Prophylactic lithium alleviates splenectomy-induced cognitive dysfunction possibly by inhibiting hippocampal TLR4 activation in aged rats

Brain Research Bulletin

Volumn 114, Issue , 2015, Pages 31-41

  Lu, Shun Mei ^a   Gui, Bo ^a   Dong, Hong Quan ^a   Zhang, Xiang ^a   Zhang, Su Su ^a   Hu, Liu Qing ^a   Liu, Hai Ling ^a   Sun, Jie ^a   Qian, Yian Ning ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Lipopolysaccharide; Lithium chloride; Microglia; Postoperative cognitive dysfunction; Splenectomy; Toll like receptor 4

Indexed keywords

INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; LITHIUM CHLORIDE; MESSENGER RNA; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; CD11B ANTIGEN; IL1B PROTEIN, RAT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOOTROPIC AGENT; TLR2 PROTEIN, RAT; TLR4 PROTEIN, RAT; TOLL LIKE RECEPTOR 2;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OPEN FIELD TEST; POSTOPERATIVE COGNITIVE DYSFUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPLENECTOMY; WESTERN BLOTTING; AGING; ANIMAL; CELL LINE; COGNITION DISORDERS; DISEASE MODEL; DRUG EFFECTS; GENETICS; IMMUNOMODULATION; METABOLISM; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; ANTIGENS, CD11B; CELL LINE; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; LITHIUM CHLORIDE; MALE; MICE; MICROGLIA; NEUROIMMUNOMODULATION; NF-KAPPA B; NOOTROPIC AGENTS; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; RNA, SMALL INTERFERING; SPLENECTOMY; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84927513122     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2015.02.008     Document Type: Article

References (65)

