Neuronal influence behind the central nervous system regulation of the immune cells

Frontiers in Integrative Neuroscience

Volumn 7, Issue SEP, 2013, Pages

  Chavarría, Anahí ^a   Cárdenas, Graciela ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

Author keywords

CD200; Central nervous system; Neuron microglia interaction; Neuron T cell interaction; Neuronal immune modulation; Neurotransmitters; Neurotrophins; Semaphorins

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; CADHERIN; CD200 ANTIGEN; CD22 ANTIGEN; CD47 ANTIGEN; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CX3CR1; FAS LIGAND; FRACTALKINE; INTERCELLULAR ADHESION MOLECULE 5; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 6; NERVE CELL ADHESION MOLECULE; NERVE GROWTH FACTOR; NEUROPEPTIDE; NEUROTRANSMITTER; NITRIC OXIDE; SEMAPHORIN; SEMAPHORIN 3A; SEMAPHORIN 7A; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE;

ALLERGIC ENCEPHALOMYELITIS; APOPTOSIS; ASTROCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CONTACT; CENTRAL NERVOUS SYSTEM; CYTOKINE PRODUCTION; GLIA CELL; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; LYMPHOCYTE PROLIFERATION; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROMODULATION; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VAGUS NERVE;

EID: 84885078550     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2013.00064     Document Type: Review

References (73)

