BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

The cellular basis of dendrite pathology in neurodegenerative diseases

  • Kweon, Jung Hyun (Department of Brain & Cognitive Sciences, DGIST) ;
  • Kim, Sunhong (Disease Target Structure Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Lee, Sung Bae (Department of Brain & Cognitive Sciences, DGIST)
  • Received : 2016.08.01
  • Published : 2017.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

One of the characteristics of the neurons that distinguishes them from other cells is their complex and polarized structure consisting of dendrites, cell body, and axon. The complexity and diversity of dendrites are particularly well recognized, and accumulating evidences suggest that the alterations in the dendrite structure are associated with many neurodegenerative diseases. Given the importance of the proper dendritic structures for neuronal functions, the dendrite pathology appears to have crucial contribution to the pathogenesis of neurodegenerative diseases. Nonetheless, the cellular and molecular basis of dendritic changes in the neurodegenerative diseases remains largely elusive. Previous studies in normal condition have revealed that several cellular components, such as local cytoskeletal structures and organelles located locally in dendrites, play crucial roles in dendrite growth. By reviewing what has been unveiled to date regarding dendrite growth in terms of these local cellular components, we aim to provide an insight to categorize the potential cellular basis that can be applied to the dendrite pathology manifested in many neurodegenerative diseases.

Keywords

References

  1. Forman MS, Trojanowski JQ and Lee VM (2004) Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat Med 10, 1055-1063 https://doi.org/10.1038/nm1113
  2. Vila M and Przedborski S (2003) Targeting programmed cell death in neurodegenerative diseases. Nat Rev Neurosci 4, 365-375 https://doi.org/10.1038/nrn1100
  3. Zoghbi HY and Orr HT (2000) Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23, 217-247 https://doi.org/10.1146/annurev.neuro.23.1.217
  4. Li X-J (1999) The early cellular pathology of Huntington's disease. Mol Neurobiol 20, 111-124 https://doi.org/10.1007/BF02742437
  5. Goldberg MS, Fleming SM, Palacino JJ et al (2003) Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J Biol Chem 278, 43628-43635 https://doi.org/10.1074/jbc.M308947200
  6. Gispert S, Ricciardi F, Kurz A et al (2009) Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One 4, e5777 https://doi.org/10.1371/journal.pone.0005777
  7. Baloyannis SJ (2009) Dendritic pathology in Alzheimer's disease. J Neurol Sci 283, 153-157 https://doi.org/10.1016/j.jns.2009.02.370
  8. Villalba RM and Smith Y (2010) Striatal spine plasticity in Parkinson's disease. Front Neuroanat 4, 133
  9. Lee SB, Bagley JA, Lee HY, Jan LY and Jan YN (2011) Pathogenic polyglutamine proteins cause dendrite defects associated with specific actin cytoskeletal alterations in Drosophila. Proc Natl Acad Sci U S A 108, 16795-16800 https://doi.org/10.1073/pnas.1113573108
  10. DiFiglia M, Sapp E, Chase KO et al (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993 https://doi.org/10.1126/science.277.5334.1990
  11. Nakano I and Hirano A (1987) Atrophic cell processes of large motor neurons in the anterior horn in amyotrophic lateral sclerosis: observation with silver impregnation method. J Neuropathol Exp Neurol 46, 40-49 https://doi.org/10.1097/00005072-198701000-00004
  12. Koleske AJ (2013) Molecular mechanisms of dendrite stability. Nat Rev Neurosci 14, 536-550 https://doi.org/10.1038/nrn3486
