Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in beta-amyloid rat model of Alzheimer's disease

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Xuan, Aiguo ^a   Long, Dahong ^a   Li, Jianhua ^a   Ji, Weidong ^a   Zhang, Meng ^b   Hong, Lepeng ^a   Liu, Jihong ^b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Amyloid ; Hydrogen sulfide; Neuroinflammation; p38 mitogen activated protein kinase; p65 nuclear factor B

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; ANTIINFLAMMATORY AGENT; HYDROGEN SULFIDE; INTERLEUKIN 1BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROPROTECTIVE AGENT; SODIUM HYDROSULFIDE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BRAIN PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DNA FRAGMENTATION; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; NERVOUS SYSTEM INFLAMMATION; NICK END LABELING; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPATIAL MEMORY; WESTERN BLOTTING;

EID: 84865055175     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-202     Document Type: Article

References (55)

1. Mildner A, Schlevogt B, Kierdorf K, Böttcher C, Erny D, Kummer MP, Quinn M, Brück W, Bechmann I, Heneka MT, Priller J, Prinz M. Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J Neurosci 2011, 31:11159-11171. 10.1523/JNEUROSCI.6209-10.2011, 21813677.
2. Eikelenboom P, van Exel E, Hoozemans JJ, Veerhuis R, Rozemuller AJ, van Gool WA. Neuroinflammation-an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegener Dis 2010, 7:38-41. 10.1159/000283480, 20160456.
3. Seabrook TJ, Jiang L, Maier M, Lemere CA. Minocycline affects microglia activation, Abeta deposition, and behavior in APP-tg mice. Glia 2006, 53:776-782. 10.1002/glia.20338, 16534778.
4. Weldon DT, Rogers SD, Ghilard JR, Finke MP, Cleary JP, O'Hare E, Esler WP, Maggio JE, Mantyh PW. Fibrillar beta-amyloid induces microglial phagocytosis, expression of inducible nitric oxide synthase, and loss of a select population of neurons in the rat CNS in vivo. J Neurosci 1998, 18:2161-2173.
5. Potter PE. Investigational medications for treatment of patients with Alzheimer disease. J Am Osteopath Assoc 2010, Suppl 8:27-36.
6. Kamoun P. Endogenous production of hydrogen sulfide in mammals. Amino Acids 2004, 26:243-254.
7. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 2009, 11:703-714. 10.1089/ars.2008.2253, 18855522.
8. Kimura Y, Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J 2004, 18:1165-1167.
9. Yin WL, He JQ, Hu B, Jiang ZS, Tang XQ. Hydrogen sulfide inhibits MPP(+)-induced apoptosis in PC12 cells. Life Sci 2009, 85:269-275. 10.1016/j.lfs.2009.05.023, 19540852.
10. Lee SW, Hu YS, Hu LF, Lu Q, Dawe GS, Moore PK, Wong PT, Bian JS. Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia 2006, 54:116-124. 10.1002/glia.20362, 16718684.
11. Nagai Y, Tsugane M, Oka J, Kimura H. Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 2004, 18:557-559.
12. Hu LF, Wong PT, Moore PK, Bian JS. Hydrogen sulfide attenuates lipopolysaccharide induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia. J Neurochem 2007, 100:1121-1128. 10.1111/j.1471-4159.2006.04283.x, 17212697.
13. Morrison LD, Smith DD, Kish SJ. Brain S-adenosylmethionine levels are severely decreased in Alzheimer's disease. J Neurochem 1996, 67:1328-1331.
14. Lee M, Schwab C, Yu S, McGeer E, McGeer PL. Astrocytes produce the antiinflammatory and neuroprotective agent hydrogen sulfide. Neurobiol Aging 2009, 30:1523-1534. 10.1016/j.neurobiolaging.2009.06.001, 19631409.
15. Gong QH, Wang Q, Pan LL, Liu XH, Huang H, Zhu YZ. Hydrogen sulfide attenuates lipopolysaccharide-induced cognitive impairment: A pro-inflammatory pathway in rats. Pharmacol Biochem BE 2010, 96:52-58.
