Neurobiology of Aging
Volume 32, Issue 12 , Pages 2287-2298 , December 2011

Association of AICD and Fe65 with Hirano bodies reduces transcriptional activation and initiation of apoptosis

  • Sangdeuk Ha
    • ,
  • Ruth Furukawa

      Affiliations

    • Corresponding Author InformationCorresponding author. Department of Cellular Biology, 724 Biological Sciences Building, University of Georgia, Athens, GA 30602, USA. Tel.: +1 706 542 3334; fax: +1 706 542 4271.
    • ,
  • Marcus Fechheimer

Received 2 June 2008 ,Revised 22 December 2009 ,Accepted 7 January 2010.

References 

  1. Alves da Costa C, Sunyach C, Pardossi-Piquard R, Sevalle J, Vincent B, Boyer N, et al. Presenilin-dependent gamma-secretase-mediated control of p53-associated cell death in Alzheimer's disease. J. Neurosci. 2006;26:6377
  2. Ballatore C, Lee VM, Trojanowski JQ. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat. Rev. Neurosci. 2007;8:663–672
  3. Banwait S, Galvan V, Zhang J, Gorostiza OF, Ataie M, Huang W, et al. C-terminal cleavage of the amyloid-beta protein precursor at Asp664: a switch associated with Alzheimer's disease. J. Alzheimer's Dis. 2008;13:1–16
  4. Butterfield DA, Griffin S, Munch G, Pasinetti GM. Amyloid beta-peptide and amyloid pathology are central to the oxidative stress and inflammatory cascades under which Alzheimer's disease brain exists. J. Alzheimer's Dis. 2002;4:193
  5. Cao X, Südhof TC. A transcriptionally active complex of APP with Fe65 and histone acetyltransferase Tip60. Science. 2001;293:115
  6. Cao X, Südhof TC. Dissection of amyloid-β precursor protein-dependent transcriptional transactivation. J. Biol. Chem. 2004;279:24601
  7. Chang KA, Kim HS, Ha TY, Ha JW, Shin KY, Jeong YH, et al. Phosphorylation of amyloid precursor protein (APP) at Thr668 regulates the nuclear translocation of the APP intracellular domain and induces neurodegeneration. Mol. Biol. Cell. 2006;26:4327
  8. Cupers P, Orlans I, Craessarts K, Annaert W, De Strooper B. The amyloid precursor protein (APP)-cytoplasmic fragment generated by gamma-secretase is rapidly degraded but distributes partially in a nuclear fraction of neurons in culture. J. Neurochem. 2001;78:1168
  9. Davis RC, Furukawa R, Fechheimer M. A cell culture model for investigation of Hirano bodies. Acta Neuropathol. (Berl.). 2008;115:205
  10. Delatour B, Mercken L, Hachimi KH, Colle MA, Padier L, Duyckaerts C. FE65 in Alzheimer's disease: neuronal distribution and association with neurofibrillary tangles. Am. J. Clin. Pathol. 2001;158:1585
  11. Ermekova KS, Zambrano N, Linn H, Minopoli G, Gertler F, Russo T, et al. The WW domain of neural protein FE65 interacts with proline-rich motifs in mena, the mammalian homolog of Drosophila enabled. J. Biol. Chem. 1997;272:32869
  12. Fulga TA, Elson-Schwab I, Khurana V, Steinhib ML, Spires TL, Hyman BT, et al. Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. Nat. Cell Biol. 2007;9:139
  13. Galloway PG, Perry G, Gambetti P. Hirano body filaments contain actin and actin-associated proteins. J. Neuropathol. Exp. Neurol. 1987;46:185
  14. Galloway PG, Perry G, Kosik KS, Gambetti P. Hirano bodies contain tau protein. Brain Res. 1987;403:337
  15. Galvan V, Gorostiza OF, Banwait S, Ataie M, Logvinova AV, Sitaraman S, et al. Reversal of Alzheimer's-like pathology and behavior in human APP transgenic mice by mutation of Asp664. Proc. Natl. Acad. Sci. U. S. A. 2006;103:7130
  16. Galvan V, Zhang J, Gorostiza OF, Sanwait S, Huang W, Ataie M, et al. Long-term prevention of Alzheimer's disease-like behavioral deficits in PDAPP mice carrying a mutation in Asp664. Behav. Brain Res. 2008;191:246
  17. Ghosal K, Vogt DL, Liang M, Shen Y, Lamb BT, Pimplikar SW. Alzheimer's disease-like pathological features in transgenic mice expressing the APP intracellular domain. Proc. Natl. Acad. Sci. U. S. A. 2009;106:18367–18372
  18. Gibson PH, Tomlinson BE. Numbers of Hirano bodies in the hippocampus of normal and demented people with Alzheimer's disease. J. Neurol. Sci. 1977;33:199