1. Althaus, H. H., and Richter-Landsberg, C. (2000). Glial cells as targets and producers of neurotrophins. Int. Rev. Cytol. 197, 203-277. doi: 10.1016/S0074-7696(00)97005-0
2. Arredondo, L. R., Deng, C., Ratts, R. B., Lovett-Racke, A. E., Holtzman, D. M., and Racke, M. K. (2001). Role of nerve growth factor in experimental autoimmune encephalomyelitis. Eur. J. Immunol. 31, 625-633.
3. Bjurstöm, H., Wang, J., Ericsson, I., Bengtsson, M., Liu, Y., Kumar-Mendu, S., et al. (2008). GABA, a natural immunomodulator of T lymphocytes. J. Neuroimmunol. 205, 44-50. doi: 10.1016/j.jneuroim.2008.08.017
4. Cardona, A. E., Pioro, E. P., Sasse, M. E., Kostenko, V., Cardona, S. M., Dijkstra, I. M., et al. (2006). Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 9, 917-924. doi: 10.1038/nn1715
5. Carson, M. J., Doose, J. M., Melchior, B., Schmid, C. D., and Ploix, C. C. (2006). CNS immune privilege: hiding in plain sight. Immunol. Rev. 213, 48-65. doi: 10.1111/j.1600-065X.2006.00441.x
6. Chang, R. C., Hudson, P., Wilson, B., Haddon, L., and Hong, J. S. (2000a). Influence of neurons on lipopolysaccharide-stimulated production of nitric oxide and tumor necrosis factor-alpha by cultured glia. Brain Res. 853, 236-244. doi: 10.1016/S0006-8993(99)02255-6
7. Chang, R. C., Hudson, P., Wilson, B., Liu, B., Abel, H., Hemperly, J., et al. (2000b). Immune modulatory effects of neural cell adhesion molecules on lipopolysaccharide-induced nitric oxide production by cultured glia. Mol. Brain Res. 81, 197-201. doi: 10.1016/S0169-328X(00)00175-3
8. Chitnis, T., Imitola, J., Wang, Y., Elyaman, W., Chawla, P., Sharuk, M., et al. (2007). Elevated neuronal expression of CD200 protects Wlds mice from inflammation-mediated neurodegeneration. Am. J. Pathol. 170, 1695-1712. doi: 10.2353/ajpath.2007.060677
9. Choi, C., and Benveniste, E. N. (2004). Fas ligand/Fas system in the brain: regulator of immune and apoptotic responses. Brain Res. Brain Res. Rev. 44, 65-81. doi: 10.1016/j.brainresrev.2003.08.007
10. Cox, F. F., Carney, D., Miller, A. M., and Lynch, M. A. (2012). CD200 fusion protein decreases microglial activation in the hippocampus of aged rats. Brain Behav. Immun. 26, 789-796. doi: 10.1016/j.bbi.2011.10.004
11. Cragnolini, A. B., Volosin, M., Huang, Y., and Friedman, W. J. (2012). Nerve growth factor induces cell cycle arrest of astrocytes. Dev. Neurobiol. 72, 766-776. doi: 10.1002/dneu.20981
12. Czopik, A. K., Bynoe, M. S., Palm, N., Raine, C. S., and Medzhitov, R. (2006). Semaphorin 7A is a negative regulator of T cell responses. Immunity 24, 591-600. doi: 10.1016/j.immuni.2006.03.013
13. Delgado, M., and Ganea, D. (2003). Neuroprotective effect of vasoactive intestinal peptide (VIP) in a mouse model of Parkinson's disease by blocking microglial activation. FASEB J. 17, 944-946.
14. Delgado, M., Pozo, D., and Ganea, D. (2004). The significance of vasoactive intestinal peptide in immunomodulation. Pharmacol. Rev. 56, 249-290. doi: 10.1124/pr.56.2.7
15. Delgado, M., Varela, N., and Gonzalez-Rey, E. (2008). Vasoactive intestinal peptide protects against beta-amyloid induced neurodegeneration by inhibiting microglia activation at multiple levels. Glia 56, 1091-1103. doi: 10.1002/glia.20681
16. Färber, K., and Kettenmann. (2005). Physiology of microglial cells. Brain Res. Brain Res. Rev. 48, 133-143. doi: 10.1016/j.brainresrev.2004.12.003
17. Färber, K., Pannasch, U., and Kettenmann, H. (2005). Dopamine and noradrenaline control distinct functions in rodent microglial cells. Mol. Cell. Neurosci. 29, 128-138. doi: 10.1016/j.mcn.2005.01.003
18. Fernandez-Martin, A., Gonzalez-Rey, E., Chorny, A., Ganea, D., and Delgado, M. (2006). Vasoactive intestinal peptide induces regulatory T cells during experimental autoimmune encephalomyelitis. Eur. J. Immunol. 36, 318-326. doi: 10.1002/eji.200535430
19. Flügel, A., Schwaiger, F. W., Neumann, H., Medana, I., Willem, M., Wekerle, H., et al. (2000). Neuronal FasL induces cell death of encephalitogenic T lymphocytes. Brain Pathol. 10, 353-364. doi: 10.1111/j.1750-3639.2000.tb00267.x
