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Cited by 550RNA Research and SplicingCellular transport and secretionAmyotrophic Lateral Sclerosis Research

RNA Granules Hitchhike on Lysosomes for Long-Distance Transport, Using Annexin A11 as a Molecular Tether

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Liao, Ya-Cheng, Fernandopulle, Michael S., Wang, Guozhen, Choi, Heejun, Hao, Ling, Drerup, Catherine M., Patel, Rajan, Qamar, Seema +15 more·2019·Cell
DOI 10.1016/j.cell.2019.08.050PMC PMC6890474
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Abstract

Long-distance RNA transport enables local protein synthesis at metabolically-active sites distant from the nucleus. This process ensures an appropriate spatial organization of proteins, vital to polarized cells such as neurons. Here, we present a mechanism for RNA transport in which RNA granules "hitchhike" on moving lysosomes. In vitro biophysical modeling, live-cell microscopy, and unbiased proximity labeling proteomics reveal that annexin A11 (ANXA11), an RNA granule-associated phosphoinositide-binding protein, acts as a molecular tether between RNA granules and lysosomes. ANXA11 possesses an N-terminal low complexity domain, facilitating its phase separation into membraneless RNA granules, and a C-terminal membrane binding domain, enabling interactions with lysosomes. RNA granule transport requires ANXA11, and amyotrophic lateral sclerosis (ALS)-associated mutations in ANXA11 impair RNA granule transport by disrupting their interactions with lysosomes. Thus, ANXA11 mediates neuronal RNA transport by tethering RNA granules to actively-transported lysosomes, performing a critical cellular function that is disrupted in ALS.

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  • SCARB2 has been identified in several PD risk genome-wide association studies.

    “SCARB2 has been identified in several PD risk genome-wide association studies (GWAS).100–103”

    From The lysosome and proteostatic stress at the intersection of pediatric neurological disorders and adult neurodegenerative diseases (2025) · cites this paper as [100]

    The Introduction discusses genetic links to ALS/FTD, not SCARB2 or Parkinson’s disease risk. Searches for SCARB2, PD risk, and genome-wide association studies found no passage in our copy addressing the claim; the occurrence of “Parkinson” in the References is an author’s surname. (LLM, conf=0.76)

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  1. Alami N.H. Smith R.B. Carrasco M.A. Williams L.A. Winborn C.S. Han S.S.W. Kiskinis E. Winborn B. Freibaum B.D. Kanagaraj A. Axonal transport of TDP-43 mRNA granules is impaired by ALS-causing mutations Neuron 81 2014 536 543 24507191 PMC3939050
  2. Baird F.J. Bennett C.L. Microtubule defects & Neurodegeneration J. Genet. Syndr. Gene Ther. 4 2013 203 24563812 PMC3930179
  3. Bakthavachalu B. Huelsmeier J. Sudhakaran I.P. Hillebrand J. Singh A. Petrauskas A. Thiagarajan D. Sankaranarayanan M. Mizoue L. Anderson E.N. RNP-Granule Assembly via Ataxin-2 Disordered Domains Is Required for Long-Term Memory and Neurodegeneration Neuron 98 2018 754 766.e4 29772202
  4. Baltz A.G. Munschauer M. Schwanhäusser B. Vasile A. Murakawa Y. Schueler M. Youngs N. Penfold-Brown D. Drew K. Milek M. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts Mol. Cell 46 2012 674 690 22681889
