Cellular and Molecular Life Sciences

, Volume 76, Issue 1, pp 1–11 | Cite as

Evolvability of the actin cytoskeleton in oligodendrocytes during central nervous system development and aging

  • Ana Isabel SeixasEmail author
  • Maria Manuela Azevedo
  • Joana Paes de Faria
  • Diogo Fernandes
  • Inês Mendes Pinto
  • João Bettencourt Relvas


The organization of actin filaments into a wide range of subcellular structures is a defining feature of cell shape and dynamics, important for tissue development and homeostasis. Nervous system function requires morphological and functional plasticity of neurons and glial cells, which is largely determined by the dynamic reorganization of the actin cytoskeleton in response to intrinsic and extracellular signals. Oligodendrocytes are specialized glia that extend multiple actin-based protrusions to form the multilayered myelin membrane that spirally wraps around axons, increasing conduction speed and promoting long-term axonal integrity. Myelination is a remarkable biological paradigm in development, and maintenance of myelin is essential for a healthy adult nervous system. In this review, we discuss how structure and dynamics of the actin cytoskeleton is a defining feature of myelinating oligodendrocytes’ biology and function. We also review “old and new” concepts to reflect on the potential role of the cytoskeleton in balancing life and death of myelin membranes and oligodendrocytes in the aging central nervous system.


Glia Myelin White matter Age-associated cognitive decline Cellular aging Brain aging Membrane remodeling 



We thank Alexandra Guedes for the illustrations in the article. Work in our laboratories was funded by the project NORTE-01-0145-FEDER-000008-Porto Neurosciences and Neurologic Disease Research Initiative at I3S, supported by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (FEDER). We also acknowledge the financial support of FEDER funds through the COMPETE 2020-Operational Programme for Competitiveness and Internationalization (POCI), Portugal 2020, and by Portuguese funds through FCT (Fundação para a Ciência e a Tecnologia)/MCTES in the framework of the project “Institute for Research and Innovation in Health Sciences” (POCI-01-0145-FEDER-007274). IMP acknowledges the support of the Marie Curie COFUND Programme “NanoTRAINforGrowth”, the EU FP7 grant agreement number 600375, and the project Nanotechnology-based functional solutions (NORTE-01–0145-FEDER-000019), co-financed by NORTE 2020, under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). MMA (SFRH/BD/90301/2012) and AIS (SFRH/BPD/79417/2011) are recipients of individual fellowships from FCT.


  1. 1.
    Kevenaar JT, Hoogenraad CC (2015) The axonal cytoskeleton: from organization to function. Front Mol Neurosci 8:44CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Kachar B, Behar T, Dubois-Dalcq M (1986) Cell shape and motility of oligodendrocytes cultured without neurons. Cell Tissue Res 244:27–38CrossRefPubMedGoogle Scholar
  3. 3.
    Wilson R, Brophy PJ (1989) Role for the oligodendrocyte cytoskeleton in myelination. J Neurosci Res 22:439–448CrossRefPubMedGoogle Scholar
  4. 4.
    Fox MA, Afshari FS, Alexander JK, Colello RJ, Fuss B (2006) Growth cone like sensorimotor structures are characteristic features of postmigratory, premyelinating oligodendrocytes. Glia 53:563–566CrossRefPubMedGoogle Scholar
  5. 5.
    Simpson PB, Armstrong RC (1999) Intracellular signals and cytoskeletal elements involved in oligodendrocyte progenitor migration. Glia 26:22–35CrossRefPubMedGoogle Scholar
  6. 6.
    Song J, Goetz BD, Baas PW, Duncan ID (2001) Cytoskeletal reorganization during the formation of oligodendrocyte processes and branches. Mol Cell Neurosci 17:624–636CrossRefPubMedGoogle Scholar
  7. 7.
    Tang DG, Tokumoto YM, Raff MC (2000) Long-term culture of purified postnatal oligodendrocyte precursor cells. Evidence for an intrinsic maturation program that plays out over months. J Cell Biol 148:971–984CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Azevedo MM, Domingues HS, Cordelieres FP, Sampaio P, Seixas AI, Relvas JB (2018) Jmy regulates oligodendrocyte differentiation via modulation of actin cytoskeleton dynamics. Glia. CrossRefPubMedGoogle Scholar
  9. 9.
