Estrogen amelioration of Aβ-induced defects in mitochondria is mediated by mitochondrial signaling pathway involving ERβ, AKAP and Drp1

Brain Research

Volumn 1616, Issue , 2015, Pages 101-111

  Sarkar, Saumyendra ^a   Jun, Sujung ^a   Simpkins, James W ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

AKAP1; Alzheimer's disease; Estrogen receptor ; Mitochondrial Fission And Fusion; Mitochondrial Movement; PKA

Indexed keywords

A KINASE ANCHORING PROTEIN 1; AMYLOID BETA PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DYNAMIN; DYNAMINE RELATED PROTEIN 1; ESTROGEN RECEPTOR BETA; OLIGOMER; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG; AKAP1 PROTEIN, RAT; AMYLOID BETA-PROTEIN (1-42); CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; DRP1 PROTEIN, RAT; ESTROGEN; MITOCHONDRIAL PROTEIN; PEPTIDE FRAGMENT;

AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; DENDRITIC CELL; ENZYME INHIBITION; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NERVE CELL; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; CELL CULTURE; CYTOLOGY; DENDRITE; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; MAMMALIAN EMBRYO; METABOLISM; ULTRASTRUCTURE;

A KINASE ANCHOR PROTEINS; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CELLS, CULTURED; DENDRITES; DYNAMINS; EMBRYO, MAMMALIAN; ESTROGEN RECEPTOR BETA; ESTROGENS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURONS; PEPTIDE FRAGMENTS; RATS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84929643029     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.04.059     Document Type: Article

References (39)