  5. Bassell G.J. Zhang H. Byrd A.L. Femino A.M. Singer R.H. Taneja K.L. Lifshitz L.M. Herman I.M. Kosik K.S. Sorting of β-actin mRNA and protein to neurites and growth cones in culture J. Neurosci. 18 1998 251 265 9412505 PMC6793411
  6. Baumann S. Pohlmann T. Jungbluth M. Brachmann A. Feldbrügge M. Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes J. Cell Sci. 125 2012 2740 2752 22357951
  7. Buchan J.R. Kolaitis R.-M. Taylor J.P. Parker R. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function Cell 153 2013 1461 1474 23791177 PMC3760148
  8. Chen J. Bardes E.E. Aronow B.J. Jegga A.G. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization Nucleic Acids Res. 37 2009 W305-11 PMC2703978 19465376
  9. Cheng X.T. Xie Y.X. Zhou B. Huang N. Farfel-Becker T. Sheng Z.H. Characterization of LAMP1-labeled nondegradative lysosomal and endocytic compartments in neurons J. Cell Biol. 217 2018 3127 3139 29695488 PMC6123004
  10. Chevalier-Larsen E. Holzbaur E.L.F. Axonal transport and neurodegenerative disease Biochim. Biophys. Acta 1762 2006 1094 1108 16730956
  11. Choi M. Chang C.Y. Clough T. Broudy D. Killeen T. MacLean B. Vitek O. MSstats: an R package for statistical analysis of quantitative mass spectrometry-based proteomic experiments Bioinformatics 30 2014 2524 2526 24794931
  12. Cioni J.-M. Lin J.Q. Holtermann A.V. Koppers M. Jakobs M.A.H. Azizi A. Turner-Bridger B. Shigeoka T. Franze K. Harris W.A. Holt C.E. Late Endosomes Act as mRNA Translation Platforms and Sustain Mitochondria in Axons Cell 176 2019 56 72.e15 30612743 PMC6333918
  13. Clark A. Meignin C. Davis I. A Dynein-dependent shortcut rapidly delivers axis determination transcripts into the Drosophila oocyte Development 134 2007 1955 1965 17442699 PMC2140221
  14. Davidovic L. Jaglin X.H. Lepagnol-Bestel A.-M. Tremblay S. Simonneau M. Bardoni B. Khandjian E.W. The fragile X mental retardation protein is a molecular adaptor between the neurospecific KIF3C kinesin and dendritic RNA granules Hum. Mol. Genet. 16 2007 3047 3058 17881655
  15. Dictenberg J. Swanger S. Antar L. Singer R. Bassell G. A direct role for FMRP in activity dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome Dev. Cell 14 2008 926 939 18539120 PMC2453222
  16. Dienstbier M. Boehl F. Li X. Bullock S.L. Egalitarian is a selective RNA-binding protein linking mRNA localization signals to the dynein motor Genes Dev. 23 2009 1546 1558 19515976 PMC2704466
  17. Dix C.I. Soundararajan H.C. Dzhindzhev N.S. Begum F. Suter B. Ohkura H. Stephens E. Bullock S.L. Lissencephaly-1 promotes the recruitment of dynein and dynactin to transported mRNAs J. Cell Biol. 202 2013 479 494 23918939 PMC3734092
  18. Dong X.P. Shen D. Wang X. Dawson T. Li X. Zhang Q. Cheng X. Zhang Y. Weisman L.S. Delling M. Xu H. PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome Nat. Commun. 1 2010 38 20802798 PMC2928581
  19. Drerup C.M. Nechiporuk A.V. In vivo analysis of axonal transport in zebrafish Methods Cell Biol. 131 2016 311 329 26794521 PMC6337719
  20. Duffy D.C. McDonald J.C. Schueller O.J.A. Whitesides G.M. Rapid prototyping of microfluidic systems in poly(dimethylsiloxane) Anal. Chem. 70 1998 4974 4984 21644679