  19. Goldman JE. The association of actin with Hirano bodies. J. Neuropathol. Exp. Neurol. 1983;42:146
  20. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science. 2002;297:353
  21. Hirano A. Hirano bodies and related neuronal inclusions. Neuropathol. Appl. Neurobiol. 1994;20:3
  22. Hu Q, Kukull WA, Bressler SL, Gray MD, Cam JA, Larson EB, et al. The human FE65 gene: genomic structure and an intronic biallelic polymorphism associated with sporadic dementia of the Alzheimer type. Human Mol. Genet. 1998;103:295
  23. Jordan-Sciutto K, Dragich J, Walcott D, Bowser R. The presence of FAC1 protein in Hirano bodies. Neuropathol. Appl. Neurobiol. 1998;24:359
  24. Kim DH, Davis RC, Furukawa R, Fechheimer M. Autophagy contributes to degradation of hirano bodies. Autophagy. 2009;5:44
  25. Kim H-S, Kim E-M, Lee J-P, Park CH, Kim S, Seo J-H, et al. C-terminal fragments of amyloid precursor protein exert neurotoxicity by inducing glycogen synthase kinase-3β expression. FASEB J. 2003;17:1951
  26. Kim HS, Kim EM, Kim NJ, Chang KA, Choi Y, Ahn KW, et al. Inhibition of histone deacetylation enhances the neurotoxicity induced by the C-terminal fragments of amyloid precursor protein. J. Neurosci. Res. 2004;75:117
  27. King GD, Turner RS. Adaptor protein interactions: modulators of amyloid precursor protein metabolism and Alzheimer's disease risk?. Exp. Neurol. 2004;185:208
  28. Kinoshita A, Shah T, Tangredi MM, Strickland DK, Hyman BT. The intracellular domain of the low density lipoprotein receptor-related protein modulates transactivation mediated by amyloid precursor protein and Fe65. J. Biol. Chem. 2003;278:41182
  29. Kinoshita A, Whelan CM, Berezovska O, Hyman BT. The gamma secretase-generated carboxyl-terminal domain of the amyloid precursor protein induces apoptosis via Tip60 in H4 cells. J. Biol. Chem. 2002;277:28530
  30. Kinoshita A, Whelan CM, Smith CJ, Berezovska O, Hyman BT. Direct visualization of the gamma secretase-generated carboxyl-terminal domain of the amyloid precursor protein: association with Fe65 and translocation to the nucleus. J. Neurochem. 2002;82:839
  31. Laas R, Hagel C. Hirano bodies and chronic alcoholism. Neuropathol. Appl. Neurobiol. 1994;20:12
  32. Lambert JC, Goumidi L, Vrieze FW, Frigard B, Harris JM, Cummings A, et al. The transcription factor LBP-1c/CP2//LSF gene on chromosome 12 is a genetic determinant of Alzheimer's disease. Human Mol. Genet. 2000;9:2275
  33. Lee SC, Zhao ML, Hirano A, Dickson DW. Inducible nitric oxide synthase immunoreactivity in the Alzheimer disease hippocampus: association with Hirano bodies, neurofibrillary tangles, and senile plaques. J. Neuropathol. Exp. Neurol. 1999;58:1163
  34. Lee VM, Goedert M, Trojanowski JQ. Neurodegenerative tauopathies. Ann. Rev. Neurosci. 2001;24:1121
  35. Lim RWL, Furukawa R, Fechheimer M. Evidence of intramolecular regulation of the Dictyostelium discoideum 34,000 dalton F-actin bundling protein. Biochemistry. 1999;38:16323
  36. Lu DC, Soriano S, Bredesen DE, Koo EH. Caspase cleavage of the amyloid precursor protein modulates amyloid beta-protein toxicity. J. Neurochem. 2003;87:733
  37. Maciver SK, Harrington CR. Two actin binding proteins, actin depolymerizing factor and cofilin, are associated with Hirano bodies. Neuroreport. 1995;6:1985
  38. Maselli AG, Davis R, Furukawa R, Fechheimer M. Formation of Hirano bodies in Dictyostelium and mammalian cells induced by expression of a modified form of an actin cross-linking protein. J. Cell Sci. 2002;115:1939
  39. Maselli AG, Furukawa R, Thomson SAM, Davis RC, Fechheimer M. Formation of Hirano bodies induced by expression of an actin cross-linking protein with a gain of function mutation. Eucaryot. Cell. 2003;2:778
  40. McLoughlin DM, Miller CCJ. The Fe65 proteins and Alzheimer's disease. J. Neurosci. Res. 2008;86:744
  41. Mitake S, Ojika K, Hirano A. Hirano bodies and Alzheimer's disease. Kao Hsiung I Hsueh Ko Hsueh Tsa Chih. 1997;13:10
