Fractalkine regulation of microglial physiology and consequences on the brain and behavior

Frontiers in Cellular Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Paolicelli, Rosa Chiara ^a   Bisht, Kanchan ^b,c   Tremblay, Marie Ève ^b,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Université Laval   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

Behavior; Development; Fractalkine; Microglia; Neurogenesis; Neurons; Synapses

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; G PROTEIN COUPLED RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

BEHAVIOR; BRAIN; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; MICROGLIA; MOLECULAR INTERACTION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 84901340197     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00129     Document Type: Review

References (72)

1. Al-Aoukaty, A., Rolstad, B., Giaid, A., and Maghazachi, A. A. (1998). MIP-3alpha, MIP-3beta and fractalkine induce the locomotion and the mobilization of intracellular calcium and activate the heterotrimeric G proteins in human natural killer cells. Immunology 95, 618-624. doi: 10.1046/j.1365-2567.1998.00603.x
2. Allen, S. J., Crown, S. E., and Handel, T. M. (2007). Chemokine: receptor structure, interactions and antagonism. Annu. Rev. Immunol. 25, 787-820. doi: 10.1146/annurev.immunol.24.021605.090529
3. Arnoux, I., Hoshiko, M., Sanz Diez, A., and Audinat, E. (2014). Paradoxical effects of minocycline in the developing mouse somatosensory cortex. Glia 62, 399-410. doi: 10.1002/glia.22612
4. 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
5. Bazan, J. F., Bacon, K. B., Hardiman, G., Wang, W., Soo, K., Rossi, D., et al. (1997). A new class of membrane-bound chemokine with a CX3C motif. Nature 385, 640-644. doi: 10.1038/385640a0
6. Bertollini, C., Ragozzino, D., Gross, C., Limatola, C., and Eusebi, F. (2006). Fractalkine/CX3CL1 depresses central synaptic transmission in mouse hippocampal slices. Neuropharmacology 51, 816-821. doi: 10.1016/j.neuropharm.2006.05.027
7. Chandrasekar, B., Mummidi, S., Perla, R. P., Bysani, S., Dulin, N. O., Liu, F., et al. (2003). Fractalkine (CX3CL1) stimulated by nuclear factor kappaB (NF-kappaB)-dependent inflammatory signals induces aortic smooth muscle cell proliferation through an autocrine pathway. Biochem. J. 373, 547-558. doi: 10.1042/bj20030207
8. Combadiere, C., Ahuja, S. K., and Murphy, P. M. (1995). Cloning, chromosomal localization and RNA expression of a human beta chemokine receptor-like gene. DNA Cell Biol. 14, 673-680. doi: 10.1089/dna.1995.14.673
9. Combadiere, C., Salzwedel, K., Smith, E. D., Tiffany, H. L., Berger, E. A., and Murphy, P. M. (1998). Identification of CX3CR1. A chemotactic receptor for the human CX3C chemokine fractalkine and a fusion coreceptor for HIV-1. J. Biol. Chem. 273, 23799-23804. doi: 10.1074/jbc.273.37.23799
10. Comerford, I., and McColl, S. R. (2011). Mini-review series: focus on chemokines. Immunol. Cell Biol. 89, 183-184. doi: 10.1038/icb.2010.164
11. Crawley, J. N. (2008). Behavioral phenotyping strategies for mutant mice. Neuron 57, 809-818. doi: 10.1016/j.neuron.2008.03.001
12. Cunningham, C. L., Martinez-Cerdeno, 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
13. Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., et al. (2005). ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752-758. doi: 10.1038/nn1472
14. Garton, K. J., Gough, P. J., Blobel, C. P., Murphy, G., Greaves, D. R., Dempsey, P. J., et al. (2001). Tumor necrosis factor-alpha-converting enzyme (ADAM17) mediates the cleavage and shedding of fractalkine (CX3CL1). J. Biol. Chem. 276, 37993-38001. doi: 10.1074/jbc.M106434200
15. 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
16. 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
17. Heinisch, S., and Kirby, L. G. (2009). Fractalkine/CX3CL1 enhances GABA synaptic activity at serotonin neurons in the rat dorsal raphe nucleus. Neuroscience 164, 1210-1223. doi: 10.1016/j.neuroscience.2009.08.075
18. Hirasawa, T., Ohsawa, K., Imai, Y., Ondo, Y., Akazawa, C., Uchino, S., et al. (2005). Visualization of microglia in living tissues using Iba1-EGFP transgenic mice. J. Neurosci. Res. 81, 357-362. doi: 10.1002/jnr.20480
19. 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
20. Hsia, A. Y., Malenka, R. C., and Nicoll, R. A. (1998). Development of excitatory circuitry in the hippocampus. J. Neurophysiol. 79, 2013-2024.
