Simvastatin enhances immune responses to Aβ vaccination and attenuates vaccination-induced behavioral alterations

Brain Research

Volumn 1356, Issue , 2010, Pages 102-111

  Kou, Jinghong ^a   Kim, Hong Duck ^b   Jin, Jingji ^a   Cao, Dongfeng ^c   Li, Ling ^c   Lalonde, Robert ^d   Fukuchi, Ken Ichiro ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITÉ DE ROUEN   (France)

Author keywords

Adenovirus; Alzheimer's disease; Amyloid; Anxiety; Sickness behavior; Statins

Indexed keywords

CHOLESTEROL; GAMMA INTERFERON; IMMUNOGLOBULIN; PSEUDOMONAS EXOTOXIN; SIMVASTATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; C57BL 6 MOUSE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; IMMUNE RESPONSE; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEROCONVERSION; SPLEEN CELL; TH2 CELL; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INHALATION; ALZHEIMER VACCINES; AMYLOID BETA-PEPTIDES; ANIMALS; ANTICHOLESTEREMIC AGENTS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; FEMALE; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; SIMVASTATIN; TH2 CELLS;

ADENOVIRIDAE; ANIMALIA; MUS; PSEUDOMONAS EXOTOXIN;

EID: 77956871813     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.07.102     Document Type: Article

References (70)

