Amyloid beta dimers/trimers potently induce cofilin-actin rods that are inhibited by maintaining cofilin-phosphorylation

Molecular Neurodegeneration

Volumn 6, Issue 1, 2011, Pages

  Davis, Richard C ^a   Marsden, Ian T ^a   Maloney, Michael T ^a,c   Minamide, Laurie S ^a   Podlisny, Marcia ^b   Selkoe, Dennis J ^b   Bamburg, James R ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; COFILIN; DIMER; MONOMER; OLIGOMER; PHOSPHATASE; TETRAMER; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSKELETON; DENTATE GYRUS; DEPHOSPHORYLATION; EMBRYO; ENZYME INHIBITION; FEMALE; GEL FILTRATION; HUMAN; HUMAN CELL; LEARNING; MEMORY; MOSSY FIBER; NERVE CELL; NONHUMAN; OXIDATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT;

RATTUS; RODENTIA;

EID: 78751649794     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-6-10     Document Type: Article

References (75)

1. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. GG Glenner CW Wong, Biochem Biophys Res Commun (Pubitemid 14104991)
2. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. J Hardy DJ Selkoe, Science 2002 297 353 356 10.1126/science.1072994 12130773 (Pubitemid 34790756)
3. Pathways towards and away from Alzheimer's disease. MP Mattson, Nature 2004 430 631 639 10.1038/nature02621 15295589 (Pubitemid 39061671)
4. Amyloid beta amyloidosis in Alzheimer's disease. DL Price SS Sisodia SE Gandy, Curr Opin Neurol 1995 8 268 274 10.1097/00019052-199508000-00004 7582041
5. Role of the beta-amyloid protein in Alzheimer's disease. SS Sisodia DL Price, FASEB J 1995 9 366 370 7896005
6. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. RE Tanzi L Bertram, Cell 2005 120 545 555 10.1016/j.cell.2005.02. 008 15734686 (Pubitemid 40269768)
7. Screening for the beta-amyloid precursor protein mutation (APP717: Val - - Ile) in extended pedigrees with early onset Alzheimer's disease. C Chartier-HarlinM F Crawford K Hamandi M Mullan A Goate J Hardy H Backhovens JJ Martin CV Broeckhoven, Neurosci Lett 1991 129 134 135 10.1016/0304-3940(91) 90738-F 1922963
8. Early-onset Alzheimer's disease caused by mutations at codon 717 of the beta-amyloid precursor protein gene. MC Chartier-Harlin F Crawford H Houlden A Warren D Hughes L Fidani A Goate M Rossor P Roques J Hardy M Mullan, Nature 1991 353 844 846 10.1038/353844a0 1944558 (Pubitemid 21912637)
9. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. A Goate MC Chartier-Harlin M Mullan J Brown F Crawford L Fidani L Giuffra A Haynes N Irving L James R Mant P Newton R Rooke P Roquis C Talbot M Pericak-Vance A Roses R Williamson M Rossor M Owen M Owen J Hardy, Nature 1991 349 704 706 10.1038/349704a0 1671712 (Pubitemid 21912142)
10. A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. J Murrell M Farlow B Ghetti MD Benson, Science 1991 254 97 99 10.1126/science.1925564 1925564 (Pubitemid 21917324)
11. Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. A Deshpande E Mina C Glabe J Busciglio, J. Neurosci 2006 26 6011 6018 10.1523/JNEUROSCI.1189-06.2006 16738244 (Pubitemid 44318367)
12. Cofilin-mediated neurodegeneration in Alzheimer's disease and other amyloidopathies. MT Maloney JR Bamburg, Mol Neurobiol 2007 35 21 44 10.1007/BF02700622 17519504
13. Phosphorylation of actin-depolymerizing factor/cofilin by LIM-kinase mediates amyloid beta-induced degeneration: a potential mechanism of neuronal dystrophy in Alzheimer's disease. L Heredia P Helguera S de Olmos G Kedikian VF Sola F LaFerla M Staufenbiel J de Olmos J Busciglio A Caceres A Lorenzo, J Neurosci 2006 26 6533 6542 10.1523/JNEUROSCI.5567-05.2006 16775141 (Pubitemid 44318334)
