Prolonged systemic inflammation persistently modifies synaptic plasticity in the hippocampus: Modulation by the stress hormones

Frontiers in Molecular Neuroscience

Volumn 6, Issue DEC, 2013, Pages

  Maggio, Nicola ^a   Shavit Stein, Efrat ^a   Dori, Amir ^a,b   Blatt, Ilan ^a,c   Chapman, Joab ^a,c  

^a SHEBA MEDICAL CENTER   (Israel)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Corticosterone; Glucocorticosteroid receptors; Hippocampus; Inflammation; LPS; LTP; Mineralocorticosteroid receptors; Synaptic plasticity

Indexed keywords

STRESS HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE PREDISPOSITION; INFLAMMATION; LONG TERM POTENTIATION; MICROGLIA; MOUSE; NERVE CELL PLASTICITY; NONHUMAN;

EID: 84889585590     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2013.00046     Document Type: Article

References (46)

1. Alfarez, D. N., Wiegert, O., and Krugers, H. J. (2006). Stress, corticosteroid hormones and hippocampal synaptic function. CNS Neurol. Disord. Drug Targets 5, 521-529. doi: 10.2174/187152706778559345
2. Avital, A., Segal, M., and Richter-Levin, G. (2006). Contrasting roles of corticosteroid receptors in hippocampal plasticity. J. Neurosci. 26, 9130-9134. doi: 10.1523/JNEUROSCI.1628-06.2006
3. Barichello, T., Martins, M. R., Reinke, A., Feier, G., Ritter, C., Quevedo, J., et al. (2005). Long-term cognitive impairment in sepsis survivors. Crit. Care Med. 33, 1671. doi: 10.1097/01.CCM.0000170192.54682.C1
4. Batzofin, B. M., Sprung, C. L., and Weiss, Y. G. (2011). The use of steroids in the treatment of severe sepsis and septic shock. Best Pract. Res. Clin. Endocrinol. Metab.25, 735-743. doi: 10.1016/j.beem.2011.05.006
5. Besedovsky, H. O., and del Rey, A. (2011). Central and peripheral cytokines mediate immune-brain connectivity. Neurochem. Res. 36, 1-6. doi: 10.1007/s11064-010-0252-x
6. Bitzer-Quintero, O. K., and Gonzalez-Burgos, I. (2012). Immune system in the brain: a modulatory role on dendritic spine morphophysiology? Neural Plast. 2012, 348642. doi: 10.1155/2012/348642
7. Chen, J., Buchanan, J. B., Sparkman, N. L., Godbout, J. P., Freund, G. G., and Johnson, R. W. (2008). Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav. Immun.22, 301-311. doi: 10.1016/j.bbi.2007.08.014
8. Chiovenda, P., Vincentelli, G. M., and Alegiani, F. (2002). Cognitive impairment in elderly ED patients: need for multidimensional assessment for better management after discharge. Am. J. Emerg. Med. 20, 332-335. doi: 10.1053/ajem.2002.33785
9. Comim, C. M., Constantino, L. C., Barichello, T., Streck, E. L., Quevedo, J., and Dal-Pizzol, F. (2009). Cognitive impairment in the septic brain. Curr. Neurovasc. Res. 6, 194-203. doi: 10.2174/156720209788970045
10. Cunningham, C., Wilcockson, D. C., Campion, S., Lunnon, K., and Perry, V. H. (2005). Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J. Neurosci.25, 9275-9284. doi: 10.1523/JNEUROSCI.2614-05.2005
11. Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W., and Kelley, K. W. (2008). From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9, 46-56. doi: 10.1038/nrn2297
12. Dilger, R. N., and Johnson, R. W. (2008). Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system. J. Leukoc. Biol. 84, 932-939. doi: 10.1189/jlb.0208108
13. Godbout, J. P., Moreau, M., Lestage, J., Chen, J., Sparkman, N. L., O'Connor, J., et al. (2008). Aging exacerbates depressive-like behavior in mice in response to activation of the peripheral innate immune system. Neuropsychopharmacology 33, 2341-2351. doi: 10.1038/sj.npp.1301649