21. Hughes, P. M., Botham, M. S., Frentzel, S., Mir, A., and Perry, V. H. (2002). Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, during acute and chronic inflammation in the rodent CNS. Glia 37, 314-327. doi: 10.1002/glia.10037.abs
22. Hulshof, S., van Haastert, E. S., Kuipers, H. F., van den Elsen, P. J., De Groot, C. J., van der Valk, P., et al. (2003). CX3CL1 and CX3CR1 expression in human brain tissue: noninflammatory control versus multiple sclerosis. J. Neuropathol. Exp. Neurol. 62, 899-907.
23. Imai, T., Hieshima, K., Haskell, C., Baba, M., Nagira, M., Nishimura, M., et al. (1997). Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell 91, 521-530. doi: 10.1016/s0092-8674(00)80438-9
24. Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., et al. (2000). Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20, 4106-4114. doi: 10.1128/mcb.20.11.4106-4114.2000
25. Kettenmann, H., Kirchhoff, F., and Verkhratsky, A. (2013). Microglia: new roles for the synaptic stripper. Neuron 77, 10-18. doi: 10.1016/j.neuron.2012.12.023
26. 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
27. 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
28. Li, Y., Du, X. F., Liu, C. S., Wen, Z. L., and Du, J. L. (2012). Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23, 1189-1202. doi: 10.1016/j.devcel.2012.10.027
29. Liang, K. J., Lee, J. E., Wang, Y. D., Ma, W., Fontainhas, A. M., Fariss, R. N., et al. (2009). Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest. Ophthalmol. Vis. Sci. 50, 4444-4451. doi: 10.1167/iovs.08-3357
30. Linnartz, B., Kopatz, J., Tenner, A. J., and Neumann, H. (2012). Sialic acid on the neuronal glycocalyx prevents complement C1 binding and complement receptor-3-mediated removal by microglia. J. Neurosci. 32, 946-952. doi: 10.1523/jneurosci.3830-11.2012
31. Maciejewski-Lenoir, D., Chen, S., Feng, L., Maki, R., and Bacon, K. B. (1999). Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. J. Immunol. 163, 1628-1635.