20. Gründemann, C., Bauer, M., Schweier, O., von Oppen, N., Lässing, U., Saudan, P., et al. (2006). Cutting edge: identification of E-cadherin as a ligand for the murine killer cell lectin-like receptor G1. J. Immunol. 176, 1311-1315.
21. Guo, H., Tong, N., Turner, T., Epstein, L. G., McDermott, M. P., Kilgannon, P., et al. (2000). Release of the neuronal glycoprotein ICAM-5 in serum after hypoxic-ischemic injury. Ann. Neurol. 48, 590-602.
22. Gyoneva, S., and Traynelis, S. F. (2013). Norepinephrine modulates the motility of resting and activated microglia via different adrenergic receptors. J. Biol. Chem. 288, 15291-15302. doi: 10.1074/jbc.M113.458901
23. 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
24. Heyen, J. R., Ye, S., Finck, B. N., and Johnson, R. W. (2000). Interleukin (IL)-10 inhibits IL-6 production in microglia by preventing activation of NF-kappaB. Mol. Brain Res. 77, 138-147. doi: 10.1016/S0169-328X(00)00042-5
25. Hoek, R. M., Ruuls, S. R., Murphy, C. A., Wright, G. J., Goddard, R., Zurawski, S. M., et al. (2000). Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 290, 1768-1771. doi: 10.1126/science.290.5497.1768
26. 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
27. Issazadeh, S., Navikas, V., Schaub, M., Sayegh, M., and Khoury, S. (1998). Kinetics of expression of costimulatory molecules and their ligands in murine relapsing experimental autoimmune encephalomyelitis in vivo. J. Immunol. 161, 1104-1112.
28. Ito, M., Maruyama, T., Saito, N., Koganei, S., Yamamoto, K., and Matsumoto, N. (2006). Killer cell lectin-like receptor G1 binds three members of the classical cadherin family to inhibit NK cell cytotoxicity. J. Exp. Med. 203, 289-295. doi: 10.1084/jem.20051986
29. Koning, N., Bö, L., Hoek, R. M., and Huitinga, I. (2007). Downregulation of macrophage inhibitory molecules in multiple sclerosis lesions. Ann. Neurol. 62, 504-514. doi: 10.1002/ana.21220
30. Koning, N., Swaab, D. F., Hoek, R. M., and Huitinga, I. (2009). Distribution of the immune inhibitory molecules CD200 and CD200R in the normal central nervous system and multiple sclerosis lesions suggests neuron-glia and glia-glia interactions. J. Neuropathol. Exp. Neurol. 68, 159-167. doi: 10.1097/NEN.0b013e3181964113
31. Krushel, L. A., Sporns, O., Cunningham, B. A., Crossin, K. L., and Edelman, G. M. (1995). Neural cell adhesion molecule (N-CAM) inhibits astrocyte proliferation after injury to different regions of the adult rat brain. Proc. Natl. Acad. Sci. U.S.A. 92, 4323-4327. doi: 10.1073/pnas.92.10.4323
32. Krushel, L. A., Tai, M. H., Cunningham, B. A., Edelman, G. M., and Crossin, K. L. (1998). Neural cell adhesion molecule (N-CAM) domains and intracellular signaling pathways involved in the inhibition of astrocyte proliferation. Proc. Natl. Acad. Sci. U.S.A. 95, 2592-2596. doi: 10.1073/pnas.95.5.2592
33. Kuhn, S. A., van Landeghem, F. K., Zacharias, R., Färber, K., Rappert, A., Pavlovic, S., et al. (2004). Microglia express GABA(B) receptors to modulate interleukin release. Mol. Cell. Neurosci. 25, 312-322. doi: 10.1016/j.mcn.2003.10.023
34. Lamy, L., Foussat, A., Brown, E. J., Bornstein, P., Ticchioni, M., and Bernard, A. (2007). Interactions between CD47 and thrombospondin reduce inflammation. J. Immunol. 178, 5930-5939.
35. Laudiero, L. B., Aloe, L., Levi-Montalcini, R., Buttinelli, C., Schilter, D., Gillessen, S., et al. (1992). Multiple sclerosis patients express increased levels of beta-nerve growth factor in cerebrospinal fluid. Neurosci. Lett. 147, 9-12. doi: 10.1016/0304-3940(92)90762-V
36. Lepelletier, Y., Moura, I. C., Hadj-Slimane, R., Renand, A., Fiorentino, S., Baude, C., et al. (2006). Immunosuppressive role of semaphoring-3A on T cell proliferation is mediated by inhibition of actin cytoskeleton reorganization. Eur. J. Immunol. 36, 1782-1793. doi: 10.1002/eji.200535601
37. Lindsberg, P. J., Launes, J., Tian, L., Välimaa, H., Subramanian, V., Sirén, J., et al. (2002). Release of soluble ICAM-5, a neuronal adhesion molecule, in acute encephalitis. Neurology 58, 446-451. doi: 10.1212/WNL.58.3.446
