The neuroinflammatory response in ALS: The roles of microglia and T cells

Neurology Research International

Volumn 2012, Issue , 2012, Pages

  Lewis, Coral Ann ^a   Manning, John ^a   Rossi, Fabio ^b   Krieger, Charles ^a,c  

^a SIMON FRASER UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84866175097     PISSN: 20901852     EISSN: 20901860     Source Type: Journal    
DOI: 10.1155/2012/803701     Document Type: Article

References (62)

1. Strong M. J., Kesavapany S., Pant H. C., The pathobiology of amyotrophic lateral sclerosis: a proteinopathy? Journal of Neuropathology and Experimental Neurology 2005 64 8 649 664 2-s2.0-23844538993 (Pubitemid 41177106)
2. Neumann M., Sampathu D. M., Kwong L. K., Truax A. C., Micsenyi M. C., Chou T. T., Bruce J., Schuck T., Grossman M., Clark C. M., McCluskey L. F., Miller B. L., Masliah E., Mackenzie I. R., Feldman H., Feiden W., Kretzschmar H. A., Trojanowski J. Q., Lee V. M. Y., Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006 314 5796 130 133 2-s2.0-33749632259 10.1126/science.1134108 (Pubitemid 44547757)
3. Dion P. A., Daoud H., Rouleau G. A., Genetics of motor neuron disorders: new insights into pathogenic mechanisms. Nature Reviews Genetics 2009 10 11 769 782 2-s2.0-70350075024 10.1038/nrg2680
4. Gurney M. E., Pu H., Chiu A. Y., Dal Canto M. C., Polchow C. Y., Alexander D. D., Caliendo J., Hentati A., Kwon Y. W., Deng H. X., Chen W., Zhai P., Sufit R. L., Siddique T., Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994 264 5166 1772 1775 2-s2.0-0028284779 (Pubitemid 24227760)
5. Shan X., Vocadlo D., Krieger C., Mislocalization of TDP-43 in the G93A mutant SOD1 transgenic mouse model of ALS. Neuroscience Letters 2009 458 2 70 74 2-s2.0-65149101697 10.1016/j.neulet.2009.04.031
6. Reaume A. G., Elliott J. L., Hoffman E. K., Kowall N. W., Ferrante R. J., Siwek D. F., Wilcox H. M., Flood D. G., Beal M. F., Brown R. H., Scott R. W., Snider W. D., Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nature Genetics 1996 13 1 43 47 2-s2.0-15844393658 10.1038/ng0596-43 (Pubitemid 26139292)
7. Ilieva H., Polymenidou M., Cleveland D. W., Non-cell autonomous toxicity in neurodegenerative disorders: aLS and beyond. Journal of Cell Biology 2009 187 6 761 772 2-s2.0-74049164709 10.1083/jcb.200908164
8. Jaarsma D., Teuling E., Haasdijk E. D., De Zeeuw C. I., Hoogenraad C. C., Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. Journal of Neuroscience 2008 28 9 2075 2088 2-s2.0-39849103473 10.1523/JNEUROSCI.5258-07.2008 (Pubitemid 351317636)
9. Boillée S., Vande Velde C., Cleveland D., ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006 52 1 39 59 2-s2.0-33749056809 10.1016/j.neuron.2006.09.018 (Pubitemid 44466358)
10. Beers D. R., Henkel J. S., Xiao Q., Zhao W., Wang J., Yen A. A., Siklos L., McKercher S. R., Appel S. H., Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences of the United States of America 2006 103 43 16021 16026 2-s2.0-33750478657 10.1073/pnas.0607423103 (Pubitemid 44657585)
11. Lepore A. C., Rauck B., Dejea C., Pardo A. C., Rao M. S., Rothstein J. D., Maragakis N. J., Focal transplantation-based astrocyte replacement is neuroprotective in a model of motor neuron disease. Nature Neuroscience 2008 11 11 1294 1301 2-s2.0-54949126674 10.1038/nn.2210
12. Appel S. H., Zhao W., Beers D. R., Henkel J. S., The microglial- motoneuron dialogue in ALS. Acta Myologica 2011 30 1 4 8 2-s2.0-79958022133
13. Nimmerjahn A., Kirchhoff F., Helmchen F., Neuroscience: resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005 308 5726 1314 1318 2-s2.0-19744380563 10.1126/science.1110647 (Pubitemid 40746128)
14. Lull M. E., Block M. L., Microglial activation and chronic neurodegeneration. Neurotherapeutics 2010 7 4 354 365 2-s2.0-77957028140 10.1016/j.nurt.2010.05.014
