Central and peripheral administration of antisense oligonucleotide targeting amyloid-β protein precursor improves learning and memory and reduces neuroinflammatory cytokines in Tg2576 (AβPPswe) mice

Journal of Alzheimer's Disease

Volumn 40, Issue 4, 2014, Pages 1005-1016

  Farr, Susan A ^a,b   Erickson, Michelle A ^c,d   Niehoff, Michael L ^b   Banks, William A ^c,d   Morley, John E ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Antisense oligonucleotide; blood brain barrier; cytokines; learning; memory; object recognition; oxidative stress; T maze; Tg2576

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ANTISENSE OLIGONUCLEOTIDE; CXCL1 CHEMOKINE; CYTOKINE; EOTAXIN; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 9; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; AMYLOID BETA PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN TISSUE; COGNITIVE DEFECT; CONTROLLED STUDY; FOOTSHOCK; LATERAL BRAIN VENTRICLE; LEARNING; LEARNING DISORDER; MALE; MEMORY; MEMORY DISORDER; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TARGETING; T-MAZE TEST; TG2576 MOUSE; WILD TYPE; ANALYSIS OF VARIANCE; ANIMAL; CHEMISTRY; DISEASE MODEL; DRUG ADMINISTRATION ROUTE; DRUG EFFECTS; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LEARNING DISORDERS; MAZE TEST; MEMORY DISORDERS; METABOLISM; TRANSGENIC MOUSE;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION ROUTES; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; HUMANS; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; OLIGORIBONUCLEOTIDES, ANTISENSE; OXIDATIVE STRESS;

EID: 84901798645     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-131883     Document Type: Article

References (48)