14. Isik, U., and Caliskan, M. (2008). Reversible EEG changes during rotavirus gastroenteritis. Brain Dev. 30, 73-76. doi: 10.1016/j.braindev.2007.05.006
15. Jefferson, A. L., Massaro, J. M., Wolf, P. A., Seshadri, S., Au, R., Vasan, R. S., et al. (2007). Inflammatory biomarkers are associated with total brain volume: the Framingham Heart Study. Neurology 68, 1032-1038. doi: 10.1212/01.wnl.0000257815.20548.df
16. Joels, M., and Krugers, H. J. (2007). LTP after stress: up or down? Neural Plast. 2007, 93202. doi: 10.1155/2007/93202
17. Joels, M., Krugers, H., and Karst, H. (2008). Stress-induced changes in hippocampal function. Prog. Brain Res. 167, 3-15. doi: 10.1016/S0079-6123(07)67001-0
18. Kohman, R. A., and Rhodes, J. S. (2013). Neurogenesis, inflammation and behavior. Brain Behav. Immun. 27, 22-32. doi: 10.1016/j.bbi.2012.09.003
19. Krugers, H. J., Zhou, M., Joels, M., and Kindt, M. (2011). Regulation of excitatory synapses and fearful memories by stress hormones. Front. Behav. Neurosci. 5:62. doi: 10.3389/fnbeh.2011.00062
20. Lynch, A. M., Walsh, C., Delaney, A., Nolan, Y., Campbell, V. A., and Lynch, M. A. (2004). Lipopolysaccharide-induced increase in signalling in hippocampus is abrogated by IL-10-a role for IL-1 beta? J. Neurochem. 88, 635-646. doi: 10.1046/j.1471-4159.2003.02157.x
21. Maggio, N., and Segal, M. (2007a). Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. J. Neurosci.27, 5757-5765. doi: 10.1523/JNEUROSCI.0155-07.2007
22. Maggio, N., and Segal, M. (2007b). Unique regulation of long term potentiation in the rat ventral hippocampus. Hippocampus 17, 10-25. doi: 10.1002/hipo.20237
23. Maggio, N., and Segal, M. (2009). Differential modulation of long-term depression by acute stress in the rat dorsal and ventral hippocampus. J. Neurosci. 29, 8633-8638. doi: 10.1523/JNEUROSCI.1901-09.2009
24. Maggio, N., and Segal, M. (2010). Corticosteroid regulation of synaptic plasticity in the hippocampus. ScientificWorldJournal 10, 462-469. doi: 10.1100/tsw.2010.48
25. Maggio, N., and Segal, M. (2011). Persistent changes in ability to express long-term potentiation/depression in the rat hippocampus after juvenile/adult stress. Biol. Psychiatry 69, 748-753. doi: 10.1016/j.biopsych.2010.11.026
26. Maggio, N., and Segal, M. (2012a). Cellular basis of a rapid effect of mineralocorticosteroid receptors activation on LTP in ventral hippocampal slices. Hippocampus 22, 267-275. doi: 10.1002/hipo.20893
27. Maggio, N., and Segal, M. (2012b). Steroid modulation of hippocampal plasticity: switching between cognitive and emotional memories. Front. Cell Neurosci. 6:12. doi: 10.3389/fncel.2012.00012
28. Maggio, N., and Segal, M. (2012c). Stress and corticosteroid modulation of seizures and synaptic inhibition in the hippocampus. Exp. Neurol. 234, 200-207. doi: 10.1016/j.expneurol.2011.12.035
29. Murray, C. L., Skelly, D. T., and Cunningham, C. (2011). Exacerbation of CNS inflammation and neurodegeneration by systemic LPS treatment is independent of circulating IL-1beta and IL-6. J. Neuroinflammation 8, 50. doi: 10.1186/1742-2094-8-50
30. Norden, D. M., and Godbout, J. P. (2013). Review: microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathol. Appl. Neurobiol. 39, 19-34. doi: 10.1111/j.1365-2990.2012.01306.x
31. Patel, G. P., and Balk, R. A. (2012). Systemic steroids in severe sepsis and septic shock. Am. J. Respir. Crit. Care Med. 185, 133-139. doi: 10.1164/rccm.201011-1897CI