  13. Park JS, Bateman MC and Goldberg MP (1996) Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol Dis 3, 215-227 https://doi.org/10.1006/nbdi.1996.0022
  14. Jan Y-N and Jan LY (2010) Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 11, 316-328
  15. Fischer RS and Fowler VM (2015) Thematic Minireview Series: The State of the Cytoskeleton in 2015. J Biol Chem 290, 17133-17136 https://doi.org/10.1074/jbc.R115.663716
  16. Gu J, Firestein BL and Zheng JQ (2008) Microtubules in dendritic spine development. J Neurosci 28, 12120-12124 https://doi.org/10.1523/JNEUROSCI.2509-08.2008
  17. Engert F and Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70 https://doi.org/10.1038/19978
  18. Maletic-Savatic M, Malinow R and Svoboda K (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923-1927 https://doi.org/10.1126/science.283.5409.1923
  19. Toni N, Buchs PA, Nikonenko I, Bron CR and Muller D (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421-425 https://doi.org/10.1038/46574
  20. Horch HW, Kruttgen A, Portbury SD and Katz LC (1999) Destabilization of cortical dendrites and spines by BDNF. Neuron 23, 353-364 https://doi.org/10.1016/S0896-6273(00)80785-0
  21. Williams DW and Truman JW (2005) Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 132, 3631-3642 https://doi.org/10.1242/dev.01928
  22. Kuo CT, Zhu S, Younger S, Jan LY and Jan YN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51, 283-290 https://doi.org/10.1016/j.neuron.2006.07.014
  23. Ori-McKenney KM, Jan LY and Jan YN (2012) Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76, 921-930 https://doi.org/10.1016/j.neuron.2012.10.008
  24. Dubey J, Ratnakaran N and Koushika SP (2015) Neurodegeneration and microtubule dynamics: death by a thousand cuts. Front Cell Neurosci 9, 343
  25. Zempel H and Mandelkow E (2014) Lost after translation: missorting of Tau protein and consequences for Alzheimer disease. Trends Neurosci 37, 721-732 https://doi.org/10.1016/j.tins.2014.08.004
  26. Feng J (2006) Microtubule: a common target for parkin and Parkinson's disease toxins. Neuroscientist 12, 469-476 https://doi.org/10.1177/1073858406293853
  27. Lin CH, Tsai PI, Wu RM and Chien CT (2010) LRRK2 G2019S mutation induces dendrite degeneration through mislocalization and phosphorylation of tau by recruiting autoactivated GSK3ss. J Neurosci 30, 13138-13149 https://doi.org/10.1523/JNEUROSCI.1737-10.2010
  28. Chen L, Stone MC, Tao J and Rolls MM (2012) Axon injury and stress trigger a microtubule-based neuroprotective pathway. Proc Natl Acad Sci U S A 109, 11842-11847 https://doi.org/10.1073/pnas.1121180109
  29. Hotulainen P and Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189, 619-629 https://doi.org/10.1083/jcb.201003008
  30. Welch MD and Mullins RD (2002) Cellular control of actin nucleation. Annu Rev Cell Dev Biol 18, 247-288 https://doi.org/10.1146/annurev.cellbio.18.040202.112133
  31. Parisiadou L and Cai H (2010) LRRK2 function on actin and microtubule dynamics in Parkinson disease. Commun Integr Biol 3, 396-400 https://doi.org/10.4161/cib.3.5.12286
  32. Fulga TA, Elson-Schwab I, Khurana V et al (2007) Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. Nat Cell Biol 9, 139-148 https://doi.org/10.1038/ncb1528
  33. Minamide LS, Striegl AM, Boyle JA, Meberg PJ and Bamburg JR (2000) Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat Cell Biol 2, 628-636 https://doi.org/10.1038/35023579
  34. Heredia L, Helguera P, de Olmos S et al (2006) Phosphorylation of actin-depolymerizing factor/cofilin by LIMkinase mediates amyloid beta-induced degeneration: a potential mechanism of neuronal dystrophy in Alzheimer's disease. J Neurosci 26, 6533-6542 https://doi.org/10.1523/JNEUROSCI.5567-05.2006