1. Goate A, Hardy J (2012)Twenty years of Alzheimer's diseasecausing mutations. J Neurochem 120(Suppl 1), 3-8.
2. Ferreira ST, Klein WL (2011) The A oligomer hypothesis for synapse falure and memory loss in Alzheimer's disease. Neurobiol Learn Mem 96, 529-543.
3. Panza F, Solfrizzi V, Frisardi V, Imbimbo BP, Capurso C, D'Introno A, Calacicco AM, Seripa D, Vendemiale G, Capurso A, Pilotto A (2009) Beyond the neurotransmitterfocused approach in treating Alzheimer's disease: Drugs targeting beta-amyloid and tau protein. Aging Clin Exp Res 216, 386-406.
4. Malik R, Roy I (2011) Making sense of therapeutics using antisense techonology. Expert Opin Drug Discov 6, 507-526.
5. Kumar VB, Farr SA, Flood JF, Kamlesh V, Franko M, BanksWA, Morley JE (2000) Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides 21, 1769-1775.
6. Morley JE, Kumar VB, Bernardo AI, Farr SA, Uezu K, Tumosa N, Flood JF (2000) Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides 21, 1761-1767.
7. Poon HF, Joshi G, Sultana R, Farr SA, BanksWA, Morley JE, Calabrese V, Butterfield DA (2004) Antisense directed at the Abeta region of the APP decreases brain oxidative maarkers in aged senescence accelerated mice. Brain Res 1018, 86-96.
8. Banks WA, Kumar VB, Farr SA, Nakaoke R, Robinson SM, Morley JE (2011) Impairments in brain-to-blood transport of amyloid-B protein precursor. J Alzheimers Dis 23, 599-605.
9. Apelt J, Bigl M, Wunderlich P, Schliefs R (2004) Aging-related increase in oxidative stress correlates with developmental pattern of beta-secretase activity and betaamyloid plaque formation in transgenic Tg2576 mice with Alzheimer-like pathology. Int J Dev Neurosci 22, 475-484.
10. Dickstein DL, Biron KE, Ujie M, Pfeifer CG, Jeffries AR, Jefferies WA (2006) Abeta peptide immunization restores blood-brain barrier integrity in Alzheimer's disease. FASEB J 20, 426-433.
11. Hsaio K, Chapman P, Nilsen S, Erkman C, Harigaya Y, Yang F, Cole G (1996) Correlative memory deficits, A elevation, and amyloid plaques in transgenic mice. Science 274, 99-102.
12. Good MA, Hale G, Staal V (2007) Impaired "Episodic-Like" object memory in adult APPswe transgenic mice. Behav Neurosci 121, 443-448.
13. Hammond RS, Tull, Stackman LE, RW (2004) On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol Learn Mem 82, 26-34.
14. Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl) 92, 180-185.
15. Erickson MA, NiehoffML, Farr SA, Morley JE, Dillman LA, Lynch KM, Banks WA (2012) Peripheral admininstration of antisense oligonucleotides targeting the amyloid-B protein precursor reverses APP and LRP-1 overexpression in the aged SAMP8 mouse brain. J Alzheimers Dis 28, 951-960.
16. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, StreitW, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21, 383-421.
17. Erickson MA, Hansen K, Banks WA (2012) Inflammationinduced dysfunction of the low-density lipoprotein receptorrelated protein-1 at the blood-brain barrier: Protection by the antioxidant N-acetylcysteine. Brain Behav Immun 26, 1085-1094.
18. Farr SA, BanksWA, La Scola ME, Flood JF, Morley JE(2000) Permanent and temporary inactivation of the hippocampus impairs T-maze footshock avoidance acquisition and retention. Brain Res 872, 242-249.
19. Quinn JF, Bussiere JR, Hammond RS, Montine TJ, Henson E, Jones RE, Stackman RWJ (2007) Chronic dietary alphalipoic acid reduces deficits in hippocampal memory of aged Tg2576 mice. Neurobiol Aging 28, 213-225.
20. Yao Y, Chinnici C, Tang H, Trojanowski JQ, Lee VM, Pratico D (2004) Brain inflammation and oxidative stress in a transgenic mouse model of Alzheimer-like brain amyloidosis. J Neuroinflammation 1, 21.
21. Practico D, Uryu K, Leight S, Trojanoswki JQ, Lee VM (2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci 21, 4183-4187.
22. Stewart S, Cacucci F, Lever C (2011) Which memory task for my mouse? A systematic review of spatial memory performance in the Tg2576 Alzheimer's mouse model. J Alzheimers Dis 26, 105-126.
23. Farr SA, Uezu K, Creonte TA, Flood JF, Morley JE (2000) Modulation of memory processing in the cingulate cortex. Pharmacol Biochem Behav 65, 363-368.
24. Dobarro M, Gerenu G, Ramirez MJ (2013) Propranolol reduces cognitive deficits, amyloid and tau pathology in Alzheimer's transgenic mice. Int J Neuropsychopharmacol 16, 2245-2257.
25. Sivilia S, Lorenzini L, Giuliani A, Gusciglio M, Fernandez M, Baldassarro VA, Mangano C, Ferraro L, Pietrini V, Baroc MF, Viscomi AR, Ottonello S, Villetti G, Imbimbo BP, Calza L, Giardino L (2013) Multi-target action of the novel anti- Alzheimer compound CHF5074: In vivo study of long term treatment in Tg2576 mice. BMC Neurosci 14, 44.
26. Perry DC, Miller BL (2013) Frontotemporal dementia. Semin Neurol 33, 336-341.
27. Manoochehri M, HueyED(2012) Diagnosis and management of behavioral issues in frontotemporal dementia. Curr Neurol Neurosci Rep 12, 528-536.
