T cell immunity to glatiramer acetate ameliorates cognitive deficits induced by chronic cerebral hypoperfusion by modulating the microenvironment

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Chen, Li ^a   Yao, Yang ^a   Wei, Changjuan ^a   Sun, Yanan ^a   Ma, Xiaofeng ^a   Zhang, Rongxin ^a   Xu, Xiaolin ^b   Hao, Junwei ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b Center for Basic Medical Science Research Tianjin Medical University ^*  (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM BINDING PROTEIN; CYTOKINE; GLATIRAMER; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL; ANIMAL BEHAVIOR; BRAIN ISCHEMIA; COGNITION DISORDERS; COMPLICATION; DEMENTIA, VASCULAR; DISEASE MODEL; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; IMMUNOLOGY; LONG TERM POTENTIATION; MALE; MAZE TEST; METABOLISM; PATHOLOGY; RAT; T LYMPHOCYTE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN ISCHEMIA; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM-BINDING PROTEINS; COGNITION DISORDERS; CYTOKINES; DEMENTIA, VASCULAR; DISEASE MODELS, ANIMAL; GLATIRAMER ACETATE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MICROFILAMENT PROTEINS; RATS; T-LYMPHOCYTES;

EID: 84942284389     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14308     Document Type: Article

References (64)

1. Giacobini, E. Cholinesterase inhibitors: new roles and therapeutic alternatives. Pharmacol Res 50, 433-440 (2004).
2. Kalaria, R. N. et al. Towards defning the neuropathological substrates of vascular dementia. J Neurol Sci 226, 75-80 (2004).
3. Xi, Y. et al. Neuronal damage, central cholinergic dysfunction and oxidative damage correlate with cognitive defcits in rats with chronic cerebral hypoperfusion. Neurobiol Learn Mem 109, 7-19 (2014).
4. Eikelenboom, P. et al. Neuroinfammation-an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegener Dis 7, 38-41 (2010).
5. Sakr, H. F. et al. Efect of dehydroepiandrosterone (DHEA) on memory and brain derived neurotrophic factor (BDNF) in a rat model of vascular dementia. J Physiol Pharmacol 65, 41-53 (2014).
6. White, K. G. & Ruske, A. C. Memory defcits in Alzheimer's disease: the encoding hypothesis and cholinergic function. Psychon Bull Rev 9, 426-437 (2002).
7. Wang, J., Zhang, H. Y. & Tang, X. C. Cholinergic defciency involved in vascular dementia: possible mechanism and strategy of treatment. Acta Pharmacol Sin 30, 879-888 (2009).
8. Scarpini, E., Scheltens, P. & Feldman, H. Treatment of Alzheimer's disease: current status and new perspectives. Lancet Neurol 2, 539-547 (2003).
9. Farkas, E., Luiten, P. G. & Bari, F. Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res Rev 54, 162-180 (2007).
10. Barker, C. F. & Billingham, R. E. Immunologically privileged sites. Adv Immunol 25, 1-54 (1977).
11. Schwartz, M., London, A. & Shechter, R. Boosting T-cell immunity as a therapeutic approach for neurodegenerative conditions: the role of innate immunity. Neuroscience 158, 1133-1142 (2009).
12. Derecki, N. C. et al. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 207, 1067-1080 (2010).
13. Radjavi, A., Smirnov, I. & Kipnis, J. Brain antigen-re active CD4+ T cells are sufcient to support learning behavior in mice with limited T cell repertoire. Brain Behav Immun 35, 58-63 (2014).
14. Kipnis, J. et al. T cell immunity to copolymer 1 confers neuroprotection on the damaged optic nerve: possible therapy for optic neuropathies. Proc Natl Acad Sci USA 97, 7446-7451 (2000).
15. Wolf, S. A. et al. CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J Immunol 182, 3979-3984 (2009).
16. Mastrangelo, M. A., Sudol, K. L., Narrow, W C. & Bowers, W J. Interferon-{gamma} diferentially afects Alzheimer's disease pathologies and induces neurogenesis in triple transgenic-AD mice. Am J Pathol 175, 2076-2088 (2009).
17. Shaked, I. et al. Protective autoimmunity: interferon-gamma enables microglia to remove glutamate without evoking infammatory mediators. J Neurochem 92, 997-1009 (2005).