32. Maggi, L., Scianni, M., Branchi, I., D'Andrea, I., Lauro, C., and Limatola, C. (2011). CX(3)CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment. Front. Cell Neurosci. 5:22. doi: 10.3389/fncel.2011.00022
33. Maggi, L., Trettel, F., Scianni, M., Bertollini, C., Eusebi, F., Fredholm, B. B., et al. (2009). LTP impairment by fractalkine/CX3CL1 in mouse hippocampus is mediated through the activity of adenosine receptor type 3 (A3R). J. Neuroimmunol. 215, 36-42. doi: 10.1016/j.jneuroim.2009.07.016
34. Marin-Teva, J. L., Dusart, I., Colin, C., Gervais, A., van Rooijen, N., and Mallat, M. (2004). Microglia promote the death of developing Purkinje cells. Neuron 41, 535-547. doi: 10.1016/s0896-6273(04)00069-8
35. Mizutani, M., Pino, P. A., Saederup, N., Charo, I. F., Ransohoff, R. M., and Cardona, A. E. (2012). The fractalkine receptor but not CCR2 is present on microglia from embryonic development throughout adulthood. J. Immunol. 188, 29-36. doi: 10.4049/jimmunol.1100421
36. Mody, M., Cao, Y., Cui, Z., Tay, K. Y., Shyong, A., Shimizu, E., et al. (2001). Genome-wide gene expression profiles of the developing mouse hippocampus. Proc. Natl. Acad. Sci. U S A 98, 8862-8867. doi: 10.1073/pnas.141244998
37. Mosher, K. I., Andres, R. H., Fukuhara, T., Bieri, G., Hasegawa-Moriyama, M., He, Y., et al. (2012). Neural progenitor cells regulate microglia functions and activity. Nat. Neurosci. 15, 1485-1487. doi: 10.1038/nn.3233
38. 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
39. Nishiyori, A., Minami, M., Ohtani, Y., Takami, S., Yamamoto, J., Kawaguchi, N., et al. (1998). Localization of fractalkine and CX3CR1 mRNAs in rat brain: does fractalkine play a role in signaling from neuron to microglia? FEBS Lett. 429, 167-172. doi: 10.1016/s0014-5793(98)00583-3
40. Pan, Y., Lloyd, C., Zhou, H., Dolich, S., Deeds, J., Gonzalo, J. A., et al. (1997). Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature 387, 611-617. doi: 10.1038/42491
41. Pan, X. D., Zhu, Y. G., Lin, N., Zhang, J., Ye, Q. Y., Huang, H. P., et al. (2011). Microglial phagocytosis induced by fibrillar beta-amyloid is attenuated by oligomeric beta-amyloid: implications for Alzheimer's disease. Mol. Neurodegener. 6:45. doi: 10.1186/1750-1326-6-45
42. Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., et al. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science 333, 1456-1458. doi: 10.1126/science.1202529
43. 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
44. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., and Bessis, A. (2012). Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. U S A 109, E197-E205. doi: 10.1073/pnas.1111098109
45. Piccinin, S., Di Angelantonio, S., Piccioni, A., Volpini, R., Cristalli, G., Fredholm, B. B., et al. (2010). CX3CL1-induced modulation at CA1 synapses reveals multiple mechanisms of EPSC modulation involving adenosine receptor subtypes. J. Neuroimmunol. 224, 85-92. doi: 10.1016/j.jneuroim.2010.05.012
46. Proudfoot, A. E. I., India, S., Hamel, D., and Handel, T. M. (2010). "Structural aspects of chemokines and their interactions with receptors and glycosaminoglycans, " in Chemokine Receptors as Drug Targets (Weinheim, Germany: Wiley-VCH Verlag GmbH and Co. KGaA), 1-32.
47. Ragozzino, D., Di Angelantonio, S., Trettel, F., Bertollini, C., Maggi, L., Gross, C., et al. (2006). Chemokine fractalkine/CX3CL1 negatively modulates active glutamatergic synapses in rat hippocampal neurons. J. Neurosci. 26, 10488-10498. doi: 10.1523/jneurosci.3192-06.2006
48. 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
49. Rossi, D. L., Hardiman, G., Copeland, N. G., Gilbert, D. J., Jenkins, N., Zlotnik, A., et al. (1998). Cloning and characterization of a new type of mouse chemokine. Genomics 47, 163-170. doi: 10.1006/geno.1997.5058
50. Rossi, D., and Zlotnik, A. (2000). The biology of chemokines and their receptors. Annu. Rev. Immunol. 18, 217-242. doi: 10.1146/annurev.immunol.18.1.217