15. Kreutzberg G. W., Microglia: a sensor for pathological events in the CNS. Trends in Neurosciences 1996 19 8 312 318 2-s2.0-0030222037 10.1016/0166-2236(96)10049-7 (Pubitemid 26349059)
16. Zhao W., Xie W., Le W., Beers D. R., He Y., Henkel J. S., Simpson E. P., Yen A. A., Xiao Q., Appel S. H., Activated microglia initiate motor neuron injury by a nitric oxide and glutamate-mediated mechanism. Journal of Neuropathology and Experimental Neurology 2004 63 9 964 977 2-s2.0-4444348187 (Pubitemid 39202499)
17. Appel S. H., Beers D. R., Henkel J. S., T cell-microglial dialogue in Parkinson's disease and amyotrophic lateral sclerosis: are we listening? Trends in Immunology 2010 31 1 7 17 2-s2.0-73149116008 10.1016/j.it.2009.09.003
18. Hoek R. H., Ruuls S. R., Murphy C. A., Wright G. J., Goddard R., Zurawski S. M., Blom B., Homola M. E., Streit W. J., Brown M. H., Barclay A. N., Sedgwick J. D., Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 2000 290 5497 1768 1771 2-s2.0-17744388105 10.1126/science.290.5497.1768 (Pubitemid 32004808)
19. Cardona A. E., Pioro E. P., Sasse M. E., Kostenko V., Cardona S. M., Dijkstra I. M., Huang D., Kidd G., Dombrowski S., Dutta R., Lee J. C., Cook D. N., Jung S., Lira S. A., Littman D. R., Ransohoff R. M., Control of microglial neurotoxicity by the fractalkine receptor. Nature Neuroscience 2006 9 7 917 924 2-s2.0-33745573660 10.1038/nn1715 (Pubitemid 43980506)
20. + T cells and neuronal damage: direct and collateral mechanisms of cytotoxicity and impaired electrical excitability. The FASEB Journal 2009 23 11 3659 3673 2-s2.0-70350548365 10.1096/fj.09-136200
21. Negrin R. S., Soiffer R.J, Immunobiology of transplantation. Hematopoietic Stem Cell Transplanation 2008 Boston, Mass, USA Humana Press 39 53
22. Kipnis J., Schwartz M., Controlled autoimmunity in CNS maintenance and repair: naturally occurring CD4+CD25+ regulatory T-cells at the crossroads of health and disease. NeuroMolecular Medicine 2005 7 3 197 206 2-s2.0-27144452325 10.1385/NMM:7:3:197 (Pubitemid 41507143)
23. Huang X., Reynolds A. D., Mosley R. L., Gendelman H. E., CD4+ T cells in the pathobiology of neurodegenerative disorders. Journal of Neuroimmunology 2009 211 1-2 3 15 2-s2.0-67349106416 10.1016/j.jneuroim.2009.04.006
24. Holmoy T., T cells in amyotrophic lateral sclerosis. European Journal of Neurology 2008 15 4 360 366 2-s2.0-41149088328 10.1111/j.1468-1331.2008.02065.x (Pubitemid 351424091)
25. Vivier E., Malissen B., Innate and adaptive immunity: specificities and signaling hierarchies revisited. Nature Immunology 2005 6 1 17 21 2-s2.0-12344335678 10.1038/ni1153 (Pubitemid 40136691)
26. Engelhardt B., Ransohoff R. M., The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends in Immunology 2005 26 9 485 495 2-s2.0-23744475685 10.1016/j.it.2005.07.004 (Pubitemid 41139258)
27. Neumann H., Medana I. M., Bauer J., Lassmann H., Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases. Trends in Neurosciences 2002 25 6 313 319 2-s2.0-0036602982 10.1016/S0166-2236(02)02154-9 (Pubitemid 34667013)
28. McMahon E. J., Bailey S. L., Miller S. D., CNS dendritic cells: critical participants in CNS inflammation? Neurochemistry International 2006 49 2 195 203 2-s2.0-33744969133 10.1016/j.neuint.2006.04.004 (Pubitemid 43867078)
29. Gehrmann J., Matsumoto Y., Kreutzberg G. W., Microglia: intrinsic immuneffector cell of the brain. Brain Research Reviews 1995 20 3 269 287 2-s2.0-0029076362 10.1016/0165-0173(94)00015-H
30. Bechmann I., Mor G., Nilsen J., Eliza M., Nitsch R., Naftolin F., FasL (CD95L, Apo1L) is expressed in the normal rat and human brain: evidence for the existence of an immunological brain barrier. Glia 1999 27 1 62 74 (Pubitemid 29311507)
