Vaccination induced changes in pro-inflammatory cytokine levels as an early putative biomarker for cognitive improvement in a transgenic mouse model for Alzheimer disease

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 7, 2014, Pages 2024-2031

  Lin, Xiaoyang ^a   Bai, Ge ^a   Lin, Linda ^a   Wu, Hengyi ^a   Cai, Jianfeng ^a   Ugen, Kenneth E ^a,b   Cao, Chuanhai ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Alzheimer disease; Amyloid beta (a ); Biomarker; Cytokine; Immunomodulation; Inflammation

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; CYTOKINE; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; ALZHEIMER DISEASE VACCINE; BIOLOGICAL MARKER;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; MEMORY DISORDER; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; TRANSGENIC MOUSE; VACCINATION; ANIMAL; BLOOD; IMMUNOLOGY; PATHOPHYSIOLOGY; TREATMENT OUTCOME;

ALZHEIMER DISEASE; ALZHEIMER VACCINES; AMYLOID BETA-PEPTIDES; ANIMALS; BIOMARKERS; CYTOKINES; MEMORY DISORDERS; MICE, TRANSGENIC; TREATMENT OUTCOME;

EID: 84907978433     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.28735     Document Type: Article

References (45)

1. Alois A. Uber Eine Eigenartige Erkankung der Hirnrinde. Zeitschrift Fuer Psychitrie (Germany) 1907; 64.
2. Eikelenboom P, Stam FC. Immunoglobulins and complement factors in senile plaques. An immunoperoxidase study. Acta Neuropathol 1982; 57:239-42; PMID:6812382; http://dx.doi.org/10.1007/BF00685397
3. Rogers J, Luber-Narod J, Styren SD, Civin WH. Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology of Alzheimer's disease. Neurobiol Aging 1988; 9:339-49; PMID:3263583 http://dx.doi.org/10.1016/S0197-4580(88)80079-4
4. Abraham WM, Sielczak MW, Wanner A, Perruchoud AP, Blinder L, Stevenson JS, Ahmed A, Yerger LD. Cellular markers of inflammation in the airways of allergic sheep with and without allergen-induced late responses. Am Rev Respir Dis 1988; 138:1565-71; PMID:3202508; http://dx.doi.org/10.1164/ajrccm/138.6.1565
5. Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, White CL 3rd, Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci U S A 1989; 86:7611-5; PMID:2529544; http://dx.doi.org/10.1073/pnas.86.19.7611
6. Sheng JG, Mrak RE, Griffin WS. Microglial interleukin-1 alpha expression in brain regions in Alzheimer's disease: correlation with neuritic plaque distribution. Neuropathol Appl Neurobiol 1995; 21:290-301; PMID:7494597; http://dx.doi.org/10.1111/j.1365-2990.1995.tb01063.x
7. Das S, Potter H. Expression of the Alzheimer amyloid-promoting factor antichymotrypsin is induced in human astrocytes by IL-1. Neuron 1995; 14:447-56; PMID:7857652; http://dx.doi.org/10.1016/0896-6273(95)90300-3
8. Suo Z, Tan J, Placzek A, Crawford F, Fang C, Mullan M. Alzheimer's beta-amyloid peptides induce inflammatory cascade in human vascular cells: the roles of cytokines and CD40. Brain Res 1998; 807:110-7; PMID:9757011; http://dx.doi.org/10.1016/S0006-8993(98)00780-X
9. Nilsson M, Husmark J, Björkman U, Ericson LE. Cytokines and thyroid epithelial integrity: interleukin-1alpha induces dissociation of the junctional complex and paracellular leakage in filter-cultured human thyrocytes. J Clin Endocrinol Metab 1998; 83:945-52; PMID:9506754
10. Potter H, Wefes IM, Nilsson LN. The inflammationinduced pathological chaperones ACT and apo-E are necessary catalysts of Alzheimer amyloid formation. Neurobiol Aging 2001; 22:923-30; PMID:11755000; http://dx.doi.org/10.1016/S0197-4580(01)00308-6
11. Patel NS, Paris D, Mathura V, Quadros AN, Crawford FC, Mullan MJ. Inflammatory cytokine levels correlate with amyloid load in transgenic mouse models of Alzheimer's disease. J Neuroinflammation 2005; 2:9; PMID:15762998; http://dx.doi.org/10.1186/1742-2094-2-9
12. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, Chishti MA, Horne P, Heslin D, French J, et al. A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 2000; 408:979-82; PMID:11140685; http://dx.doi.org/10.1038/35050110