51. Ruchaya, P. J., Paton, J. F., Murphy, D., and Yao, S. T. (2012). A cardiovascular role for fractalkine and its cognate receptor, CX3CR1, in the rat nucleus of the solitary tract. Neuroscience 209, 119-127. doi: 10.1016/j.neuroscience.2012.02.018
52. 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
53. Schwaeble, W. J., Stover, C. M., Schall, T. J., Dairaghi, D. J., Trinder, P. K., Linington, C., et al. (1998). Neuronal expression of fractalkine in the presence and absence of inflammation. FEBS Lett. 439, 203-207. doi: 10.1016/s0014-5793(98)01384-2
54. Scianni, M., Antonilli, L., Chece, G., Cristalli, G., Di Castro, M. A., Limatola, C., et al. (2013). Fractalkine (CX3CL1) enhances hippocampal N-methyl-D-aspartate receptor (NMDAR) function via D-serine and adenosine receptor type A2 (A2AR) activity. J. Neuroinflammation 10:108. doi: 10.1186/1742-2094-10-108
55. Shigemoto-Mogami, Y., Hoshikawa, K., Goldman, J. E., Sekino, Y., and Sato, K. (2014). Microglia enhance neurogenesis and oligodendrogenesis in the early postnatal subventricular zone. J. Neurosci. 34, 2231-2243. doi: 10.1523/jneurosci.1619-13.2014
56. 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
57. Sierra, A., Encinas, J. M., Deudero, J. J., Chancey, J. H., Enikolopov, G., Overstreet-Wadiche, L. S., et al. (2010). Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7, 483-495. doi: 10.1016/j.stem.2010.08.014
58. Sousa, N., Almeida, O. F., and Wotjak, C. T. (2006). A hitchhiker's guide to behavioral analysis in laboratory rodents. Genes Brain Behav. 5(Suppl. 2), 5-24. doi: 10.1111/j.1601-183x.2006.00228.x
59. Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., et al. (2007). The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178. doi: 10.1016/j.cell.2007.10.036
60. Sunnemark, D., Eltayeb, S., Nilsson, M., Wallstrom, E., Lassmann, H., Olsson, T., et al. (2005). CX3CL1 (fractalkine) and CX3CR1 expression in myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis: kinetics and cellular origin. J. Neuroinflammation 2:17. doi: 10.1186/1742-2094-2-17
61. Tarozzo, G., Bortolazzi, S., Crochemore, C., Chen, S. C., Lira, A. S., Abrams, J. S., et al. (2003). Fractalkine protein localization and gene expression in mouse brain. J. Neurosci. Res. 73, 81-88. doi: 10.1002/jnr.10645
62. Tremblay, M. E. (2011). The role of microglia at synapses in the healthy CNS: novel insights from recent imaging studies. Neuron Glia Biol. 7, 67-76. doi: 10.1017/s1740925x12000038
63. Tremblay, M. E., Lowery, R. L., and Majewska, A. K. (2010). Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 8:e1000527. doi: 10.1371/journal.pbio.1000527
64. Tremblay, M. E., Zettel, M. L., Ison, J. R., Allen, P. D., and Majewska, A. K. (2012). Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices. Glia 60, 541-558. doi: 10.1002/glia.22287
65. 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
66. Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S., and Nabekura, J. (2009). Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29, 3974-3980. doi: 10.1523/jneurosci.4363-08.2009
67. Wakselman, S., Bechade, C., Roumier, A., Bernard, D., Triller, A., and Bessis, A. (2008). Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. J. Neurosci. 28, 8138-8143. doi: 10.1523/jneurosci.1006-08.2008
68. Wolf, Y., Yona, S., Kim, K. W., and Jung, S. (2013). Microglia, seen from the CX3CR1 angle. Front. Cell Neurosci. 7:26. doi: 10.3389/fncel.2013.00026
69. 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
70. Zhang, M., Xu, G., Liu, W., Ni, Y., and Zhou, W. (2012). Role of fractalkine/CX3CR1 interaction in light-induced photoreceptor degeneration through regulating retinal microglial activation and migration. PLoS One 7:e35446. doi: 10.1371/journal.pone.0035446
71. Zlotnik, A., and Yoshie, O. (2000). Chemokines: a new classification system and their role in immunity. Immunity 12, 121-127. doi: 10.1016/S1074-7613(00)80165-X
72. Zlotnik, A., and Yoshie, O. (2012). The chemokine superfamily revisited. Immunity 36, 705-716. doi: 10.1016/j.immuni.2012.05.008