Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2015, Article ID 689404, 8 pages
http://dx.doi.org/10.1155/2015/689404
Review Article

Fractalkine Signaling and Microglia Functions in the Developing Brain

1Institut National de la Santé et de la Recherche Médicale (INSERM), U1128, 75006 Paris, France
2Université Paris Descartes, 75006 Paris, France
3Focus Program Translational Neuroscience (FTN) and Institute for Microscopic Anatomy and Neurobiology, Johannes Gutenberg University Mainz, Hanns-Dieter-Hüsch-Weg 19, 55128 Mainz, Germany

Received 23 February 2015; Accepted 29 April 2015

Academic Editor: Tomas Bellamy

Copyright © 2015 Isabelle Arnoux and Etienne Audinat. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M.-È. Tremblay, B. Stevens, A. Sierra, H. Wake, A. Bessis, and A. Nimmerjahn, “The role of microglia in the healthy brain,” The Journal of Neuroscience, vol. 31, no. 45, pp. 16064–16069, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Kettenmann, F. Kirchhoff, and A. Verkhratsky, “Microglia: new roles for the synaptic stripper,” Neuron, vol. 77, no. 1, pp. 10–18, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. M. W. Salter and S. Beggs, “Sublime microglia: expanding roles for the guardians of the CNS,” Cell, vol. 158, pp. 15–24, 2014. View at Publisher · View at Google Scholar
  4. K. Kierdorf, D. Erny, T. Goldmann et al., “Microglia emerge from erythromyeloid precursors via Pu.1-and Irf8-dependent pathways,” Nature Neuroscience, vol. 16, no. 3, pp. 273–280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. F. Ginhoux, M. Greter, M. Leboeuf et al., “Fate mapping analysis reveals that adult microglia derive from primitive macrophages,” Science, vol. 330, no. 6005, pp. 841–845, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Schulz, E. G. Perdiguero, L. Chorro et al., “A lineage of myeloid cells independent of Myb and hematopoietic stem cells,” Science, vol. 335, no. 6077, pp. 86–90, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. U.-K. Hanisch and H. Kettenmann, “Microglia: active sensor and versatile effector cells in the normal and pathologic brain,” Nature Neuroscience, vol. 10, no. 11, pp. 1387–1394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. R. M. Ransohoff and V. H. Perry, “Microglial physiology: unique stimuli, specialized responses,” Annual Review of Immunology, vol. 27, pp. 119–145, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. G. P. Morris, I. A. Clark, R. Zinn, and B. Vissel, “Microglia: a new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research,” Neurobiology of Learning and Memory, vol. 105, pp. 40–53, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. U. B. Eyo and M. E. Dailey, “Microglia: key elements in neural development, plasticity, and pathology,” Journal of Neuroimmune Pharmacology, vol. 8, no. 3, pp. 494–509, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Wolf, S. Yona, K.-W. Kim, and S. Jung, “Microglia, seen from the CX3CR1 angle,” Frontiers in Cellular Neuroscience, vol. 7, article 26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. G. K. Sheridan and K. J. Murphy, “Neuron-glia crosstalk in health and disease: fractalkine and CX3CR1 take centre stage,” Open Biology, vol. 3, no. 1, Article ID 130181, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. R. C. Paolicelli, K. Bisht, and M.-È. Tremblay, “Fractalkine regulation of microglial physiology and consequences on the brain and behavior,” Frontiers in Cellular Neuroscience, vol. 8, article 129, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Limatola and R. M. Ransohoff, “Modulating neurotoxicity through CX3CL1/CX3CR1 signaling,” Frontiers in Cellular Neuroscience, vol. 8, article 229, 2014. View at Publisher · View at Google Scholar
  15. K. Biber, H. Neumann, K. Inoue, and H. W. G. M. Boddeke, “Neuronal ‘On’ and ‘Off’ signals control microglia,” Trends in Neurosciences, vol. 30, no. 11, pp. 596–602, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. A. E. Cardona, E. P. Pioro, M. E. Sasse et al., “Control of microglial neurotoxicity by the fractalkine receptor,” Nature Neuroscience, vol. 9, no. 7, pp. 917–924, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. J. M. Morganti, K. R. Nash, B. A. Grimmig et al., “The soluble isoform of CX3CL1 is necessary for neuroprotection in a mouse model of Parkinson's disease,” Journal of Neuroscience, vol. 32, no. 42, pp. 14592–14601, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Rosito, C. Lauro, G. Chece et al., “Trasmembrane chemokines CX3CL1 and CXCL16 drive interplay between neurons, microglia and astrocytes to counteract pMCAO and excitotoxic neuronal death,” Frontiers in Cellular Neuroscience, vol. 8, article 193, 2014. View at Publisher · View at Google Scholar
