A Novel Retro-Inverso Peptide Inhibitor Reduces Amyloid Deposition, Oxidation and Inflammation and Stimulates Neurogenesis in the APPswe/PS1ΔE9 Mouse Model of Alzheimer's Disease

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Parthsarathy, Vadivel ^a   McClean, Paula L ^a   Hölscher, Christian ^a   Taylor, Mark ^b   Tinker, Claire ^b   Jones, Glynn ^b   Kolosov, Oleg ^c   Salvati, Elisa ^d   Gregori, Maria ^d   Masserini, Massimo ^d   Allsop, David ^b  

^a UNIVERSITY OF ULSTER   (United Kingdom)

^b LANCASTER UNIVERSITY   (United Kingdom)

^c LANCASTER UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; PROTEIN INHIBITOR; RI OR2 TAT; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BINDING AFFINITY; BLOOD BRAIN BARRIER; BRAIN CORTEX; CELL ACTIVATION; CELL COUNT; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFICACY; HUMAN; HUMAN CELL; MALE; MICROGLIA; MOUSE; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN BINDING; TREATMENT RESPONSE;

ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BLOOD-BRAIN BARRIER; CELL LINE; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; INFLAMMATION; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; NEUROGENESIS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEPTIDES; PERMEABILITY; PLAQUE, AMYLOID; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

EID: 84873127460     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054769     Document Type: Article

References (56)

