Amyloid-β and Proinflammatory Cytokines Utilize a Prion Protein-Dependent Pathway to Activate NADPH Oxidase and Induce Cofilin-Actin Rods in Hippocampal Neurons
Neurites of neurons under acute or chronic stress form bundles of filaments (rods) containing 1:1 cofilin:actin, which impair transport and synaptic function. Rods contain disulfide cross-linked cofilin and are induced by treatments resulting in oxidative stress. Rods form rapidly (5–30 min) in >80% of cultured hippocampal or cortical neurons treated with excitotoxic levels of glutamate or energy depleted (hypoxia/ischemia or mitochondrial inhibitors). In contrast, slow rod formation (50% of maximum response in ~6 h) occurs in a subpopulation (~20%) of hippocampal neurons upon exposure to soluble human amyloid-β dimer/trimer (Aβd/t) at subnanomolar concentrations. Here we show that proinflammatory cytokines (TNFα, IL-1β, IL-6) also induce rods at the same rate and within the same neuronal population as Aβd/t. Neurons from prion (PrPC)-null mice form rods in response to glutamate or antimycin A, but not in response to proinflammatory cytokines or Aβd/t. Two pathways inducing rod formation were confirmed by demonstrating that NADPH-oxidase (NOX) activity is required for prion-dependent rod formation, but not for rods induced by glutamate or energy depletion. Surprisingly, overexpression of PrPC is by itself sufficient to induce rods in over 40% of hippocampal neurons through the NOX-dependent pathway. Persistence of PrPC-dependent rods requires the continuous activity of NOX. Removing inducers or inhibiting NOX activity in cells containing PrPC-dependent rods causes rod disappearance with a half-life of about 36 min. Cofilin-actin rods provide a mechanism for synapse loss bridging the amyloid and cytokine hypotheses for Alzheimer disease, and may explain how functionally diverse Aβ-binding membrane proteins induce synaptic dysfunction.
Minamide LS, Maiti S, Boyle JA, Davis RC, Coppinger JA, et al. (2010) Isolation and characterization of cytoplasmic cofilin actin rods. J Biol Chem 285: 5450–5460. doi: 10.1074/jbc.m109.063768
[3]
Cichon J, Sun C, Chen B, Jiang M, Chen XA, Sun Y, et al. (2012) Cofilin aggregation blocks intracellular trafficking and induces synaptic loss in hippocampal neurons. J Biol Chem 287: 3919–29. doi: 10.1074/jbc.m111.301911
[4]
Maloney MT, Minamide LS, Kinley AW, Boyle JA, Bamburg JR (2005) 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. J Neurosci 25: 11313-11321. Erratum in: J Neurosci 26: 354. doi: 10.1523/jneurosci.3711-05.2005
[5]
Bamburg JR, Bernstein BW, Davis RC, Flynn KC, Goldsbury C, et al. (2010) ADF/cofilin-actin rods in neurodegenerative diseases. Curr Alzheimer Res 7: 241–250. doi: 10.2174/156720510791050902
[6]
Masters CL, Selkoe DJ (2012) Biochemistry of amyloid β-protein and amyloid deposits in Alzheimer disease. Cold Spring Harbor Perspect Med 2012 2: a006262. doi: 10.1101/cshperspect.a006262
[7]
Davis RC, Marsden IT, Maloney MT, Minamide LS, Podlisny M, et al. (2011) Amyloid beta dimers/trimers potently induce cofilin-actin rods that are inhibited by maintaining cofilin phosphorylation. Mol Neurodegen 6: 10. doi: 10.1186/1750-1326-6-10
[8]
Gu J, Lee CW, Fan Y, Komlos D, Tang X, et al. (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13: 1208–1215. doi: 10.1038/nn.2634
[9]
Mi J, Shaw AE, Pak CW, Walsh KP, Minamide LS, et al. (2013) A genetically encoded reporter for imaging cofilin-actin rods in living neurons. PLoS One 8(12): e83609. doi: 10.1371/journal.pone.0083609
[10]