18. Shechter, R. et al. Infltrating blood-derived macrophages are vital cells playing an anti-infammatory role in recovery from spinal cord injury in mice. PLoS Med 6, e1000113 (2009).
19. Angelov, D. N. et al. T erapeutic vaccine for acute and chronic motor neuron diseases: implications for amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 100, 4790-4795 (2003).
20. Kipnis, J. et al. Neuronal survival afer CNS insult is determined by a genetically encoded autoimmune response. J Neuro sci 21, 4564-4571 (2001).
21. Avidan, H., Kipnis, J., Butovsky, O., Caspi, R. R. & Schwartz, M. Vaccination with autoantigen protects against aggregated beta-amyloid and glutamate toxicity by controlling microglia: efect of CD4 + CD25+ T cells. Eur J Immunol 34, 3434-3445 (2004).
22. Blurton-Jones, M. et al. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci USA 106, 13594-13599 (2009).
23. Aharoni, R., Meshorer, A., Sela, M. & Arnon, R. Oral treatment of mice with copolymer 1 (glatiramer acetate) results in the accumulation of specifc T2 cells in the central nervous system. J Neuroimmunol 126, 58-68 (2002).
24. Kerschensteiner, M., Stadelmann, C., Dechant, G., Wekerle, H. & Hohlfeld, R. Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann Neurol 53, 292-304 (2003).
25. Aharoni, R. et al. Specifc T2 cells accumulate in the central nervous system of mice protected against experimental autoimmune encephalomyelitis by copolymer 1. Proc Natl Acad Sci USA 97, 11472-11477 (2000).
26. Palumbo, M. L., Trinchero, M. F., Zorrilla-Zubilete, M. A., Schinder, A. F. & Genaro, A. M. Glatiramer acetate reverts stress-induced alterations on adult neurogenesis and behavior. Involvement of T1/T2 balance. Brain Behav Immun 26, 429-438 (2012).
27. Ni, J. W, Matsumoto, K., Li, H. B., Murakami, Y & Watanabe, H. Neuronal damage and decrease of central acetylcholine level following permanent occlusion of bilateral common carotid arteries in rat. Brain Res 673, 290-296 (1995).
28. D'Hooge, R. & De Deyn, P. P. Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36, 60-90 (2001).
29. Malenka, R. C. & Nicoll, R. A. Long-term potentiation-a decade of progress? Science 285, 1870-1874 (1999).
30. Walsh, D. M. & Selkoe, D. J. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44, 181-193 (2004).
31. Selkoe, D. J. Alzheimer's disease is a synaptic failure. Science 298, 789-791 (2002).
32. Suh, H. W. et al. The reduction of antinociceptive efect of morphine administered intraventricularly is correlated with the decrease of serotonin release from the spinal cord in streptozotocin-induced diabetic rats. Gen Pharmacol 27, 445-450 (1996).
33. Kipnis, J. & Schwartz, M. Dual action of glatiramer acetate (Cop-1) in the treatment of CNS autoimmune and neurodegenerative disorders. Trends Mol Med 8, 319-323 (2002).
34. Schwartz, M., Shaked, I., Fisher, J., Mizrahi, T. & Schori, H. Protective autoimmunity against the enemy within: fghting glutamate toxicity. Trends Neurosci 26, 297-302 (2003).
35. Kipnis, J., Derecki, N. C., Yang, C. & Scrable, H. Immunity and cognition: what do age-related dementia, HIV-dementia and 'chemo-brain' have in common? Trends Immunol 29, 455-463 (2008).
36. Monteggia, L. M. et al. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc Natl Acad Sci USA 101, 10827-10832 (2004).
37. Kerschensteiner, M. et al. Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in infammatory brain lesions: a neuroprotective role of infammation? J Exp Med 189, 865-870 (1999).
38. Chen, M., Valenzuela, R. M. & Dhib-Jalbut, S. Glatiramer acetate-reactive T cells produce brain-derived neurotrophic factor. J Neurol Sci 215, 37-44 (2003).
39. Awatsuji, H. et al. Interleukin-4 and-5 as modulators of nerve growth factor synthesis/secretion in astrocytes. J Neurosci Res 34, 539-545 (1993).
40. Ziv, Y. et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9, 268-275 (2006).
41. Schwartz, M. & Kipnis, J. Autoimmunity on alert: naturally occurring regulatory CD4(+)CD25(+) T cells as part of the evolutionary compromise between a 'need' and a 'risk'. Trends Immunol 23, 530-534 (2002).