1. O. Aktas, S. Waiczies, A. Smorodchenko, J. Dorr, B. Seeger, T. Prozorovski, S. Sallach, M. Endres, S. Brocke, R. Nitsch, and F. Zipp Treatment of relapsing paralysis in experimental encephalomyelitis by targeting Th1 cells through atorvastatin J. Exp. Med. 197 2003 725 733
2. T. Aprahamian, R. Bonegio, J. Rizzo, H. Perlman, D.J. Lefer, I.R. Rifkin, and K. Walsh Simvastatin treatment ameliorates autoimmune disease associated with accelerated atherosclerosis in a murine lupus model J. Immunol. 177 2006 3028 3034
3. M. Arora, L. Chen, M. Paglia, I. Gallagher, J.E. Allen, Y.M. Vyas, A. Ray, and P. Ray Simvastatin promotes Th2-type responses through the induction of the chitinase family member Ym1 in dendritic cells Proc. Natl. Acad. Sci. U.S.A. 103 2006 7777 7782
4. L. Brydon, C. Walker, A. Wawrzyniak, D. Whitehead, H. Okamura, J. Yajima, A. Tsuda, and A. Steptoe Synergistic effects of psychological and immune stressors on inflammatory cytokine and sickness responses in humans Brain Behav. Immun. 23 2009 217 224
5. E. Check Nerve inflammation halts trial for Alzheimer's drug Nature 415 2002 462
6. M. Citron, D. Westaway, W. Xia, G. Carlson, T. Diehl, G. Levesque, K. Johnson-Wood, M. Lee, P. Seubert, A. Davis, D. Kholodenko, R. Motter, R. Sherrington, B. Perry, H. Yao, R. Strome, I. Lieberburg, J. Rommens, S. Kim, D. Schenk, P. Fraser, H.P. St George, and D.J. Selkoe Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice Nat. Med. 3 1997 67 72
7. D.H. Cribbs, A. Ghochikyan, V. Vasilevko, M. Tran, I. Petrushina, N. Sadzikava, D. Babikyan, P. Kesslak, T. Kieber-Emmons, C.W. Cotman, and M.G. Agadjanyan Adjuvant-dependent modulation of Th1 and Th2 responses to immunization with beta-amyloid Int. Immunol. 15 2003 505 514
8. R. Dantzer, J.C. O'Connor, G.G. Freund, R.W. Johnson, and K.W. Kelley From inflammation to sickness and depression: when the immune system subjugates the brain Nat. Rev. Neurosci. 9 2008 46 56
9. K. Fassbender, M. Simons, C. Bergmann, M. Stroick, D. Lutjohann, P. Keller, H. Runz, S. Kuhl, T. Bertsch, K. von Bergmann, M. Hennerici, K. Beyreuther, and T. Hartmann Simvastatin strongly reduces levels of Alzheimer's disease beta-amyloid peptides Abeta 42 and Abeta 40 in vitro and in vivo Proc. Natl. Acad. Sci. U.S.A. 98 2001 5856 5861
10. I. Ferrer, R.M. Boada, M.L. Sanchez Guerra, M.J. Rey, and F. Costa-Jussa Neuropathology and pathogenesis of encephalitis following amyloid-beta immunization in Alzheimer's disease Brain Pathol. 14 2004 11 20
11. D. Games, D. Adams, R. Alessandrini, R. Barbour, P. Berthelette, C. Blackwell, T. Carr, J. Clemens, T. Donaldson, and F. Gillespie Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein Nature 373 1995 523 527
12. S. Gilman, M. Koller, R.S. Black, L. Jenkins, S.G. Griffith, N.C. Fox, L. Eisner, L. Kirby, M.B. Rovira, F. Forette, and J.M. Orgogozo Clinical effects of Abeta immunization (AN1792) in patients with AD in an interrupted trial Neurology 64 2005 1553 1562
13. A. Goate, M.C. Chartier-Harlin, M. Mullan, J. Brown, F. Crawford, L. Fidani, L. Giuffra, A. Haynes, N. Irving, and L. James Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease Nature 349 1991 704 706 (Pubitemid 21912142)
14. R. Hakamada-Taguchi, Y. Uehara, K. Kuribayashi, A. Numabe, K. Saito, H. Negoro, T. Fujita, T. Toyo-oka, and T. Kato Inhibition of hydroxymethylglutaryl- coenzyme a reductase reduces Th1 development and promotes Th2 development Circ. Res. 93 2003 948 956
15. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
16. A. Hasselberg, K. Schon, A. Tarkowski, and N. Lycke Role of CTA1R7K-COL-DD as a novel therapeutic mucosal tolerance-inducing vector for treatment of collagen-induced arthritis Arthritis Rheum. 60 2009 1672 1682
17. I.C. Ho, and L.H. Glimcher Transcription: tantalizing times for T cells Cell 109 Suppl 2002 S109 S120
