R-flurbiprofen improves tau, but not Aß pathology in a triple transgenic model of Alzheimer's disease

Brain Research

Volumn 1541, Issue , 2013, Pages 115-127

  Carreras, Isabel ^a,b   McKee, Ann C ^a,b   Choi, Ji Kyung ^c   Aytan, Nurgul ^a,b   Kowall, Neil W ^a,b   Jenkins, Bruce G ^c   Dedeoglu, Alpaslan ^a,b,c  

^a VA BOSTON HEALTHCARE SYSTEM   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

3xTg AD mice; A ; Hyperphosphorylated tau; Magnetic resonance spectroscopy; R flurbiprofen

Indexed keywords

AMYLOID BETA PROTEIN; FLURBIPROFEN; GLUTAMIC ACID; GLUTAMINE; TARENFLURBIL; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; COGNITION; CONTROLLED STUDY; ENANTIOMER; HIPPOCAMPAL CA1 REGION; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MAZE TEST; MEMORY CONSOLIDATION; MOUSE; NEUROCHEMISTRY; NEUROPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SPATIAL MEMORY; SUBICULUM; SYNAPSE; TRANSGENIC MOUSE; TREATMENT RESPONSE;

MUS; MUS MUSCULUS;

3XTG-AD MICE; ASS; HYPERPHOSPHORYLATED TAU; MAGNETIC RESONANCE SPECTROSCOPY; R-FLURBIPROFEN;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; DISEASE MODELS, ANIMAL; FLURBIPROFEN; GLUTAMIC ACID; GLUTAMINE; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE SPECTROSCOPY; MAZE LEARNING; MICE; MICE, TRANSGENIC; TAU PROTEINS;

EID: 84887989347     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.10.025     Document Type: Article

References (80)