16. Qu K, Chen CP, Halliwell B, Moore PK, Wong PT. Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke 2006, 37:889-893. 10.1161/01.STR.0000204184.34946.41, 16439695.
17. Huang HJ, Liang KC, Chen CP, Chen CM, Hsieh-Li HM. Intrahippocampal administration of A beta(1-40) impairs spatial learning and memory in hyperglycemic mice. Neurobiol Learn Mem 2007, 87:483-494. 10.1016/j.nlm.2006.11.006, 17241793.
18. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984, 11:47-60. 10.1016/0165-0270(84)90007-4, 6471907.
19. Srivareerat M, Tran TT, Salim S, Aleisa AM, Alkadhi KA. Chronic nicotine restores normal Aβ levels and prevents short-term memory and E-LTP impairment in Aβ rat model of Alzheimer's disease. Neurobiol Aging 2011, 32:834-844. 10.1016/j.neurobiolaging.2009.04.015, 19464074.
20. Bagheri M, Roghani M, Joghataei MT, Mohseni S. Genistein inhibits aggregation of exogenous amyloid-beta1-40 and alleviates astrogliosis in the hippocampus of rats. Brain Res 2012, 1429:145-154.
21. Miguel-Hidalgo JJ, Cacabelos R. Beta-amyloid(1-40)-induced neurodegeneration in the rat hippocampal neurons of the CA1 subfield. Acta Neuropathol 1998, 95:455-465. 10.1007/s004010050825, 9600591.
22. Walsh DM, Selkoe DJ. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 2004, 44:181-193. 10.1016/j.neuron.2004.09.010, 15450169.
23. Hashimoto T, Adams KW, Fan Z, McLean PJ, Hyman BT. Characterization of oligomer formation of amyloid-beta peptide using a split-luciferase complementation assay. J Biol Chem 2011, 286:27081-27091. 10.1074/jbc.M111.257378, 3149301, 21652708.
24. Shin RW, Ogino K, Kondo A, Saido TC, Trojanowski JQ, Kitamoto T, Tateishi J. Amyloid beta-protein (Abeta) 1-40 but not Abeta1-42 contributes to the experimental formation of Alzheimer disease amyloid fibrils in rat brain. J Neurosci 1997, 17:8187-8193.
25. Yamaguchi Y, Miyashita H, Tsunekawa H, Mouri A, Kim HC, Saito K, Matsuno T, Kawashima S, Nabeshima T. Effects of a novel cognitive enhancer, spiro[imidazo-[1,2-a] pyridine -3,2- indan]-2(3H)-one (ZSET1446), on learning impairments induced by amyloid-beta1-40 in the rat. J Pharmacol Exp Ther 2006, 317:1079-1087. 10.1124/jpet.105.098640, 16474004.
26. Zou K, Kim D, Kakio A, Byun K, Gong JS, Kim J, Kim M, Sawamura N, Nishimoto S, Matsuzaki K, Lee B, Yanagisawa K, Michikawa M. Amyloid beta-protein (Abeta)1-40 protects neurons from damage induced by Abeta1-42 in culture and in rat brain. J Neurochem 2003, 87:609-619. 10.1046/j.1471-4159.2003.02018.x, 14535944.
27. Yu Y, Zhou L, Sun M, Zhou T, Zhong K, Wang H, Liu Y, Liu X, Xiao R, Ge J, Tu P, Fan DS, Lan Y, Hui C, Chui D. Xylocoside G reduces amyloid-β induced neurotoxicity by inhibiting NF-κB signaling pathway in neuronal cells. J Alzheimers Dis 2012, 30:263-275.
28. Hwang DY, Chae KR, Kang TS, Hwang JH, Lim CH, Kang HK, Goo JS, Lee MR, Lim HJ, Min SH, Cho JY, Hong JT, Song CW, Paik SG, Cho JS, Kim YK. Alterations in behavior, amyloid beta-42, caspase-3, and Cox-2 in mutant PS2 transgenic mouse model of Alzheimer's disease. FASEB J 2002, 6:805-813.