38. Liu, Y., Teige, I., Birnir, B., and Issazadeh-Navikas, S. (2006). Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat. Med. 12, 518-525. doi: 10.1038/nm1402
39. Lyons, A., McQuillan, K., Deighan, B. F., O'Reilly, J. A., Downer, E. J., Murphy, A. C., et al. (2009). Decreased neuronal CD200 expression in IL-4 deficient mice result in increased neuroinflammation in response to lipopolysaccharide. Brain Behav. Immun. 23, 1020-1027. doi: 10.1016/j.bbi.2009.05.060
40. Majed, H. H., Chandran, S., Niclou, S. P., Nicholas, R. S., Wilkins, A., Wing, M. G., et al. (2006). A novel role for Sema-3A in neuroprotection from injury mediated by activated microglia. J. Neurosci. 26, 1730-1738. doi: 10.1523/JNEUROSCI.0702-05.2006
41. Medana, I., Li, Z., Flügel, A., Tschopp, J., Wekerle, H., and Neumann, H. (2001). Fas ligand (CD95L) protects neurons against perforin-mediated T lymphocyte cytotoxicity. J. Immunol. 167, 674-681.
42. Mizuno, T., Kawanokuchi, J., Numata, K., and Suzumura, A. (2003). Production and neuroprotective functions of fractalkine in the central nervous system. Brain Res. 979, 65-70. doi: 10.1016/S0006-8993(03)02867-1
43. Mizuno, T., Yoshihara, Y., Kagamiyama, H., Ohsawa, K., Imai, Y., Kohsaka, S., et al. (1999). Neuronal adhesion molecule telencephalin induces rapid cell spreading of microglia. Brain Res. 849, 58-66. doi: 10.1016/S0006-8993(99)01984-8
44. Moretti, S., Procopio, A., Lazzarini, R., Rippo, M. R., Testa, R., Marra, M., et al. (2008). Semaphorin3A signaling controls Fas (CD95)-mediated apoptosis by promoting Fas translocation into lipid rafts. Blood 111, 2290-2299. doi: 10.1182/blood-2007-06-096529
45. Mott, R. T., Ait-Ghezala, G., Town, T., Mori, T., Vendrame, M., Zeng, J., et al. (2004). Neuronal expression of CD22: novel mechanism for inhibiting microglial proinflammatory cytokine production. Glia 46, 369-379. doi: 10.1002/glia.20009
46. Neumann, H., Misgeld, T., Matsumuro, K., and Wekerle, H. (1998). Neurotrophins inhibit major histocompatibility class II inducibility of microglia: involvement of the p75 neurotrophin receptor. Proc. Natl. Acad. Sci. U.S.A. 95, 5779-5784. doi: 10.1073/pnas.95.10.5779
47. 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
48. Pratt, B. M., and McPherson, J. M. (1997). TGF-beta in the central nervous system: potential roles in ischemic injury and neurodegenerative diseases. Cytokine Growth Factor Rev. 8, 267-292. doi: 10.1016/S1359-6101(97)00018-X
49. Reinhold, M. I., Lindberg, F. P., Plas, D., Reynolds, S., Peters, M. G., and Brown, E. J. (1995). In vivo expression of alternatively spliced forms of integrin-associated protein (CD47). J. Cell Sci. 108, 3419-3425.
50. Rijkers, E. S., de Ruiter, T., Baridi, A., Veninga, H., Hoek, R. M., and Meyaard, L. (2008). The inhibitory CD200R is differentially expressed on human and mouse T and B lymphocytes. Mol. Immunol. 45, 1126-1135. doi: 10.1016/j.molimm.2007.07.013
51. Roney, K., Holl, E., and Ting, J. (2013). Immune plexins and semaphorins: old proteins, new immune functions. Protein Cell 4, 17-26. doi: 10.1007/s13238-012-2108-4
52. Saenz, B., Pérez-H, J., Chavarría, A. (2010). Regulatory T cells in central nervous system: in health and disease. Cent. Nerv. Syst. Agents Med. Chem. 10, 326-336. doi: 10.2174/187152410793429674
53. Sawada, M., Suzumura, A., Hosoya, H., Marunouchi, T., and Nagatsu, T. (1999). Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia. J. Neurochem. 72, 1466-1471. doi: 10.1046/j.1471-4159.1999.721466.x
54. Simonini, M. V., Polak, P. E., Sharp, A., McGuire, S., Galea, E., and Feinstein, D. L. (2010). Increasing CNS noradrenaline reduces EAE severity. J. Neuroimmune Pharmacol. 5, 252-259. doi: 10.1007/s11481-009-9182-2
55. Smith, R. E., Patel, V., Seatter, S. D., Deehan, M. R., Brown, M. H., Brooke, G. P., et al. (2003). A novel MyD-1 (SIRP-1alpha) signaling pathway that inhibits LPS-induced TNFalpha production by monocytes. Blood 102, 2532-2540. doi: 10.1182/blood-2002-11-3596