1. P.S. Aisen The potential of anti-inflammatory drugs for the treatment of Alzheimer's disease Lancet Neurol. 1 2002 279 284
2. H. Akiyama, S. Barger, S. Barnum, B. Bradt, J. Bauer, G.M. Cole, N.R. Cooper, P. Eikelenboom, M. Emmerling, B.L. Fiebich, C.E. Finch, S. Frautschy, W.S. Griffin, H. Hampel, M. Hull, G. Landreth, L. Lue, R. Mrak, I.R. Mackenzie, P.L. McGeer, M.K. O'Banion, J. Pachter, G. Pasinetti, C. Plata-Salaman, J. Rogers, R. Rydel, Y. Shen, W. Streit, R. Strohmeyer, I. Tooyoma, F.L. Van Muiswinkel, R. Veerhuis, D. Walker, S. Webster, B. Wegrzyniak, G. Wenk, and T. Wyss-Coray Inflammation and Alzheimer's disease Neurobiol. Aging 21 2000 383 421
3. G.W. Arendash, M.F. Garcia, D.A. Costa, J.R. Cracchiolo, I.M. Wefes, and H. Potter Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition NeuroReport 15 2004 1751 1754
4. C. Balducci, B. Mehdawy, L. Mare, A. Giuliani, L. Lorenzini, S. Sivilia, L. Giardino, L. Calza, A. Lanzillotta, I. Sarnico, M. Pizzi, A. Usiello, A.R. Viscomi, S. Ottonello, G. Villetti, B.P. Imbimbo, G. Nistico, G. Forloni, and R. Nistico The gamma-secretase modulator CHF5074 restores memory and hippocampal synaptic plasticity in plaque-free Tg2576 mice J. Alzheimer's Dis. 24 2011 799 816
5. T.A. Bayer, O. Wirths, K. Majtenyi, T. Hartmann, G. Multhaup, K. Beyreuther, and C. Czech Key factors in Alzheimer's disease: beta-amyloid precursor protein processing, metabolism and intraneuronal transport Brain Pathol. 11 2001 1 11
6. D. Beher, E.E. Clarke, J.D. Wrigley, A.C. Martin, A. Nadin, I. Churcher, and M.S. Shearman Selected non-steroidal anti-inflammatory drugs and their derivatives target gamma-secretase at a novel site. Evidence for an allosteric mechanism J. Biol. Chem. 279 2004 43419 43426
7. K. Bhaskar, M. Konerth, O.N. Kokiko-Cochran, A. Cardona, R.M. Ransohoff, and B.T. Lamb Regulation of tau pathology by the microglial fractalkine receptor Neuron 68 2010 19 31
8. L.M. Billings, S. Oddo, K.N. Green, J.L. McGaugh, and F.M. LaFerla Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice Neuron 45 2005 675 688
9. K. Blennow, M.J. de Leon, and H. Zetterberg Alzheimer's disease Lancet 368 2006 387 403
10. H. Braak, and E. Braak Frequency of stages of Alzheimer-related lesions in different age categories Neurobiol. Aging 18 1997 351 357
11. R. Brookmeyer, E. Johnson, K. Ziegler-Graham, and H.M. Arrighi Forecasting the global burden of Alzheimer's disease Alzheimers Dement. 3 2007 186 191
12. B. Bulic, J. Ness, S. Hahn, A. Rennhack, T. Jumpertz, and S. Weggen Chemical biology, molecular mechanism and clinical perspective of gamma-secretase modulators in Alzheimer's disease Curr. Neuropharmacol. 9 2011 598 622
13. A. Carabaza, F. Cabre, E. Rotllan, M. Gomez, M. Gutierrez, M.L. Garcia, and D. Mauleon Stereoselective inhibition of inducible cyclooxygenase by chiral nonsteroidal antiinflammatory drugs J. Clin. Pharmacol. 36 1996 505 512
14. J.-K. Choi, A. Dedeoglu, and B.G. Jenkins Application of MR spectroscopy to mouse models of neurodegeneration NMR Biomed. 20 2007 216 237
15. J.K. Choi, B.G. Jenkins, I. Carreras, S. Kaymakcalan, K. Cormier, N.W. Kowall, and A. Dedeoglu Anti-inflammatory treatment in AD mice protects against neuronal pathology Exp. Neurol. 223 2010 377 384
16. A. Dedeoglu, J.K. Choi, K. Cormier, N.W. Kowall, and B.G. Jenkins Magnetic resonance spectroscopic analysis of Alzheimer's disease mouse brain that express mutant human APP shows altered neurochemical profile Brain Res. 1012 2004 60 65
