1,160
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

SQSTM1-mediated clearance of cytoplasmic mutant TARDBP/TDP-43 in the monkey brain

, , , , , , , , , , , , & show all
Pages 1955-1968 | Received 30 Mar 2021, Accepted 29 Nov 2021, Published online: 22 Dec 2021

References

  • Neumann M, Sampathu DM, Kwong LK, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006;314(5796):130–133.
  • Chen-Plotkin AS, Lee VM, Trojanowski JQ, et al. TAR DNA-binding protein 43 in neurodegenerative disease. Nat Rev Neurol. 2010;6(4):211–220.
  • Cohen TJ, Lee VM, Trojanowski JQ, et al. TDP-43 functions and pathogenic mechanisms implicated in TDP-43 proteinopathies. Trends Mol Med. 2011;17(11):659–667.
  • Hasegawa M, Nonaka T, Masuda-Suzukake M, et al. Prion-like mechanisms and potential therapeutic targets in neurodegenerative disorders. Pharmacol Ther. 2017;172:22–33.
  • Josephs KA, Whitwell JL, Weigand SD, et al. TDP-43 is a key player in the clinical features associated with Alzheimer’s disease. Acta Neuropathol. 2014;127(6):811–824.
  • McAleese KE, Walker L, Erskine D, et al. TDP-43 pathology in Alzheimer’s disease, dementia with Lewy bodies and ageing. Brain Pathol. 2016;27(4):472–479.
  • Buratti E, Brindisi A, Giombi M, et al. TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail - An important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. J Biol Chem. 2005;280(45):37572–37584.
  • Prakash A, Kumar V, Banerjee A, et al. Structural heterogeneity in RNA recognition motif 2 (RRM2) of TAR DNA-binding protein 43 (TDP-43): clue to amyotrophic lateral sclerosis. J Biomol Struct Dyn. 2020;39(1):357–367.
  • Freibaum BD, Chitta RK, High AA, et al. Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery. J Proteome Res. 2010;9(2):1104–1120.
  • Lagier-Tourenne C, Cleveland DW. Rethinking ALS: the FUS about TDP-43. Cell. 2009;136(6):1001–1004.
  • Polymenidou M, Lagier-Tourenne C, Hutt KR, et al. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci. 2011;14(4):459–468.
  • Ayala YM, De Conti L, Avendano-Vazquez SE, et al. TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 2011;30(2):277–288.
  • Tollervey JR, Curk T, Rogelj B, et al. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci. 2011;14(4):452–458.
  • Buratti E, Baralle FE. Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. Journal of Biological Chemistry. 2001;276(39):36337–36343.
  • Tank EM, Figueroa-Romero C, Hinder LM, et al. Abnormal RNA stability in amyotrophic lateral sclerosis. Nat Commun. 2018;9(1):2845.
  • Colombrita C, Onesto E, Megiorni F, et al. TDP-43 and FUS RNA-binding proteins bind distinct sets of cytoplasmic messenger RNAs and differently regulate their post-transcriptional fate in motoneuron-like cells. J Biol Chem. 2012;287(19):15635–15647.
  • Costessi L, Porro F, Iaconcig A, et al. TDP-43 regulates beta-adducin (Add2) transcript stability. RNA Biol. 2014;11(10):1280–1290.
  • Strong MJ, Volkening K, Hammond R, et al. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol Cell Neurosci. 2007;35(2):320–327.
  • Volkening K, Leystra-Lantz C, Yang W, et al. Tar DNA binding protein of 43 kDa (TDP-43), 14-3-3 proteins and copper/zinc superoxide dismutase (SOD1) interact to modulate NFL mRNA stability. Implications for altered RNA processing in amyotrophic lateral sclerosis (ALS). Brain Res. 2009;1305:168–182.
  • Wang IF, Wu LS, Chang HY, et al. TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J Neurochem. 2008;105(3):797–806.
  • Blauwendraat C, Wilke C, Simon-Sanchez J, et al. The wide genetic landscape of clinical frontotemporal dementia: systematic combined sequencing of 121 consecutive subjects. Genet Med. 2018;20(2):240–249.
  • Deng Z, Lim J, Wang Q, et al. ALS-FTLD-linked mutations of SQSTM1/p62 disrupt selective autophagy and NFE2L2/NRF2 anti-oxidative stress pathway. Autophagy. 2020;16(5):917–931.
  • Deng Z, Purtell K, Lachance V, et al. Autophagy receptors and neurodegenerative diseases. Trends Cell Biol. 2017;27(7):491–504.
  • Cha-Molstad H, Yu JE, Feng Z, et al. p62/SQSTM1/Sequestosome-1 is an N-recognin of the N-end rule pathway which modulates autophagosome biogenesis. Nat Commun. 2017;8(1):102.
  • Laurin N, Brown JP, Morissette J, et al. Recurrent mutation of the gene encoding sequestosome 1 (SQSTM1/p62) in Paget disease of bone. Am J Hum Genet. 2002;70(6):1582–1588.