McDonald JM, Savva GM, Brayne C, Welzel AT, Forster G, et al. (2010) The presence of sodium dodecyl sulphate-stable Abeta dimers is strongly associated with Alzheimer-type dementia. Brain 133: 1328–1341. doi: 10.1093/brain/awq065
[11]
McDonald JM, Cairns NJ, Taylor-Reinwald L, Holtzman D, Walsh DM (2012) The levels of water-soluble and triton-soluble Aβ are increased in Alzheimer's disease brain. Brain Res 1450: 138–147. doi: 10.1016/j.brainres.2012.02.041
[12]
Benilova I, De Strooper B (2013) Promiscuous Alzheimer's amyloid: yet another partner. Science 341: 1354–1355. doi: 10.1126/science.1244166
[13]
Carlisle HJ, Manzerra P, Marcora E, Kennedy MB (2008) SynGAP regulates steady-state and activity-dependent phosphorylation of cofilin. J Neurosci 28: 13673–13683. doi: 10.1523/jneurosci.4695-08.2008
[14]
Kim T, Vidal GS, Djurisic M, William CM, Birnbaum ME, et al. (2013) Human LilrB2 is a β-amyloid receptor and its murine homolog PirB regulates synaptic plasticity in an Alzheimer's model. Science 341: 1399–1404. doi: 10.1126/science.1242077
[15]
Roh S-E, Woo JA, Lakshmana MK, Uhlar C, Ankala V, et al. (2013) Mitochondrial dysfunction and calcium deregulation by RanBP9-cofilin pathway. FASEB J 27: 4776–4789. doi: 10.1096/fj.13-234765
[16]
Bernstein BW, Shaw AE, Minamide LS, Pak CW, Bamburg JR (2012) Incorporation of cofilin into rods depends on disulfide intermolecular bonds: implications for actin regulation and neurodegenerative disease. J Neurosci 32: 6670–6681. doi: 10.1523/jneurosci.6020-11.2012
[17]
Keller JN, Schmitt FA, Scheff SW, Ding Q, Chen Q, et al. (2005) Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 64: 1152–1156. doi: 10.1212/01.wnl.0000156156.13641.ba
[18]
Mrak RE, Griffin WS (2005) Potential inflammatory biomarkers in Alzheimer's disease. J. Alzheimers Dis 8: 369–375.
[19]
Griffin WS, Barger SW (2010) Neuroinflammatory cytokines- the common thread in Alzheimer's pathogenesis. US Neurol 6: 19–27.
[20]
Barth BM, Gustafson SJ, Hankins JL, Kaiser JM, Haakenson JK, et al. (2012) Ceramide kinase regulates TNFα-stimulated NADPH oxidase activity and eicosanoid biosynthesis in neuroblastoma cells. Cell Signal 24: 1126–1133. doi: 10.1016/j.cellsig.2011.12.020
[21]
Ansari MA, Scheff SW (2011) NADPH-oxidase activation and cognition in Alzheimer disease progression. Free Radic Biol Med 51: 171–178. doi: 10.1016/j.freeradbiomed.2011.03.025
[22]
Bruce-Keller AJ, Gupta S, Knight AG, Beckett TL, McMullen JM, et al. (2011) Cognitive impairment in humanized APPxPS1 mice is linked to Aβ1-42 and NOX activation. Neurobiol Dis 44: 317–326. doi: 10.1016/j.nbd.2011.07.012
[23]
Sorce S, Krause KH, Jaquet V (2012) Targeting NOX enzymes in the central nervous system: therapeutic opportunities. Cell Mol Life Sci 69: 2387–2407. doi: 10.1007/s00018-012-1014-5
[24]
Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457: 1128–1132. doi: 10.1038/nature07761
[25]
Santuccione A, Sytnyk V, Leshchyns”ka I, Schachner M (2005) Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol 169: 341–354. doi: 10.1083/jcb.200409127
[26]
Um JW, Kaufman AC, Kostylev M, Heiss JK, Stagi M, et al. (2013) Metabotropic glutamate receptor 5 is a coreceptor for Alzheimer Aβ oligomer bound to cellular prion protein. Neuron 79: 887–902. doi: 10.1016/j.neuron.2013.06.036
[27]
Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, et al. (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzhemier's disease mouse models. Cell 142: 387–397. doi: 10.1016/j.cell.2010.06.036
[28]
Um JW, Nygaard HB, Heiss JK, Kostylev MA, Stagi M, et al. (2012) Alzheimer amyloid-β oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat Neurosci 15: 1227–1235. doi: 10.1038/nn.3178