    Nawaz S et al (2015) Actin filament turnover drives leading edge growth during myelin sheath formation in the central nervous system. Dev Cell 34:139–151CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Kirby BB, Takada N, Latimer AJ, Shin J, Carney TJ, Kelsh RN, Appel B (2006) In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 9:1506–1511CrossRefPubMedGoogle Scholar
  11. 11.
    Hughes EG, Kang SH, Fukaya M, Bergles DE (2013) Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci 16:668–676CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Hughes EG, Appel B (2016) The cell biology of CNS myelination. Curr Opin Neurobiol 39:93–100CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Domingues HS, Cruz A, Chan JR, Relvas JB, Rubinstein B, Pinto IM (2018) Mechanical plasticity during oligodendrocyte differentiation and myelination. Glia 66:5–14CrossRefPubMedGoogle Scholar
  14. 14.
    Zuchero JB et al (2015) CNS myelin wrapping is driven by actin disassembly. Dev Cell 34:152–167CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Boggs JM, Rangaraj G (2000) Interaction of lipid-bound myelin basic protein with actin filaments and calmodulin. Biochemistry 39:7799–7806CrossRefPubMedGoogle Scholar
  16. 16.
    Nawaz S, Kippert A, Saab AS, Werner HB, Lang T, Nave KA, Simons M (2009) Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in oligodendroglial cells and its rapid perturbation by elevated calcium. J Neurosci 29:4794–4807CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Snaidero N et al (2014) Myelin membrane wrapping of CNS axons by PI(3,4,5)P3-dependent polarized growth at the inner tongue. Cell 156:277–290CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kippert A, Fitzner D, Helenius J, Simons M (2009) Actomyosin contractility controls cell surface area of oligodendrocytes. BMC Cell Biol. 10:71CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Wang H, Tewari A, Einheber S, Salzer JL, Melendez-Vasquez CV (2008) Myosin II has distinct functions in PNS and CNS myelin sheath formation. J Cell Biol 182:1171–1184CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Sloane JA, Vartanian TK (2007) Myosin Va controls oligodendrocyte morphogenesis and myelination. J Neurosci 27:11366–11375CrossRefPubMedGoogle Scholar
  21. 21.
    Yamazaki R, Ishibashi T, Baba H, Yamaguchi Y (2016) Knockdown of unconventional myosin ID expression induced morphological change in oligodendrocytes. ASN Neuro. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Buttery PC, ffrench-Constant C (2001) Process extension and myelin sheet formation in maturing oligodendrocytes. Prog Brain Res 132:115–130CrossRefPubMedGoogle Scholar
  23. 23.
    Cahoy JD et al (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Dugas JC, Tai YC, Speed TP, Ngai J, Barres BA (2006) Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26:10967–10983CrossRefPubMedGoogle Scholar
  25. 25.
    Nielsen JA, Maric D, Lau P, Barker JL, Hudson LD (2006) Identification of a novel oligodendrocyte cell adhesion protein using gene expression profiling. J Neurosci 26:9881–9891CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Zhang Y et al (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34:11929–11947CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Bacon C, Lakics V, Machesky L, Rumsby M (2007) N-WASP regulates extension of filopodia and processes by oligodendrocyte progenitors, oligodendrocytes, and Schwann cells-implications for axon ensheathment at myelination. Glia 55:844–858CrossRefPubMedGoogle Scholar
  28. 28.
    Kim HJ, DiBernardo AB, Sloane JA, Rasband MN, Solomon D, Kosaras B, Kwak SP, Vartanian TK (2006) WAVE1 is required for oligodendrocyte morphogenesis and normal CNS myelination. J Neurosci 26:5849–5859CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Brockschnieder D, Sabanay H, Riethmacher D, Peles E (2006) Ermin, a myelinating oligodendrocyte-specific protein that regulates cell morphology. J Neurosci 26:757–762CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Zhang B et al (2005) Juxtanodin: an oligodendroglial protein that promotes cellular arborization and 2′,3′-cyclic nucleotide-3′-phosphodiesterase trafficking. Proc Natl Acad Sci USA 102:11527–11532CrossRefPubMedGoogle Scholar
  31. 31.