  35. Ye B, Zhang YW, Jan LY and Jan YN (2006) The secretory pathway and neuron polarization. J Neurosci 26, 10631-10632 https://doi.org/10.1523/JNEUROSCI.3271-06.2006
  36. Luscher C, Nicoll RA, Malenka RC and Muller D (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3, 545-550 https://doi.org/10.1038/75714
  37. Hanus C and Ehlers MD (2008) Secretory Outposts for the Local Processing of Membrane Cargo in Neuronal Dendrites. Traffic 9, 1437-1445 https://doi.org/10.1111/j.1600-0854.2008.00775.x
  38. Horton AC and Ehlers MD (2003) Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci 23, 6188-6199 https://doi.org/10.1523/JNEUROSCI.23-15-06188.2003
  39. Gardiol A, Racca C and Triller A (1999) Dendritic and postsynaptic protein synthetic machinery. J Neurosci 19, 168-179 https://doi.org/10.1523/JNEUROSCI.19-01-00168.1999
  40. Ye B, Zhang Y, Song W, Younger SH, Jan LY and Jan YN (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130, 717-729 https://doi.org/10.1016/j.cell.2007.06.032
  41. Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ and Ehlers MD (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48, 757-771 https://doi.org/10.1016/j.neuron.2005.11.005
  42. Sengupta D and Linstedt AD (2011) Control of organelle size: the Golgi complex. Annu Rev Cell Dev Biol 27, 57-77 https://doi.org/10.1146/annurev-cellbio-100109-104003
  43. Lin CH, Li H, Lee YN, Cheng YJ, Wu RM and Chien CT (2015) Lrrk regulates the dynamic profile of dendritic Golgi outposts through the golgin Lava lamp. J Cell Biol 210, 471-483 https://doi.org/10.1083/jcb.201411033
  44. Fujita Y, Mizuno Y, Takatama M and Okamoto K (2008) Anterior horn cells with abnormal TDP-43 immunoreactivities show fragmentation of the Golgi apparatus in ALS. J Neurol Sci 269, 30-34 https://doi.org/10.1016/j.jns.2007.12.016
  45. Hubley MJ, Locke BR and Moerland TS (1996) The effects of temperature, pH, and magnesium on the diffusion coefficient of ATP in solutions of physiological ionic strength. Biochim Biophys Acta 1291, 115-121 https://doi.org/10.1016/0304-4165(96)00053-0
  46. Rizzuto R, De Stefani D, Raffaello A and Mammucari C (2012) Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 13, 566-578 https://doi.org/10.1038/nrm3412
  47. KoRN ED, Carlier M-F and Pantaloni D (1987) Actin polymerization and ATP hydrolysis. Science 238, 638-644 https://doi.org/10.1126/science.3672117
  48. Redmond L and Ghosh A (2005) Regulation of dendritic development by calcium signaling. Cell Calcium 37, 411-416 https://doi.org/10.1016/j.ceca.2005.01.009
  49. Greenwood SM and Connolly CN (2007) Dendritic and mitochondrial changes during glutamate excitotoxicity. Neuropharmacology 53, 891-898 https://doi.org/10.1016/j.neuropharm.2007.10.003
  50. Li Z, Okamoto K-I, Hayashi Y and Sheng M (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873-887 https://doi.org/10.1016/j.cell.2004.11.003
  51. Tsubouchi A, Tsuyama T, Fujioka M et al (2009) Mitochondrial protein Preli-like is required for development of dendritic arbors and prevents their regression in the Drosophila sensory nervous system. Development 136, 3757-3766 https://doi.org/10.1242/dev.042135
  52. Burte F, Carelli V, Chinnery PF and Yu-Wai-Man P (2015) Disturbed mitochondrial dynamics and neurodegenerative disorders. Nat Rev Neurol 11, 11-24
  53. Whitworth AJ and Pallanck LJ (2009) The PINK1/Parkin pathway: a mitochondrial quality control system? J Bioenerg Biomembr 41, 499-503 https://doi.org/10.1007/s10863-009-9253-3