14. ADDLs and the signaling web that leads to Alzheimer's disease. GA Krafft WL Klein, Neuropharmacology 2010 59 230 242 10.1016/j.neuropharm.2010.07.012 20650286
15. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. MP Lambert AK Barlow BA Chromy C Edwards R Freed M Liosatos TE Morgan I Rozovsky B Trommer K Viola C Zhang CE Finch GA Krafft WL Klein, Proc Natl Acad Sci USA 1998 95 6448 6453 10.1073/pnas.95.11. 6448 9600986
16. Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. HW Wang JF Pasternak H Kuo H Ristic MP Lambert B Chromy KL Viola WL Klein WB Stine GA Krafft BL Trommer, Brain Res 2002 924 133 140 10.1016/S0006-8993(01)03058-X 11750898 (Pubitemid 34102301)
17. Temporal memory deficits in Alzheimer's mouse models: rescue by genetic deletion of BACE1. M Ohno L Chang W Tseng H Oakley M Citron WL Klein R Vassar JF Disterhoft, Eur J Neurosci 2006 23 251 260 10.1111/j.1460-9568.2005.04551.x 16420434
18. Partial reduction of BACE1 improves synaptic plasticity, recent and remote memories in Alzheimer's disease transgenic mice. R Kimura L Devi M Ohno, J Neurochem 2010 113 248 261 10.1111/j.1471-4159.2010.06608.x 20089133
19. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. DM Walsh I Klyubin JV Fadeeva WK Cullen R Anwyl MS Wolfe MJ Rowan DJ Selkoe, Nature 2002 416 535 539 10.1038/416535a 11932745 (Pubitemid 34288854)
20. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. JP Cleary DM Walsh JJ Hofmeister GM Shankar MA Kuskowski DJ Selkoe KH Ashe, Nat Neurosci 2005 8 79 84 10.1038/nn1372 15608634 (Pubitemid 41236735)
21. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. GM Shankar S Li TH Mehta A Garcia-Munoz NE Shepardson I Smith FM Brett MA Farrell MJ Rowan CA Lemere CM Regan DM Walsh BL Sabatini DJ Selkoe, Nat Med 2008 14 837 842 10.1038/nm1782 18568035
22. The presence of sodium dodecyl sulphate-stable Abeta dimers is strongly associated with Alzheimer-type dementia. JM McDonald GM Savva C Brayne AT Welzel G Forster GM Shankar DJ Selkoe PG Ince DM Walsh Medical Research Council Cognitive Function and Ageing Study, Brain 2010 133 1328 1341 10.1093/brain/awq065 20403962
23. Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. M Townsend GM Shankar T Mehta DM Walsh DJ Selkoe, J Physiol 2006 572 477 492 10.1113/jphysiol.2005.103754 16469784
24. A oligomers inhibit synapse remodelling necessary for memory consolidation. DB Freir R Fedriani D Scully IM Smith DJ Selkoe DM Walsh CM Regan, Neurobiol Aging 2010 2010 Jan 22 20097446
25. Cognitive effects of cell-derived and synthetically derived Abeta oligomers. MN Reed JJ Hofmeister L Jungbauer AT Weizel C Yu MA Sherman S Lesne MJ Ladu DM Walsh KH Ashe JP Cleary, Neurobiol Aging 2009 2009 Dec 21
26. Cytoskeletal pathologies of Alzheimer disease. JR Bamburg GS Bloom, Cell Motil Cytoskel 2009 66 635 649 10.1002/cm.20388
27. Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. LS Minamide AM Striegl JA Boyle PJ Meberg JR Bamburg, Nat Cell Biol 2000 2 628 636 10.1038/35023579 10980704
28. Chronophin mediates an ATP-sensing mechanism of cofilin dephosphorylation and neuronal cofilin-actin rod formation. TY Huang LS Minamide JR Bamburg GM Bokoch, Dev Cell 2008 15 691 703 10.1016/j.devcel.2008.09.017 19000834
29. Mapping cofilin-actin rods in stressed hippocampal slices and the role of cdc42 in amyloid -induced rods. RC Davis MT Maloney LS Minamide KC Flynn MA Stonebraker JR Bamburg, J Alz Dis 2009 18 35 50