    Lourenco T, Paes de Faria J, Bippes CA, Maia J, Lopes-da-Silva JA, Relvas JB, Graos M (2016) Modulation of oligodendrocyte differentiation and maturation by combined biochemical and mechanical cues. Sci Rep 6:21563CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Mitew S, Hay CM, Peckham H, Xiao J, Koenning M, Emery B (2014) Mechanisms regulating the development of oligodendrocytes and central nervous system myelin. Neuroscience 276:29–47CrossRefPubMedGoogle Scholar
  33. 33.
    O’Meara RW, Michalski J-P, Anderson C, Bhanot K, Rippstein P, Kothary R (2013) Integrin-linked kinase regulates process extension in oligodendrocytes via control of actin cytoskeletal dynamics. J Neurosci 33:9781–9793CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Michalski JP, Cummings SE, O’Meara RW, Kothary R (2016) Integrin-linked kinase regulates oligodendrocyte cytoskeleton, growth cone, and adhesion dynamics. J Neurochem 136:536–549CrossRefPubMedGoogle Scholar
  35. 35.
    Forrest AD, Beggs HE, Reichardt LF, Dupree JL, Colello RJ, Fuss B (2009) Focal adhesion kinase (FAK): a regulator of CNS myelination. J Neurosci Res 87:3456–3464CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Machacek M et al (2009) Coordination of Rho GTPase activities during cell protrusion. Nature 461:99–103CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Sperber BR, Boyle-Walsh EA, Engleka MJ, Gadue P, Peterson AC, Stein PL, Scherer SS, McMorris FA (2001) A unique role for Fyn in CNS myelination. J Neurosci 21:2039–2047CrossRefPubMedGoogle Scholar
  38. 38.
    Liang X, Draghi NA, Resh MD (2004) Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 24:7140–7149CrossRefPubMedGoogle Scholar
  39. 39.
    Ackerman SD, Garcia C, Piao X, Gutmann DH, Monk KR (2015) The adhesion GPCR Gpr56 regulates oligodendrocyte development via interactions with Galpha12/13 and RhoA. Nat Commun 6:6122CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Giera S et al (2015) The adhesion G protein-coupled receptor GPR56 is a cell-autonomous regulator of oligodendrocyte development. Nat Commun 6:6121CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Mi S et al (2005) LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 8:745–751CrossRefPubMedGoogle Scholar
  42. 42.
    Thurnherr T et al (2006) Cdc42 and Rac1 signaling are both required for and act synergistically in the correct formation of myelin sheaths in the CNS. J Neurosci 26:10110–10119CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Martin-Vilchez S, Whitmore L, Asmussen H, Zareno J, Horwitz R, Newell-Litwa K (2017) RhoGTPase regulators orchestrate distinct stages of synaptic development. PLoS One 12:e0170464CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Feltri LM, Suter U, Relvas JB (2008) The function of RhoGTPases in axon ensheathment and myelination. Glia 56:1508–1517CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Bartzokis G (2004) Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease. Neurobiol Aging 25:5–18 (author reply 49-62) CrossRefPubMedGoogle Scholar
  46. 46.
    Peters A, Josephson K, Vincent SL (1991) Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex. Anat Rec 229:384–398CrossRefPubMedGoogle Scholar
  47. 47.
    Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson WD (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392–1401CrossRefPubMedGoogle Scholar
  48. 48.
    Tripathi RB, Jackiewicz M, McKenzie IA, Kougioumtzidou E, Grist M, Richardson WD (2017) Remarkable stability of myelinating oligodendrocytes in mice. Cell Rep 21:316–323CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Hughes EG, Orthmann-Murphy JL, Langseth AJ, Bergles DE (2018) Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex. Nat Neurosci 21:696–706CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Hill RA, Li AM, Grutzendler J (2018) Lifelong cortical myelin plasticity and age-related degeneration in the live mammalian brain. Nat Neurosci 21:683–695CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Young KM, Psachoulia K, Tripathi RB, Dunn SJ, Cossell L, Attwell D, Tohyama K, Richardson WD (2013) Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 77:873–885CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Yeung MS et al (2014) Dynamics of oligodendrocyte generation and myelination in the human brain. Cell 159:766–774CrossRefPubMedGoogle Scholar
  53. 53.
    Xiao L et al (2016) Rapid production of new oligodendrocytes is required in the earliest stages of motor-skill learning. Nat Neurosci 19:1210–1217CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Gibson EM et al (2014) Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science 344:1252304CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Makinodan M, Rosen KM, Ito S, Corfas G (2012) A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337:1357–1360CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullen F (2005) Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8:1148–1150CrossRefPubMedGoogle Scholar
  57. 57.