17. J.L. Eriksen, S.A. Sagi, T.E. Smith, S. Weggen, P. Das, D.C. McLendon, V.V. Ozols, K.W. Jessing, K.H. Zavitz, E.H. Koo, and T.E. Golde NSAIDs and enantiomers of flurbiprofen target gamma-secretase and lower Abeta 42 in vivo J. Clin. Invest. 112 2003 440 449
18. G. Geisslinger, J. Lotsch, S. Menzel, G. Kobal, and K. Brune Stereoselective disposition of flurbiprofen in healthy subjects following administration of the single enantiomers Br. J. Clin. Pharmacol. 37 1994 392 394
19. S. Ghosh, M.D. Wu, S.S. Shaftel, S. Kyrkanides, F.M. LaFerla, J.A. Olschowka, and M.K. O'Banion Sustained interleukin-1beta overexpression exacerbates tau pathology despite reduced amyloid burden in an Alzheimer's mouse model J. Neurosci. 33 2013 5053 5064
20. M.L. Giuffrida, F. Caraci, B. Pignataro, S. Cataldo, P. De Bona, V. Bruno, G. Molinaro, G. Pappalardo, A. Messina, A. Palmigiano, D. Garozzo, F. Nicoletti, E. Rizzarelli, and A. Copani Beta-amyloid monomers are neuroprotective J. Neurosci. 29 2009 10582 10587
21. S.G. Greenberg, P. Davies, J.D. Schein, and L.I. Binder Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau J. Biol. Chem. 267 1992 564 569
22. S. Grosch, I. Tegeder, K. Schilling, T.J. Maier, E. Niederberger, and G. Geisslinger Activation of c-Jun-N-terminal-kinase is crucial for the induction of a cell cycle arrest in human colon carcinoma cells caused by flurbiprofen enantiomers FASEB J. 17 2003 1316 1318
23. S. Hahn, T. Bruning, J. Ness, E. Czirr, S. Baches, H. Gijsen, C. Korth, C.U. Pietrzik, B. Bulic, and S. Weggen Presenilin-1 but not amyloid precursor protein mutations present in mouse models of Alzheimer's disease attenuate the response of cultured cells to gamma-secretase modulators regardless of their potency and structure J. Neurochem. 116 2011 385 395
24. 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
25. M.T. Heneka, M. Sastre, L. Dumitrescu-Ozimek, I. Dewachter, J. Walter, T. Klockgether, and F. Van Leuven Focal glial activation coincides with increased BACE1 activation and precedes amyloid plaque deposition in APP[V717I] transgenic mice J. Neuroinflammation 2 2005 22
26. B.P. Imbimbo, E. Del Giudice, V. Cenacchi, R. Volta, G. Villetti, F. Facchinetti, B. Riccardi, P. Puccini, N. Moretto, F. Grassi, S. Ottonello, and A. Leon In vitro and in vivo profiling of CHF5022 and CHF5074 Two beta-amyloid1-42 lowering agents Pharmacol. Res. 55 2007 318 328
27. B.P. Imbimbo An update on the efficacy of non-steroidal anti-inflammatory drugs in Alzheimer's disease Expert Opin. Invest. Drugs 18 2009 1147 1168
28. B.P. Imbimbo Why did tarenflurbil fail in Alzheimer's disease? J. Alzheimer's Dis. 17 2009 757 760
29. K. Iqbal, C. Alonso Adel, S. Chen, M.O. Chohan, E. El-Akkad, C.X. Gong, S. Khatoon, B. Li, F. Liu, A. Rahman, H. Tanimukai, and I. Grundke-Iqbal Tau pathology in Alzheimer disease and other tauopathies Biochim. Biophys. Acta 1739 2005 198 210
30. K. Iqbal, F. Liu, C.X. Gong, C. Alonso Adel, and I. Grundke-Iqbal Mechanisms of tau-induced neurodegeneration Acta Neuropathol. 118 2009 53 69
31. C.R., Jr. Jack, D.S. Knopman, W.J. Jagust, L.M. Shaw, P.S. Aisen, M.W. Weiner, R.C. Petersen, and J.Q. Trojanowski Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade Lancet 9 2010 119 128