  21. Fallini C. Zhang H. Su Y. Silani V. Singer R.H. Rossoll W. Bassell G.J. The survival of motor neuron (SMN) protein interacts with the mRNA-binding protein HuD and regulates localization of poly(A) mRNA in primary motor neuron axons J. Neurosci. 31 2011 3914 3925 21389246 PMC3070748
  22. Farías G.G. Guardia C.M. De Pace R. Britt D.J. Bonifacino J.S. BORC/kinesin-1 ensemble drives polarized transport of lysosomes into the axon Proc. Natl. Acad. Sci. USA 114 2017 E2955 E2964 28320970 PMC5389300
  23. Fernandopulle M.S. Prestil R. Grunseich C. Wang C. Gan L. Ward M.E. Transcription Factor-Mediated Differentiation of Human iPSCs into Neurons Curr. Protoc. Cell Biol. 79 2018 e51–e48 PMC6993937 29924488
  24. Fu M.M. Holzbaur E.L. Integrated regulation of motor-driven organelle transport by scaffolding proteins Trends Cell Biol. 24 2014 564 574 24953741 PMC4177981
  25. Gang H. Galvagnion C. Meisl G. Müller T. Pfammatter M. Buell A.K. Levin A. Dobson C.M. Mu B. Knowles T.P.J. Microfluidic Diffusion Platform for Characterizing the Sizes of Lipid Vesicles and the Thermodynamics of Protein-Lipid Interactions Anal. Chem. 90 2018 3284 3290 29313342
  26. Gáspár I. Sysoev V. Komissarov A. Ephrussi A. An RNA-binding atypical tropomyosin recruits kinesin-1 dynamically to oskar mRNPs EMBO J. 36 2017 319 333 28028052 PMC5286366
  27. Gagnon J.A. Kreiling J.A. Powrie E.A. Wood T.R. Mowry K.L. Directional transport is mediated by a Dynein-dependent step in an RNA localization pathway PLoS Biol. 11 2013 e1001551 23637574 PMC3640089
  28. Gershoni-Emek N. Altman T. Ionescu A. Costa C.J. Gradus-Pery T. Willis D.E. Perlson E. Localization of RNAi machinery to axonal branch points and growth cones is facilitated by mitochondria and is disrupted in ALS Front. Mol. Neurosci. 11 2018 311 30233312 PMC6134038
  29. Glock C. Heumüller M. Schuman E.M. mRNA transport & local translation in neurons Curr. Opin. Neurobiol. 45 2017 169 177 28633045
  30. Gopal P.P. Nirschl J.J. Klinman E. Holzbaur E.L.F. Amyotrophic lateral sclerosis-linked mutations increase the viscosity of liquid-like TDP-43 RNP granules in neurons Proc. Natl. Acad. Sci. USA 114 2017 E2466 E2475 28265061 PMC5373408
  31. Guerreiro R. Brás J. Hardy J. SnapShot: Genetics of ALS and FTD Cell 160 2015 798 798.e1 25679767
  32. Guimaraes S.C. Schuster M. Bielska E. Dagdas G. Kilaru S. Meadows B.R.A. Schrader M. Steinberg G. Peroxisomes, lipid droplets, and endoplasmic reticulum “hitchhike” on motile early endosomes J. Cell Biol. 211 2015 945 954 26620910 PMC4674278
  33. Higuchi Y. Ashwin P. Roger Y. Steinberg G. Early endosome motility spatially organizes polysome distribution J. Cell Biol. 204 2014 343 357 24493587 PMC3912533
  34. Hirokawa N. Niwa S. Tanaka Y. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease Neuron 68 2010 610 638 21092854
  35. Hung V. Udeshi N.D. Lam S.S. Loh K.H. Cox K.J. Pedram K. Carr S.A. Ting A.Y. Spatially resolved proteomic mapping in living cells with the engineered peroxidase APEX2 Nat. Protoc. 11 2016 456 475 26866790 PMC4863649
  36. Hyman A.A. Brangwynne C.P. Beyond stereospecificity: liquids and mesoscale organization of cytoplasm Dev. Cell 21 2011 14 16 21763600
  37. Hyman A.A. Weber C.A. Jülicher F. Liquid-liquid phase separation in biology Annu. Rev. Cell Dev. Biol. 30 2014 39 58 25288112