30. ADF/cofilin-actin rods in neurodegenerative diseases. JR Bamburg BW Bernstein RC Davis KC Flynn C Goldsbury JR Jensen MT Maloney IT Marsden LS Minamide CW Pak AE Shaw IT Whiteman O Wiggan, Curr Alzheimer Res 2010 7 241 250 10.2174/156720510791050902 20088812
31. Reactive oxygen species (ROS) regulate a slingshot-cofilin activation pathway. JS Kim TY Huang GM Bokoch, Mol Biol Cell 2009 20 2650 2660 10.1091/mbc.E09-02-0131 19339277
32. Ca(2+) influx through P2X receptors induces actin cytoskeleton reorganization by the formation of cofilin rods in neurites. K Homma Y Niino K Hotta K Oka, Mol Cell Neurosci 2008 37 261 270 10.1016/j.mcn.2007.10.001 17993279 (Pubitemid 351173848)
33. Formation of actin-ADF/cofilin rods transiently retards decline of mitochondri8al potential and ATP in stressed neurons. BW Bernstein H Chen JA Boyle JR Bamburg, Am J Physiol Cell Physiol 2006 291 828 C839 10.1152/ajpcell.00066.2006 16738008
34. Beta-secretase-cleaved amyloid precursor protein accumulates at actin inclusions induced in neurons by stress or amyloid beta: a feedforward mechanism for Alzheimer's disease. MT Maloney LS Minamide AW Kinley JA Boyle JR Bamburg, J Neurosci 2005 25 11313 11321 10.1523/JNEUROSCI.3711-05.2005 16339026 (Pubitemid 43083705)
35. The dentate gyrus in Alzheimer's disease. TG Ohm, Prog Brain Res 2007 163 723 740 full-text 17765747 (Pubitemid 47321460)
36. Isolation and characterization of cofilin-actin rods from stressed cells. LS Minamide S Maiti JA Boyle RC Davis JA Coppinger Y Bao TY Huang J Yates GM Bokoch JR Bamburg, J Biol Chem 2010 285 5450 5460 10.1074/jbc.M109.063768 20022956
37. Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. TA Fulga I Elson-Schwab V Khurana ML Steinhilb TL Spires BT Hyman MB Feany, Nat Cell Biol 2007 9 139 148 10.1038/ncb1528 17187063 (Pubitemid 46420856)
38. Activated ADF/cofilin sequesters phosphorylated microtubule associated protein during assembly of Alzheimer-like neuronal cytoskeletal striations. IT Whiteman OL Gervasio KM Cullen GJ Guillemin EV Jeong PK Witting ST Antao LS Minamide JR Bamburg C Goldsbury, J Neurosci 2009 29 12994 13005 10.1523/JNEUROSCI.3531-09.2009 19828813
39. Cofilin expression induces cofilin-actin rod formation and disrupts synaptic structure and function in Aplysia synapses. DH Jang JH Han SH Lee YS Lee H Park SH Lee H Kim BK Kaang, Proc Natl Acad Sci USA 2005 102 16072 16077 10.1073/pnas.0507675102 16247020 (Pubitemid 41552869)
40. Axonal transport and Alzheimer's disease. GB Stokin LS Goldstein, Annu Rev Biochem 2006 75 607 627 10.1146/annurev.biochem.75.103004.142637 16756504 (Pubitemid 44118045)
41. Striation is the characteristic abnormality in Alzheimer disease. ME Velasco MA Smith SL Siedlak A Nunomura G Perry, Brain Res 1998 813 329 333 10.1016/S0006-8993(98)01034-8 9838181 (Pubitemid 29009649)
42. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patient with Alzheimer's disease. CA Davies DMA Mann PQ Sumpter PO Yates, J Neurol Sci 1987 78 151 164 10.1016/0022-510X(87)90057-8 3572454 (Pubitemid 17031709)
43. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. GM Shankar BL Bloodgood M Townsend DM Walsh DJ Selkoe BL Sabatini, J Neurosci 2007 27 2866 2875 10.1523/JNEUROSCI.4970-06.2007 17360908 (Pubitemid 46438992)
44. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. KN Dahlgren AM Manelli WB Stine Jr LK Baker GA Krafft MJ LaDu, J Biol Chem 2002 277 32046 32053 10.1074/jbc.M201750200 12058030 (Pubitemid 34969015)