  • Fecto F, Yan J, Vemula SP, et al. SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch Neurol. 2011;68(11):1440–1446.
  • Rubino E, Rainero I, Chio A, et al. SQSTM1 mutations in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Neurology. 2012;79(15):1556–1562.
  • van der Zee J, Van Langenhove T, Kovacs GG, et al. Rare mutations in SQSTM1 modify susceptibility to frontotemporal lobar degeneration. Acta Neuropathol. 2014;128(3):397–410.
  • Arai T, Nonaka T, Hasegawa M, et al. Neuronal and glial inclusions in frontotemporal dementia with or without motor neuron disease are immunopositive for p62. Neurosci Lett. 2003;342(1–2):41–44.
  • Kawakami I, Arai T, Hasegawa M, et al. The basis of clinicopathological heterogeneity in TDP-43 proteinopathy. Acta Neuropathol. 2019;138(5):751–770.
  • Mann DM, Rollinson S, Robinson A, et al. Dipeptide repeat proteins are present in the p62 positive inclusions in patients with frontotemporal lobar degeneration and motor neurone disease associated with expansions in C9ORF72. Acta Neuropathol Commun. 2013;1(1):68.
  • Babu JR, Geetha T, Wooten MW, et al. Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J Neurochem. 2005;94(1):192–203.
  • Ramesh Babu J, Lamar Seibenhener M, Peng J, et al. Genetic inactivation of p62 leads to accumulation of hyperphosphorylated tau and neurodegeneration. J Neurochem. 2008;06(1):107–120.
  • Hadano S, Mitsui S, Pan L, et al. Functional links between SQSTM1 and ALS2 in the pathogenesis of ALS: cumulative impact on the protection against mutant SOD1-mediated motor dysfunction in mice. Hum Mol Genet. 2016;25(15):3321–3340.
  • Tanji K, Odagiri S, Miki Y, et al. p62 deficiency enhances alpha-synuclein pathology in mice. Brain Pathol. 2015;25(5):552–564.
  • Doi H, Adachi H, Katsuno M, et al. p62/SQSTM1 differentially removes the toxic mutant androgen receptor via autophagy and inclusion formation in a spinal and bulbar muscular atrophy mouse model. J Neurosci. 2013;33(18):7710–7727.
  • Gendron TF, Rademakers R, Petrucelli L, et al. TARDBP mutation analysis in TDP-43 proteinopathies and deciphering the toxicity of mutant TDP-43. J Alzheimers Dis. 2013;33(Suppl 1):S35–45.
  • Huang C, Tong J, Bi F, et al. Mutant TDP-43 in motor neurons promotes the onset and progression of ALS in rats. J Clin Invest. 2012;122(1):107–118.
  • Shan X, Chiang PM, Price DL, et al. Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc Natl Acad Sci U S A. 2010;107(37):16325–16330.
  • Watanabe S, Oiwa K, Murata Y, et al. ALS-linked TDP-43(M337V) knock-in mice exhibit splicing deregulation without neurodegeneration. Mol Brain. 2020;13(1). DOI:https://doi.org/10.1186/s13041-020-0550-4.
  • Wegorzewska I, Bell S, Cairns NJ, et al. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A. 2009;106(44):18809–18814.
  • Yan S, Wang CE, Wei W, et al. TDP-43 causes differential pathology in neuronal versus glial cells in the mouse brain. Hum Mol Genet. 2014;23(10):2678–2693.
  • Mitchell JC, Constable R, So E, et al. Wild type human TDP-43 potentiates ALS-linked mutant TDP-43 driven progressive motor and cortical neuron degeneration with pathological features of ALS. Acta Neuropathol Commun. 2015;3(1):36.
  • Wils H, Kleinberger G, Janssens J, et al. TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A. 2010;107(8):3858–3863.
  • Wang G, Yang H, Yan S, et al. Cytoplasmic mislocalization of RNA splicing factors and aberrant neuronal gene splicing in TDP-43 transgenic pig brain. Mol Neurodegener. 2015;10(1):42.
  • Yin P, Guo XY, Yang WL, et al. Caspase-4 mediates cytoplasmic accumulation of TDP-43 in the primate brains. Acta Neuropathol. 2019;137(6):919–937.
  • Yin P, Bai DZ, Zhu LH, et al. Cytoplasmic TDP-43 impairs the activity of the ubiquitin-proteasome system. Exp Neurol. 2021;345:113833.
  • Melamed Z, Lopez-Erauskin J, Baughn MW, et al. Premature polyadenylation-mediated loss of stathmin-2 is a hallmark of TDP-43-dependent neurodegeneration. Nat Neurosci. 2019;22(2):180–190.
  • Klim JR, Williams LA, Limone F, et al. ALS-implicated protein TDP-43 sustains levels of STMN2, a mediator of motor neuron growth and repair. Nat Neurosci. 2019;22(2):167–179.
  • Ling JP, Pletnikova O, Troncoso JC, et al. TDP-43 repression of nonconserved cryptic exons is compromised in ALS-FTD. Science. 2015;349(6248):650–655.