29. Dragunow M, Faull RL, Lawlor P, Beilharz EJ, Singleton K, Walker EB, Mee E. In situ evidence for DNA fragmentation in Huntington's disease striatum and Alzheimer's disease temporal lobes. Neuroreport 1995, 6:1053-1057. 10.1097/00001756-199505090-00026, 7632894.
30. Tweedie D, Ferguson RA, Fishman K, Frankola KA, Van Praag H, Holloway HW, Luo W, Li Y, Caracciolo L, Russo I, Barlati S, Ray B, Lahiri DK, Bosetti F, Greig NH, Rosi S. Tumor necrosis factor-α synthesis inhibitor 3,6′-dithiothalidomide attenuates markers of inflammation. Alzheimer pathology and behavioral deficits in animal models of neuroinflammation and Alzheimer's disease. J Neuroinflammation 2012, 9:106. 10.1186/1742-2094-9-106, 3405480, 22642825.
31. Liu S, Liu Y, Hao W, Wolf L, Kiliaan AJ, Penke B, Rübe CE, Walter J, Heneka MT, Hartmann T, Menger MD, Fassbender K. TLR2 is a primary receptor for Alzheimer's amyloid β peptide to trigger neuroinflammatory activation. J Immunol 2012, 188:1098-1107. 10.4049/jimmunol.1101121, 22198949.
32. Maeda J, Ji B, Irie T, Tomiyama T, Maruyama M, Okauchi T, Staufenbiel M, Iwata N, Ono M, Saido TC, Suzuki K, Mori H, Higuchi M, Suhara T. Longitudinal, quantitative assessment of amyloid, neuroinflammation, and anti-amyloid treatment in a living mouse model of Alzheimer's disease enabled by positron emission tomography. J Neurosci 2007, 27:10957-10968. 10.1523/JNEUROSCI.0673-07.2007, 17928437.
33. Zhu LH, Bi W, Qi RB, Wang HD, Wang ZG, Zeng Q, Zhao YR, Lu DX. Luteolin reduces primary hippocampal neurons death induced by neuroinflammation. Neurol Res 2011, 33:927-934. 10.1179/1743132811Y.0000000023, 22080993.
34. Lee JY, Cho E, Ko YE, Kim I, Lee KJ, Kwon SU, Kang DW, Kim JS. Ibudilast, a phosphodiesterase inhibitor with anti-inflammatory activity, protects against ischemic brain injury in rats. Brain Res 2012, 1431:97-106.
35. Liu T, Jin H, Sun QR, Xu JH, Hu HT. The neuroprotective effects of tanshinone IIA on β-amyloid-induced toxicity in rat cortical neurons. Neuropharmacology 2010, 59:595-604. 10.1016/j.neuropharm.2010.08.013, 20800073.
36. Franciosi S, Ryu JK, Choi HB, Radov L, Kim SU, McLarnon JG. Broad-spectrum effects of 4-aminopyridine to modulate amyloid beta1-42-induced cell signaling and functional responses in human microglia. J Neurosci 2006, 26:11652-11664. 10.1523/JNEUROSCI.2490-06.2006, 17093087.
37. Peila R, Launer LJ. Inflammation and dementia: epidemiologic evidence. Acta Neurol Scand Suppl 2006, 185:102-106.
38. Morales I, Farías G, Maccioni RB. Neuroimmunomodulation in the pathogenesis of Alzheimer's disease. Neuroimmunomodulation 2010, 17:202-204. 10.1159/000258724, 20134203.
39. Angelopoulos P, Agouridaki H, Vaiopoulos H, Siskou E, Doutsou K, Costa V, Baloyiannis SI. Cytokines in Alzheimer's disease and vascular dementia. Int J Neurosci 2008, 118:1659-1672. 10.1080/00207450701392068, 18937113.
40. Forlenza OV, Diniz BS, Talib LL, Mendonça VA, Ojopi EB, Gattaz WF, Teixeira AL. Increased serum IL-1beta level in Alzheimer's disease and mild cognitive impairment. Dement Geriatr Cogn Disord 2009, 28:507-512. 10.1159/000255051, 19996595.