45. In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. WB Stine Jr KN Dahlgren GA Krafft MJ LaDu, J Biol Chem 2003 278 11612 11622 10.1074/jbc.M210207200 12499373 (Pubitemid 36792723)
46. Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. CS Atwood G Perry H Zeng Y Kato WD Jones KQ Ling X Huang RD Moir D Wang LM Sayre M Smith SG Chen AI Bush, Biochemistry 2004 43 560 568 10.1021/bi0358824 14717612 (Pubitemid 38082580)
47. Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer's disease beta-amyloid. KJ Barnham F Haeffner GD Ciccotosto CC Curtain D Tew C Mavros K Beyreuther D Carrington CL Masters RA Cherny R Cappai AI Bush, FASEB J 2004 18 1427 1429 15231727 (Pubitemid 39561603)
48. The redox chemistry of the Alzheimer's disease amyloid peptide. DG Smith R Cappai KJ Barnham, Biocheim Biophys Acta 2007 1768 1976 1990 10.1016/j.bbamem.2007.02.002 (Pubitemid 47125850)
49. Isolated hippocampal neurons in cryopreserved long-term cultures: development of neuroarchitecture and sensitivity to NMDA. MP Mattson SB Kater, Int J Dev Neurosci 1988 6 439 452 10.1016/0736-5748(88)90050-0 2849287
50. A simple method for organotypic cultures of nervous tissue. L Stoppini PA Buchs D Muller, J Neurosci Methods 1991 37 173 182 10.1016/0165-0270(91)90128-M 1715499
51. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. UK Laemmli, Nature 1970 227 680 685 10.1038/227680a0 5432063
52. Isolation of low-n amyloid -protein oligomers from cultured cells, CSF, and brain. GM Shankar AT Welzel JM McDonald DJ Selkoe DM Walsh, Methods Mol Biol 2011 670 33 44 full-text 20967581
53. ADF/cofilin controls cell polarity during fibroblast migration. HR Dawe LS Minamide JR Bamburg LP Cramer, Curr Biol 2003 13 252 257 10.1016/S0960- 9822(03)00040-X 12573223 (Pubitemid 36178305)
54. Interplay between componets of a novel LIM kinase-slingshot phosphatase complex regulates cofilin. J Soosairajah S Maiti O Wiggan P Sarmiere N Moussi B Sarcevic R Sampath JR Bamburg O Bernard, EMBO J 2005 24 473 486 10.1038/sj.emboj.7600543 15660133 (Pubitemid 40343250)
55. Cdc42 regulates cofilin during the establishment of neuronal polarity. BK Garvalov KC Flynn D Neukirchen L Meyn N Teusch X Wu C Brakebusch JR Bamburg F Bradke, J Neurosci 2007 27 13117 13129 10.1523/JNEUROSCI.3322-07.2007 18045906 (Pubitemid 350220488)
56. Cross-reactivity of antibodies to actin- depolymerizing factor/cofilin family proteins and identification of the major epitope recognized by a mammalian actin-depolymerizing factor/cofilin antibody. AE Shaw LS Minamide CL Bill JD Funk S Maiti JR Bamburg, Electrophoresis 2004 25 2611 2620 10.1002/elps.200406017 15300782 (Pubitemid 39193672)
57. A cofilin-like protein is involved in the regulation of actin assembly in developing skeletal muscle. H Abe S Ohshima T Obinata, J Biochem 1989 106 696 702 2691511 (Pubitemid 19241841)
58. Amyloid beta oligomers are inefficiently measured by enzyme-linked immunosorbant assay. C Stenh H Englund A Lord AS Johansson CG Almeida P Gellerfors P Greengard GK Gouras L Lannfelt LN Nilsson, Ann Neurol 2005 58 147 50 10.1002/ana.20524 15984012 (Pubitemid 40962471)
59. Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. D Puzzo L Privitera E Leznik M Fa A Staniszewski A Palmeri O Arancio, J Neurosci 2008 28 14537 14545 10.1523/JNEUROSCI.2692-08.2008 19118188
60. Production and use of replication-deficient adenovirus for transgene expression in neurons. LS Minamide AE Shaw PD Sarmiere O Wiggan MT Maloney BW Bernstein JM Sneider JA Gonzalez JR Bamburg, Methods Cell Biol 2003 71 387 416 full-text 12884701