  38. Ikonomov O.C. Sbrissa D. Shisheva A. YM201636, an inhibitor of retroviral budding and PIKfyve-catalyzed PtdIns(3,5)P2 synthesis, halts glucose entry by insulin in adipocytes Biochem. Biophys. Res. Commun. 382 2009 566 570 19289105 PMC3910513
  39. Jain S. Wheeler J.R. Walters R.W. Agrawal A. Barsic A. Parker R. ATPase-Modulated Stress Granules Contain a Diverse Proteome and Substructure Cell 164 2016 487 498 26777405 PMC4733397
  40. Jung H. Yoon B.C. Holt C.E. Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair Nat. Rev. Neurosci. 13 2012 308 324 22498899 PMC3682205
  41. Khong A. Parker R. mRNP architecture in translating and stress conditions reveals an ordered pathway of mRNP compaction J. Cell Biol. 217 2018 4124 4140 30322972 PMC6279387
  42. Khong A. Matheny T. Jain S. Mitchell S.F. Wheeler J.R. Parker R. The stress granule transcriptome reveals principles of mRNA accumulation in stress granules Mol. Cell 68 2017 808 820.e5, e5 29129640 PMC5728175
  43. Kim H.J. Kim N.C. Wang Y.-D. Scarborough E.A. Moore J. Diaz Z. MacLea K.S. Freibaum B. Li S. Molliex A. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS Nature 495 2013 467 473 23455423 PMC3756911
  44. Kimmel C.B. Ballard W.W. Kimmel S.R. Ullmann B. Schilling T.F. Stages of embryonic development of the zebrafish Dev. Dyn. 203 1995 253 310 8589427
  45. Knowles R.B. Sabry J.H. Martone M.E. Deerinck T.J. Ellisman M.H. Bassell G.J. Kosik K.S. Translocation of RNA granules in living neurons J. Neurosci. 16 1996 7812 7820 8987809 PMC6579227
  46. Krichevsky A.M. Kosik K.S. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation Neuron 32 2001 683 696 11719208
  47. Langdon E.M. Qiu Y. Ghanbari Niaki A. McLaughlin G.A. Weidmann C.A. Gerbich T.M. Smith J.A. Crutchley J.M. Termini C.M. Weeks K.M. mRNA structure determines specificity of a polyQ-driven phase separation Science 360 2018 922 927 29650703 PMC6192030
  48. Leung K.M. van Horck F.P.G. Lin A.C. Allison R. Standart N. Holt C.E. Asymmetrical β-actin mRNA translation in growth cones mediates attractive turning to netrin-1 Nat. Neurosci. 9 2006 1247 1256 16980963 PMC1997306
  49. Mandal A. Pinter K. Drerup C.M. Analyzing Neuronal Mitochondria in vivo Using Fluorescent Reporters in Zebrafish Front. Cell Dev. Biol. 6 2018 144 30410881 PMC6209631
  50. Markmiller S. Soltanieh S. Server K.L. Mak R. Jin W. Fang M.Y. Luo E.-C. Krach F. Yang D. Sen A. Context-Dependent and Disease-Specific Diversity in Protein Interactions within Stress Granules Cell 172 2018 590 604.e13 29373831 PMC5969999
  51. Martin K.C. Ephrussi A. mRNA localization: gene expression in the spatial dimension Cell 136 2009 719 730 19239891 PMC2819924
  52. Michell R.H. Heath V.L. Lemmon M.A. Dove S.K. Phosphatidylinositol 3,5-bisphosphate: metabolism and cellular functions Trends Biochem. Sci. 31 2006 52 63 16364647
  53. Milovanovic D. Wu Y. Bian X. De Camilli P. A liquid phase of synapsin and lipid vesicles Science 361 2018 604 607 29976799 PMC6191856
  54. Mittag T. Parker R. Multiple Modes of Protein-Protein Interactions Promote RNP Granule Assembly J. Mol. Biol. 430 2018 4636 4649 30099026 PMC6204294
  55. Münch C. Rosenbohm A. Sperfeld A.D. Uttner I. Reske S. Krause B.J. Sedlmeier R. Meyer T. Hanemann C.O. Stumm G. Ludolph A.C. Heterozygous R1101K mutation of the DCTN1 gene in a family with ALS and FTD Ann. Neurol. 58 2005 777 780 16240349