  19. S.-H. Cho, B. Sun, Y. Zhou et al., “CX3CR1 protein signaling modulates microglial activation and protects against plaque-independent cognitive deficits in a mouse model of Alzheimer disease,” The Journal of Biological Chemistry, vol. 286, no. 37, pp. 32713–32722, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Lee, N. H. Varvel, M. E. Konerth et al., “CX3CR1 deficiency alters microglial activation and reduces beta-amyloid deposition in two Alzheimer's disease mouse models,” American Journal of Pathology, vol. 177, no. 5, pp. 2549–2562, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Lee, G. Xu, T. R. Jay et al., “Opposing effects of membrane-anchored CX3CL1 on amyloid and tau pathologies via the p38 MAPK pathway,” The Journal of Neuroscience, vol. 34, no. 37, pp. 12538–12546, 2014. View at Publisher · View at Google Scholar
  22. K. R. Nash, D. C. Lee, J. B. Hunt et al., “Fractalkine overexpression suppresses tau pathology in a mouse model of tauopathy,” Neurobiology of Aging, vol. 34, no. 6, pp. 1540–1548, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. Á. Dénes, S. Ferenczi, J. Halász, Z. Környei, and K. J. Kovács, “Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse,” Journal of Cerebral Blood Flow and Metabolism, vol. 28, no. 10, pp. 1707–1721, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. S. G. Soriano, L. S. Amaravadi, Y. F. Wang et al., “Mice deficient in fractalkine are less susceptible to cerebral ischemia-reperfusion injury,” Journal of Neuroimmunology, vol. 125, no. 1-2, pp. 59–65, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. Z. Tang, Y. Gan, Q. Liu, J. Yin, J. Shi, and F. Shi, “CX3CR1 deficiency suppresses activation and neurotoxicity of microglia/macrophage in experimental ischemic stroke,” Journal of Neuroinflammation, vol. 11, no. 1, article 26, 2014. View at Publisher · View at Google Scholar
  26. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, “Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo,” Science, vol. 308, no. 5726, pp. 1314–1318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Davalos, J. Grutzendler, G. Yang et al., “ATP mediates rapid microglial response to local brain injury in vivo,” Nature Neuroscience, vol. 8, no. 6, pp. 752–758, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Wake, A. J. Moorhouse, S. Jinno, S. Kohsaka, and J. Nabekura, “Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals,” The Journal of Neuroscience, vol. 29, no. 13, pp. 3974–3980, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. M.-E. Tremblay, R. L. Lowery, and A. K. Majewska, “Microglial interactions with synapses are modulated by visual experience,” PLoS Biology, vol. 8, no. 11, Article ID e1000527, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Dissing-Olesen, J. M. LeDue, R. L. Rungta, J. K. Hefendehl, H. B. Choi, and B. A. MacVicar, “Activation of neuronal NMDA receptors triggers transient ATP-mediated microglial process outgrowth,” Journal of Neuroscience, vol. 34, no. 32, pp. 10511–10527, 2014. View at Publisher · View at Google Scholar
  31. U. B. Eyo, J. Peng, P. Swiatkowski, A. Mukherjee, A. Bispo, and L. Wu, “Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus,” Journal of Neuroscience, vol. 34, no. 32, pp. 10528–10540, 2014. View at Publisher · View at Google Scholar
  32. K. J. Liang, J. E. Lee, Y. D. Wang et al., “Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling,” Investigative Ophthalmology and Visual Science, vol. 50, no. 9, pp. 4444–4451, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Sierra, J. M. Encinas, J. J. P. Deudero et al., “Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis,” Cell Stem Cell, vol. 7, no. 4, pp. 483–495, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. A. D. Bachstetter, J. M. Morganti, J. Jernberg et al., “Fractalkine and CX3CR1 regulate hippocampal neurogenesis in adult and aged rats,” Neurobiology of Aging, vol. 32, no. 11, pp. 2030–2044, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. J. T. Rogers, J. M. Morganti, A. D. Bachstetter et al., “CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity,” Journal of Neuroscience, vol. 31, no. 45, pp. 16241–16250, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Ragozzino, S. Di Angelantonio, F. Trettel et al., “Chemokine fractalkine/CX3CL1 negatively modulates active glutamatergic synapses in rat hippocampal neurons,” Journal of Neuroscience, vol. 26, no. 41, pp. 10488–10498, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Scianni, L. Antonilli, G. Chece et al., “Fractalkine (CX3CL1) enhances hippocampal N-methyl-d-aspartate receptor (NMDAR) function via d-serine and adenosine receptor type A2 (A2AR) activity,” Journal of Neuroinflammation, vol. 10, article 108, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. G. K. Sheridan, A. Wdowicz, M. Pickering et al., “CX3CL1 is up-regulated in the rat hippocampus during memory-associated synaptic plasticity,” Frontiers in Cellular Neuroscience, vol. 8, p. 233, 2014. View at Publisher · View at Google Scholar