41. Alkam T, Nitta A, Mizoguchi H, Saito K, Seshima M, Itoh A, Yamada K, Nabeshima T. Restraining tumor necrosis factor-alpha by thalidomide prevents the amyloid beta-induced impairment of recognition memory in mice. Behav Brain Res 2008, 189:100-106. 10.1016/j.bbr.2007.12.014, 18325608.
42. Koenigsknecht-Talboo J, Landreth GE. Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J Neurosci 2005, 25:8240-8249. 10.1523/JNEUROSCI.1808-05.2005, 16148231.
43. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 1996, 16:1066-1071.
44. Li L, Bhatia M, Zhu YZ, Zhu YC, Ramnath RD, Wang ZJ, Anuar FB, Whiteman M, Salto-Tellez M, Moore PK. Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J 2005, 19:1196-1198.
45. Lee M, Sparatore A, Del Soldato P, McGeer E, McGeer PL. Hydrogen sulfide-releasing NSAIDs attenuate neuroinflammation induced by microglial and astrocytic activation. Glia 2010, 58:103-113. 10.1002/glia.20905, 19544392.
46. Gong QH, Wang Q, Pan LL, Liu XH, Huang H, Zhu YZ. Hydrogen sulfide attenuates lipopolysaccharide-induced cognitive impairment: a pro-inflammatory pathway in rats. Pharmacol Biochem Behav 2010, 96:52-58. 10.1016/j.pbb.2010.04.006, 20399805.
47. Giovannini MG, Scal C, Prosperi C, Bellucci A, Vannucchi MG, Rosi S, Pepeu G, Casamenti F. Beta-amyloid-induced inflammation and cholinergic hypofunction in the rat brain in vivo: involvement of the p38MAPK pathway. Neurobiol Dis 2002, 11:257-274. 10.1006/nbdi.2002.0538, 12505419.
48. Ji C, Aisa HA, Yang N, Li Q, Wang T, Zhang L, Qu K, Zhu HB, Zuo PP. Gossypium herbaceam extracts inhibited NF-kappaB activation to attenuate spatial memory impairment and hippocampal neurodegeneration induced by amyloid-beta in rats. J Alzheimers Dis 2008, 14:271-283.
49. Minogue AM, Lynch AM, Loane DJ, Herron CE, Lynch MA. Modulation of amyloid-beta-induced and age-associated changes in rat hippocampus by eicosapentaenoic acid. J Neurochem 2007, 103:914-926. 10.1111/j.1471-4159.2007.04848.x, 17711425.
50. Wang C, Li J, Liu Q, Yang R, Zhang JH, Cao YP, Sun XJ. Hydrogen-rich saline reduces oxidative stress and inflammation by inhibit of JNK and NF-κB activation in a rat model of amyloid-beta-induced Alzheimer's disease. Neurosci Lett 2011, 491:127-132. 10.1016/j.neulet.2011.01.022, 21238541.
51. Zhu X, Rottkamp CA, Hartzler A, Sun Z, Takeda A, Boux H, Shimohama S, Perry G, Smith MA. Activation of MKK6, an upstream activator of p38, in Alzheimer's disease. J Neurochem 2001, 79:311-318.
52. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C. Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc Natl Acad Sci U S A 1997, 94:2642-2647. 10.1073/pnas.94.6.2642, 20142, 9122249.
53. Kitamura Y, Shimohama S, Ota T, Matsuoka Y, Nomura Y, Taniguchi T. Alteration of transcription factors NF-kappaB and STAT1 in Alzheimer's disease brains. Neurosci Lett 1997, 237:17-20. 10.1016/S0304-3940(97)00797-0, 9406869.
54. Chen J, Zhou Y, Mueller-Steiner S, Chen LF, Kwon H, Yi S, Mucke L, Gan L. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J Biol Chem 2005, 280:40364-40374. 10.1074/jbc.M509329200, 16183991.
55. Ebenezer PJ, Weidner AM, LeVine H, Markesbery WR, Murphy MP, Zhang L, Dasuri K, Fernandez-Kim SO, Bruce-Keller AJ, Gavilán E, Keller JN. Neuron specific toxicity of oligomeric amyloid-β: role for JUN-kinase and oxidative stress. J Alzheimers Dis 2010, 22:839-848. 3412400, 20858948.