Impaired recruitment of neuroprotective microglia and T cells during acute neuronal injury coincides with increased neuronal vulnerability in an amyotrophic lateral sclerosis model

Experimental Neurology

Volumn 234, Issue 2, 2012, Pages 437-445

  Kawamura, Mami Fukunaga ^a   Yamasaki, Ryo ^a   Kawamura, Nobutoshi ^a   Tateishi, Takahisa ^a   Nagara, Yuko ^a   Matsushita, Takuya ^a   Ohyagi, Yasumasa ^a   Kira, Jun ichi ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis (ALS); Cu Zn superoxide dismutase 1 (SOD1); Microglia; Neuroprotection; Neurotrophic factor; T cell

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MESSENGER RNA; NEUROTROPHIC FACTOR; SOMATOMEDIN C;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL COUNT; CELL LOSS; CELL VIABILITY; CONTROLLED STUDY; FEMALE; HYPOGLOSSAL NERVE; HYPOGLOSSAL NUCLEUS; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; LYMPHOCYTIC INFILTRATION; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXOTOMY; HYPOGLOSSAL NERVE; MICE; MICE, TRANSGENIC; MICROGLIA; MOTOR NEURONS; NEURONS; SUPEROXIDE DISMUTASE; T-LYMPHOCYTES;

EID: 84858159644     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.01.015     Document Type: Article

References (35)

1. Alexianu M.E., Kozovska M., Appel S.H. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 2001, 57:1282-1289.
2. 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 Immunol. 2011, 31:7-17.
3. Barbeito A.G., Mesci P., Boillée S. Motor neuron-immune interactions: the vicious circle of ALS. J. Neural. Transm. 2010, 117:981-1000.
4. 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. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15558-15563.
5. 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.
6. Boillée S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
7. Boillée S., Vande Velde C., Cleveland D.W. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006, 52:39-59.
8. Byram S.C., Carson M.J., DeBoy C.A., Serpe C.J., Sanders V.M., Jones K.J. CD4-positive T cell-mediated neuroprotection requires dual compartment antigen presentation. J. Neurosci. 2004, 24:4333-4339.
9. Chiu A.Y., Zhai P., Dal Canto M.C., Peters T.M., Kwon Y.W., Prattis S.M., Gurney M.E. Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis. Mol. Cell. Neurosci. 1995, 6:349-362.
10. Clement A.M., Nguyen M.D., Roberts E.A., Garcia M.L., Boillée S., Rule M., McMahon A.P., Doucette W., Siwek D., Ferrante R.J., Brown R.H., Julien J.P., Goldstein L.S., Cleveland D.W. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003, 302:113-117.
11. Deboy C.A., Xin J., Byram S.C., Serpe C.J., Sanders V.M., Jones K.J. Immune-mediated neuroprotection of axotomized mouse facial motoneurons is dependent on the IL-4/STAT6 signaling pathway in CD4(+) T cells. Exp. Neurol. 2006, 201:212-224.
12. Ferrucci M., Spalloni A., Bartalucci A., Cantafora E., Fulceri F., Nutini M., Longone P., Paparelli A., Fornai F. A systematic study of brainstem motor nuclei in a mouse model of ALS, the effects of lithium. Neurobiol. Dis. 2010, 37:370-383.
13. Fischer L.R., Culver D.G., Tennant P., Davis A.A., Wang M., Castellano-Sanchez A., Khan J., Polak M.A., Glass J.D. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 2004, 185:232-240.
14. 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., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
15. Haynes S.E., Hollopeter G., Yang G., Kurpius D., Dailey M.E., Gan W.B., Julius D. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 2006, 9:1512-1519.
16. Henkel J.S., Beers D.R., Zhao W., Appel S.H. Microglia in ALS: the good, the bad, and the resting. J. Neuroimmune Pharmacol. 2009, 4:389-398.
17. Kawamata T., Akiyama H., Yamada T., McGeer P.L. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am. J. Pathol. 1992, 140:691-707.
18. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29:13435-13444.
19. Lowrie M.B., Vrbová G. Dependence of postnatal motoneurones on their targets: review and hypothesis. Trends Neurosci. 1992, 15:80-84.
20. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461.
21. Moran L.B., Graeber M.B. The facial nerve axotomy model. Brain Res. Rev. 2004, 44:154-178.
22. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
23. Philips T., Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 2011, 10:253-263.
24. Pollin M.M., McHanwell S., Slater C.R. The effect of age on motor neurone death following axotomy in the mouse. Development 1991, 112:83-89.
25. Pramatarova A., Laganière J., Roussel J., Brisebois K., Rouleau G.A. Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J. Neurosci. 2001, 21:3369-3374.
26. Raivich G., Jones L.L., Kloss C.U., Werner A., Neumann H., Kreutzberg G.W. Immune surveillance in the injured nervous system: T-lymphocytes invade the axotomized mouse facial motor nucleus and aggregate around sites of neuronal degeneration. J. Neurosci. 1998, 18:5804-5816.
27. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
28. Serpe C.J., Coers S., Sanders V.M., Jones K.J. CD4+ T, but not CD8+ or B, lymphocytes mediate facial motoneuron survival after facial nerve transection. Brain Behav. Immun. 2003, 17:393-402.
29. Serpe C.J., Byram S.C., Sanders V.M., Jones K.J. Brain-derived neurotrophic factor supports facial motoneuron survival after facial nerve transection in immunodeficient mice. Brain Behav. Immun. 2005, 19:173-180.
30. Snider W.D., Elliott J.L., Yan Q. Axotomy-induced neuronal death during development. J. Neurobiol. 1992, 23:1231-1246.
31. Torvik A., Soreide A.J. The perineuronal glial reaction after axotomy. Brain Res. 1975, 95:519-529.
32. Vega-Avelaira D., Moss A., Fitzgerald M. Age-related changes in the spinal cord microglial and astrocytic response profile to nerve injury. Brain Behav. Immun. 2007, 21:617-623.
33. Wang L., Sharma K., Grisotti G., Roos R.P. The effect of mutant SOD1 dismutase activity on non-cell autonomous degeneration in familial amyotrophic lateral sclerosis. Neurobiol. Dis. 2009, 35:234-240.
34. Xiao Q., Zhao W., Beers D.R., Yen A.A., Xie W., Henkel J.S., Appel S.H. Mutant SOD1(G93A) microglia are more neurotoxic relative to wild-type microglia. J. Neurochem. 2007, 102:2008-2019.
35. Yamasaki R., Tanaka M., Fukunaga M., Tateishi T., Kikuchi H., Motomura K., Matsushita T., Ohyagi Y., Kira J. Restoration of microglial function by granulocyte-colony stimulating factor in ALS model mice. J. Neuroimmunol. 2010, 229:51-62.