1. Brookmeyer R, Gray S, Kawas C, (1998) Projections of Alzheimer's disease in the United States and the public health impact of delaying disease onset. Am J Public Health 88: 1337-1342.
2. American Health Assistance Foundation website. Available: http://www.ahaf.org/alzheimers/about. Accessed 2012 Nov 1.
3. Hardy J, Allsop D (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12, 383-388.
4. Karran E, Mercken M, De Strooper B, (2011) The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat Rev Drug Discov 10: 698-712.
5. Ma QL, Yang F, Rosario ER, Ubeda OJ, Beech W, et al. (2009) β-amyloid oligomers induce phosphorylation of tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling: suppression by omega-3 fatty acids and curcumin. J Neurosci 29: 9078-9089.
6. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, et al. (1998) Diffusible, nonfibrillar ligands derived from Aβ 1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95: 6448-6453.
7. Wang HW, Pasternak JF, Kuo H, Ristic H, Lambert MP, et al. (2002) Soluble oligomers of β amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res 924: 133-140.
8. Walsh DM, Klybin I, Fadeeva JV, Cullen WK, Anwyl R, et al. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539.
9. Kim HJ, Chae SC, Lee DK, Chromy B, Lee SC, et al. (2003) Selective neuronal degeneration induced by soluble oligomeric amyloid β protein. FASEB J 17: 118-120.
10. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, et al. (2005) Natural oligomers of the amyloid-β protein specifically disrupt cognitive function. Nature Neurosci 8: 79-84.
11. Walsh DM, Selkoe DJ, (2007) Aβ oligomers- a decade of discovery. J Neurochem 101: 1172-1184.
12. Haass C, Selkoe DJ, (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nature Rev Mol Cell Biol 8: 101-112.
13. Citron M, (2010) Alzheimer's disease: strategies for disease modification. Nat Rev Drug Discov 9: 387-398.
14. De Felice FG, Vieira MN, Saraiva LM, Figueroa-Villar JD, Farcia-Abreu J, et al. (2004) Targeting the neurotoxic species in Alzheimer's disease: inhibitors of Aβ oligomerization. FASEB J 18: 1366-1372.
15. Howlett D, (2011) APP transgenic mice and their application to drug discovery. Histol Histopathol 26: 1611-1632.
16. Taylor M, Moore S, Mayes J, Parkin E, Beeg M, et al. (2010) Development of a proteolytically stable retro-inverso peptide inhibitor of β-amyloid oligomerization as a potential novel treatment for Alzheimer's disease. Biochemistry 20: 3261-3272.
17. Tjernberg LO, Näslund J, Lindqvist F, Johansson J, Karlström AR, et al. (1996) Arrest of β-amyloid fibril formation by a pentapeptide ligand. J Biol Chem 271: 8545-8548.
18. Tjernberg LO, Callaway DJO, Tjernberg A, Hahne S, Lilliehöök C, et al. (1999) A molecular model of Alzheimer amyloid β-peptide fibril formation. J Biol Chem 274: 12619-12625.
19. Sciarretta KL, Gordon DJ, Meredith SC, (2006) Peptide-based inhibitors of amyloid assembly. Methods Enzymol 413: 273-312.
20. Soto C, Kindy MS, Baumann M, Frangione B, (1996) Inhibition of Alzheimer's amyloidosis by peptides that prevent β-sheet conformation. Biochem Biophys Res Commun 226: 672-680.
21. Soto C, Sigurdsson EM, Morelli L, Kumar RA, Castano EM, et al. (1998) β-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer's therapy. Nature Med 4: 822-826.
22. Gordon DJ, Sciarretta KL, Meredith SC, (2001) Inhibition of β-amyloid (40) fibrillogenesis and disassembly of β-amyloid (40) fibrils by short β-amyloid congeners containing N-methyl amino acids at alternate residues. Biochemistry 40: 8237-8245.
23. Kokkoni N, Stott K, Amijee H, Mason JM, Doig AJ, (2006) N-Methylated peptide inhibitors of β-amyloid aggregation and toxicity. Optimization of the inhibitor structure. Biochemistry 45: 9906-9918.
24. Ghanta J, Shen CL, Kiessling LL, Murphy RM, (1996) A strategy for designing inhibitors of β-amyloid toxicity. J Biol Chem 271: 29525-29528.
25. Poduslo JF, Curran GL, Kumar A, Frangione B, Soto C, (1999) β-sheet breaker peptide inhibitor of Alzheimer's amyloidogenesis with increased blood-brain barrier permeability and resistance to proteolytic degradation in plasma. J Neurobiol 39: 371-382.
26. Findeis MA, Musso GM, Arico-Muendel CC, Benjamin HW, Hundal AM, et al. (1999) Modified-peptide inhibitors of amyloid β-peptide polymerization. Biochemistry 38: 6791-6800.
27. Green M, Loewenstein PM, (1988) Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55: 1179-1188.
28. Aguilar MI, Small DH, (2005) Surface plasmon resonance for the analysis of β-amyloid interactions and fibril formation in Alzheimer's disease research. Neurotox Res 7: 17-27.
29. Horcas I, Fernandez R, Gomez-Rodriquez JM, Colchero J, Gomez-Herrero J, et al. (2007) WSXM: a software for scanning probe microscopy and a tool for nanotechnology. Rev Sci Instrum 78: 013705.
