A Neuronal Microtubule-Interacting Agent, NAPVSIPQ, Reduces Tau Pathology and Enhances Cognitive Function in a Mouse Model of Alzheimer’s Disease
10.1124/jpet.107.130526
Crossref journal-article
Elsevier BV
The Journal of Pharmacology and Experimental Therapeutics (78)
Bibliography

Matsuoka, Y., Jouroukhin, Y., Gray, A. J., Ma, L., Hirata-Fukae, C., Li, H.-F., Feng, L., Lecanu, L., Walker, B. R., Planel, E., Arancio, O., Gozes, I., & Aisen, P. S. (2008). A Neuronal Microtubule-Interacting Agent, NAPVSIPQ, Reduces Tau Pathology and Enhances Cognitive Function in a Mouse Model of Alzheimer’s Disease. The Journal of Pharmacology and Experimental Therapeutics, 325(1), 146–153.

Authors 13
  1. Yasuji Matsuoka (first)
  2. Yan Jouroukhin (additional)
  3. Audrey J. Gray (additional)
  4. Li Ma (additional)
  5. Chiho Hirata-Fukae (additional)
  6. Hui-Fang Li (additional)
  7. Li Feng (additional)
  8. Laurent Lecanu (additional)
  9. Benjamin R. Walker (additional)
  10. Emmanuel Planel (additional)
  11. Ottavio Arancio (additional)
  12. Illana Gozes (additional)
  13. Paul S. Aisen (additional)
References 43 Referenced 178
  1. Ahlijanian MK, Barrezueta NX, Williams RD, Jakowski A, Kowsz KP, McCarthy S, Coskran T, Carlo A, Seymour PA, Burkhardt JE, et al. (2000) Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad SciUSA 97: 2910–2915. (10.1073/pnas.040577797)
  2. Alcalay RN, Giladi E, Pick CG, and Gozes I (2004) Intranasal administration of NAP, a neuroprotective peptide, decreases anxiety-like behavior in aging mice in the elevated plus maze. Neurosci Lett 361: 128–131. (10.1016/j.neulet.2003.12.005)
  3. Alonso AC, Zaidi T, Grundke-Iqbal I, and Iqbal K (1994) Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease. Proc Natl Acad SciUSA 91: 5562–5566. (10.1073/pnas.91.12.5562)
  4. Ashur-Fabian O, Segal-Ruder Y, Skutelsky E, Brenneman DE, Steingart RA, Giladi E, and Gozes I (2003) The neuroprotective peptide NAP inhibits the aggregation of the beta-amyloid peptide. Peptides 24: 1413–1423. (10.1016/j.peptides.2003.08.005)
  5. Bassan M, Zamostiano R, Davidson A, Pinhasov A, Giladi E, Perl O, Bassan H, Blat C, Gibney G, Glazner G, et al. (1999) Complete sequence of a novel protein containing a femtomolar-activity-dependent neuroprotective peptide. J Neurochem 72: 1283–1293. (10.1046/j.1471-4159.1999.0721283.x)
  6. Braak H and Braak E (1995) Staging of Alzheimer’s disease-related neurofibrillary changes. Neurobiol Aging 16: 271–278. (10.1016/0197-4580(95)00021-6)
  7. Bramblett GT, Goedert M, Jakes R, Merrick SE, Trojanowski JQ, and Lee VM (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer’s disease recapitulates development and contributes to reduced microtubule binding. Neuron 10: 1089–1099. (10.1016/0896-6273(93)90057-X)
  8. Divinski I, Holtser-Cochav M, Vulih-Schultzman I, Steingart RA, and Gozes I (2006) Peptide neuroprotection through specific interaction with brain tubulin. J Neurochem 98: 973–984. (10.1111/j.1471-4159.2006.03936.x)
  9. Divinski I, Mittelman L, and Gozes I (2004) A femtomolar acting octapeptide interacts with tubulin and protects astrocytes against zinc intoxication. J Biol Chem 279: 28531–28538. (10.1074/jbc.M403197200)
  10. Djordjevic J, Jones-Gotman M, De Sousa K, and Chertkow H (2008) Olfaction in patients with mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging, in press. (10.1016/j.neurobiolaging.2006.11.014)
  11. Engel T, Goni-Oliver P, Lucas JJ, Avila J, and Hernandez F (2006) Chronic lithium administration to FTDP-17 tau and GSK-3beta overexpressing mice prevents tau hyperphosphorylation and neurofibrillary tangle formation, but pre-formed neurofibrillary tangles do not revert. J Neurochem 99: 1445–1455. (10.1111/j.1471-4159.2006.04139.x)