31. Magnus T., Schreiner B., Korn T., Jack C., Guo H., Antel J., Ifergan I., Chen L., Bischof F., Bar-Or A., Wiendl H., Microglial expression of the B7 family member B7 homolog 1 confers strong immune inhibition: Implications for immune responses and autoimmunity in the CNS. Journal of Neuroscience 2005 25 10 2537 2546 2-s2.0-20144378485 10.1523/JNEUROSCI.4794-04.2005 (Pubitemid 40365165)
32. Troost D., Van den Oord J. J., Vianney de Jong J. M. B., Immunohistochemical characterization of the inflammatory infiltrate in amyotrophic lateral sclerosis. Neuropathology and Applied Neurobiology 1990 16 5 401 410 2-s2.0-0025185079 (Pubitemid 20334861)
33. Engelhardt J. I., Tajti J., Appel S. H., Lymphocytic infiltrates in the spinal cord in amyotrophic lateral sclerosis. Archives of Neurology 1993 50 1 30 36 2-s2.0-0027473452 (Pubitemid 23019197)
34. Kawamata T., Akiyama H., Yamada T., McGeer P. L., Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. American Journal of Pathology 1992 140 3 691 707 2-s2.0-0026605961
35. Turner M. R., Cagnin A., Turkheimer F. E., Miller C. C. J., Shaw C. E., Brooks D. J., Leigh P. N., Banati R. B., Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiology of Disease 2004 15 3 601 609 2-s2.0-1842471942 10.1016/j.nbd.2003.12.012 (Pubitemid 38429975)
36. Zhang R., Gascon R., Miller R. G., Gelinas D. F., Mass J., Lancero M., Narvaez A., McGrath M. S., MCP-1 chemokine receptor CCR2 is decreased on circulating monocytes in sporadic amyotrophic lateral sclerosis (sALS). Journal of Neuroimmunology 2006 179 1-2 87 93 2-s2.0-33749150137 10.1016/j.jneuroim. 2006.06.008 (Pubitemid 44468128)
37. Zhang R., Miller R. G., Gascon R., Champion S., Katz J., Lancero M., Narvaez A., Honrada R., Ruvalcaba D., McGrath M. S., Circulating endotoxin and systemic immune activation in sporadic Amyotrophic Lateral Sclerosis (sALS). Journal of Neuroimmunology 2009 206 1-2 121 124 2-s2.0-58149279447 10.1016/j.jneuroim.2008.09.017
38. Swarup V., Phaneuf D., Dupré N, Deregulation of TDP-43 in amyotrophic lateral sclerosis triggers nuclear factor κ B-mediated pathogenic pathways. The Journal of Experimental Medicine 2011 208 12 2429 2447
39. Hall E. D., Oostveen J. A., Gurney M. E., Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 1998 23 3 249 256 (Pubitemid 28259722)
40. Chiu I. M., Chen A., Zheng Y., Kosaras B., Tsiftsoglou S. A., Vartanian T. K., Brown R. H., Carroll M. C., T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proceedings of the National Academy of Sciences of the United States of America 2008 105 46 17913 17918 2-s2.0-56649100689 10.1073/pnas.0804610105
41. Beers D. R., Henkel J. S., Zhao W., Wang J., Appel S. H., CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proceedings of the National Academy of Sciences of the United States of America 2008 105 40 15558 15563 2-s2.0-55749110043 10.1073/pnas.0807419105
42. Zhu S., Stavrovskaya I. G., Drozda M., Kim B. Y. S., Ona V., Li M., Sarang S., Liu A. S., Hartley D. M., Wu D. C., Guilans S., Ferrante R. J., Przedborski S., Kristal B. S., Friedlander R. M., Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002 417 6884 74 78 2-s2.0-0037007645 10.1038/417074a (Pubitemid 34498818)
43. Van Den Bosch L., Tilkin P., Lemmens G., Robberecht W., Minocycline delays disease onset and mortality in a transgenic model of ALS. NeuroReport 2002 13 8 1067 1070 2-s2.0-0037067009 (Pubitemid 34587742)
44. Kriz J., Nguyen M. D., Julien J. P., Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiology of Disease 2002 10 3 268 278 2-s2.0-0036406903 10.1006/nbdi.2002.0487 (Pubitemid 35217580)
45. Xiao Q., Zhao W., Beers D. R., Yen A. A., Xie W., Henkel J. S., Appel S. H., Mutant SOD1G93A microglia are more neurotoxic relative to wild-type microglia. Journal of Neurochemistry 2007 102 6 2008 2019 2-s2.0-34548233140 10.1111/j.1471-4159.2007.04677.x (Pubitemid 47329270)