13. Morgan D, Diamond DM, Gottschall PE, Ugen KE, Dickey C, Hardy J, Duff K, Jantzen P, DiCarlo G, Wilcock D, et al. A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 2000; 408:982-5; PMID:11140686; http://dx.doi.org/10.1038/35050116
14. Thatte U. AN-1792 (Elan). Curr Opin Investig Drugs 2001; 2:663-7; PMID:11569944
15. Birmingham K, Frantz S. Set back to Alzheimer vaccine studies. Nat Med 2002; 8:199-200; PMID:11875473; http://dx.doi.org/10.1038/nm0302-199b
16. Mathews PM, Nixon RA. Setback for an Alzheimer's disease vaccine: lessons learned. Neurology 2003; 61:7-8; PMID:12847147; http://dx.doi.org/10.1212/WNL.61.1.7
17. Orgogozo JM, Gilman S, Dartigues JF, Laurent B, Puel M, Kirby LC, Jouanny P, Dubois B, Eisner L, Flitman S, et al. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 2003; 61:46-54; PMID:12847155; http://dx.doi.org/10.1212/01.WNL.0000073623.84147.A8
18. Chong Y. Effect of a carboxy-terminal fragment of the Alzheimer's amyloid precursor protein on expression of proinflammatory cytokines in rat glial cells. Life Sci 1997; 61:2323-33; PMID:9408055; http://dx.doi.org/10.1016/S0024-3205(97)00936-3
19. McGeer EG, McGeer PL. The role of the immune system in neurodegenerative disorders. Mov Disord 1997; 12:855-8; PMID:9399206; http://dx.doi.org/10.1002/mds.870120604
20. Vom Berg J, Prokop S, Miller KR, Obst J, Kälin RE, Lopategui-Cabezas I, Wegner A, Mair F, Schipke CG, Peters O, et al. Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease-like pathology and cognitive decline. Nat Med 2012; 18:1812-9; PMID:23178247; http://dx.doi.org/10.1038/nm.2965
21. Sastre M, Klockgether T, Heneka MT. Contribution of inflammatory processes to Alzheimer's disease: molecular mechanisms. Int J Dev Neurosci 2006; 24:167-76; PMID:16472958; http://dx.doi.org/10.1016/j.ijdevneu.2005.11.014
22. Ferrer I, Boada Rovira M, Sánchez Guerra ML, Rey MJ, Costa-Jussá F. Neuropathology and pathogenesis of encephalitis following amyloid-beta immunization in Alzheimer's disease. Brain Pathol 2004; 14:11-20; PMID:14997933; http://dx.doi.org/10.1111/j.1750-3639.2004.tb00493.x
23. Kim HD, Cao Y, Kong FK, Van Kampen KR, Lewis TL, Ma Z, Tang DC, Fukuchi K. Induction of a Th2 immune response by co-administration of recombinant adenovirus vectors encoding amyloid beta-protein and GM-CSF. Vaccine 2005; 23:2977-86; PMID:15811643; http://dx.doi.org/10.1016/j.vaccine.2004.12.015
24. Maier M, Seabrook TJ, Lazo ND, Jiang L, Das P, Janus C, Lemere CA. Short amyloid-beta (Abeta) immunogens reduce cerebral Abeta load and learning deficits in an Alzheimer's disease mouse model in the absence of an Abeta-specific cellular immune response. J Neurosci 2006; 26:4717-28; PMID:16672644; http://dx.doi.org/10.1523/JNEUROSCI.0381-06.2006
25. Okura Y, Miyakoshi A, Kohyama K, Park IK, Staufenbiel M, Matsumoto Y. Nonviral Abeta DNA vaccine therapy against Alzheimer's disease: longterm effects and safety. Proc Natl Acad Sci U S A 2006; 103:9619-24; PMID:16769900; http://dx.doi.org/10.1073/pnas.0600966103
26. Seabrook TJ, Thomas K, Jiang L, Bloom J, Spooner E, Maier M, et al. Dendrimeric Abeta1-15 is an effective immunogen in wildtype and APP-tg mice. Neurobiol Aging 2007; 28:813-23 PMID:16725229
27. Nikolic WV, Bai Y, Obregon D, Hou H, Mori T, Zeng J, Ehrhart J, Shytle RD, Giunta B, Morgan D, et al. Transcutaneous beta-amyloid immunization reduces cerebral beta-amyloid deposits without T cell infiltration and microhemorrhage. Proc Natl Acad Sci U S A 2007; 104:2507-12; PMID:17264212; http://dx.doi.org/10.1073/pnas.0609377104
28. DaSilva KA, Brown ME, McLaurin J. Reduced oligomeric and vascular amyloid-beta following immunization of TgCRND8 mice with an Alzheimer's DNA vaccine. Vaccine 2009; 27:1365-76; PMID:19150380; http://dx.doi.org/10.1016/j.vaccine.2008.12.044
29. Pride M, Seubert P, Grundman M, Hagen M, Eldridge J, Black RS. Progress in the active immunotherapeutic approach to Alzheimer's disease: clinical investigations into AN1792-associated meningoencephalitis. Neurodegener Dis 2008; 5:194-6; PMID:18322388; http://dx.doi.org/10.1159/000113700
