Tsai, H. H., Wong, M., et al. (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478, 382-386. doi: 10.1038/nature10487
93. Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., et al. (2012). Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691-705. doi: 10.1016/j.neuron.2012.03.026
94. Schilling, M., Strecker, J. K., Ringelstein, E. B., Kiefer, R., and Schabitz, W. R. (2009). Turn-over of meningeal and perivascular macrophages in the brain of MCP-1-, CCR-2-or double knockout mice. Exp. Neurol. 219, 583-585. doi: 10.1016/j.expneurol.2009.07.003
95. Schneider, O. D., Weiss, A. A., and Miller, W. E. (2009). Pertussis toxin signals through the TCR to initiate cross-desensitization of the chemokine receptor CXCR4. J. Immunol. 182, 5730-5739. doi: 10.4049/jimmunol.0803114
96. Schönemeier, B., Kolodziej, A., Schulz, S., Jacobs, S., Hoellt, V., and Stumm, R. (2008a). Regional and cellular localization of the CXCl12/SDF-1 chemokine receptor CXCR7 in the developing and adult rat brain. J. Comp. Neurol. 510, 207-220. doi: 10.1002/cne.21780
97. Schönemeier, B., Schulz, S., Hoellt, V., and Stumm, R. (2008b). Enhanced expression of the CXCl12/SDF-1 chemokine receptor CXCR7 after cerebral ischemia in the rat brain. J. Neuroimmunol. 198, 39-45. doi: 10.1016/j.jneuroim.2008.04.010
98. Schultheiß, C., Abe, P., Hoffmann, F., Mueller, W., Kreuder, A. E., Schutz, D., et al. (2013). CXCR4 prevents dispersion of granule neuron precursors in the adult dentate gyrus. Hippocampus 23, 1345-1358. doi: 10.1002/hipo.22180
99. Schulz, M., and Engelhardt, B. (2005). The circumventricular organs participate in the immunopathogenesis of experimental autoimmune encephalomyelitis. Cerebrospinal Fluid Res. 2:8. doi: 10.5772/29792
100. Serot, J. M., Bene, M. C., Foliguet, B., and Faure, G. C. (2000). Monocyte-derived IL-10-secreting dendritic cells in choroid plexus epithelium. J. Neuroimmunol. 105, 115-119. doi: 10.1016/s0165-5728(99)00240-4
101. Serrats, J., Schiltz, J. C., Garcia-Bueno, B., Van Rooijen, N., Reyes, T. M., and Sawchenko, P. E. (2010). Dual roles for perivascular macrophages in immune-to-brain signaling. Neuron 65, 94-106. doi: 10.1016/j.neuron.2009.11.032
102. Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y., Abramova, N., et al. (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340. doi: 10.1126/science.1095505
103. Shen, Q., Wang, Y., Kokovay, E., Lin, G., Chuang, S. M., Goderie, S. K., et al. (2008). Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3, 289-300. doi: 10.1016/j.stem.2008.07.026
104. Sheridan, G. K., and Murphy, K. J. (2013). Neuron-glia crosstalk in health and disease: fractalkine and CX3CR1 take centre stage. Open Biol. 3:130181. doi: 10.1098/rsob.130181
105. Sierra, A., Beccari, S., Diaz-Aparicio, I., Encinas, J. M., Comeau, S., and Tremblay, M. E. (2014). Surveillance, phagocytosis and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plast. 2014:610343. doi: 10.1155/2014/610343
106. Smith, X., Schneider, H., Kohler, K., Liu, H., Lu, Y., and Rudd, C. E. (2013). The chemokine CXCL12 generates costimulatory signals in T cells to enhance phosphorylation and clustering of the adaptor protein SLP-76. Sci. Signal. 6:ra65. doi: 10.1126/scisignal.2004018
107. Song, N., Huang, Y., Shi, H., Yuan, S., Ding, Y., Song, X., et al. (2009). Overexpression of platelet-derived growth factor-BB increases tumor pericyte content via stromal-derived factor-1alpha/CXCR4 axis. Cancer Res. 69, 6057-6064. doi: 10.1158/0008-5472.CAN-08-2007
108. Stowe, A. M., Wacker, B. K., Cravens, P. D., Perfater, J. L., Li, M. K., Hu, R., et al. (2012). CCL2 upregulation triggers hypoxic preconditioning-induced protection from stroke. J. Neuroinflammation 9:33. doi: 10.1186/1742-2094-9-33
109. Strazielle, N., and Ghersi-Egea, J. F. (2000). Choroid plexus in the central nervous system: biology and physiopathology. J. Neuropathol. Exp. Neurol. 59, 561-574.
110. Stumm, R. K., Rummel, J., Junker, V., Culmsee, C., Pfeiffer, M., Krieglstein, J., et al. (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, 5865-5878.