18. C. Hock, U. Konietzko, J.R. Streffer, J. Tracy, A. Signorell, B. Muller-Tillmanns, U. Lemke, K. Henke, E. Moritz, E. Garcia, M.A. Wollmer, D. Umbricht, D.J. de Quervain, M. Hofmann, A. Maddalena, A. Papassotiropoulos, and R.M. Nitsch Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease Neuron 38 2003 547 554
19. L. Holcomb, M.N. Gordon, E. McGowan, X. Yu, S. Benkovic, P. Jantzen, K. Wright, I. Saad, R. Mueller, D. Morgan, S. Sanders, C. Zehr, K. O'Campo, J. Hardy, C.M. Prada, C. Eckman, S. Younkin, K. Hsiao, and K. Duff Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes Nat. Med. 4 1998 97 100
20. K. Hsiao, P. Chapman, S. Nilsen, C. Eckman, Y. Harigaya, S. Younkin, F. Yang, and G. Cole Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice Science 274 1996 99 102
21. R.M. Jacobson, A. Swan, A. Adegbenro, S.L. Ludington, P.C. Wollan, and G.A. Poland Making vaccines more acceptable-methods to prevent and minimize pain and other common adverse events associated with vaccines Vaccine 19 2001 2418 2427
22. C. Janus, J. Pearson, J. McLaurin, P.M. Mathews, Y. Jiang, S.D. Schmidt, M.A. Chishti, P. Horne, D. Heslin, J. French, H.T. Mount, R.A. Nixon, M. Mercken, C. Bergeron, P.E. Fraser, P. George-Hyslop, and D. Westaway A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease Nature 408 2000 979 982
23. H. Jick, G.L. Zornberg, S.S. Jick, S. Seshadri, and D.A. Drachman Statins and the risk of dementia Lancet 356 2000 1627 1631
24. H.D. Kim, J.J. Jin, J.A. Maxwell, and K. Fukuchi Enhancing Th2 immune responses against amyloid protein by a DNA prime-adenovirus boost regimen for Alzheimer's disease Immunol. Lett. 112 2007 30 38
25. H.D. Kim, J.A. Maxwell, F.K. Kong, D.C. Tang, and K. Fukuchi Induction of anti-inflammatory immune response by an adenovirus vector encoding 11 tandem repeats of Abeta1-6: toward safer and effective vaccines against Alzheimer's disease Biochem. Biophys. Res. Commun. 336 2005 84 92
26. H.D. Kim, K. Tahara, J.A. Maxwell, R. Lalonde, T. Fukuiwa, K. Fujihashi, K.R. Van Kampen, F.K. Kong, D.C. Tang, and K.I. Fukuchi Nasal inoculation of an adenovirus vector encoding 11 tandem repeats of Abeta1-6 upregulates IL-10 expression and reduces amyloid load in a Mo/Hu APPswe PS1dE9 mouse model of Alzheimer's disease J. Gene. Med. 9 2007 88 98
27. A. Kowalska, D. Pruchnik-Wolinska, J. Florczak, R. Modestowicz, J. Szczech, W. Kozubski, G. Rossa, and M. Wender Genetic study of familial cases of Alzheimer's disease Acta Biochim. Pol. 51 2004 245 252 (Pubitemid 38608822)
28. R. Lalonde, H.D. Kim, J.A. Maxwell, and K. Fukuchi Exploratory activity and spatial learning in 12-month-old APP(695)SWE/co + PS1/DeltaE9 mice with amyloid plaques Neurosci. Lett. 390 2005 87 92
29. P.Y. Lee, P.O. Scumpia, J.A. Byars, K.M. Kelly, H. Zhuang, J.S. Shuster, D.W. Theriaque, M.S. Segal, W.H. Reeves, and M.L. Brantly Short-term atorvastatin treatment enhances specific antibody production following tetanus toxoid vaccination in healthy volunteers Vaccine 24 2006 4035 4040
30. G. Li, R. Higdon, W.A. Kukull, E. Peskind, M.K. Van Valen, D. Tsuang, G. van Belle, W. McCormick, J.D. Bowen, L. Teri, G.D. Schellenberg, and E.B. Larson Statin therapy and risk of dementia in the elderly: a community-based prospective cohort study Neurology 63 2004 1624 1628
31. G. Li, E.B. Larson, J.A. Sonnen, J.B. Shofer, E.C. Petrie, A. Schantz, E.R. Peskind, M.A. Raskind, J.C. Breitner, and T.J. Montine Statin therapy is associated with reduced neuropathologic changes of Alzheimer disease Neurology 69 2007 878 885
32. L. Li, D. Cao, H. Kim, R. Lester, and K. Fukuchi Simvastatin enhances learning and memory independent of amyloid load in mice Ann. Neurol. 60 2006 729 739
33. J.K. Liao, and U. Laufs Pleiotropic effects of statins Annu. Rev. Pharmacol. Toxicol. 45 2005 89 118