32. P.T. Jantzen, K.E. Connor, G. DiCarlo, G.L. Wenk, J.L. Wallace, A.M. Rojiani, D. Coppola, D. Morgan, and M.N. Gordon Microglial activation and beta-amyloid deposit reduction caused by a nitric oxide-releasing nonsteroidal anti-inflammatory drug in amyloid precursor protein plus presenilin-1 transgenic mice J. Neurosci. 22 2002 2246 2254
33. B.G. Jenkins, P. Klivenyi, E. Kustermann, O.A. Andreassen, R.J. Ferrante, B.R. Rosen, and M.F. Beal Nonlinear decrease over time in N-acetyl aspartate levels in the absence of neuronal loss and increases in glutamine and glucose in transgenic Huntington's disease mice J. Neurochem. 74 2000 2108 2119
34. B.G. Jenkins, O.A. Andreassen, A. Dedeoglu, B. Leavitt, M. Hayden, D. Borchelt, C.A. Ross, R.J. Ferrante, and M.F. Beal Effects of CAG repeat length, HTT protein length and protein context on cerebral metabolism measured using magnetic resonance spectroscopy in transgenic mouse models of Huntington's disease J. Neurochem. 95 2005 553 562
35. J. Kim, L. Onstead, S. Randle, R. Price, L. Smithson, C. Zwizinski, D.W. Dickson, T. Golde, and E. McGowan Abeta40 inhibits amyloid deposition in vivo J. Neurosci. 27 2007 627 633
36. M. Kitazawa, S. Oddo, T.R. Yamasaki, K.N. Green, and F.M. LaFerla Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease J. Neurosci. 25 2005 8843 8853
37. A. Klegeris, J. Maguire, and P.L. McGeer S- but not R-enantiomers of flurbiprofen and ibuprofen reduce human microglial and THP-1 cell neurotoxicity J. Neuroimmunol. 152 2004 73 77
38. W.E. Klunk, C. Xu, K. Panchalingam, R.J. McClure, and J.W. Pettegrew Quantitative 1H and 31P MRS of PCA extracts of postmortem Alzheimer's disease brain Neurobiol. Aging 17 1996 349 357
39. T. Kukar, S. Prescott, J.L. Eriksen, V. Holloway, M.P. Murphy, E.H. Koo, T.E. Golde, and M.M. Nicolle Chronic administration of R-flurbiprofen attenuates learning impairments in transgenic amyloid precursor protein mice BMC Neurosci. 8 2007 54
40. I. Kuperstein, K. Broersen, I. Benilova, J. Rozenski, W. Jonckheere, M. Debulpaep, A. Vandersteen, I. Segers-Nolten, K. Van Der Werf, V. Subramaniam, D. Braeken, G. Callewaert, C. Bartic, R. D'Hooge, I.C. Martins, F. Rousseau, J. Schymkowitz, and B. De Strooper Neurotoxicity of Alzheimer's disease Abeta peptides is induced by small changes in the Abeta42 to Abeta40 ratio EMBO J. 29 2010 3408 3420
41. P.N. Lacor, M.C. Buniel, P.W. Furlow, A.S. Clemente, P.T. Velasco, M. Wood, K.L. Viola, and W.L. Klein Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease J. Neurosci. 27 2007 796 807
42. D.C. Lee, J. Rizer, M.L. Selenica, P. Reid, C. Kraft, A. Johnson, L. Blair, M.N. Gordon, C.A. Dickey, and D. Morgan LPS-induced inflammation exacerbates phospho-tau pathology in rTg4510 mice J. Neuroinflammation 7 2010 56
43. V.M. Lee, M. Goedert, and J.Q. Trojanowski Neurodegenerative tauopathies Annu. Rev. Neurosci. 24 2001 1121 1159
44. J. Lewis, D.W. Dickson, W.L. Lin, L. Chisholm, A. Corral, G. Jones, S.H. Yen, N. Sahara, L. Skipper, D. Yager, C. Eckman, J. Hardy, M. Hutton, and E. McGowan Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP Science 293 2001 1487 1491
45. Y. Li, L. Liu, S.W. Barger, and W.S. Griffin Interleukin-1 mediates pathological effects of microglia on tau phosphorylation and on synaptophysin synthesis in cortical neurons through a p38-MAPK pathway J. Neurosci. 23 2003 1605 1611
46. S.F. Lichtenthaler, D. Beher, H.S. Grimm, R. Wang, M.S. Shearman, C.L. Masters, and K. Beyreuther The intramembrane cleavage site of the amyloid precursor protein depends on the length of its transmembrane domain Proc. Natl. Acad. Sci. USA 99 2002 1365 1370