  42. Mori H, Tomonaga M, Baba N, Kanaya K. The structure analysis of Hirano bodies by digital processing on electron micrographs. Acta Neuropathol. 1986;71:32
  43. Muller T, Concannon CG, Ward MW, Walsh CM, Tirniceriu AL, Tribl F, et al. Modulation of gene expression and cytoskeletal dynamics of the amyloid precursor protein intracellular domain (AICD). Mol. Biol. Cell. 2007;18:201
  44. Munoz DG, Wang D, Greenberg BD. Hirano bodies accumulate C-terminal sequences of beta-amyloid precursor protein (beta-APP) epitopes. J. Neuropathol. Exp. Neurol. 1993;52:14
  45. Ogata J, Budzilovich GN, Cravioto H. A study of rod-like structures (Hirano bodies) in 240 normal and pathological brains. Acta Neuropathol. 1972;21:61
  46. Okamoto K, Hirai S, Hirano A. Hirano bodies in myelinated fibers of hepatic encephalopathy. Acta Neuropathol. 1982;58:307
  47. Perkinton MS, Standen CL, Lau KF, Kesavapany S, Byers HL, Ward M, et al. The c-Abl tyrosine kinase phosphorylates the Fe65 adaptor protein to stimulate Fe65/amyloid precursor protein nuclear signaling. J. Biol. Chem. 2004;279:22084
  48. Peterson C, Kress Y, Vallee R, Goldman JE. High molecular weight microtubule-associated proteins bind to actin lattices (Hirano bodies). Acta Neuropathol. 1988;77:168
  49. Previll LA, Crosby ME, Castellani RJ, Bowser R, Perry G, Smith MA, et al. Increased expression of p130 in Alzheimer's disease. Neurochem. Res. 2007;32:639
  50. Raychaudhuri M, Mukhopadhyay D. AICD and its adapters-In search of new players. J. Alzheimer's Dis. 2007;11:343
  51. Sabo SL, Ikin AF, Buxbaum JD, Greengard P. The amyloid precursor protein and its regulatory protein FE65, in growth cones and synapses in vitro and in vivo. J. Neurosci. 2003;23:5407
  52. Saganich MJ, Schroeder BE, Galvan V, Bredesen DE, Koo EH, Heinemann SF. Deficits in synaptic transmission and learning in amyloid precursor protein (APP) transgenic mice require c-terminal cleavage of APP. J. Neurosci. 2006;26:13428
  53. Sastre M, Scott Turner R, Levy E. X11 Interaction with β-amyloid precursor protein modulates its cellular stabilization and reduced amyloid β-protein secretion. J. Biol. Chem. 1998;273:22351
  54. Schmidt ML, Lee VM, Trojanowski JQ. Analysis of epitopes shared by Hirano bodies and neurofilament proteins in normal and Alzheimer's disease hippocampus. Lab. Invest. 1989;60:513
  55. Schochet SS, McCormick WF. Ultrastructure of Hirano bodies. Acta Neuropathol. 1972;21:50
  56. Shao CY, Crary JF, Rao C, Sacktor TC, Mirra SS. Atypical protein kinase C in neurodegenerative disease II: PKC ι/λ in tauopathies and α-synucleinopathies. J. Neuropathol. Exp. Neurol. 2006;65:327
  57. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, et al. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science. 2005;307:1282
  58. Tu H, Nelson O, Bezprozvanny A, Wang Z, Lee SF, Hao YH, et al. Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations. Cell. 2006;126:981
  59. von Rotz RC, Kohli BM, Bosset J, Meier M, Suzuki T, Nitsch RM, et al. The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J. Cell Sci. 2004;117:4435
  60. Xu Y, Kim HS, Joo Y, Choi Y, Chang KA, Park CH, et al. Intracellular domains of amyloid precursor-like protein 2 interact with CP2 transcription factor in the nucleus and induce glycogen synthase kinase-3beta expression. Cell Death Diff. 2007;14:79
  61. Yamamoto T, Hirano A. Hirano bodies in the perikaryon of the Purkinje cell in a case of Alzheimer's disease. Acta Neuropathol. 1985;67:167
  62. Zambrano N, Minopoli G, de Candia P, Russo T. The Fe65 adaptor protein interacts through its PID1 domain with the transcription factor CP2/FSF/LBP1. J. Biol. Chem. 1998;273:20128
  63. Zhao Q, Lee FS. The transcriptional activity of the APP intracellular domain-Fe65 complex is inhibited by activation of the NF-kappaB pathway. Biochemistry. 2003;42:3627

PII: S0197-4580(10)00032-1

doi: 10.1016/j.neurobiolaging.2010.01.003

Neurobiology of Aging
Volume 32, Issue 12 , Pages 2287-2298 , December 2011

Article Tools

* Image Usage & Resolution