Effects of the C57BL/6 strain background on tauopathy progression in the rTg4510 mouse model

Molecular Neurodegeneration

Volumn 9, Issue 1, 2014, Pages

  Bailey, Rachel M ^a,b   Howard, John ^a,b   Knight, Joshua ^a,b   Sahara, Naruhiko ^a,b   Dickson, Dennis W ^b   Lewis, Jada ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Behavior; C57BL 6; Morris water maze; Neurodegeneration; rTg4510; Strain background; Tau; Tauopathy; Transgenic mouse models

Indexed keywords

TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL/6N MOUSE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; TAUOPATHY;

ANIMALS; BLOTTING, WESTERN; BRAIN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHENOTYPE; TAU PROTEINS; TAUOPATHIES;

EID: 84892729075     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-9-8     Document Type: Article

References (46)

1. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, Gwinn-Hardy K, Paul Murphy M, Baker M, Yu X, et al. Nat Genet 2000 25 402 405 10.1038/78078 10932182
2. Tau suppression in a neurodegenerative mouse model improves memory function. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E, et al. Science (New York, NY) 2005 309 476 481 10.1126/science.1113694
3. Induction of tau pathology by intracerebral infusion of amyloid-beta-containing brain extract and by amyloid-beta deposition in APP x Tau transgenic mice. Bolmont T, Clavaguera F, Meyer-Luehmann M, Herzig MC, Radde R, Staufenbiel M, Lewis J, Hutton M, Tolnay M, Jucker M, Am J Pathol 2007 171 2012 2020 10.2353/ajpath.2007.070403 18055549
4. Decreased locomotor activity in mice expressing tTA under control of the CaMKII alpha promoter. McKinney BC, Schneider JS, Schafer GL, Lowing JL, Mohan S, Zhao MX, Heng MY, Albin RL, Seasholtz AF, Akil H, Murphy GG, Genes, Brain, Behavior 2008 7 203 213 10.1111/j.1601-183X.2007.00339.x
5. Strain background influences neurotoxicity and behavioral abnormalities in mice expressing the tetracycline transactivator. Han HJ, Allen CC, Buchovecky CM, Yetman MJ, Born HA, Marin MA, Rodgers SP, Song BJ, Lu HC, Justice MJ, et al. J Neurosci 2012 32 10574 10586 10.1523/JNEUROSCI.0893-12.2012 22855807
6. Altered thymic selection by overexpressing cellular FLICE inhibitory protein in T cells causes lupus-like syndrome in a BALB/c but not C57BL/6 strain. Qiao G, Li Z, Minto AW, Shia J, Yang L, Bao L, Tschopp J, Gao JX, Wang J, Quigg RJ, Zhang J, Cell Death Differ 2010 17 522 533 10.1038/cdd.2009.143 19816511
7. Regulation of basement membrane-reactive B cells in BXSB, (NZBxNZW)F1, NZB, and MRL/lpr lupus mice. Clark AG, Fan Q, Brady GF, Mackin KM, Coffman ED, Weston ML, Foster MH, Autoimmunity 2013 46 188 204 10.3109/08916934.2012.746671 23157336
8. Control of memory formation through regulated expression of a CaMKII transgene. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER, Science (New York, NY) 1996 274 1678 1683 10.1126/science.274.5293.1678
9. A GFP-equipped bidirectional expression module well suited for monitoring tetracycline-regulated gene expression in mouse. Krestel HE, Mayford M, Seeburg PH, Sprengel R, Nucleic Acids Res 2001 29 39 10.1093/nar/29.7.e39 11266574
10. Developing tTA transgenic rats for inducible and reversible gene expression. Zhou H, Huang C, Yang M, Landel CP, Xia PY, Liu YJ, Xia XG, Int J Biol Sci 2009 5 171 181 19214245
11. Mechanisms of tau-induced neurodegeneration. Iqbal K, Liu F, Gong CX, Alonso Adel C, Grundke-Iqbal I, Acta Neuropathol 2009 118 53 69 10.1007/s00401-009-0486-3 19184068
12. Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. Otvos L Jr, Feiner L, Lang E, Szendrei GI, Goedert M, Lee VM, J Neurosci Res 1994 39 669 673 10.1002/jnr.490390607 7534834
13. Conformational change as one of the earliest alterations of tau in Alzheimer's disease. Weaver CL, Espinoza M, Kress Y, Davies P, Neurobiol Aging 2000 21 719 727 10.1016/S0197-4580(00)00157-3 11016541
14. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, Guimaraes A, Yue M, Lewis J, Carlson G, et al. J Neurosci 2005 25 10637 10647 10.1523/JNEUROSCI.3279-05.2005 16291936
15. A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Greenberg SG, Davies P, Proc Natl Acad Sci U S A 1990 87 5827 5831 10.1073/pnas.87.15.5827 2116006
16. What are we measuring when we test strain differences in anxiety in mice? O'Leary TP, Gunn RK, Brown RE, Behav Genet 2013 43 34 50 10.1007/s10519-012- 9572-8 23288504
17. Structural learning and the hippocampus. Aggleton JP, Sanderson DJ, Pearce JM, Hippocampus 2007 17 723 734 10.1002/hipo.20323 17598160
18. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Spires TL, Orne JD, SantaCruz K, Pitstick R, Carlson GA, Ashe KH, Hyman BT, Am J Pathol 2006 168 1598 1607 10.2353/ajpath.2006.050840 16651626
19. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. Berger Z, Roder H, Hanna A, Carlson A, Rangachari V, Yue M, Wszolek Z, Ashe K, Knight J, Dickson D, et al. J Neurosci 2007 27 3650 3662 10.1523/JNEUROSCI.0587-07.2007 17409229
20. Apoptosis in transgenic mice expressing the P301L mutated form of human tau. Ramalho RM, Viana RJ, Castro RE, Steer CJ, Low WC, Rodrigues CM, Mol Med 2008 14 309 317 18368144
21. In vivo imaging reveals dissociation between caspase activation and acute neuronal death in tangle-bearing neurons. Spires-Jones TL, de Calignon A, Matsui T, Zehr C, Pitstick R, Wu HY, Osetek JD, Jones PB, Bacskai BJ, Feany MB, et al. J Neurosci 2008 28 862 867 10.1523/JNEUROSCI.3072-08.2008 18216194
22. Aging analysis reveals slowed tau turnover and enhanced stress response in a mouse model of tauopathy. Dickey C, Kraft C, Jinwal U, Koren J, Johnson A, Anderson L, Lebson L, Lee D, Dickson D, de Silva R, et al. Am J Pathol 2009 174 228 238 10.2353/ajpath.2009.080764 19074615
23. LPS- induced inflammation exacerbates phospho-tau pathology in rTg4510 mice. Lee DC, Rizer J, Selenica ML, Reid P, Kraft C, Johnson A, Blair L, Gordon MN, Dickey CA, Morgan D, J Neuroinflammation 2010 7 56 10.1186/1742-2094-7-56 20846376
24. Structural and functional changes in tau mutant mice neurons are not linked to the presence of NFTs. Rocher AB, Crimins JL, Amatrudo JM, Kinson MS, Todd-Brown MA, Lewis J, Luebke JI, Exp Neurol 2010 223 385 393 10.1016/j.expneurol.2009.07.029 19665462
25. Soluble tau species, not neurofibrillary aggregates, disrupt neural system integration in a tau transgenic model. Fox LM, William CM, Adamowicz DH, Pitstick R, Carlson GA, Spires-Jones TL, Hyman BT, J Neuropathol Exp Neurol 2011 70 588 595 10.1097/NEN.0b013e318220a658 21666499
26. Hyperdynamic microtubules, cognitive deficits, and pathology are improved in tau transgenic mice with low doses of the microtubule-stabilizing agent BMS-241027. Barten DM, Fanara P, Andorfer C, Hoque N, Wong PY, Husted KH, Cadelina GW, Decarr LB, Yang L, Liu V, et al. J Neurosci 2012 32 7137 7145 10.1523/JNEUROSCI.0188-12.2012 22623658
27. CREB-activity and nmnat2 transcription are down-regulated prior to neurodegeneration, while NMNAT2 over-expression is neuroprotective, in a mouse model of human tauopathy. Ljungberg MC, Ali YO, Zhu J, Wu CS, Oka K, Zhai RG, Lu HC, Hum Mol Genet 2012 21 251 267 10.1093/hmg/ddr492 22027994
28. Inhibition of sirtuin 2 with sulfobenzoic acid derivative AK1 is non-toxic and potentially neuroprotective in a mouse model of frontotemporal dementia. Spires-Jones TL, Fox LM, Rozkalne A, Pitstick R, Carlson GA, Kazantsev AG, Front Pharmacol 2012 3 42 22416232
29. Tau accumulation activates the unfolded protein response by impairing endoplasmic reticulum-associated degradation. Abisambra JF, Jinwal UK, Blair LJ, O'Leary JC III, Li Q, Brady S, Wang L, Guidi CE, Zhang B, Nordhues BA, et al. J Neurosci 2013 33 9498 9507 10.1523/JNEUROSCI.5397-12.2013 23719816