[29]
Barry AE, Klyubin I, Mc Donald JM, Mably AJ, Farrell MA, et al. (2011) Alzheimer's disease brain-derived amyloid-β-mediated inhibition of LTP in vivo is prevented by immunotargeting cellular prion protein. J Neurosci 31: 7259–7263. doi: 10.1523/jneurosci.6500-10.2011
[30]
Chung E, Ji Y, Sun Y, Kascsak RJ, Kascsak RB, et al. (2010) Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in Alzheimer disease model mouse. BMC Neurosci 11: 130. doi: 10.1186/1471-2202-11-130
[31]
Barth BM, Stewart-Smeets S, Kuhn TB (2009) Proinflammatory cytokines provoke oxidative damage to actin in neuronal cells mediated by Rac1 and NADPH oxidase. Mol Cell Neurosci 41: 274–285. doi: 10.1016/j.mcn.2009.03.007
[32]
Sudduth TL, Schmitt FA, Nelson PT, Wilcock DM (2013) Neuroinflammatory phenotype in early Alzheimer's disease. Neurobiol Aging 34: 1051–1059. doi: 10.1016/j.neurobiolaging.2012.09.012
[33]
Gimbel DA, Nygaard HB, Coffey EE, Gunther EC, Laurén J, et al. (2010) Memory impairment in transgenic Alzheimer mice require cellular prion protein. J Neurosci 30: 6367–6374. doi: 10.1523/jneurosci.0395-10.2010
[34]
Lambeth JD (2007) Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med 43: 332–347. doi: 10.1016/j.freeradbiomed.2007.03.027
[35]
Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245–313. doi: 10.1152/physrev.00044.2005
[36]
Lambeth JD, Krause KH, Clark RA (2008) NOX enzymes as novel targets for drug development. Semin Immunopathol 30: 339–363. doi: 10.1007/s00281-008-0123-6
[37]
Sorce S, Krause KH (2009) NOX enzymes in the central nervous system: from signaling to disease. Antioxid Redox Signal 11: 2481–2504. doi: 10.1089/ars.2009.2578
[38]
Kawahara T, Ritsick D, Cheng G, Lambeth JD (2005) Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation. J Biol Chem 280: 31859–31869. doi: 10.1074/jbc.m501882200
[39]
He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, et al. (1998) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95: 2509–2514. doi: 10.1073/pnas.95.5.2509
[40]
Altenhofer S, Radermacher KA, Kleikers PW, Wingler K, Schmidt HH (2014) Evolution of NADPH oxidase inhibitors: selectivity and mechanisms for target engagement. Antioxid Redox Signal 2014 Feb 26 [Epub ahead of print].
[41]
Mo G-L, Li Y, Du R-H, Dai D-Z, Cong X-D, et al.. (2014) Isoproterenol induced stressful reactions in the brain are characterized by inflammation due to activation of NADPH oxidase and ER stress: attenuated by apocyanin, Rehmannia complex and triterpene acids. Neurochem Res 2014 Feb 26 [Epub ahead of print]
[42]
Bate C, Williams A (2011) Amyloid-β-induced synapse damage is mediated via cross-linkage of cellular prion proteins. J Biol Chem 286: 37955–37963. doi: 10.1074/jbc.m111.248724
[43]
Haigh CL, Edwards K, Brown DR (2005) Copper binding is the governing determinant of prion protein turnover. Mol Cell Neurosci 30: 186–196. doi: 10.1016/j.mcn.2005.07.001
[44]
Campos SB, Ashworth SL, Wean S, Hosford M, Sandoval RM, et al. (2009) Cytokine-induced F-actin reorganization in endothelial cells involves RhoA activation. Am J Physiol Renal Physiol 296: F486–495. doi: 10.1152/ajprenal.00112.2008
[45]
Bernstein BW, Chen H, Boyle JA, Bamburg JR (2006) Formation of actin-ADF/cofilin rods transiently retards decline of mitochondrial potential and ATP in stressed neurons. Am J Physiol Cell Physiol 291: C828–839. doi: 10.1152/ajpcell.00066.2006
[46]
Davis RC, Maloney MT, Minamide LS, Flynn KC, Stonebraker MA, et al. (2009) Mapping cofilin-actin rods in stressed hippocampal slices and the role of cdc42 in amyloid-β-induced rods. J Alzheimers Dis 18: 35–50.