61. CSF biomarkers in the prediction of cerebral and clinical change in mild cognitive impairment and Alzheimer's disease. AM Fjell KB Walhovd C Fennema-Notestine LK McEvoy DJ Hagler D Holland JB Brewer AM Dale Alzheimer's Disease Neuroimaging Initiative, J Neurosci 2010 30 2088 2101 10.1523/JNEUROSCI.3785-09.2010 20147537
62. Mass spectrometric characterization of brain amyloid beta isoform signatures in familial and sporadic Alzheimer's disease. E Portelius N Bogdanovic MK Gustavsson I Volkmann G Brinkmalm H Zetterberg B Winblad K Blennow, Acta Neuropathol 2010 120 185 193 10.1007/s00401-010-0690-1 20419305
63. Beta-amyloid expression, release and extracellular disposition in aged rat brain slices. J Marksteiner C Humpel, Mol Psychiatry 2008 13 939 952 10.1038/sj.mp.4002072 17712316
64. Amyloid-beta peptide (Abeta) neurotoxicity is modulated by the rate of peptide aggregation: Abeta dimers and trimers correlate with neurotoxicity. LW Hung GD Ciccotosto E Giannakis DJ Tew K Perez CL Masters R Cappai JD Wade KJ Barnham, J Neurosci 2008 28 11950 11958 10.1523/JNEUROSCI.3916-08.2008 19005060
65. Amyloid - induced amyloid- secretion: a possible feed-forward mechanism in Alzheimer disease. IT Marsden LS Minamide JR Bamburg, J Alz Dis 2011
66. Low-density lipoprotein receptor-related protein 1 (LRP1) mediates neuronal Abeta42 uptake and lysosomal trafficking. RA Fuentealba Q Liu J Zhang T Kanekiyo X Hu JM Lee MJ LaDu G Bu, PLoS One 2010 5 11884 10.1371/journal.pone. 0011884 20686698
67. Protection of synapses against Alzheimer's-linked toxins: Insulin signaling prevents the pathogenic binding of A oligomers. Felice FG De MNN Vieira TR Bomfim H Decker PT Velasco MP Lambert KL Viola WQ Zhao ST Ferreira WL Klein, Proc Nat'l Acad Sci USA 2009 106 1971 1976
68. SynGAP regulates steady-state and activity-dependent phosphorylation of cofilin. HJ Carlisle P Manzerra E Marcora MB Kennedy, J Neurosci 2008 28 13673 13683 10.1523/JNEUROSCI.4695-08.2008 19074040
69. Dopamine D4 receptors regulate AMPA receptor trafficking and glutamatergic transmission in GABAergic interneurons of prefronatl cortex. EY Yuen Z Yan, J Neurosci 2009 14 550 562 10.1523/JNEUROSCI.5050-08.2009
70. ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. J Gu CW Lee Y Fan D Komols X Tang C Sun G Chen K Yu HC Hartzell JR Bamburg JQ Zheng, Nat Neurosci 2010 13 1208 1215 10.1038/nn.2634 20835250
71. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. RGM Morris, Eur J Neurosci 2006 23 2829 2846 10.1111/j.1460-9568.2006.04888.x 16819972 (Pubitemid 43882862)
72. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. K Nakazawa MC Quirk RA Chitwood M Watanabe MF Yeckel LD Sun A Kata CA Carr D Johnston MA Wilson S Tonegawa, Science 2002 297 211 218 10.1126/science.1071795 12040087 (Pubitemid 34761276)
73. Deterioration threshold of synaptic morphology in aging and senile dementia of Alzheimer's type. C Bertoni-Freddari P Fattoretti T Casoli U Caselli W Meier-Ruge, Anal Quant Cytol Histol 1996 18 209 213 8790834 (Pubitemid 26189789)
74. Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. SW Scheff DA Price, Neurobiol Aging 2003 24 1029 1046 10.1016/j.neurobiolaging.2003.08.002 14643375 (Pubitemid 37487881)
75. Synaptic and neuritic alterations during the progression of Alzheimer's disease. E Masliah M Mallory L Hansen R Deteresa M Alford R Terry, Neurosci Lett 1994 174 67 72 10.1016/0304-3940(94)90121-X 7970158 (Pubitemid 24205235)