56. Sporns, O., Edelman, G. M., and Crossin, K. L. (1995). The neural cell adhesion molecule (N-CAM) inhibits proliferation in primary cultures of rat astrocytes. Proc. Natl. Acad. Sci. U.S.A. 92, 542-546. doi: 10.1073/pnas.92.2.542
57. Strle, K., Zhou, J., Shen, W. H., Broussard, S. R., Johnson, R. W., Freund, G. G., et al. (2001). Interleukin-10 in the brain. Crit. Rev. Immunol. 21, 427-449. doi: 10.1615/CritRevImmunol.v21.i5.20
58. Suzumura, A., Sawada, M., Yamamoto, H., Marunouchi, T. (1993). Transforming growth factor-beta suppresses activation and proliferation of microglia in vitro. J. Immunol. 151, 2150-2218.
59. Szelényi, J. (2001). Cytokines and the central nervous system. Brain Res. Bull. 54, 329-338. doi: 10.1016/S0361-9230(01)00428-2
60. Szelényi, J., and Vizi, E. S. (2007). The catecholamine cytokine balance: interaction between the brain and the immune system. Ann. N.Y. Acad. Sci. 1113, 311-324. doi: 10.1196/annals.1391.026
61. Tabakman, R., Lecht, S., Sephanova, S., Arien-Zaray, H., and Lazarovici, P. (2004). Interactions between the cells of the immune and nervous system: neurotrophins as neuroprotection mediators in CNS injury. Prog. Brain Res. 146, 387-401. doi: 10.1016/S0079-6123(03)46024-X
62. Tan, J., Town, T., and Mullan, M. (2000). CD45 inhibits CD40L-induced microglial activation via negative regulation of the Src/p44/42 MAPK pathway. J. Biol. Chem. 275, 37224-37231. doi: 10.1074/jbc.M002006200
63. Tian, L., Kilgannon, P., Yoshihara, Y., Mori, K., Gallatin, W. M., Carpén, O., et al. (2000). Binding of T lymphocytes to hippocampal neurons through ICAM-5 (telencephalin) and characterization of its interaction with the leukocyte integrin CD11a/CD18. Eur. J. Immunol. 30, 810-818.
64. Tian, L., Lappalainen, J., Autero, M., Hänninen, S., Rauvala, H., and Gahmberg, C. G. (2008). Shedded neuronal ICAM-5 suppresses T-cell activation. Blood 111, 3615-3625. doi: 10.1182/blood-2007-09-111179
65. Tian, L., Rauvala, H., and Gahmberg, C. G. (2009). Neuronal regulation of immune responses in the central nervous system. Trends Immunol. 30, 91-99. doi: 10.1016/j.it.2008.11.002
66. Tzeng, S. F., and Huang, H. Y. (2003). Downregulation of inducible nitric oxide synthetase by neurotrophin-3 in microglia. J. Cell Biochem. 90, 227-233. doi: 10.1002/jcb.10658
67. Tzeng, S. F., Huang, H. Y., Lee, T. I., and Jwo, J. K. (2005). Inhibition of lipopolysaccharide-induced microglial activation by preexposure to neurotrophin-3. J. Neurosci. Res. 81, 666-676. doi: 10.1002/jnr.20586
68. Walker, D. G., Dalsing-Hernandez, J. E., Campbell, N. A., and Lue, L. F. (2009). Decreased expression of CD200 and CD200 receptor in Alzheimer's disease: a potential mechanism leading to chronic inflammation. Exp. Neurol. 215, 5-19. doi: 10.1016/j.expneurol.2008.09.003
69. Wei, R., and Jonakait, G. M. (1999). Neurotrophins and the anti-inflammatory agents interleukin 4(IL-4), IL-10, IL-11 and transforming growth factor-beta1 (TGF-beta1) down-regulate T cell costimulatory molecules B7 and CD40 on cultured rat microglia. J. Neuroimmunol. 95, 8-18. doi: 10.1016/S0165-5728(98)00248-3
70. Zhang, S., Cherwinski, H., Sedgwick, J. D., and Phillips, J. H. (2004). Molecular mechanisms of CD200 inhibition of mast cell activation. J. Immunol. 173, 6786-6793.
71. Zhang, S., Wang, X. J., Tian, L. P., Pan, J., Lu, G. Q., Zhang, Y. J., et al. (2011). CD200-CD200R dysfunction exacerbates microglial activation and dopaminergic neurodegeneration in a rat model of Parkinson's disease. J. Neuroinflammation 8, 154. doi: 10.1186/1742-2094-8-154
72. Zhu, Y., Hou, H., Nikolic, W. V., Ehrhart, J., Rrapo, E., Bickford, P., et al. (2008). CD45RB is a novel molecular therapeutic target to inhibit Abeta peptide-induced microglial MAPK activation. PLoS ONE 3:e2135. doi: 10.1371/journal.pone.0002135
73. Zujovic, V., Benavides, J., Vigé, X., Carter, C., and Taupin, V. (2000). Fractalkine modulates TNF-alpha secretion and neurotoxicity induced by microglial activation. Glia 29, 305-315.