[47]
Jonsson T, Atwal JK, Steinberg S, Snaedal J, Jonsson PV, et al. (2012) A mutation in APP protects against Alzheimer's disease and age-related cognitive decline. Nature 488: 96–99. doi: 10.1038/nature11283
[48]
Pluta R, Furmaga-Jablonska W, Maciejewski R, Ulamek-Koziol M, Jablonski M (2013) Brain ischemia activates β- and γ-secretase cleavage of amyloid precursor protein: significance in sporadic Alzheimer's disease. Mol Neurobiol 47: 425–434. doi: 10.1007/s12035-012-8360-z
[49]
Moore BD, Chakrabart P, Levites Y, Kukar TL, Baine A-M, et al. (2012) Overlapping profiles of Aβ peptides in the Alzheimer's disease and pathological aging brains. Alz Res Therapy 4: 18. doi: 10.1186/alzrt121
[50]
Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837–842. doi: 10.1038/nm1782
[51]
Atwood CS, Perry G, Zheng H, Kato Y, Jones WD, et al. (2004) Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. Biochemistry 43: 560–568. doi: 10.1021/bi0358824
[52]
Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, et al. (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8: 79–84. doi: 10.1038/nn1372
[53]
Cacquevel M, Lebeurrier N, Chéenne S, Vivien D (2004) Cytokines in neuroinflammation and Alzheimer's disease. Curr Drug Targets 5: 529–534. doi: 10.2174/1389450043345308
[54]
Amor S, Puentes F, Baker D, van der Valk P (2010) Inflammation in neurodegenerative diseases. Immunology 129: 154–169. doi: 10.1111/j.1365-2567.2009.03225.x
[55]
Liu L, Chan C (2014) The role of inflammasome in Alzheimer's disease. Ageing Res Rev 15C: 6–15. doi: 10.1016/j.arr.2013.12.007
Vossel KA, Beagle AJ, Rabinovici GD, Shu H, Lee SE, et al. (2013) Seizures and epileptiform activity in the early stages of Alzheimer disease. J Am Med Assoc Neurol 70: 1158–1166. doi: 10.1001/jamaneurol.2013.136
[59]
Breunig JJ, Guillot-Sestier M-V, Town T (2013) Brain injury, neuroinflammation and Alzheimer's disease. Front Aging Res 5: 26. doi: 10.3389/fnagi.2013.00026
[60]
Orsucci D, Mancuso M, Ienco EC, Simoncini C, Siciliano G, et al. (2013) Vascular factors and mitochondrial dysfunction: a central role in the pathogenesis of Alzheimer's disease. Curr Neurovasc Res. 10: 76–80. doi: 10.2174/1567202611310010010
[61]
Sauer H, Wefer K, Vetrugno V, Pocchiari M, Gissel C, et al. (2003) Regulation of intrinsic prion protein by growth factors and TNFα: the role of intracellular reactive oxygen species. Free Rad Biol Med 35: 586–594. doi: 10.1016/s0891-5849(03)00360-5
[62]
Yazdanpanah B, Wiegmann K, Tchikov V, Krut O, Pongratz C, et al. (2009) Riboflavin kinase couples TNF receptor 1 to NADPH oxidase. Nature 460: 1159–1163. doi: 10.1038/nature08206
[63]
Vural P, Degirmencioglu S, Parildar-Karpuzoglu, Dogru-Abbasoglu S, Hanagasi HA, et al. (2009) The combinations of TNFalpha-308 and IL-6-174 or IL-10-1082 genes polymorphisms suggest an association with susceptibility to sporadic late-onset Alzheimer's disease. Acta Neurol Scand 120: 396–401. doi: 10.1111/j.1600-0404.2009.01230.x