    Scholz J, Klein MC, Behrens TE, Johansen-Berg H (2009) Training induces changes in white-matter architecture. Nat Neurosci 12:1370–1371CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    McKenzie IA, Ohayon D, Li H, de Faria JP, Emery B, Tohyama K, Richardson WD (2014) Motor skill learning requires active central myelination. Science 346:318–322CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Marques S et al (2016) Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science 352:1326–1329CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Darr AJ et al (2017) Identification of genome-wide targets of Olig2 in the adult mouse spinal cord using ChIP-Seq. PLoS One 12:e0186091CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Guttmann CR, Jolesz FA, Kikinis R, Killiany RJ, Moss MB, Sandor T, Albert MS (1998) White matter changes with normal aging. Neurology 50:972–978CrossRefPubMedGoogle Scholar
  62. 62.
    Morrison JH, Hof PR (1997) Life and death of neurons in the aging brain. Science 278:412–419CrossRefPubMedGoogle Scholar
  63. 63.
    Gunning-Dixon FM, Raz N (2000) The cognitive correlates of white matter abnormalities in normal aging: a quantitative review. Neuropsychology 14:224–232CrossRefPubMedGoogle Scholar
  64. 64.
    Peters A, Rosene DL, Moss MB, Kemper TL, Abraham CR, Tigges J, Albert MS (1996) Neurobiological bases of age-related cognitive decline in the rhesus monkey. J Neuropathol Exp Neurol 55:861–874CrossRefPubMedGoogle Scholar
  65. 65.
    Liu H, Yang Y, Xia Y, Zhu W, Leak RK, Wei Z, Wang J, Hu X (2017) Aging of cerebral white matter. Ageing Res Rev 34:64–76CrossRefPubMedGoogle Scholar
  66. 66.
    Peters A, Sethares C, Killiany RJ (2001) Effects of age on the thickness of myelin sheaths in monkey primary visual cortex. J Comp Neurol 435:241–248CrossRefPubMedGoogle Scholar
  67. 67.
    Stahon KE, Bastian C, Griffith S, Kidd GJ, Brunet S, Baltan S (2016) Age-related changes in axonal and mitochondrial ultrastructure and function in white matter. J Neurosci 36:9990–10001CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Peters A, Kemper T (2012) A review of the structural alterations in the cerebral hemispheres of the aging rhesus monkey. Neurobiol Aging 33:2357–2372CrossRefPubMedGoogle Scholar
  69. 69.
    Sturrock RR (1976) Changes in neurologia and myelination in the white matter of aging mice. J Gerontol 31:513–522CrossRefPubMedGoogle Scholar
  70. 70.
    Peters A, Sethares C (2002) Aging and the myelinated fibers in prefrontal cortex and corpus callosum of the monkey. J Comp Neurol 442:277–291CrossRefPubMedGoogle Scholar
  71. 71.
    Bowley MP, Cabral H, Rosene DL, Peters A (2010) Age changes in myelinated nerve fibers of the cingulate bundle and corpus callosum in the rhesus monkey. J Comp Neurol 518:3046–3064CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Sandell JH, Peters A (2002) Effects of age on the glial cells in the rhesus monkey optic nerve. J Comp Neurol 445:13–28CrossRefPubMedGoogle Scholar
  73. 73.
    Jahn O, Tenzer S, Werner HB (2009) Myelin proteomics: molecular anatomy of an insulating sheath. Mol Neurobiol 40:55–72CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Ishii A, Dutta R, Wark GM, Hwang SI, Han DK, Trapp BD, Pfeiffer SE, Bansal R (2009) Human myelin proteome and comparative analysis with mouse myelin. Proc Natl Acad Sci USA 106:14605–14610CrossRefPubMedGoogle Scholar
  75. 75.
    Toyama BH, Savas JN, Park SK, Harris MS, Ingolia NT, Yates JR 3rd, Hetzer MW (2013) Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154:971–982CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Malone MJ, Szoke MC (1982) Neurochemical studies in aging brain. I. Structural changes in myelin lipids. J Gerontol 37:262–267CrossRefPubMedGoogle Scholar
  77. 77.