  • Chang CK, Wu TH, Wu CY, et al. The N-terminus of TDP-43 promotes its oligomerization and enhances DNA binding affinity. Biochem Biophys Res Commun. 2012;425(2):219–224.
  • Mompean M, Romano V, Pantoja-Uceda D, et al. The TDP-43 N-terminal domain structure at high resolution. FEBS J. 2016;283(7):1242–1260.
  • Qin H, Lim LZ, Wei Y, et al. TDP-43 N terminus encodes a novel ubiquitin-like fold and its unfolded form in equilibrium that can be shifted by binding to ssDNA. Proc Natl Acad Sci U S A. 2014;111(52):18619–18624.
  • Komatsu M, Waguri S, Koike M, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell. 2007;131(6):1149–1163.
  • Ma S, Attarwala IY, Xie XQ, et al. SQSTM1/p62: a potential target for neurodegenerative disease. ACS Chem Neurosci. 2019;10(5):2094–2114.
  • Shin WH, Park JH, Chung KC, et al. The central regulator p62 between ubiquitin proteasome system and autophagy and its role in the mitophagy and Parkinson’s disease. BMB Rep. 2020;53(1):56–63.
  • Kabashi E, Valdmanis PN, Dion P, et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet. 2008;40(5):572–574.
  • Renton AE, Chio A, Traynor BJ, et al. State of play in amyotrophic lateral sclerosis genetics. Nat Neurosci. 2014;17(1):17–23.
  • Koyama A, Sugai A, Kato T, et al. Increased cytoplasmic TARDBP mRNA in affected spinal motor neurons in ALS caused by abnormal autoregulation of TDP-43. Nucleic Acids Res. 2016;44(12):5820–5836.
  • White MA, Kim E, Duffy A, et al. TDP-43 gains function due to perturbed autoregulation in a Tardbp knock-in mouse model of ALS-FTD. Nat Neurosci. 2018;21(4):552–563.
  • Gitcho MA, Bigio EH, Mishra M, et al. TARDBP 3ʹ-UTR variant in autopsy-confirmed frontotemporal lobar degeneration with TDP-43 proteinopathy. Acta Neuropathol. 2009;118(5):633–645.
  • Swarup V, Phaneuf D, Dupre N, et al. Deregulation of TDP-43 in amyotrophic lateral sclerosis triggers nuclear factor kappaB-mediated pathogenic pathways. J Exp Med. 2011;208(12):2429–2447.
  • Uchida A, Sasaguri H, Kimura N, et al. Non-human primate model of amyotrophic lateral sclerosis with cytoplasmic mislocalization of TDP-43. Brain. 2012;135(Pt 3):833–846.
  • Brady OA, Meng P, Zheng Y, et al. Regulation of TDP-43 aggregation by phosphorylation and p62/SQSTM1. J Neurochem. 2011;116(2):248–259.
  • Tanji K, Zhang HX, Mori F, et al. p62/sequestosome 1 binds to TDP-43 in brains with frontotemporal lobar degeneration with TDP-43 inclusions. J Neurosci Res. 2012;90(10):2034–2042.
  • Gal J, Strom AL, Kilty R, et al. p62 accumulates and enhances aggregate formation in model systems of familial amyotrophic lateral sclerosis. J Biol Chem. 2007;282(15):11068–11077.
  • Zatloukal K, Stumptner C, Fuchsbichler A, et al. p62 is a common component of cytoplasmic inclusions in protein aggregation diseases. Am J Pathol. 2002;160(1):255–263.
  • Kumar S, Phaneuf D, Cordeau P, et al. Induction of autophagy mitigates TDP-43 pathology and translational repression of neurofilament mRNAs in mouse models of ALS/FTD. Mol Neurodegener. 2021;16(1):1.
  • Ormeno F, Hormazabal J, Moreno J, et al. Chaperone Mediated Autophagy Degrades TDP-43 Protein and Is Affected by TDP-43 Aggregation. Front Mol Neurosci. 2020;13:19.
  • Jackson LK, Lin W-L, Miriyala S, et al. p62 pathology model in the rat substantia nigra with filamentous inclusions and progressive neurodegeneration. PLoS One. 2017;12(1):e0169291.
  • Mitsui S, Otomo A, Nozaki M, et al. Systemic over expression of SQSTM1/p62 accelerates disease onset in a SOD1H46R-expressing ALS mouse model. Mol Brain. 2018;11(1):30.
  • Seibenhener ML, Zhao T, Yf D, et al. Behavioral effects of SQSTM1/p62 overexpression in mice: support for a mitochondrial role in depression and anxiety. Behav Brain Res. 2013;248:94–103.
  • Aparicio R, Rana A, Walker DW, et al. Upregulation of the autophagy adaptor p62/SQSTM1 prolongs health and lifespan in middle-aged Drosophila. Cell Rep. 2019;28(4):1029–1040.e5.
  • Du YF, Wooten MC, Gearing M, et al. Age-associated oxidative damage to the p62 promoter: implications for Alzheimer disease. Free Radic Biol Med. 2009;46(4):492–501.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.