Rushworth JV, Hooper NM (2011) Lipid rafts: linking Alzheimer's amyloid-β production, aggregation, and toxicity at neuronal membranes. Int J Alz Dis doi:10.4061/2011/603052
[66]
Bate C, Williams A (2012) Neurodegeneration induced by clustering of sialylated glycosylphosphatidylinositols of prion proteins. J Biol Chem 287: 7935–7944. doi: 10.1074/jbc.m111.275743
[67]
Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, et al. (2005) Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308: 1435–1439. doi: 10.1126/science.1110837
[68]
Hernandez-Rapp J, Martin-Lanneree S, Hirsch TZ, Launay J-M, Mouillet-Richard S (2014) Hijacking PrPC-dependent signal transduction: when prions impair Aβ clearance. Front Aging Neurosci 6 : doi:10.3389/fnagi
[69]
Bernstein BW, Bamburg JR (2010) ADF/cofilin: a functional node in cell biology. Trends Cell Biol 20: 187–195. doi: 10.1016/j.tcb.2010.01.001
[70]
Klamt F, Zdanov S, Levine RL, Pariser A, Zhang Y, et al. (2009) Oxidant-induced apoptosis is mediated by oxidation of the actin-regulatory protein cofilin. Nat Cell Biol 11: 1241–1246. doi: 10.1038/ncb1968
[71]
Woo JA, Jung AR, Lakshmana MK, Bedrossian A, Lim Y, et al. (2012) Pivotal role of the RanBP9-cofilin pathway in Aβ-induced apoptosis and neurodegeneration. Cell Death Differ 19: 1413–1423. doi: 10.1038/cdd.2012.14
[72]
Mucke L, Selkoe DJ (2012) Neurotoxicity of amyloid β-protein: synaptic and network dysfunction. Cold Spring Harbor Perspect Med 2012 doi: 10.110/cshperspect.a006338
[73]
Huang TY, Minamide LS, Bamburg JR, Bokoch GM (2008) Chronophin serves as an ATP-sensing mechanism for cofilin dephosphorylation and neuronal cofilin-actin rod formation. Develop Cell 15: 691–703. doi: 10.1016/j.devcel.2008.09.017
[74]
Wang CH, Wu SB, Wu YT, Wei YH (2013) Oxidative stress response elicted by mitochondrial dysfunction: implication in the pathophysiology of aging. Exp Biol Med (Maywood) 238: 450–460. doi: 10.1177/1535370213493069
[75]
Gohla A, Bokoch GM (2002) 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr Biol 12: 1704–1710. doi: 10.1016/s0960-9822(02)01184-3
[76]
Nagata-Ohashi K, Ohta Y, Goto K, Chiba S, Mori R, et al. (2004) A pathway of neuregulin-induced activation of cofilin-phosphatase slingshot and cofilin in lamellipodia. J Cell Biol 165: 465–471. doi: 10.1083/jcb.200401136
[77]
Kim JS, Huang TY, Bokoch GM (2009) Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol Biol Cell 20: 2650–2660. doi: 10.1091/mbc.e09-02-0131
[78]
Moya KL, Sales N, Hassig R, Creminon C, Grassi J, et al. (2000) Immunolocalization of the cellular prion protein in normal brain. Microsc Res Tech 50: 58–65. doi: 10.1002/1097-0029(20000701)50:1<58::aid-jemt9>3.0.co;2-5
[79]
Beringue V, Mallinson G, Kaisar M, Tayebi M, Sattar Z, et al. (2003) Regional heterogeneity of cellular prion protein isoforms in the mouse brain. Brain 126: 2065–2073. doi: 10.1093/brain/awg205
[80]
Barmada S, Piccardo P, Yamaguchi K, Ghetti B, Harris DA (2004) GFP-tagged prion protein is correctly localized and functionally active in the brains of transgenic mice. Neurobiol Dis 16: 527–537. doi: 10.1016/j.nbd.2004.05.005
[81]