46. Gowing G., Dequen F., Soucy G., Julien J. P., Absence of tumor necrosis factor- α does not affect motor neuron disease caused by superoxide dismutase 1 mutations. Journal of Neuroscience 2006 26 44 11397 11402 2-s2.0-33750962014 10.1523/JNEUROSCI.0602-06.2006 (Pubitemid 44772169)
47. Gowing G., Philips T., Van Wijmeersch B., Audet J. N., Dewil M., Van Den Bosch L., Billiau A. D., Robberecht W., Julien J. P., Ablation of proliferating microglia does not affect motor neuron degeneration in amyotrophic lateral sclerosis caused by mutant superoxide dismutase. Journal of Neuroscience 2008 28 41 10234 10244 2-s2.0-55049120934 10.1523/JNEUROSCI.3494-08.2008
48. Beers D. R., Zhao W., Liao B., Kano O., Wang J., Huang A., Appel S. H., Henkel J. S., Neuroinflammation modulates distinct regional and temporal clinical responses in ALS mice. Brain, Behavior, and Immunity 2011 25 5 1025 1035 2-s2.0-79957927732 10.1016/j.bbi.2010.12.008
49. Henkel J. S., Beers D. R., Zhao W., Appel S. H., Microglia in ALS: the good, the bad, and the resting. Journal of Neuroimmune Pharmacology 2009 4 4 389 398 2-s2.0-70449525135 10.1007/s11481-009-9171-5
50. Banerjee R., Mosley R. L., Reynolds A. D., Dhar A., Jackson-Lewis V., Gordon P. H., Przedborski S., Gendelman H. E., Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS One 2008 3 7 2-s2.0-50549098607 10.1371/journal.pone.0002740 e2740
51. Beers D. R., Henkel J. S., Zhao W., Wang J., Huang A., Wen S., Liao B., Appel S. H., Endogenous regulatory T lymphocytes ameliorate amyotrophic lateral sclerosis in mice and correlate with disease progression in patients with amyotrophic lateral sclerosis. Brain 2011 134 1293 1314 2-s2.0-79957528028 10.1093/brain/awr074
52. Hume D. A., The mononuclear phagocyte system. Current Opinion in Immunology 2006 18 1 49 53 2-s2.0-30044434256 10.1016/j.coi.2005.11.008 (Pubitemid 43049647)
53. Lawson L. J., Perry V. H., Gordon S., Turnover of resident microglia in the normal adult mouse brain. Neuroscience 1992 48 2 405 415 2-s2.0-0026552605 10.1016/0306-4522(92)90500-2
54. Hickey W. F., Kimura H., Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 1988 239 4837 290 292 2-s2.0-0023949553 (Pubitemid 18061496)
55. Kennedy D. W., Abkowitz J. L., Kinetics of central nervous system microglial and macrophage engraftment: analysis using a transgenic bone marrow transplantation model. Blood 1997 90 3 986 993 2-s2.0-0030787644 (Pubitemid 27314131)
56. Vallières L., Sawchenko P. E., Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity. Journal of Neuroscience 2003 23 12 5197 5207 2-s2.0-0037775809 (Pubitemid 36793248)
57. Lewis C. A. B., Solomon J. N., Rossi F. M., Krieger C., Bone marrow-derived cells in the central nervous system of a mouse model of amyotrophic lateral sclerosis are associated with blood vessels and express CX3CR1. Glia 2009 57 13 1410 1419 2-s2.0-70349154606 10.1002/glia.20859
58. + monocytes only under defined host conditions. Nature Neuroscience 2007 10 12 1544 1553 2-s2.0-36448955070 10.1038/nn2015 (Pubitemid 350175884)
59. Li Y. Q., Chen P., Jain V., Reilly R. M., Wong C. S., Early radiation-induced endothelial cell loss and blood-spinal cord barrier breakdown in the rat spinal cord. Radiation Research 2004 161 2 143 152 2-s2.0-1642499459 10.1667/RR3117 (Pubitemid 38129807)
60. Ajami B., Bennett J. L., Krieger C., Tetzlaff W., Rossi F. M. V., Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nature Neuroscience 2007 10 12 1538 1543 2-s2.0-36448994709 10.1038/nn2014 (Pubitemid 350175883)
61. Massengale M., Wagers A. J., Vogel H., Weissman I. L., Hematopoietic cells maintain hematopoietic fates upon entering the brain. Journal of Experimental Medicine 2005 201 10 1579 1589 2-s2.0-19344364684 10.1084/jem.20050030 (Pubitemid 40721003)
62. Ajami B., Bennett J. L., Krieger C., McNagny K. M., Rossi F. M. V., Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nature Neuroscience 2011 141 9 142 149 2-s2.0-79960656860 10.1038/nn.2887