1. D. Attwell, and A. Gibb Neuroenergetics and the kinetic design of excitatory synapses Nat. Rev. Neurosci. 6 2005 841 849
2. S. Barghorn, V. Nimmrich, A. Stribinger, C. Krantz, P. Keller, B. Janson, M. Bahr, M. Schmidt, R.S. Bitner, J. Harlan, E. Barlow, U. Ebert, and H. Hilen Globular amyloid β-peptide1-42 oligomer-a homogenous and stable neuropathological protein in Alzheimer's disease J. Neurochem. 95 2005 834 847
3. B. Sheng, X. Wang, B. Su, H.G. Lee, G. Casadesus, G. Perry, and X. Zhu Impaired mitochondrial biogenesis contributes to mitochondrial dysfunction in Alzheimer's disease J. Neurochem. 120 2012 419 429
4. M.J. Calkins, M. Manczak, P. Mao, U. Shirendeb, and P.H. Reddy Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease Hum. Mol.Genet. 20 2011 4515 4529
5. M.J. Calkins, and P.H. Reddy Amyloid beta impairs mitochondrial anterograde transport and degenerates synapses in Alzheimer's disease neurons Biochim. Biophys. Acta 1812 2011 507 513
6. L. Cardone, A. Carlucci, A. Affaitati, A. Livigni, T. DeCristofaro, C. Garbi, S. Varrone, A. Ullrich, M.E. Gottesman, E.V. Avvedimento, and A. Feliciello Mitochondrial AKAP121 binds and targets protein tyrosine phosphatase D1, a novel positive regulator of src signaling Mol. Cell. Biol. 24 2004 4613 4626
7. A. Carlucci, L. Lignitto, and A. Feliciello Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome Trends Cell Biol. 18 2008 604 613
8. G.M. Cereghetti, A. Stangherlin, O. Martins de Brito, C.R. Chang, C. Blackstone, P. Bernardi, and L. Scorrano Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria Proc. Natl. Acad. Sci. U.S.A. 105 2008 15803 15808
9. J.T. Cribbs, and S. Strack Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death EMBO Rep. 8 2007 939 944
10. C.R. Chang, and C. Blackstone Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology J. Biol. Chem. 282 2007 21583 21587
11. D.T. Chang, A.S. Honick, and I.J. Reynolds Mitochondrial trafficking to synapses in cultured primary cortical neurons J. Neurosci. 26 2006 7035 7045
12. J. Côté, and S. Richard Tudor domains bind symmetrical dimethylated arginines J. Biol. Chem. 280 2005 28476 28483
13. A.S. Dickey, and S. Strack PKA/AKAP1 and PP2A/Bβ2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics J. Neurosci. 31 2011 15716 15726
14. H. Du, L. Guo, S. Yan, A.A. Sosunov, G.M. McKhann, and S.S. Yan Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model Proc. Natl. Acad. Sci. U. S. A. 107 2010 18670 18675
15. A. Feliciello, M.E. Gottesman, and E.V. Avvedimento cAMP-PKA signaling to the mitochondria: protein scaffolds, mRNA and phosphatases Cell Signal. 17 2005 279 287
16. S. Fransson, A. Ruusala, and P. Aspenström The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking Biochem. Biophys. Res. Commun. 344 2006 500 510
17. E.M. Izhikevich Polychronization: computation with Spikes Neural Comput. 18 2006 245 282
18. M. Le Romancer, I. Treilleux, N. Leconte, Y. Robin-Lespinasse, S. Sentis, K. Bouchekioua-Bouzaghou, S. Goddard, S. Gobert-Gosse, and L. Corbo Regulation of estrogen rapid signaling through arginine methylation by PRMT1 Mol. Cell 31 2008 212 221
19. Z. Li, K. Okamoto, Y. Hayashi, and M. Sheng The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses Cell 119 2004 873 887
20. F. Liu, M. Day, L.C. Muñiz, D. Bitran, R. Arias, R. Revilla-Sanchez, S. Grauer, G. Zhang, C. Kelly, V. Pulito, A. Sung, R.F. Mervis, R. Navarra, W.D. Hirst, P.H. Reinhart, K.L. Marquis, S.J. Moss, M.N. Pangalos, and N.J. Brandon Activation of estrogen receptor-β regulates hippocampal synaptic plasticity and improves memory Nat. Neurosci. 11 2008 334 343
21. A. Livigni, A. Scorziello, S. Agnese, A. Adornetto, A. Carlucci, C. Garbi, I. Castaldo, L. Annunziato, E.V. Avvedimento, and A. Feliciello Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism Mol. Biol. Cell 17 2006 263 271
22. J.W. Lustbader, M. Cirilli, C. Lin, H.W. Xu, K. Takuma, N. Wang, C. Caspersen, X. Chen, S. Pollak, M. Chaney, F. Trinchese, S. Liu, F. Gunn-Moore, L.F. Lue, D.G. Walker, P. Kuppusamy, Z.L. Zewier, O. Arancio, D. Stern, S.S. Yan, and H. Wu ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease Science 304 2004 448 452
23. M. Manczak, M.J. Calkins, and P.H. Reddy Impaired mitochondrial dynamics and abnormal interaction of amyloid beta with mitochondrial protein Drp1 in neurons from patients with Alzheimer's disease: implications for neuronal damage Hum. Mol. Genet. 20 2011 2495 2509
24. M. Manczak, and P.H. Reddy Abnormal interaction between the mitochondrial fission protein Drp1 and hyperphosphorylated tau in Alzheimer's disease neurons: implications for mitochondrial dysfunction and neuronal damage Hum. Mol. Genet. 21 2012 2538 2547
25. R.A. Merrill, R.K. Dagda, A.S. Dickey, J.T. Cribbs, S.H. Green, Y.M. Usachev, and S. Strack Mechanism of neuroprotective mitochondrial remodeling by PKA/AKAP1 PLoS Biol. 9 4 2011 e1000612
26. A. Pedram, M. Razandi, D.C. Wallace, and E.R. Levin Functional estrogen receptors in the mitochondria of breast cancer cells Mol. Biol. Cell. 17 2006 2125 2137
27. V. Rhein, X. Song, A. Wiesner, L.M. Ittner, G. Baysang, F. Meier, L. Ozmen, H. Bluethmann, S. Dröse, U. Brandt, E. Savaskan, C. Czech, J. Götz, and A. Eckert Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice Proc. Natl. Acad. Sci. U. S. A. 2009 106 2009 20057 20062
28. Y. Rui, P. Tiwari, Z. Xie, and J.Q. Zheng Acute impairment of mitochondrial trafficking by beta-amyloid peptides in hippocampal neurons J. Neurosci. 26 2006 10480 10487
29. 2+-dependent control of mitochondrial dynamics by the Miro GTPase Proc. Natl. Acad. Sci. U. S. A. 105 2008 20728 20733
30. D.F. Silva, J.E. Selfridge, J. Lu, L. E., N. Roy, L. Hutfles, J.M. Burns, E.K. Michaelis, S. Yan, S.M. Cardoso, and R.H. Swerdlow Bioenergetic flux, mitochondrial mass and mitochondrial morphology dynamics in AD and MCI cybrid cell lines Hum. Mol. Genet. 22 2013 3931 3946
31. D.F. Suen, K.L. Norris, and R.J. Youle Mitochondrial dynamics and apoptosis Genes Dev. 22 2008 1577 1590
32. P. Verstreken, C.V. Ly, K.J. Venken, T.W. Koh, Y. Zhou, and H.J. Bellen Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions Neuron 47 2005 365 378
33. O.V. Vitolo, A. Sant'Angelo, V. Costanzo, F. Battaglia, O. Arancio, and M. Shelanski Amyloid beta-peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling Proc. Natl. Acad. Sci. U. S. A. 99 2002 13217 13221
34. X. Wang, B. Su, H.G. Lee, X. Li, G. Perry, M.A. Smith, and X. Zhu Impaired balance of mitochondrial fission and fusion in Alzheimer's disease J. Neurosci. 29 2009 9090 9103
35. Z. Wang, H. Jiang, S. Chen, F. Du, and X. Wang The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways Cell 148 2012 228 243
36. X. Wang, B. Sua, S.L. Siedlak, P.I. Moreirab, H. Fujioka, Y. Wang, G. Casadesus, and X. Zhu Amyloid-β overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins Proc. Natl. Acad. Sci. U. S. A. 105 2008 19318 19323
37. S.H. Yang, S.N. Sarkar, R. Liu, E.J. Perez, X. Wang, Y. Wen, L.J. Yan, and J.W. Simpkins Estrogen receptor β as a mitochondrial vulnerability factor J. Biol. Chem. 284 2009 9540 9548
38. J. Yao, R.W. Irwin, L. Zhao, J. Nilsen, R.T. Hamilton, and R.D. Brinton Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease Proc. Natl. Acad. Sci. U. S. A. 106 2009 14670 14675
39. J. Yao, L. Zhao, Z. Mao, S. Chen, K.C. Wong, and J. Brington, R.D. Potentiation of brain mitochondrial function by S-equol and R/S-equol estrogen receptor β-selective phytoSERM treatments Brain Res. 1514 2013 128 141