Brown P, Preece M, Brandel JP, Sato T, McShane L, et al. (2000) Iatrogenic Creutzfeldt-Jakob disease at the millenium. Neurology 55: 1075–1081. doi: 10.1212/wnl.55.8.1075
[82]
Ironside JW, Head MW (2004) Neuropathology and molecular biology of variant Creutzfeldt-Jakob disease. Curr Top Microbiol Immunol 284: 133–159. doi: 10.1007/978-3-662-08441-0_6
[83]
He J, Li X, Yang J, Huang J, Fu X, et al. (2013) The association between the methionine/valine (M/V) polymorphism (rs1799990) in the PRNP gene and the risk of Alzheimer disease: An update by meta-analysis. J Neurol Sci 326: 89–95. doi: 10.1016/j.jns.2013.01.020
[84]
Solforosi L, Criado JR, McGavern DB, Wirz S, Sánchez-Alavez M, et al. (2004) Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303: 1514–1516. doi: 10.1126/science.1094273
[85]
Mouillet-Richard S, Ermonval M, Chebassier C, Laplanche JL, Lehmann S, et al.. (2000) Signal transduction through prion protein. Science 289: , 1925–1928.
[86]
Maulik M, Westaway D, Jhamandas JH, Kar S (2013) Role of cholesterol in APP metabolism and its significance in Alzheimer's disease pathogenesis. Mol Neurobiol 47: 37–63. doi: 10.1007/s12035-012-8337-y
[87]
Syed I, Szulc ZM, Ogretmen B, Kowluru A (2012) L-threo-C6-pyridonium-ceramide bromide, a novel cationic ceramide, induces NADPH oxidase activation, mitochondrial dysfunction and loss in cell viability in INS 832/13 β-cells. Cell Physiol Biochem 30: 1051–1058. doi: 10.1159/000341481
[88]
Sagy-Bross C, Hadad N, Levy R (2013) Cytosolic phospholipase A2α upregulation mediates apoptotic neuronal death induced by aggregated amyloid-β peptide 1-42. Neurochem Int 63: 541–550. doi: 10.1016/j.neuint.2013.09.007
[89]
Pluta R, Jablonski M, Ulamek-Koziol M, Kocki J, Brzozowska J, et al. (2013) Sporadic Alzheimer's disease begins as episodes of brain ischemia and ischemically dysregulated Alzheimer's disease genes. Mol Neurobiol 48: 500–515. doi: 10.1007/s12035-013-8439-1
[90]
Minamide LS, Shaw AE, Sarmiere PD, Wiggan O, Maloney MT, et al. (2003) Production and use of replication-deficient adenoviruses for transgene expression in neurons. Methods Cell Biol 71: 387–416. doi: 10.1016/s0091-679x(03)01019-7
[91]
Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, et al. (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99: 7877–7882. doi: 10.1073/pnas.082243699
[92]
Morgan TE, Lockerbie RO, Minamide LS, Browning MD, Bamburg JR (1993) Isolation and characterization of a regulated form of actin depolymerizing factor. J Cell Biol 122: 623–633.
[93]
Walsh DM, Klyubin 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. doi: 10.1038/416535a
[94]
Shaw AE, Minamide LS, Bill C, Funk JD, Maiti S, et al. (2004) Cross-reactivity of antibodies to ADF/cofilin family proteins and identification of the major epitope recognized by a mammalian ADF/cofilin antibody. Electrophoresis 25: 2611–2620. doi: 10.1002/elps.200406017
[95]
Abe H, Oshima S, Obinata T (1989) A cofilin-like protein is involved in the regulation of actin assembly in developing skeletal muscle. J Biochem (Tokyo) 106: 696–702.