111. Sugiyama, T., Kohara, H., Noda, M., and Nagasawa, T. (2006). Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25, 977-988. doi: 10.1016/j.immuni.2006.10.016
112. Tanegashima, K., Suzuki, K., Nakayama, Y., Tsuji, K., Shigenaga, A., Otaka, A., et al. (2013). CXCL14 is a natural inhibitor of the CXCL12-CXCR4 signaling axis. FEBS Lett. 587, 1731-1735. doi: 10.1016/j.febslet.2013.04.046
113. Tavazoie, M., Van Der Veken, L., Silva-Vargas, V., Louissaint, M., Colonna, L., Zaidi, B., et al. (2008). A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279-288. doi: 10.1016/j.stem.2008.07.025
114. Teng, H., Zhang, Z. G., Wang, L., Zhang, R. L., Zhang, L., Morris, D., et al. (2008). Coupling of angiogenesis and neurogenesis in cultured endothelial cells and neural progenitor cells after stroke. J. Cereb. Blood Flow Metab. 28, 764-771. doi: 10.1038/sj.jcbfm.9600573
115. Tiveron, M. C., Boutin, C., Daou, P., Moepps, B., and Cremer, H. (2010). Expression and function of CXCR7 in the mouse forebrain. J. Neuroimmunol. 224, 72-79. doi: 10.1016/j.jneuroim.2010.05.011
116. Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., et al. (2013). Layer V cortical neurons require microglial support for survival during postnatal development. Nat. Neurosci. 16, 543-551. doi: 10.1038/nn.3358
117. van der Meer, P., Ulrich, A. M., Gonzalez-Scarano, F., and Lavi, E. (2000). Immunohistochemical analysis of CCR2, CCR3, CCR5 and CXCR4 in the human brain: potential mechanisms for HIV dementia. Exp. Mol. Pathol. 69, 192-201. doi: 10.1006/exmp.2000.2336
118. van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034. doi: 10.1038/4151030a
119. Virgintino, D., Errede, M., Rizzi, M., Girolamo, F., Strippoli, M., Walchli, T., et al. (2013). The CXCL12/CXCR4/CXCR7 ligand-receptor system regulates neuro-glio-vascular interactions and vessel growth during human brain development. J. Inherit. Metab. Dis. 36, 455-466. doi: 10.1007/s10545-012-9574-y
120. Wang, Y., Huang, J., Li, Y., and Yang, G. Y. (2012). Roles of chemokine CXCL12 and its receptors in ischemic stroke. Curr. Drug Targets 13, 166-172. doi: 10.2174/138945012799201603
121. Williams, J. L., Patel, J. R., Daniels, B. P., and Klein, R. S. (2014). Targeting CXCR7/ACKR3 as a therapeutic strategy to promote remyelination in the adult central nervous system. J. Exp. Med. 211, 791-799. doi: 10.1084/jem.20131224
122. Wilson, E. H., Weninger, W., and Hunter, C. A. (2010). Trafficking of immune cells in the central nervous system. J. Clin. Invest. 120, 1368-1379. doi: 10.1172/JCI41911
123. Yamaguchi, J., Kusano, K. F., Masuo, O., Kawamoto, A., Silver, M., Murasawa, S., et al. (2003). Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107, 1322-1328. doi: 10.1161/01.cir.0000055313.77510.22
124. Yamamoto, T., Yamashita, A., Yamada, K., and Hata, R. (2011). Immunohistochemical localization of chemokine CXCL14 in rat hypothalamic neurons. Neurosci. Lett. 487, 335-340. doi: 10.1016/j.neulet.2010.10.051
125. Zachariae, C. O. (1993). Chemotactic cytokines and inflammation. Biological properties of the lymphocyte and monocyte chemotactic factors ELCF, MCAF and IL-8. Acta Derm. Venereol. Suppl. (Stockh) 181, 1-37.
126. Zhan, Y., Paolicelli, R. C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., et al. (2014). Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17, 400-406. doi: 10.1038/nn.3641
127. Zhang, Z. G., Zhang, L., Jiang, Q., and Chopp, M. (2002). Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ. Res. 90, 284-288. doi: 10.1161/hh0302.104460
128. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660. doi: 10.1016/j.cell.2008.01.033
129. Zheng, H., Fu, G., Dai, T., and Huang, H. (2007). Migration of endothelial progenitor cells mediated by stromal cell-derived factor-1alpha/CXCR4 via PI3K/Akt/eNOS signal transduction pathway. J. Cardiovasc. Pharmacol. 50, 274-280. doi: 10.1097/fjc.0b013e318093ec8f
130. Zhu, B., Xu, D., Deng, X., Chen, Q., Huang, Y., Peng, H., et al. (2012). CXCL12 enhances human neural progenitor cell survival through a CXCR7-and CXCR4-mediated endocytotic signaling pathway. Stem Cells 30, 2571-2583. doi: 10.1002/stem.1239