1. Acharjee S., Nayani N., Tsutsui M., Hill M.N., Ousman S.S., Pittman Q.J. Altered cognitive-emotional behavior in early experimental autoimmune encephalitis - cytokine and hormonal correlates. Brain Behav. Immun. 2013, 33:164-172.
2. Ajami B., Bennett J.L., Krieger C., Tetzlaff W., Rossi F.M. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 2007, 10(12):1538-1543.
3. Alarcon J.M., Malleret G., Touzani K., Vronskaya S., Ishii S., Kandel E.R., et al. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 2004, 42(6):947-959.
4. An L.N., Yue Y., Guo W.Z., Miao Y.L., Mi W.D., Zhang H., et al. Surgical trauma induces iron accumulation and oxidative stress in a rodent model of postoperative cognitive dysfunction. Biol. Trace Elem. Res. 2013, 151(2):277-283.
5. Asavarut P., Zhao H., Gu J., Ma D. The role of HMGB1 in inflammation-mediated organ injury. Acta Anaesthesiol. Taiwan 2013, 51(1):28-33.
6. Bagchi A., Herrup E.A., Warren H.S., Trigilio J., Shin H.S., Valentine C., et al. MyD88-dependent and MyD88-independent pathways in synergy, priming, and tolerance between TLR agonists. J. Immunol. 2007, 178(2):1164-1171.
7. Barrientos R.M., Frank M.G., Hein A.M., Higgins E.A., Watkins L.R., Rudy J.W., et al. Time course of hippocampal IL-1 beta and memory consolidation impairments in aging rats following peripheral infection. Brain Behav. Immun. 2009, 23(1):46-54.
8. Belarbi K., Jopson T., Tweedie D., Arellano C., Luo W., Greig N.H., et al. TNF-alpha protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J. Neuroinflamm. 2012, 9:23.
9. Bian Q., Shi T., Chuang D.M., Qian Y. Lithium reduces ischemia-induced hippocampal CA1 damage and behavioral deficits in gerbils. Brain Res. 2007, 1184:270-276.
10. Blalock E.M., Phelps J.T., Pancani T., Searcy J.L., Anderson K.L., Gant J.C., et al. Effects of long-term pioglitazone treatment on peripheral and central markers of aging. PLoS ONE 2010, 5(4):e10405.
11. Chalecka-Franaszek E., Chuang D.M. Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(15):8745-8750.
12. Cheong M.H., Lee S.R., Yoo H.S., Jeong J.W., Kim G.Y., Kim W.J., et al. Anti-inflammatory effects of Polygala tenuifolia root through inhibition of NF-kappaB activation in lipopolysaccharide-induced BV2 microglial cells. J. Ethnopharmacol. 2011, 137(3):1402-1408.
13. Cibelli M., Fidalgo A.R., Terrando N., Ma D., Monaco C., Feldmann M., et al. Role of interleukin-1beta in postoperative cognitive dysfunction. Ann. Neurol. 2010, 68(3):360-368.
14. Crack P.J., Bray P.J. Toll-like receptors in the brain and their potential roles in neuropathology. Immunol. Cell Biol. 2007, 85(6):476-480.
15. Cuschieri J., Bulger E., Garcia I., Jelacic S., Maier R.V. Calcium/calmodulin-dependent kinase II is required for platelet-activating factor priming. Shock 2005, 23(2):99-106.
16. Dantzer R., Konsman J.P., Bluthe R.M., Kelley K.W. Neural and humoral pathways of communication from the immune system to the brain: parallel or convergent?. Auton. Neurosci. 2000, 85(1-3):60-65.
17. Dong H., Zhang X., Dai X., Lu S., Gui B., Jin W., et al. Lithium ameliorates lipopolysaccharide-induced microglial activation via inhibition of toll-like receptor 4 expression by activating the PI3K/Akt/FoxO1 pathway. J. Neuroinflamm. 2014, 11(1):140.
18. Fidalgo A.R., Cibelli M., White J.P., Nagy I., Maze M., Ma D. Systemic inflammation enhances surgery-induced cognitive dysfunction in mice. Neurosci. Lett. 2011, 498(1):63-66.
19. Fidalgo A.R., Cibelli M., White J.P., Nagy I., Wan Y., Ma D. Isoflurane causes neocortical but not hippocampal-dependent memory impairment in mice. Acta Anaesthesiol. Scand. 2012, 56(8):1052-1057.
20. Frank M.G., Barrientos R.M., Hein A.M., Biedenkapp J.C., Watkins L.R., Maier S.F. IL-1RA blocks E. coli-induced suppression of Arc and long-term memory in aged F344xBN F1 rats. Brain Behav. Immun. 2010, 24(2):254-262.
21. Gildengers A.G., Butters M.A., Aizenstein H.J., Marron M.M., Emanuel J., Anderson S.J., et al. Longer lithium exposure is associated with better white matter integrity in older adults with bipolar disorder. Bipolar Disord. 2014, [Epub ahead of print]. 10.1111/bdi.12260.
22. Gui B., Su M., Chen J., Jin L., Wan R., Qian Y. Neuroprotective effects of pretreatment with propofol in LPS-induced BV-2 microglia cells: role of TLR4 and GSK-3beta. Inflammation 2012, 35(5):1632-1640.