47. G.P. Lim, F. Yang, T. Chu, P. Chen, W. Beech, B. Teter, T. Tran, O. Ubeda, K.H. Ashe, S.A. Frautschy, and G.M. Cole Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease J. Neurosci. 20 2000 5709 5714
48. G.P. Lim, F. Yang, T. Chu, E. Gahtan, O. Ubeda, W. Beech, J.B. Overmier, K. Hsiao-Ashec, S.A. Frautschy, and G.M. Cole Ibuprofen effects on Alzheimer pathology and open field activity in APPsw transgenic mice Neurobiol. Aging 22 2001 983 991
49. K.M. Lucin, and T. Wyss-Coray Immune activation in brain aging and neurodegeneration: too much or too little? Neuron 64 2009 110 122
50. A. Lleo, O. Berezovska, L. Herl, S. Raju, A. Deng, B.J. Bacskai, M.P. Frosch, M. Irizarry, and B.T. Hyman Nonsteroidal anti-inflammatory drugs lower Abeta42 and change presenilin 1 conformation Nat. Med. 10 2004 1065 1066
51. P.L. McGeer, and J. Rogers Anti-inflammatory agents as a therapeutic approach to Alzheimer's disease Neurology 42 1992 447 449
52. P.L. McGeer, M. Schulzer, and E.G. McGeer Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease: a review of 17 epidemiologic studies Neurology 47 1996 425 432
53. P.L. McGeer, and E.G. McGeer NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies Neurobiol. Aging 28 2007 639 647
54. A.C. McKee, I. Carreras, L. Hossain, H. Ryu, W.L. Klein, S. Oddo, F.M. LaFerla, B.G. Jenkins, N.W. Kowall, and A. Dedeoglu Ibuprofen reduces Abeta, hyperphosphorylated tau and memory deficits in Alzheimer mice Brain Res. 1207 2008 225 236
55. T. Morihara, T. Chu, O. Ubeda, W. Beech, and G.M. Cole Selective inhibition of Abeta42 production by NSAID R-enantiomers J. Neurochem. 83 2002 1009 1012
56. S. Oddo, A. Caccamo, J.D. Shepherd, M.P. Murphy, T.E. Golde, R. Kayed, R. Metherate, M.P. Mattson, Y. Akbari, and F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 2003 409 421
57. S. Oddo, V. Vasilevko, A. Caccamo, M. Kitazawa, D.H. Cribbs, and F.M. LaFerla Reduction of soluble Abeta and tau, but not soluble Abeta alone, ameliorates cognitive decline in transgenic mice with plaques and tangles J. Biol. Chem. 281 2006 39413 39423
58. M. Olabarria, H.N. Noristani, A. Verkhratsky, and J.J. Rodriguez Concomitant astroglial atrophy and astrogliosis in a triple transgenic animal model of Alzheimer's disease Glia 58 2010 831 838
59. J.W. Pettegrew, W.E. Klunk, K. Panchalingam, R.J. McClure, and J.A. Stanley Magnetic resonance spectroscopic changes in Alzheimer's disease Ann. N. Y. Acad. Sci. 826 1997 282 306
60. Z. Pfund, D.C. Chugani, C. Juhasz, O. Muzik, H.T. Chugani, I.B. Wilds, N. Seraji-Bozorgzad, and G.J. Moore Evidence for coupling between glucose metabolism and glutamate cycling using FDG PET and 1H magnetic resonance spectroscopy in patients with epilepsy J. Cereb. Blood Flow Metab. 20 2000 871 878
61. J.L. Price, and J.C. Morris Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease Ann. Neurol. 45 1999 358 368
62. B.D. Ross, S. Bluml, R. Cowan, E. Danielsen, N. Farrow, and R. Gruetter In vivo magnetic resonance spectroscopy of human brain: the biophysical basis of dementia Biophys. Chem. 68 1997 161 172
63. D.J. Selkoe Alzheimer's disease: genes, proteins, and therapy Physiol. Rev. 81 2001 741 766
64. D.J. Selkoe Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior Behav. Brain Res. 192 2008 106 113