  12. Franklin KBJ and Paxinos G (1997) The Mouse Brain in Streotaxic Coordinates, Academic Press, London, UK.
  13. Frick KM, Burlingame LA, Arters JA, and Berger-Sweeney J (2000) Reference memory, anxiety and estrous cyclicity in C57BL/6NIA mice are affected by age and sex. Neuroscience 95: 293–307. (10.1016/S0306-4522(99)00418-2)
  14. Gordon I, Genis I, Grauer E, Sehayek E, and Michaelson DM (1996) Biochemical and cognitive studies of apolipoprotein-E-deficient mice. Mol Chem Neuropathol 28: 97–103. (10.1007/BF02815210)
  15. Gozes I and Divinski I (2004) The femtomolar-acting NAP interacts with microtubules: novel aspects of astrocyte protection. J Alzheimers Dis 6: S37–S41. (10.3233/JAD-2004-6S605)
  16. Gozes I, Giladi E, Pinhasov A, Bardea A, and Brenneman DE (2000) Activity-dependent neurotrophic factor: intranasal administration of femtomolar-acting peptides improve performance in a water maze. J Pharmacol Exp Ther 293: 1091–1098. (10.1016/S0022-3565(24)39336-X)
  17. Gozes I, Morimoto BH, Tiong J, Fox A, Sutherland K, Dangoor D, Holser-Cochav M, Vered K, Newton P, Aisen PS, et al. (2005) NAP: research and development of a peptide derived from activity-dependent neuroprotective protein (ADNP). CNS Drug Rev 11: 353–368. (10.1111/j.1527-3458.2005.tb00053.x)
  18. Greenberg SG and Davies P (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad SciUSA 87: 5827–5831. (10.1073/pnas.87.15.5827)
  19. Hashiguchi M, Saito T, Hisanaga S, and Hashiguchi T (2002) Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/Thr205 of human tau. J Biol Chem 277: 44525–44530. (10.1074/jbc.M207426200)
  20. Horikoshi Y, Sakaguchi G, Becker AG, Gray AJ, Duff K, Aisen PS, Yamaguchi H, Maeda M, Kinoshita N, and Matsuoka Y (2004) Development of Aβ terminal end-specific antibodies and sensitive ELISA for Aβ variant. Biochem Biophys Res Commun 319: 733–737. (10.1016/j.bbrc.2004.05.051)
  21. Kosik KS, Orecchio LD, Binder L, Trojanowski JQ, Lee VM, and Lee G (1988) Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1: 817–825. (10.1016/0896-6273(88)90129-8)
  22. Kulaga HM, Leitch CC, Eichers ER, Badano JL, Lesemann A, Hoskins BE, Lupski JR, Beales PL, Reed RR, and Katsanis N (2004) Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat Genet 36: 994–998. (10.1038/ng1418)
  23. Lee JJ and Swain SM (2006) Peripheral neuropathy induced by microtubule-stabilizing agents. J Clin Oncol 24: 1633–1642. (10.1200/JCO.2005.04.0543)
  24. Lindwall G and Cole RD (1984) Phosphorylation affects the ability of tau protein to promote microtubule assembly. J Biol Chem 259: 5301–5305. (10.1016/S0021-9258(17)42989-9)
  25. Maccioni RB, Lavados M, Guillon M, Mujica C, Bosch R, Farias G, and Fuentes P (2006) Anomalously phosphorylated tau and Aβ fragments in the CSF correlates with cognitive impairment in MCI subjects. Neurobiol Aging 27: 237–244. (10.1016/j.neurobiolaging.2005.01.011)
  26. Matsuoka Y, Gray AJ, Hirata-Fukae C, Minami SS, Waterhouse EG, Mattson MP, LaFerla FM, Gozes I, and Aisen PS (2007) Intranasal NAP administration reduces accumulation of amyloid peptide and tau hyperphosphorylation in a transgenic mouse model of Alzheimer’s disease at early pathological stage. J Mol Neurosci 31: 165–170. (10.1385/JMN/31:02:165)
  27. Melnikova I (2007) Therapies for Alzheimer’s disease. Nat Rev Drug Discov 6: 341–342. (10.1038/nrd2314)
  28. Mercken M, Vandermeeren M, Lubke U, Six J, Boons J, Van de Voorde A, Martin JJ, and Gheuens J (1992) Monoclonal antibodies with selective specificity for Alzheimer Tau are directed against phosphatase-sensitive epitopes. Acta Neuropathol 84: 265–272. (10.1007/BF00227819)
  29. Michaelis ML (2006) Ongoing in vivo studies with cytoskeletal drugs in tau transgenic mice. Curr Alzheimer Res 3: 215–219. (10.2174/156720506777632880)
  30. Morimoto BH, de Lannoy I, Liu X, Yang Y, Fox A, Tiong J, and Gozes I (2006) Pharmacokinetics of the neuroprotective peptide, NAPVSIPQ, in serial samples of plasma and CSF after intravenous or intranasal administration. Drug Metab Rev 38 (Suppl 2): 213–214.