23. Hartigan G.P. The use of lithium salts in affective disorders. Br. J. Psychiatry 1963, 109:810-814.
24. He Z., Zhu Y., Jiang H. Toll-like receptor 4 mediates lipopolysaccharide-induced collagen secretion by phosphoinositide3-kinase-Akt pathway in fibroblasts during acute lung injury. J. Recept. Signal. Transduct. Res. 2009, 29(2):119-125.
25. He H.J., Wang Y., Le Y., Duan K.M., Yan X.B., Liao Q., et al. Surgery upregulates high mobility group box-1 and disrupts the blood-brain barrier causing cognitive dysfunction in aged rats. CNS Neurosci. Ther. 2012, 18(12):994-1002.
26. Heo D.K., Lim H.M., Nam J.H., Lee M.G., Kim J.Y. Regulation of phagocytosis and cytokine secretion by store-operated calcium entry in primary isolated murine microglia. Cell Signal. 2014, 27(1):177-186.
27. Hovens I.B., Schoemaker R.G., van der Zee E.A., Absalom A.R., Heineman E., van Leeuwen B.L. Postoperative cognitive dysfunction: involvement of neuroinflammation and neuronal functioning. Brain Behav. Immun. 2014, 38:202-210.
28. Ji M., Dong L., Jia M., Liu W., Zhang M., Ju L., et al. Epigenetic enhancement of brain-derived neurotrophic factor signaling pathway improves cognitive impairments induced by isoflurane exposure in aged rats. Mol. Neurobiol. 2014, 50(3):937-944.
29. Joseph J.D., Peng Y., Mak D.O., Cheung K.H., Vais H., Foskett J.K., et al. General anesthetic isoflurane modulates inositol 1,4,5-trisphosphate receptor calcium channel opening. Anesthesiology 2014, 121(3):528-537.
30. Kapila A.K., Watts H.R., Wang T., Ma D. The impact of surgery and anesthesia on post-operative cognitive decline and Alzheimer's disease development: biomarkers and preventive strategies. J. Alzheimers Dis. 2014, 41(1):1-13.
31. Kim S.Y., Jeong E., Joung S.M., Lee J.Y. PI3K/Akt contributes to increased expression of Toll-like receptor 4 in macrophages exposed to hypoxic stress. Biochem. Biophys. Res. Commun. 2012, 419(3):466-471.
32. King M.K., Jope R.S. Lithium treatment alleviates impaired cognition in a mouse model of fragile X syndrome. Genes Brain Behav. 2013, 12(7):723-731.
33. King M.K., Pardo M., Cheng Y., Downey K., Jope R.S., Beurel E. Glycogen synthase kinase-3 inhibitors: rescuers of cognitive impairments. Pharmacol. Ther. 2014, 141(1):1-12.
34. Kirshenboim N., Plotkin B., Shlomo S.B., Kaidanovich-Beilin O., Eldar-Finkelman H. Lithium-mediated phosphorylation of glycogen synthase kinase-3beta involves PI3 kinase-dependent activation of protein kinase C-alpha. J. Mol. Neurosci. 2004, 24(2):237-245.
35. Kohman R.A., Rhodes J.S. Neurogenesis, inflammation and behavior. Brain Behav. Immun. 2013, 27(1):22-32.
36. Krenk L., Rasmussen L.S., Kehlet H. New insights into the pathophysiology of postoperative cognitive dysfunction. Acta Anaesthesiol. Scand. 2010, 54(8):951-956.
37. Li Z., Cao Y., Li L., Liang Y., Tian X., Mo N., et al. Prophylactic angiotensin type 1 receptor antagonism confers neuroprotection in an aged rat model of postoperative cognitive dysfunction. Biochem. Biophys. Res. Commun. 2014, 449(1):74-80.
38. Lu S.M., Yu C.J., Liu Y.H., Dong H.Q., Zhang X., Zhang S.S., et al. S100A8 contributes to postoperative cognitive dysfunction in mice undergoing tibial fracture surgery by activating the TLR4/MyD88 pathway. Brain Behav. Immun. 2015, 44:221-234.
39. Lyman M., Lloyd D.G., Ji X., Vizcaychipi M.P., Ma D. Neuroinflammation: the role and consequences. Neurosci. Res. 2014, 79:1-12.
40. Monk T.G., Price C.C. Postoperative cognitive disorders. Curr. Opin. Crit. Care 2011, 17(4):376-381.
41. Monk T.G., Weldon B.C., Garvan C.W., Dede D.E., van der Aa M.T., Heilman K.M., et al. Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology 2008, 108(1):18-30.
42. Nocjar C., Hammonds M.D., Shim S.S. Chronic lithium treatment magnifies learning in rats. Neuroscience 2007, 150(4):774-788.
43. Norden D.M., Godbout J.P. Review: microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathol. Appl. Neurobiol. 2013, 39(1):19-34.
44. Okun E., Griffioen K.J., Lathia J.D., Tang S.C., Mattson M.P., Arumugam T.V. Toll-like receptors in neurodegeneration. Brain Res. Rev. 2009, 59(2):278-292.