    Tse KH, Herrup K (2017) DNA damage in the oligodendrocyte lineage and its role in brain aging. Mech Ageing Dev 161:37–50CrossRefPubMedGoogle Scholar
  78. 78.
    DiLoreto R, Murphy CT (2015) The cell biology of aging. Mol Biol Cell 26:4524–4531CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Amberg D, Leadsham JE, Kotiadis V, Gourlay CW (2012) Cellular ageing and the actin cytoskeleton. Subcell Biochem 57:331–352CrossRefPubMedGoogle Scholar
  80. 80.
    Arani A et al (2015) Measuring the effects of aging and sex on regional brain stiffness with MR elastography in healthy older adults. Neuroimage 111:59–64CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Patzig J et al (2016) Septin/anillin filaments scaffold central nervous system myelin to accelerate nerve conduction. Elife 5:e17119CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Peters A (2009) The effects of normal aging on myelinated nerve fibers in monkey central nervous system. Front Neuroanat 3:11CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Peters A (1996) Age-related changes in oligodendrocytes in monkey cerebral cortex. J Comp Neurol 371:153–163CrossRefPubMedGoogle Scholar
  84. 84.
    Safaiyan S et al (2016) Age-related myelin degradation burdens the clearance function of microglia during aging. Nat Neurosci 19:995–998CrossRefGoogle Scholar
  85. 85.
    Galatro TF et al (2017) Transcriptomic analysis of purified human cortical microglia reveals age-associated changes. Nat Neurosci 20:1162–1171CrossRefPubMedGoogle Scholar
  86. 86.
    Yao Y, Lacroix D, Mak AF (2016) Effects of oxidative stress-induced changes in the actin cytoskeletal structure on myoblast damage under compressive stress: confocal-based cell-specific finite element analysis. Biomech Model Mechanobiol 15:1495–1508CrossRefPubMedGoogle Scholar
  87. 87.
    Wong SW, Sun S, Cho M, Lee KK, Mak AF (2015) H2O2 exposure affects myotube stiffness and actin filament polymerization. Ann Biomed Eng 43:1178–1188CrossRefPubMedGoogle Scholar
  88. 88.
    Gourlay CW, Carpp LN, Timpson P, Winder SJ, Ayscough KR (2004) A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 164:803–809CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Celeste Morley S, Sun GP, Bierer BE (2003) Inhibition of actin polymerization enhances commitment to and execution of apoptosis induced by withdrawal of trophic support. J Cell Biochem 88:1066–1076CrossRefPubMedGoogle Scholar
  90. 90.
    Ben-Zvi A, Miller EA, Morimoto RI (2009) Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci USA 106:14914–14919CrossRefPubMedGoogle Scholar
  91. 91.
    Baird NA et al (2014) HSF-1-mediated cytoskeletal integrity determines thermotolerance and life span. Science 346:360–363CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Higuchi R, Vevea JD, Swayne TC, Chojnowski R, Hill V, Boldogh IR, Pon LA (2013) Actin dynamics affect mitochondrial quality control and aging in budding yeast. Curr Biol 23:2417–2422CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Hirano A (1994) Hirano bodies and related neuronal inclusions. Neuropathol Appl Neurobiol 20:3–11CrossRefPubMedGoogle Scholar
  94. 94.
    Cichon J, Sun C, Chen B, Jiang M, Chen XA, Sun Y, Wang Y, Chen G (2012) Cofilin aggregation blocks intracellular trafficking and induces synaptic loss in hippocampal neurons. J Biol Chem 287:3919–3929CrossRefPubMedGoogle Scholar
  95. 95.
    Mustafa AG, Wang JA, Carrico KM, Hall ED (2011) Pharmacological inhibition of lipid peroxidation attenuates calpain-mediated cytoskeletal degradation after traumatic brain injury. J Neurochem 117:579–588CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.i3S - Instituto de Investigação e Inovação em SaúdeUniversidade do PortoPortoPortugal
  2. 2.IBMC - Instituto de Biologia Molecular e CelularPortoPortugal
  3. 3.Instituto Superior TécnicoUniversidade de LisboaLisbonPortugal
  4. 4.International Iberian Nanotechnology Laboratory - INLBragaPortugal
  5. 5.The Discoveries Centre for Regeneration and Precision MedicinePortoPortugal

Personalised recommendations