42. Fiore, M. et al. Learning performances, brain NGF distribution and NPY levels in transgenic mice expressing TNF-alpha. Behav Brain Res 112, 165-175 (2000).
43. Heyser, C. J., Masliah, E., Samimi, A., Campbell, I. L. & Gold, L. H. Progressive decline in avoidance learning paralleled by infammatory neurodegeneration in transgenic mice expressing interleukin 6 in the brain. Proc Natl Acad Sci USA 94, 1500-1505 (1997).
44. Fontaine, V. et al. Neurodegenerative and neuroprotective efects of tumor Necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. J Neurosci 22, RC216 (2002).
45. Marchetti, L., Klein, M., Schlett, K., Pfzenmaier, K. & Eisel, U. L. Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-D-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J Biol Chem 279, 32869-32881 (2004).
46. Cheng, B., Christakos, S. & Mattson, M. P. Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 12, 139-153 (1994).
47. Kaufmann, I. et al. Lymphocyte subsets and the role of TH1/TH2 balance in stressed chronic pain patients. Neuroimmun omodulation 14, 272-280 (2007).
48. Schwarz, M. J., Chiang, S., Muller, N. & Ackenheil, M. T-helper-1 and T-helper-2 responses in psychiatric disorders. Brain Behav Immun 15, 340-370 (2001).
49. Benner, E. J. et al. Terapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease. Proc Natl Acad Sci USA 101, 9435-9440 (2004).
50. Schori, H., Robenshtok, E., Schwartz, M. & Hourvitz, A. Post-intoxication vaccination for protection of neurons against the toxicity of nerve agents. Toxicol Sci 87, 163-168 (2005).
51. Wiesemann, E. et al. Glatiramer acetate (GA) induces IL-13/IL-5 secretion in naive T cells. J Neuroimmunol 119, 137-144 (2001).
52. Miller, A. et al. Treatment of multiple sclerosis with copolymer-1 (Copaxone): implicating mechanisms of T1 to T2/T3 immune-deviation. J Neuroimmunol 92, 113-121 (1998).
53. Dabbert, D. et al. Glatiramer acetate (copolymer-1)-specifc, human T cell lines: cytokine profile and suppression of T cell lines reactive against myelin basic protein. Neurosci Lett 289, 205-208 (2000).
54. DeKosky, S. T. et al. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann Neurol 51, 145-155 (2002).
55. Mufson, E. J. et al. Loss of nucleus basalis neurons containing trkA immunoreactivity in individuals with mild cognitive impairment and early Alzheimer's disease. J Comp Neurol 427, 19-30 (2000).
56. Davis, K. L. et al. Cholinergic markers in elderly patients with early signs of Alzheimer disease. JAMA 281, 1401-1406 (1999).
57. Blake, M. G., Krawczyk, M. C., Baratti, C. M. & Boccia, M. M. Neuropharmacology of memory consolidation and reconsolidation: Insights on central cholinergic mechanisms. J Physiol Paris (2014).
58. Oda, Y. Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol Int 49, 921-937 (1999).
59. Kasashima, S. et al. Neurons with choline acetyltransferase immunoreactivity and mRNA are present in the human cerebral cortex. Histochem Cell Biol 111, 197-207 (1999).
60. Hut, R. A. & Van der Zee, E. A. The cholinergic system, circadian rhythmicity, and time memory. Behav Brain Res 221, 466-480 (2011).
61. Giacobini, E. Long-term stabilizing efect of cholinesterase inhibitors in the therapy of Alzheimer' disease. J Neural Transm Suppl, 181-187 (2002).
62. Nagy, P. M. & Aubert, I. Overexpression of the vesicular acetylcholine transporter increased acetylcholine release in the hippocampus. Neuroscience 218, 1-11 (2012).
63. Jiang, H., Zhang, J., Zhu, H., Li, H. & Zhang, X. Nerve growth factor prevents the apoptosis-associated increase in acetylcholinesterase activity afer hydrogen peroxide treatment by activating Akt. Acta Biochim Biophys Sin (Shanghai) 39, 46-56 (2007).
64. Butovsky, O. et al. Glatiramer acetate fghts against Alzheimer's disease by inducing dendritic-like microglia expressing insulinlike growth factor 1. Proc Natl Acad Sci USA 103, 11784-11789 (2006).