34. S.I. McFarlane, R. Muniyappa, R. Francisco, and J.R. Sowers Clinical review 145: pleiotropic effects of statins: lipid reduction and beyond J. Clin. Endocrinol. Metab. 87 2002 1451 1458
35. J. McLaurin, R. Cecal, M.E. Kierstead, X. Tian, A.L. Phinney, M. Manea, J.E. French, M.H. Lambermon, A.A. Darabie, M.E. Brown, C. Janus, M.A. Chishti, P. Horne, D. Westaway, P.E. Fraser, H.T. Mount, M. Przybylski, and P. George-Hyslop Therapeutically effective antibodies against amyloid-beta peptide target amyloid-beta residues 4-10 and inhibit cytotoxicity and fibrillogenesis Nat. Med. 8 2002 1263 1269
36. E. Mira, B. Leon, D.F. Barber, S. Jimenez-Baranda, I. Goya, L. Almonacid, G. Marquez, A. Zaballos, A. Martinez, J.V. Stein, C. Ardavin, and S. Manes Statins induce regulatory T cell recruitment via a CCL1 dependent pathway J. Immunol. 181 2008 3524 3534
37. A. Monsonego Immunogenic aspects of amyloid B-peptide: implications for pathogenesis and treatment of Alzheimer's disease Proceedings VIII Conference on Alzheimer's Disease and Related Disorders 423 2005
38. A. Monsonego, J. Imitola, S. Petrovic, V. Zota, A. Nemirovsky, R. Baron, Y. Fisher, T. Owens, and H.L. Weiner Abeta-induced meningoencephalitis is IFN-gamma-dependent and is associated with T cell-dependent clearance of Abeta in a mouse model of Alzheimer's disease Proc. Natl. Acad. Sci. U.S.A. 103 2006 5048 5053
39. A. Monsonego, R. Maron, V. Zota, D.J. Selkoe, and H.L. Weiner Immune hyporesponsiveness to amyloid beta-peptide in amyloid precursor protein transgenic mice: implications for the pathogenesis and treatment of Alzheimer's disease Proc. Natl. Acad. Sci. U.S.A. 98 2001 10273 10278
40. C. Morgan, M. Zappitelli, and P. Gill Statin prophylaxis and inflammatory mediators following cardiopulmonary bypass: a systematic review Crit. Care. 13 2009 R165
41. D. Morgan, D.M. Diamond, P.E. Gottschall, K.E. Ugen, C. Dickey, J. Hardy, K. Duff, P. Jantzen, G. DiCarlo, D. Wilcock, K. Connor, J. Hatcher, C. Hope, M. Gordon, and G.W. Arendash A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease Nature 408 2000 982 985
42. K.M. Murphy, and S.L. Reiner The lineage decisions of helper T cells Nat. Rev. Immunol. 2 2002 933 944
43. J.A. Nicoll, D. Wilkinson, C. Holmes, P. Steart, H. Markham, and R.O. Weller Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report Nat. Med. 9 2003 448 452
44. J.M. Orgogozo, S. Gilman, J.F. Dartigues, B. Laurent, M. Puel, L.C. Kirby, P. Jouanny, B. Dubois, L. Eisner, S. Flitman, B.F. Michel, M. Boada, A. Frank, and C. Hock Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization Neurology 61 2003 46 54
45. R.R. Packard, S. Schlegel, D. Senouf, F. Burger, P. Sigaud, T. Perneger, C.A. Siegrist, and F. Mach Atorvastatin treatment and vaccination efficacy J. Clin. Pharmacol. 47 2007 1022 1027
46. S.S. Petanceska, S. DeRosa, V. Olm, N. Diaz, A. Sharma, T. Thomas-Bryant, K. Duff, M. Pappolla, and L.M. Refolo Statin therapy for Alzheimer's disease: will it work? J. Mol. Neurosci. 19 2002 155 161
47. M. Pfeifer, S. Boncristiano, L. Bondolfi, A. Stalder, T. Deller, M. Staufenbiel, P.M. Mathews, and M. Jucker Cerebral hemorrhage after passive anti-Abeta immunotherapy Science 298 2002 1379
48. D.L. Price, and S.S. Sisodia Cellular and molecular biology of Alzheimer's disease and animal models Annu. Rev. Med. 45 1994 435 446
49. M.M. Racke, L.I. Boone, D.L. Hepburn, M. Parsadainian, M.T. Bryan, D.K. Ness, K.S. Piroozi, W.H. Jordan, D.D. Brown, W.P. Hoffman, D.M. Holtzman, K.R. Bales, B.D. Gitter, P.C. May, S.M. Paul, and R.B. DeMattos Exacerbation of cerebral amyloid angiopathy-associated microhemorrhage in amyloid precursor protein transgenic mice by immunotherapy is dependent on antibody recognition of deposited forms of amyloid beta J. Neurosci. 25 2005 629 636
50. D.S. Robinson, and A. O'Garra Further checkpoints in Th1 development Immunity 16 2002 755 758