  31. Morris RG, Garrud P, Rawlins JN, and O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297: 681–683. (10.1038/297681a0)
  32. Mudher A, Shepherd D, Newman TA, Mildren P, Jukes JP, Squire A, Mears A, Drummond JA, Berg S, MacKay D, et al. (2004) GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol Psychiatry 9: 522–530. (10.1038/sj.mp.4001483)
  33. Noble W, Planel E, Zehr C, Olm V, Meyerson J, Suleman F, Gaynor K, Wang L, LaFrancois J, Feinstein B, et al. (2005) Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad SciUSA 102: 6990–6995. (10.1073/pnas.0500466102)
  34. Oddo S, Billings L, Kesslak JP, Cribbs DH, and LaFerla FM (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the Proteasome. Neuron 43: 321–332. (10.1016/j.neuron.2004.07.003)
  35. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, and LaFerla FM (2003) Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular Aβ and synaptic dysfunction. Neuron 39: 409–421. (10.1016/S0896-6273(03)00434-3)
  36. Plattner F, Angelo M, and Giese KP (2006) The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J Biol Chem 281: 25457–25465. (10.1074/jbc.M603469200)
  37. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, Gerstein H, Yu GQ, and Mucke L (2007) Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer’s disease mouse model. Science 316: 750–754. (10.1126/science.1141736)
  38. Sánchez-Andrade G, James BM, and Kendrick KM (2005) Neural encoding of olfactory recognition memory. J Reprod Dev 51: 547–558. (10.1262/jrd.17031)
  39. SantaCruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E, et al. (2005) Tau suppression in a neurode-generative mouse model improves memory function. Science 309: 476–481. (10.1126/science.1113694)
  40. Spittaels K, Van Den HC, Van Dorpe J, Geerts H, Mercken M, Bruynseels K, Lasrado R, Vandezande K, Laenen I, Boon T, et al. (2000) Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J Biol Chem 275: 41340–41349. (10.1074/jbc.M006219200)
  41. Vulih-Shultzman I, Pinhasov A, Mandel S, Grigoriadis N, Touloumi O, Pittel Z, and Gozes I (2007) Activity-dependent neuroprotective protein snippet NAP reduces tau hyperphosphorylation and enhances learning in a novel transgenic mouse model. J Pharmacol Exp Ther 323: 438–449. (10.1124/jpet.107.129551)
  42. Wilson RS, Arnold SE, Schneider JA, Tang Y, and Bennett DA (2007) The relationship between cerebral Alzheimer’s disease pathology and odour identification in old age. J Neurol Neurosurg Psychiatry 78: 30–35. (10.1136/jnnp.2006.099721)
  43. Zhang B, Maiti A, Shively S, Lakhani F, Donald-Jones G, Bruce J, Lee EB, Xie SX, Joyce S, Li C, et al. (2005) Microtubule-binding drugs offset tau sequestration by stabilizing microtubules and reversing fast axonal transport deficits in a tauopathy model. Proc Natl Acad SciUSA 102: 227–231. (10.1073/pnas.0406361102)
Dates
Type When
Created 17 years, 7 months ago (Jan. 16, 2008, 8:45 p.m.)
Deposited 6 months, 2 weeks ago (Feb. 19, 2025, 5:35 p.m.)
Indexed 3 days, 2 hours ago (Sept. 3, 2025, 6:42 a.m.)
Issued 17 years, 5 months ago (April 1, 2008)
Published 17 years, 5 months ago (April 1, 2008)
Published Print 17 years, 5 months ago (April 1, 2008)
Funders 0

None

@article{Matsuoka_2008, title={A Neuronal Microtubule-Interacting Agent, NAPVSIPQ, Reduces Tau Pathology and Enhances Cognitive Function in a Mouse Model of Alzheimer’s Disease}, volume={325}, ISSN={0022-3565}, url={http://dx.doi.org/10.1124/jpet.107.130526}, DOI={10.1124/jpet.107.130526}, number={1}, journal={The Journal of Pharmacology and Experimental Therapeutics}, publisher={Elsevier BV}, author={Matsuoka, Yasuji and Jouroukhin, Yan and Gray, Audrey J. and Ma, Li and Hirata-Fukae, Chiho and Li, Hui-Fang and Feng, Li and Lecanu, Laurent and Walker, Benjamin R. and Planel, Emmanuel and Arancio, Ottavio and Gozes, Illana and Aisen, Paul S.}, year={2008}, month=apr, pages={146–153} }