  39. L. Maggi, M. Scianni, I. Branchi, I. D'Andrea, C. Lauro, and C. Limatola, “CX3CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment,” Frontiers in Cellular Neuroscience, vol. 5, p. 22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Bessis, C. Béchade, D. Bernard, and A. Roumier, “Microglial control of neuronal death and synaptic properties,” Glia, vol. 55, no. 3, pp. 233–238, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Shigemoto-Mogami, K. Hoshikawa, J. E. Goldman, Y. Sekino, and K. Sato, “Microglia enhance neurogenesis and oligodendrogenesis in the early postnatal subventricular zone,” Journal of Neuroscience, vol. 34, no. 6, pp. 2231–2243, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. I. Arnoux, M. Hoshiko, A. S. Diez, and E. Audinat, “Paradoxical effects of minocycline in the developing mouse somatosensory cortex,” Glia, vol. 62, no. 3, pp. 399–410, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Ueno, Y. Fujita, T. Tanaka et al., “Layer V cortical neurons require microglial support for survival during postnatal development,” Nature Neuroscience, vol. 16, no. 5, pp. 543–551, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. I. Arnoux, M. Hoshiko, L. Mandavy, E. Avignone, N. Yamamoto, and E. Audinat, “Adaptive phenotype of microglial cells during the normal postnatal development of the somatosensory ‘Barrel’ cortex,” Glia, vol. 61, no. 10, pp. 1582–1594, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Squarzoni, G. Oller, G. Hoeffel et al., “Microglia modulate wiring of the embryonic forebrain,” Cell Reports, vol. 8, no. 5, pp. 1271–1279, 2014. View at Publisher · View at Google Scholar
  46. C. Rigato, R. Buckinx, H. Le-Corronc, J. M. Rigo, and P. Legendre, “Pattern of invasion of the embryonic mouse spinal cord by microglial cells at the time of the onset of functional neuronal networks,” Glia, vol. 59, no. 4, pp. 675–695, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. R. C. Paolicelli, G. Bolasco, F. Pagani et al., “Synaptic pruning by microglia is necessary for normal brain development,” Science, vol. 333, no. 6048, pp. 1456–1458, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Hoshiko, I. Arnoux, E. Avignone, N. Yamamoto, and E. Audinat, “Deficiency of the microglial receptor CX3CR1 impairs postnatal functional development of thalamocortical synapses in the barrel cortex,” Journal of Neuroscience, vol. 32, no. 43, pp. 15106–15111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. B. K. Fiske and P. C. Brunjes, “Microglial activation in the developing rat olfactory bulb,” Neuroscience, vol. 96, no. 4, pp. 807–815, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. S. E. Haynes, G. Hollopeter, G. Yang et al., “The P2Y12 receptor regulates microglial activation by extracellular nucleotides,” Nature Neuroscience, vol. 9, no. 12, pp. 1512–1519, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Avignone, L. Ulmann, F. Levavasseur, F. Rassendren, and E. Audinat, “Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling,” Journal of Neuroscience, vol. 28, no. 37, pp. 9133–9144, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Y. Hua and S. J. Smith, “Neural activity and the dynamics of central nervous system development,” Nature Neuroscience, vol. 7, no. 4, pp. 327–332, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. D. P. Schafer, E. K. Lehrman, A. G. Kautzman et al., “Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner,” Neuron, vol. 74, no. 4, pp. 691–705, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Zhan, R. C. Paolicelli, F. Sforazzini et al., “Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior,” Nature Neuroscience, vol. 17, no. 3, pp. 400–406, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. E. C. Beattie, D. Stellwagen, W. Morishita et al., “Control of synaptic strength by glial TNFα,” Science, vol. 295, no. 5563, pp. 2282–2285, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Stellwagen, E. C. Beattie, J. Y. Seo, and R. C. Malenka, “Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-α,” The Journal of Neuroscience, vol. 25, no. 12, pp. 3219–3228, 2005. View at Publisher · View at Google Scholar
  57. C. N. Parkhurst, G. Yang, I. Ninan et al., “Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor,” Cell, vol. 155, no. 7, pp. 1596–1609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Blank and M. Prinz, “Microglia as modulators of cognition and neuropsychiatric disorders,” Glia, vol. 61, no. 1, pp. 62–70, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. C. C. H. Petersen, “The functional organization of the barrel cortex,” Neuron, vol. 56, no. 2, pp. 339–355, 2007. View at Publisher · View at Google Scholar · View at Scopus