28. Ognibene E, Middei S, Daniele S, Adriani W, Ghirardi O, Caprioli A, Laviola G (2005) Aspects of spatial memory and behavioral disinhibition in Tg2576 transgenic mice as a model of Alzheimer's disease. Behav Brain Res 156, 225-232.
29. Miners JS, Baig S, Palmer J, Palmer LE, Kehoe PG, Love S (2008) Abeta-degrading enzymes in Alzheimer's disease. Brain Pathol 18, 240-252.
30. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K, Xu F, Parisi M, LaRue B, HuHW, Spijkers P, Guo H, Song X, Lenting PJ, Van Norstrand WE, ZlokovicBV(2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 43, 333-344.
31. Ito S, Ohtsuki S, Kamiie J, Nezu Y, Terasaki T (2007) Cerebral clearance of human amyloid-beta peptide (1-40) across the blood-brain barrier is reduced by self-aggregation and formation of low-density lipoprotein receptor-related protein-1 ligand complexes. J Neurochem 103, 2482-2490.
32. Rakover I, Arbel M, Solomon B (2007) Immunotherapy against APP beta-secretase cleavage site improves cognitive function and reduces neuroinflammation in Tg2576 mice without a significant effect on brain abeta level. Neurodegener Dis 4, 392-402.
33. Morley JE, Farr SA, Banks WA, Johnson SN, Yamada KA, Xu L (2010) A physiological role for amyloid-beta protein: Enhancement of learning and memory. J Alzheimers Dis 19, 441-449.
34. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, Jones T, Banati RB (2001) In-vivo measurement of activated microglia in dementia. Lancet 358, 461-467.
35. Eidson P, Archer HA, Gerhard A, Hinz R, Pavese N, Turkheimer FE, Hammers A, Tai YF, Fox N, Kennedy A, Rossor M, Brooks DJ (2008) Microglia, amyloid, and cognition in Alzheimer's disease: An [11C](R) PK1195-PET study. Neurobiol Dis 32, 412-419.
36. Hoozemans JJ, Veerhuis R, Rozemuller JM, Eikelenboon P (2006) Neuroinflammation and regeneration in the early stages of Alzheimer's disease pathology. Int J Dev Neurosci 24, 157-165.
37. Morimoto K, Horio J, Satoh H, Sue L, Beach T, Arita S, Tooyama I, KonishiY(2011) Expression profiles of cytokines in the brain of Alzheimer's disease (AD) patients compared to the brain of non-demented patients with and without increasing AD pathology. J Alzheimers Dis 25, 59-76.
38. Sly LM, Krzesicki RF, Brashler JR, Buhl AE, McKinley DD, Carter DB, Chin JE (2001) Endogenous brain cytokinemRNA and inflammatory responses to lipolysaccharide are elevated in the Tg2576 mouse model of Alzheimer's disease. Brain Res Bull 56, 581-588.
39. Lue LF, Rydel R, Brigham EF, Yang LB, Hampel H, Murphy GM Jr, Brachova L, Yan SD, Walker DG, Shen Y, Rogers J (2001) Inflammatory repertiore of Alzheimer's disease and nondemented elderly microglia in virto. Glia 35, 72-79.
40. Kawahara K, Suenobu M, Yoshida A, Koga K, Hyodo A, Ohtsuka H, Kuniyasu A, Tamamaki N, Sugimoto Y, Nakayama H (2012) Intracerebral microinjection of interleukin-4/interleukin-13 reduces B-amyloid accumulation in the ipsilateral side and improves cognitive deficits in young amyloid precursor protein 23 mice. Neuroscience 207, 243-260.
41. Villeda SA, Luo J, Mosher KO, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, Lucin KM, Czirr E, Park JS, Couillard-Despres S, Aigner L, Peskind ER, Kaye JA, Quinn JF, Galasko DR, Xie XS, Rando TA, Wyss-Coray T (2011) The aging systemic millieu negatively regulates neurogenesis and cognitive funciton. Nature 477, 90-94.
42. BanksWA, Farr SA, ButtW, Kumar VB, FrankoMW, Morley JE (2001) Delivery across the blood-brain barrier of antisense directed against amyloid beta: Reversal of learning and memory deficits in mice overexpressing amyloid precursor protein. J Pharmacol Exp Ther 297, 1113-1121.
43. Banks WA, Jaeger LB, Urayama A, Kumar VB, Hileman SM, Gaskin FS, Llanza NV, Farr SA, Morley JE (2006) Preproenkephalin targeted antisenses cross the blood-brain barrier to reduced brain methionine enkephalin levels and increase voluntary ethanol drinking. Peptides 27, 784-796.
44. Schneider T, Becker A, Ringe K, Reinhold A, Firsching R, Sabel BA (2008) Brain tumor therapy by combined vaccination and antisense oligonucleotide delivery with nanoparticles. J Neuroimmunol 195, 21-27.
45. Hemmrich K, Kroncke KD, Suschek CV, Bolb-Bachofen V (2005) What sense lies in antisense inhibition of inducible nitric oxide synthase expression? Nitric Oxide 12, 183-199.
46. BanksWA(2001) Leptin transport across the blood-brain barrier: Implications for the cause and treatment of obesity. Curr Pharm Des 7, 125-133.
47. Banks WA, Kastin AJ, Huang W, Jaspan JB, Maness LM (1996) Leptin enters the brain by a saturable system independent of insulin. Peptides 17, 305-311.
48. Banks WA, Farr SA, Morley JE (2002-2003) Entry of bloodborne cytokines into the central nervous system: Effects of cognitive processes. Neuroimmunomodulation 10, 319-327.