30. Kutzler MA, Cao C, Bai Y, Dong H, Choe PY, Saulino V, McLaughlin L, Whelan A, Choo AY, Weiner DB, et al. Mapping of immune responses following wild-type and mutant ABeta42 plasmid or peptide vaccination in different mouse haplotypes and HLA Class II transgenic mice. Vaccine 2006; 24:4630-9; PMID:16157426; http://dx.doi.org/10.1016/j.vaccine.2005.08.036
31. Subramanian S, D'Souza R, Divya Shree AN. Identification and mapping of linear antigenic determinants of human amyloid ß(1-42) peptide. J Immunoassay Immunochem 2012; 33:26-34; PMID:22181818; http://dx.doi.org/10.1080/15321819.2011.591477
32. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, et al. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 2000; 6:916-9; PMID:10932230; http://dx.doi.org/10.1038/78682
33. Wilcock DM, DiCarlo G, Henderson D, Jackson J, Clarke K, Ugen KE, Gordon MN, Morgan D. Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation. J Neurosci 2003; 23:3745-51; PMID:12736345
34. Wang W, Fan L, Xu D, Wen Z, Yu R, Ma Q. Immunotherapy for Alzheimer's disease. Acta Biochim Biophys Sin (Shanghai) 2012; 44:807-14; PMID:22899646; http://dx.doi.org/10.1093/abbs/gms065
35. Austin L, Arendash GW, Gordon MN, Diamond DM, DiCarlo G, Dickey C, Ugen K, Morgan D. Short-term beta-amyloid vaccinations do not improve cognitive performance in cognitively impaired APP + PS1 mice. Behav Neurosci 2003; 117:478-84; PMID:12802876; http://dx.doi.org/10.1037/0735-7044.117.3.478
36. Arendash GW, Schleif W, Rezai-Zadeh K, Jackson EK, Zacharia LC, Cracchiolo JR, Shippy D, Tan J. Caffeine protects Alzheimer's mice against cognitive impairment and reduces brain beta-amyloid production. Neuroscience 2006; 142:941-52; PMID:16938404; http://dx.doi.org/10.1016/j.neuroscience.2006.07.021
37. Costa DA, Cracchiolo JR, Bachstetter AD, Hughes TF, Bales KR, Paul SM, et al. Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol Aging 2007;28:831-44 PMID:16730391
38. Rezai-Zadeh K, Shytle D, Sun N, Mori T, Hou H, Jeanniton D, Ehrhart J, Townsend K, Zeng J, Morgan D, et al. Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice. J Neurosci 2005; 25:8807-14; PMID:16177050; http://dx.doi.org/10.1523/JNEUROSCI.1521-05.2005
39. Rutten K, Prickaerts J, Blokland A. Rolipram reverses scopolamine-induced and time-dependent memory deficits in object recognition by different mechanisms of action. Neurobiol Learn Mem 2006; 85:132-8; PMID:16242977; http://dx.doi.org/10.1016/j.nlm.2005.09.002
40. Arendash WG, Sanchez-Ramos JTM, Takashi, Mamcarz M, Runfeldt M, Wang L, Zhang G. Electromagnetic Field Treatment Protects Against and Reverses Cognitive Impairment in Alzheimer's Disease Mice. J Alzheimers Dis 2010; 19:191-210; PMID:20061638
41. Michaud JP, Hallé M, Lampron A, Thériault P, Préfontaine P, Filali M, Tribout-Jover P, Lanteigne AM, Jodoin R, Cluff C, et al. Toll-like receptor 4 stimulation with the detoxified ligand monophosphoryl lipid A improves Alzheimer's disease-related pathology. Proc Natl Acad Sci U S A 2013; 110:1941-6; PMID:23322736; http://dx.doi.org/10.1073/pnas.1215165110
42. Michaud M, Balardy L, Moulis G, Gaudin C, Peyrot C, Vellas B, Cesari M, Nourhashemi F. Proinflammatory cytokines, aging, and age-related diseases. J Am Med Dir Assoc 2013; 14:877-82; PMID:23792036; http://dx.doi.org/10.1016/j.jamda.2013.05.009
43. Cao C, Lin X, Wahi MM, Jackson EA, Potter H Jr. Successful adjuvant-free vaccination of BALB/c mice with mutated amyloid beta peptides. BMC Neurosci 2008; 9:25; PMID:18282292; http://dx.doi.org/10.1186/1471-2202-9-25
44. Costa DA, Nilsson LN, Bales KR, Paul SM, Potter H. Apolipoprotein is required for the formation of filamentous amyloid, but not for amorphous Abeta deposition, in an AbetaPP/PS double transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 2004; 6:509-14; PMID:15505373
45. Moore BD, Chakrabarty P, Levites Y, Kukar TL, Baine AM, Moroni T, Ladd TB, Das P, Dickson DW, Golde TE. Overlapping profiles of Aβ peptides in the Alzheimer's disease and pathological aging brains. Alzheimers Res Ther 2012; 4:18; PMID:22621179; http://dx.doi.org/10.1186/alzrt121