45. Ransohoff R.M. Microgliosis: the questions shape the answers. Nat. Neurosci. 2007, 10(12):1507-1509.
46. Rosczyk H.A., Sparkman N.L., Johnson R.W. Neuroinflammation and cognitive function in aged mice following minor surgery. Exp. Gerontol. 2008, 43(9):840-846.
47. Schlecker C., Boehmerle W., Jeromin A., DeGray B., Varshney A., Sharma Y., et al. Neuronal calcium sensor-1 enhancement of InsP3 receptor activity is inhibited by therapeutic levels of lithium. J. Clin. Investig. 2006, 116(6):1668-1674.
48. Shim S.S., Hammonds M.D., Ganocy S.J., Calabrese J.R. Effects of sub-chronic lithium treatment on synaptic plasticity in the dentate gyrus of rat hippocampal slices. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31(2):343-347.
49. Son H., Yu I.T., Hwang S.J., Kim J.S., Lee S.H., Lee Y.S., et al. Lithium enhances long-term potentiation independently of hippocampal neurogenesis in the rat dentate gyrus. J. Neurochem. 2003, 85(4):872-881.
50. Steinmetz J., Christensen K.B., Lund T., Lohse N., Rasmussen L.S. Long-term consequences of postoperative cognitive dysfunction. Anesthesiology 2009, 110(3):548-555.
51. Tan W.F., Cao X.Z., Wang J.K., Lv H.W., Wu B.Y., Ma H. Protective effects of lithium treatment for spatial memory deficits induced by tau hyperphosphorylation in splenectomized rats. Clin. Exp. Pharmacol. Physiol. 2010, 37(10):1010-1015.
52. Tan H., Cao J., Zhang J., Zuo Z. Critical role of inflammatory cytokines in impairing biochemical processes for learning and memory after surgery in rats. J. Neuroinflamm. 2014, 11:93.
53. Terrando N., Monaco C., Ma D., Foxwell B.M., Feldmann M., Maze M. Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(47):20518-20522.
54. Terrando N., Eriksson L.I., Ryu J.K., Yang T., Monaco C., Feldmann M., et al. Resolving postoperative neuroinflammation and cognitive decline. Ann. Neurol. 2011, 70(6):986-995.
55. Valentim A.M., Di Giminiani P., Ribeiro P.O., Rodrigues P., Olsson I.A., Antunes L.M. Lower isoflurane concentration affects spatial learning and neurodegeneration in adult mice compared with higher concentrations. Anesthesiology 2010, 113(5):1099-1108.
56. Vizcaychipi M.P., Watts H.R., O'Dea K.P., Lloyd D.G., Penn J.W., Wan Y., et al. The therapeutic potential of atorvastatin in a mouse model of postoperative cognitive decline. Ann. Surg. 2014, 259(6):1235-1244.
57. Wan Y., Xu J., Ma D., Zeng Y., Cibelli M., Maze M. Postoperative impairment of cognitive function in rats: a possible role for cytokine-mediated inflammation in the hippocampus. Anesthesiology 2007, 106(3):436-443.
58. Wang Y., He H., Li D., Zhu W., Duan K., Le Y., et al. The role of the TLR4 signaling pathway in cognitive deficits following surgery in aged rats. Mol. Med. Rep. 2013, 7(4):1137-1142.
59. Wang Y., Ge P., Yang L., Wu C., Zha H., Luo T., et al. Protection of ischemic post conditioning against transient focal ischemia-induced brain damage is associated with inhibition of neuroinflammation via modulation of TLR2 and TLR4 pathways. J. Neuroinflamm. 2014, 11:15.
60. Wei H. The role of calcium dysregulation in anesthetic-mediated neurotoxicity. Anesth. Analg. 2011, 113(5):972-974.
61. Wu X., Lu Y., Dong Y., Zhang G., Zhang Y., Xu Z., et al. The inhalation anesthetic isoflurane increases levels of proinflammatory TNF-alpha, IL-6, and IL-1beta. Neurobiol. Aging 2012, 33(7):1364-1378.
62. Yu L., Sun L., Chen S. Protective effect of senegenin on splenectomy-induced postoperative cognitive dysfunction in elderly rats. Exp. Ther. Med. 2014, 7(4):821-826.
63. Zhao L., Wang F., Gui B., Hua F., Qian Y. Prophylactic lithium alleviates postoperative cognition impairment by phosphorylating hippocampal glycogen synthase kinase-3beta (Ser9) in aged rats. Exp. Gerontol. 2011, 46(12):1031-1036.
64. Zhu H.T., Bian C., Yuan J.C., Chu W.H., Xiang X., Chen F., et al. Curcumin attenuates acute inflammatory injury by inhibiting the TLR4/MyD88/NF-kappaB signaling pathway in experimental traumatic brain injury. J. Neuroinflamm. 2014, 11:59.
65. Zuloaga D.G., Poort J.E., Jordan C.L., Breedlove S.M. Male rats with the testicular feminization mutation of the androgen receptor display elevated anxiety-related behavior and corticosterone response to mild stress. Horm. Behav. 2011, 60(4):380-388.