30. Fractalkine overexpression suppresses tau pathology in a mouse model of tauopathy. Nash KR, Lee DC, Hunt JB Jr, Morganti JM, Selenica ML, Moran P, Reid P, Brownlow M, Guang-Yu Yang C, Savalia M, et al. Neurobiol Aging 2013 34 1540 1548 10.1016/j.neurobiolaging.2012.12.011 23332170
31. Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy. Selenica ML, Brownlow M, Jimenez JP, Lee DC, Pena G, Dickey CA, Gordon MN, Morgan D, Neurodegener Dis 2013 11 165 181 10.1159/000337230 22796753
32. Robust cytoplasmic accumulation of phosphorylated TDP-43 in transgenic models of tauopathy. Clippinger AK, D'Alton S, Lin WL, Gendron TF, Howard J, Borchelt DR, Cannon A, Carlomagno Y, Chakrabarty P, Cook C, et al. Acta Neuropathol 2013 126 39 50 10.1007/s00401-013-1123-8 23666556
33. In vivo functional brain mapping in a conditional mouse model of human tauopathy (tau(P301L)) reveals reduced neural activity in memory formation structures. Perez PD, Hall G, Kimura T, Ren Y, Bailey RM, Lewis J, Febo M, Sahara N, Mol Neurodegeneration 2013 8 9 10.1186/1750-1326-8-9
34. Genetic and behavioral differences among five inbred mouse strains commonly used in the production of transgenic and knockout mice. Bothe GW, Bolivar VJ, Vedder MJ, Geistfeld JG, Genes, Brain, Behavior 2004 3 149 157 10.1111/j.1601-183x.2004.00064.x
35. Identification of loci determining susceptibility to the lethal effects of amyloid precursor protein transgene overexpression. Krezowski J, Knudson D, Ebeling C, Pitstick R, Giri RK, Schenk D, Westaway D, Younkin L, Younkin SG, Ashe KH, Carlson GA, Hum Mol Genet 2004 13 1989 1997 10.1093/hmg/ddh210 15254013
36. Behavioral differences among C57BL/6 substrains: implications for transgenic and knockout studies. Bryant CD, Zhang NN, Sokoloff G, Fanselow MS, Ennes HS, Palmer AA, McRoberts JA, J Neurogenet 2008 22 315 331 10.1080/01677060802357388 19085272
37. Genetic differences among C57BL/6 substrains. Mekada K, Abe K, Murakami A, Nakamura S, Nakata H, Moriwaki K, Obata Y, Yoshiki A, Exp Anim 2009 58 141 149 10.1538/expanim.58.141 19448337
38. Genetic polymorphisms among C57BL/6 mouse inbred strains. Zurita E, Chagoyen M, Cantero M, Alonso R, Gonzalez-Neira A, Lopez-Jimenez A, Lopez-Moreno JA, Landel CP, Benitez J, Pazos F, Montoliu L, Transgenic Res 2011 20 481 489 10.1007/s11248-010-9403-8 20506040
39. Transgene instability in mice injected with an in vitro methylated Igf2 gene. Pravtcheva DD, Wise TL, Mutation Res 2003 529 35 50 10.1016/S0027-5107(03) 00110-6 12943918
40. Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Holmes A, Wrenn CC, Harris AP, Thayer KE, Crawley JN, Genes, Brain, Behavior 2002 1 55 69 10.1046/j.1601-1848. 2001.00005.x
41. Survey of embryonic stem cell line source strains in the water maze reveals superior reversal learning of 129S6/SvEvTac mice. Clapcote SJ, Roder JC, Behav Brain Res 2004 152 35 48 15135967
42. Genetic modulation of tau phosphorylation in the mouse. Brich J, Shie FS, Howell BW, Li R, Tus K, Wakeland EK, Jin LW, Mumby M, Churchill G, Herz J, Cooper JA, J Neurosci 2003 23 187 192 12514215
43. Identification of Stk25 as a genetic modifier of Tau phosphorylation in Dab1-mutant mice. Matsuki T, Zaka M, Guerreiro R, van der Brug MP, Cooper JA, Cookson MR, Hardy JA, Howell BW, PloS one 2012 7 31152 10.1371/journal.pone. 0031152 22355340
44. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Cruz JC, Tseng HC, Goldman JA, Shih H, Tsai LH, Neuron 2003 40 471 483 10.1016/S0896-6273(03)00627-5 14642273
45. The N terminal region of human tau is present in Alzheimer's disease protein A68 and is incorporated into paired helical filaments. Crowe A, Ksiezak-Reding H, Liu WK, Dickson DW, Yen SH, Am J Pathol 1991 139 1463 1470 1721492
46. Paxinos G, Franklin KBJ, The mouse brain in stereotaxic coordinates San Diego: Academic Press 2 2001 and Stroke