65. G.M. Shankar, S. Li, T.H. Mehta, A. Garcia-Munoz, N.E. Shepardson, I. Smith, F.M. Brett, M.A. Farrell, M.J. Rowan, C.A. Lemere, C.M. Regan, D.M. Walsh, B.L. Sabatini, and D.J. Selkoe Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nat. Med. 14 2008 837 842
66. J.G. Sheng, S.G. Zhu, R.A. Jones, W.S. Griffin, and R.E. Mrak Interleukin-1 promotes expression and phosphorylation of neurofilament and tau proteins in vivo Exp. Neurol. 163 2000 388 391
67. T.K. Shonk, R.A. Moats, P. Gifford, T. Michaelis, J.C. Mandigo, J. Izumi, and B.D. Ross Probable Alzheimer disease: diagnosis with proton MR spectroscopy [see comments] Radiology 195 1995 65 72
68. G.J. Szpunar, K.S. Albert, and J.G. Wagner Pharmacokinetics of flurbiprofen in man. II. Plasma protein binding Res. Commun. Chem. Pathol. Pharmacol. 64 1989 17 30
69. I. Tegeder, E. Niederberger, E. Israr, H. Guhring, K. Brune, C. Euchenhofer, S. Grosch, and G. Geisslinger Inhibition of NF-kappaB and AP-1 activation by R- and S-flurbiprofen FASEB J. 15 2001 2 4
70. K.P. Townsend, and D. Pratico Novel therapeutic opportunities for Alzheimer's disease: focus on nonsteroidal anti-inflammatory drugs FASEB J. 19 2005 1592 1601
71. M. Townsend, Y. Qu, A. Gray, Z. Wu, T. Seto, M. Hutton, M.S. Shearman, and R.E. Middleton Oral treatment with a gamma-secretase inhibitor improves long-term potentiation in a mouse model of Alzheimer's disease J. Pharmacol. Exp. Ther. 333 2010 110 119
72. N.J. van Haeringen, A.A. van Sorge, J.L. Van Delft, and V.M. Carballosa Core-Bodelier Flurbiprofen and enantiomers in ophthalmic solution tested as inhibitors of prostanoid synthesis in human blood J. Ocul. Pharmacol. Ther. 16 2000 345 352
73. W.J. Wechter, A.E. Bigornia, E.D. Murray Jr., and W.S. Jee Chiral pharmacokinetics of Rac-flurbiprofen and pharmacodynamics of anabolic bone response in the normal rat Chirality 6 1994 457 459
74. S. Weggen, J.L. Eriksen, P. Das, S.A. Sagi, R. Wang, C.U. Pietrzik, K.A. Findlay, T.E. Smith, M.P. Murphy, T. Bulter, D.E. Kang, N. Marquez-Sterling, T.E. Golde, and E.H. Koo A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity Nature 414 2001 212 216
75. S. Weggen, J.L. Eriksen, S.A. Sagi, C.U. Pietrzik, V. Ozols, A. Fauq, T.E. Golde, and E.H. Koo Evidence that nonsteroidal anti-inflammatory drugs decrease amyloid beta 42 production by direct modulation of gamma-secretase activity J. Biol. Chem. 278 2003 31831 31837
76. G.K. Wilcock, S.E. Black, S.B. Hendrix, K.H. Zavitz, E.A. Swabb, and M.A. Laughlin Efficacy and safety of tarenflurbil in mild to moderate Alzheimer's disease: a randomised phase II trial Lancet Neurol. 7 2008 483 493
77. M.J. Winton, E.B. Lee, E. Sun, M.M. Wong, S. Leight, B. Zhang, J.Q. Trojanowski, and V.M. Lee Intraneuronal APP, not free Abeta peptides in 3xTg-AD mice: implications for tau versus Abeta-mediated Alzheimer neurodegeneration J. Neurosci. 31 2011 7691 7699
78. S. Wynne, and D. Djakiew NSAID inhibition of prostate cancer cell migration is mediated by Nag-1 Induction via the p38 MAPK-p75(NTR) pathway Mol. Cancer Res. 8 2010 1656 1664
79. Q. Yan, J. Zhang, H. Liu, S. Babu-Khan, R. Vassar, A.L. Biere, M. Citron, and G. Landreth Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease J. Neurosci. 23 2003 7504 7509
80. X. Zhao, G.W. Rebeck, H.S. Hoe, and P.M. Andrews Tarenflurbil protection from cytotoxicity is associated with an upregulation of neurotrophins J. Alzheimer's Dis. 15 2008 397 407