30. Imai Y, Kohsaka S (2002) Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 40, 164-174.
31. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S, (1996) A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 224: 855-862.
32. Gleeson JG, Lin PT, Flanagan LA, Walsh CA, (1999) Doublecortin is a microtubule associated protein and is expressed widely by migrating neurons. Neuron 23: 257-71.
33. Ramanathan S, Pooyan S, Stein S, Prasad PD, Wang J, et al. (2009) Targeting the sodium-dependent multivitamin transporter (SMVT) for improving the oral absorption properties of a retro-inverso Tat nonapeptide. Mol Phar 6: 836-848.
34. Dietz GP, Bähr M, (2004) Delivery of bioactive molecules into the cell: the Trojan horse approach. Mol Cell Neurosci 27: 85-131.
35. Zhang X, Jin Y, Plummer MR, Pooyan S, Gunaseelan S, et al. (2007) Endocytosis and membrane potential are required for HeLa cell uptake of R.I.-CKTat9, a retro-inverso Tat cell penetrating peptide. Neuroscience 150: 40-49.
36. Repici M, Centeno C, Tomasi S, Forloni G, Bonny C, et al. (2001) Time-course of c-Jun N-terminal kinase activation after cerebral ischemia and effect of D-JNKI1 on c-Jun and caspase-3 activation. Pharm Res 18: 950-956.
37. Zhang G, Leibowitz MJ, Sinko PJ, Stein S, (2003) Multiple-peptide conjugates for binding β-amyloid plaques of Alzheimer's disease. Bioconj Chem 14: 86-92.
38. Paresce D, Chung H, Maxfield F, (1997) Slow degradation of aggregates of the Alzheimer's disease amyloid β-protein by microglial cells. J Biol Chem 114: 29390-29397.
39. McClean P, Parthsarathy V, Faivre E, Hölscher C, (2011) The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J Neurosci 31: 6587-6594.
40. Chafekar SM, Malda H, Merkx M, Meijer EW, Viertl D, et al. (2007) Branched KLVFF tetramers strongly potentiate inhibition of β-amyloid aggregation. ChemBioChem 8: 1857-1864.
41. Taylor M, Moore S, Mourtas S, Niarakis A, Re F, et al. (2011) Effect of curcumin-associated and lipid ligand-functionalized nanoliposomes on aggregation of the Alzheimer's Aβ peptide. Nanomedicine 7: 541-550.
42. Hölscher C, (1998) Possible causes of Alzheimer's disease: amyloid fragments, free radicals, and calcium homeostasis. Neurobiol Dis 5: 129-141.
43. Tabner BJ, El-Agnaf OM, Turnbull S, German MJ, Paleologou KE, et al. (2005) Hydrogen peroxide is generated during the very early stages of aggregation of the amyloid peptides implicated in Alzheimer's disease and familial British dementia. J Biol Chem 280: 35789-35792.
44. Kagan BL, Thundimadathil J, (2010) Amyloid peptide pores and the β sheet conformation. Adv Exp Med Biol 677: 150-167.
45. Nunomura A, Tamaoki T, Motohashi N, Nakamura M, McKeel DW, et al. (2012) The earliest stage of cognitive impairment in transition from normal aging to Alzheimer disease is marked by prominent RNA oxidation in vulnerable neurons. J Neuropathol Exp Neurol 71: 233-241.
46. Cunningham C, Skelly DT, (2011) Non-steroidal anti-inflammatory drugs and cognitive function: are prostaglandins at the heart of cognitive impairment in dementia and delirium? J Neuroimmune Pharmacol 7: 60-73.
47. Monje ML, Toda H, Palmer TD, (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765.
48. Mangialasche F, Solomon A, Winblad B, Mecocci P, Kivipelto M, (2010) Alzheimer's disease: clinical trials and drug development. Lancet Neurol 9: 702-716.
49. Klaver DW, Wilce MC, Cui H, Hung AC, Gasperini R, et al. (2010) Is BACE1 a suitable therapeutic target for the treatment of Alzheimer's disease? Current strategies and future directions. Biol Chem 391: 849-859.
50. Wolfe MS, (2008) Inhibition and modulation of γ-secretase for Alzheimer's disease. Neurotherapeutics 5: 391-398.
51. Schenk D, (2002) Amyloid-β immunotherapy for Alzheimer's disease: the end of the beginning. Nat Rev Neurosci 3: 824-828.
52. Yang F, Lim GP, Begum AN, Ubeda OJ, Simmons MR, et al. (2005) Curcumin inhibits formation of amyloid β oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280: 5892-5901.
53. Chen SY, Chen Y, Li YP, Chen SH, Tan JH, et al. (2011) Design, synthesis, and biological evaluation of curcumin analogues as multifunctional agents for the treatment of Alzheimer's disease. Bioorg Med Chem 19: 5596-5604.
54. Cramer PE, Cirrito JR, Wesson DW, Lee CY, Karlo JC, et al. (2012) ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models. Science 335: 1503-1506.
55. Scherzer-Attali R, Pellarin R, Convertino M, Frydman-Marom A, Egoz-Matia N, et al. (2010) Complete phenotypic recovery of an Alzheimer's disease model by a quinone-tryptophan hybrid aggregation inhibitor. PLoS One 5: e11101.
56. Zhang Y, He JS, Wang X, Wang J, Bao FX, et al. (2011) Administration of amyloid-β42 oligomer-specific monoclonal antibody improved memory performance in SAMP8 mice. J Alzheimers Dis 23: 551-561.