  54. Barten DM, Fanara P, Andorfer C et al (2012) Hyperdynamic microtubules, cognitive deficits, and pathology are improved in tau transgenic mice with low doses of the microtubule-stabilizing agent BMS-241027. J Neurosci 32, 7137-7145 https://doi.org/10.1523/JNEUROSCI.0188-12.2012
  55. Zhang B, Carroll J, Trojanowski JQ et al (2012) The microtubule-stabilizing agent, epothilone D, reduces axonal dysfunction, neurotoxicity, cognitive deficits, and Alzheimer-like pathology in an interventional study with aged tau transgenic mice. J Neurosci 32, 3601-3611 https://doi.org/10.1523/JNEUROSCI.4922-11.2012
  56. Cartelli D, Casagrande F, Busceti CL et al (2013) Microtubule alterations occur early in experimental parkinsonism and the microtubule stabilizer epothilone D is neuroprotective. Sci Rep 3, 1837 https://doi.org/10.1038/srep01837
  57. Tseng HC, Zhou Y, Shen Y and Tsai LH (2002) A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett 523, 58-62 https://doi.org/10.1016/S0014-5793(02)02934-4
  58. Lei P, Ayton S, Bush AI and Adlard PA (2011) GSK-3 in Neurodegenerative Diseases. Int J Alzheimers Dis 2011, 189246
  59. Cheung ZH and Ip NY (2012) Cdk5: a multifaceted kinase in neurodegenerative diseases. Trends Cell Biol 22, 169-175 https://doi.org/10.1016/j.tcb.2011.11.003
  60. Noh MY, Chun K, Kang BY et al (2013) Newly developed glycogen synthase kinase-3 (GSK-3) inhibitors protect neuronal cells death in amyloid-beta induced cell model and in a transgenic mouse model of Alzheimer's disease. Biochem Biophys Res Commun 435, 274-281 https://doi.org/10.1016/j.bbrc.2013.04.065
  61. Sereno L, Coma M, Rodriguez M et al (2009) A novel GSK-3beta inhibitor reduces Alzheimer's pathology and rescues neuronal loss in vivo. Neurobiol Dis 35, 359-367 https://doi.org/10.1016/j.nbd.2009.05.025
  62. Lovestone S, Boada M, Dubois B et al (2015) A phase II trial of tideglusib in Alzheimer's disease. J Alzheimers Dis 45, 75-88 https://doi.org/10.3233/JAD-141959
  63. Ori-McKenney KM, McKenney RJ, Huang HH et al (2016) Phosphorylation of beta-Tubulin by the Down Syndrome Kinase, Minibrain/DYRK1a, Regulates Microtubule Dynamics and Dendrite Morphogenesis. Neuron 90, 551-563 https://doi.org/10.1016/j.neuron.2016.03.027
  64. Eira J, Silva CS, Sousa MM and Liz MA (2016) The cytoskeleton as a novel therapeutic target for old neurodegenerative disorders. Prog Neurobiol 141, 61-82 https://doi.org/10.1016/j.pneurobio.2016.04.007
  65. Saal KA, Koch JC, Tatenhorst L et al (2015) AAV.shRNAmediated downregulation of ROCK2 attenuates degeneration of dopaminergic neurons in toxin-induced models of Parkinson's disease in vitro and in vivo. Neurobiol Dis 73, 150-162 https://doi.org/10.1016/j.nbd.2014.09.013
  66. Quassollo G, Wojnacki J, Salas DA et al (2015) A RhoA Signaling Pathway Regulates Dendritic Golgi Outpost Formation. Curr Biol 25, 971-982 https://doi.org/10.1016/j.cub.2015.01.075
  67. Cifelli JL, Dozier L, Chung T, Patrick GN and Yang J (2016) Benzothiazole Amphiphiles Promote the Formation of Dendritic Spines in Primary Hippocampal Neurons. J Biol Chem 291, 11981-11992

Cited by

  1. Golgi Outpost Synthesis Impaired by Toxic Polyglutamine Proteins Contributes to Dendritic Pathology in Neurons vol.20, pp.2, 2017, https://doi.org/10.1016/j.celrep.2017.06.059
  2. Pharmacological intervention of early neuropathy in neurodegenerative diseases vol.119, 2017, https://doi.org/10.1016/j.phrs.2017.02.003
  3. vol.115, pp.33, 2018, https://doi.org/10.1073/pnas.1801117115
  4. Mechanisms of protein toxicity in neurodegenerative diseases vol.75, pp.17, 2018, https://doi.org/10.1007/s00018-018-2854-4