32. Rabchevsky, A. G., Degos, J. D., and Dreyfus, P. A. (1999). Peripheral injections of Freund's adjuvant in mice provoke leakage of serum proteins through the blood-brain barrier without inducing reactive gliosis. Brain Res. 832, 84-96. doi: 10.1016/S0006-8993(99)01479-1
33. Segal, M., Vlachos, A., and Korkotian, E. (2010). The spine apparatus, synaptopodin, and dendritic spine plasticity. Neuroscientist 16, 125-131. doi: 10.1177/1073858409355829
34. Semmler, A., Frisch, C., Debeir, T., Ramanathan, M., Okulla, T., Klockgether, T., et al. (2007). Long-term cognitive impairment, neuronal loss and reduced cortical cholinergic innervation after recovery from sepsis in a rodent model. Exp. Neurol.204, 733-740. doi: 10.1016/j.expneurol.2007.01.003
35. Sherwin, R. L., Garcia, A. J., and Bilkovski, R. (2012). Do low-dose corticosteroids improve mortality or shock reversal in patients with septic shock? A systematic review and position statement prepared for the American Academy of Emergency Medicine. J. Emerg. Med. 43, 7-12. doi: 10.1016/j.jemermed.2011.08.015
36. Staykova, M. A., Linares, D., Fordham, S. A., Paridaen, J. T., and Willenborg, D. O. (2008). The innate immune response to adjuvants dictates the adaptive immune response to autoantigens. J. Neuropathol. Exp. Neurol. 67, 543-554. doi: 10.1097/NEN.0b013e31817713cc
37. Sundelof, J., Kilander, L., Helmersson, J., Larsson, A., Ronnemaa, E., Degerman-Gunnarsson, M., et al. (2009). Systemic inflammation and the risk of Alzheimer's disease and dementia: a prospective population-based study. J. Alzheimers Dis. 18, 79-87. doi: 10.3233/JAD-2009-1126.
38. Timmermans, W., Xiong, H., Hoogenraad, C. C., and Krugers, H. J. (2013). Stress and excitatory synapses: from health to disease. Neuroscience 248, 626-636. doi: 10.1016/j.neuroscience.2013.05.043
39. Trollor, J. N., Smith, E., Agars, E., Kuan, S. A., Baune, B. T., Campbell, L., et al. (2012). The association between systemic inflammation and cognitive performance in the elderly: the Sydney Memory and Ageing Study. Age (Dordr.) 34, 1295-1308. doi: 10.1007/s11357-011-9301-x
40. van den Boogaard, M., Ramakers, B. P., van Alfen, N., van Der Werf, S. P., Fick, W. F., Hoedemaekers, C. W., et al. (2010). Endotoxemia-induced inflammation and the effect on the human brain. Crit. Care 14, R81. doi: 10.1186/cc9001
41. Vlachos, A., Korkotian, E., Schonfeld, E., Copanaki, E., Deller, T., and Segal, M. (2009). Synaptopodin regulates plasticity of dendritic spines in hippocampal neurons. J. Neurosci. 29, 1017-1033. doi: 10.1523/JNEUROSCI.5528-08.2009
42. Vlachos, A., Maggio, N., and Segal, M. (2008). Lack of correlation between synaptopodin expression and the ability to induce LTP in the rat dorsal and ventral hippocampus. Hippocampus 18, 1-4. doi: 10.1002/hipo.20373
43. Wiegert, O., Joels, M., and Krugers, H. J. (2008). Corticosteroid hormones, synaptic strength and emotional memories: corticosteroid modulation of memory-a cellular and molecular perspective. Prog. Brain Res. 167, 269-271. doi: 10.1016/S0079-6123(07)67021-6
44. Wiersinga, W. J. (2011). Current insights in sepsis: from pathogenesis to new treatment targets. Curr. Opin. Crit. Care 17, 480-486. doi: 10.1097/MCC.0b013e32834a4aeb
45. Wofford, J. L., Loehr, L. R., and Schwartz, E. (1996). Acute cognitive impairment in elderly ED patients: etiologies and outcomes. Am. J. Emerg. Med. 14, 649-653. doi: 10.1016/S0735-6757(96)90080-7
46. Young, G. B. (1995). Neurologic complications of systemic critical illness. Neurol. Clin. 13, 645-658.