51. E.I. Rogaev, R. Sherrington, E.A. Rogaeva, G. Levesque, M. Ikeda, Y. Liang, H. Chi, C. Lin, K. Holman, and T. Tsuda Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene Nature 376 1995 775 778
52. R.S. Rosenson Pluripotential mechanisms of cardioprotection with HMG-CoA reductase inhibitor therapy Am. J. Cardiovasc. Drugs 1 2001 411 420
53. D. Schenk, R. Barbour, W. Dunn, G. Gordon, H. Grajeda, T. Guido, K. Hu, J. Huang, K. Johnson-Wood, K. Khan, D. Kholodenko, M. Lee, Z. Liao, I. Lieberburg, R. Motter, L. Mutter, F. Soriano, G. Shopp, N. Vasquez, C. Vandevert, S. Walker, M. Wogulis, T. Yednock, D. Games, and P. Seubert Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse Nature 400 1999 173 177
54. D.B. Schenk, and T. Yednock The role of microglia in Alzheimer's disease: friend or foe? Neurobiol. Aging. 23 2002 677 679
55. D.J. Selkoe Alzheimer's disease: a central role for amyloid J. Neuropathol. Exp. Neurol. 53 1994 438 447
56. J. Shepherd, G.J. Blauw, M.B. Murphy, E.L. Bollen, B.M. Buckley, S.M. Cobbe, I. Ford, A. Gaw, M. Hyland, J.W. Jukema, A.M. Kamper, P.W. Macfarlane, A.E. Meinders, J. Norrie, C.J. Packard, I.J. Perry, D.J. Stott, B.J. Sweeney, C. Twomey, and R.G. Westendorp Pravastatin in elderly individuals at risk of vascular disease (PROSPER): a randomised controlled trial Lancet 360 2002 1623 1630
57. R. Sherrington, E.I. Rogaev, Y. Liang, E.A. Rogaeva, G. Levesque, M. Ikeda, H. Chi, C. Lin, G. Li, and K. Holman Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease Nature 375 1995 754 760
58. K. Shimada, J.K. Park, and H. Daida T helper 1/T helper 2 balance and HMG-CoA reductase inhibitors in acute coronary syndrome: statins as immunomodulatory agents? Eur. Heart J. 27 2006 2916 2918
59. C.A. Siegrist Mechanisms underlying adverse reactions to vaccines J. Comp. Pathol. 137 Suppl 1 2007 S46 S50
60. J.B. Sun, C. Czerkinsky, and J. Holmgren Mucosally induced immunological tolerance, regulatory T cells and the adjuvant effect by cholera toxin B subunit Scand. J. Immunol. 71 2010 1 11
61. Z. Suo, J. Tan, A. Placzek, F. Crawford, C. Fang, and M. Mullan Alzheimer's beta-amyloid peptides induce inflammatory cascade in human vascular cells: the roles of cytokines and CD40 Brain Res. 807 1998 110 117
62. T. Town, J. Tan, N. Sansone, D. Obregon, T. Klein, and M. Mullan Characterization of murine immunoglobulin G antibodies against human amyloid-beta1-42 Neurosci. Lett. 307 2001 101 104
63. C.Y. Wang, P.Y. Liu, and J.K. Liao Pleiotropic effects of statin therapy: molecular mechanisms and clinical results Trends Mol. Med. 14 2008 37 44
64. H.L. Weiner, and D.J. Selkoe Inflammation and therapeutic vaccination in CNS diseases Nature 420 2002 879 884
65. D.M. Wilcock, G. DiCarlo, D. Henderson, J. Jackson, K. Clarke, K.E. Ugen, M.N. Gordon, and D. Morgan Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation J. Neurosci. 23 2003 3745 3751
66. B. Wolozin, W. Kellman, P. Ruosseau, G.G. Celesia, and G. Siegel Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3- methyglutaryl coenzyme A reductase inhibitors Arch. Neurol. 57 2000 1439 1443
67. C.E. Wright, P.C. Strike, L. Brydon, and A. Steptoe Acute inflammation and negative mood: mediation by cytokine activation Brain Behav. Immun. 19 2005 345 350
68. M. Yamamoto, T. Kiyota, M. Horiba, J.L. Buescher, S.M. Walsh, H.E. Gendelman, and T. Ikezu Interferon-gamma and tumor necrosis factor-alpha regulate amyloid-beta plaque deposition and beta-secretase expression in Swedish mutant APP transgenic mice Am. J. Pathol. 170 2007 680 692
69. S. Youssef, O. Stuve, J.C. Patarroyo, P.J. Ruiz, J.L. Radosevich, E.M. Hur, M. Bravo, D.J. Mitchell, R.A. Sobel, L. Steinman, and S.S. Zamvil The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease Nature 420 2002 78 84
70. E. Zamrini, G. McGwin, and J.M. Roseman Association between statin use and Alzheimer's disease Neuroepidemiology 23 2004 94 98