  56. Murakami T. Qamar S. Lin J.Q. Schierle G.S.K. Rees E. Miyashita A. Costa A.R. Dodd R.B. Chan F.T.S. Michel C.H. ALS/FTD Mutation-Induced Phase Transition of FUS Liquid Droplets and Reversible Hydrogels into Irreversible Hydrogels Impairs RNP Granule Function Neuron 88 2015 678 690 26526393 PMC4660210
  57. Nadezhdina E.S. Lomakin A.J. Shpilman A.A. Chudinova E.M. Ivanov P.A. Microtubules govern stress granule mobility and dynamics Biochim. Biophys. Acta 1803 2010 361 371 20036288
  58. Nakayama K. Ohashi R. Shinoda Y. Yamazaki M. Abe M. Fujikawa A. Shigenobu S. Futatsugi A. Noda M. Mikoshiba K. RNG105/caprin1, an RNA granule protein for dendritic mRNA localization, is essential for long-term memory formation eLife 6 2017 29677 PMC5697933 29157358
  59. Nicolas A. Kenna K.P. Renton A.E. Ticozzi N. Faghri F. Chia R. Dominov J.A. Kenna B.J. Nalls M.A. Keagle P. ITALSGEN Consortium Genomic Translation for ALS Care (GTAC) Consortium ALS Sequencing Consortium NYGC ALS Consortium Answer ALS Foundation Clinical Research in ALS and Related Disorders for Therapeutic Development (CReATe) Consortium SLAGEN Consortium French ALS Consortium Project MinE ALS Sequencing Consortium Genome-wide Analyses Identify KIF5A as a Novel ALS Gene Neuron 97 2018 1268 1283.e6 29566793 PMC5867896
  60. Obholzer N. Wolfson S. Trapani J.G. Mo W. Nechiporuk A. Busch-Nentwich E. Seiler C. Sidi S. Söllner C. Duncan R.N. Boehland A. Nicolson T. Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells J. Neurosci. 28 2008 2110 2118 18305245 PMC6671858
  61. Pohlmann T. Baumann S. Haag C. Albrecht M. Feldbrügge M. A FYVE zinc finger domain protein specifically links mRNA transport to endosome trafficking eLife 4 2015 1 27 PMC4466420 25985087
  62. Pu J. Schindler C. Jia R. Jarnik M. Backlund P. Bonifacino J.S. BORC, a multisubunit complex that regulates lysosome positioning Dev. Cell 33 2015 176 188 25898167 PMC4788105
  63. Puls I. Jonnakuty C. LaMonte B.H. Holzbaur E.L.F. Tokito M. Mann E. Floeter M.K. Bidus K. Drayna D. Oh S.J. Mutant dynactin in motor neuron disease Nat. Genet. 33 2003 455 456 12627231
  64. Qin D. Xia Y. Whitesides G.M. Soft lithography for micro- and nanoscale patterning Nat. Protoc. 5 2010 491 502 20203666
  65. Ramaswami M. Taylor J.P. Parker R. Altered ribostasis: RNA-protein granules in degenerative disorders Cell 154 2013 727 736 23953108 PMC3811119
  66. Salogiannis J. Egan M.J. Reck-Peterson S.L. Peroxisomes move by hitchhiking on early endosomes using the novel linker protein PxdA J. Cell Biol. 212 2016 289 296 26811422 PMC4748578
  67. Salogiannis J. Reck-Peterson S.L. Hitchhiking: A Non-Canonical Mode of Microtubule-Based Transport Trends Cell Biol. 27 2017 141 150 27665063 PMC5258766
  68. Shi Y. Lin S. Staats K.A. Li Y. Chang W.-H. Hung S.-T. Hendricks E. Linares G.R. Wang Y. Son E.Y. Haploinsufficiency leads to neurodegeneration in C9ORF72 ALS/FTD human induced motor neurons Nat. Med. 24 2018 313 325 29400714 PMC6112156
  69. Shin Y. Berry J. Pannucci N. Haataja M.P. Toettcher J.E. Brangwynne C.P. Spatiotemporal Control of Intracellular Phase Transitions Using Light-Activated optoDroplets Cell 168 2017 159 171.e14 28041848 PMC5562165
  70. Skibinski G. Parkinson N.J. Brown J.M. Chakrabarti L. Lloyd S.L. Hummerich H. Nielsen J.E. Hodges J.R. Spillantini M.G. Thusgaard T. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia Nat. Genet. 37 2005 806 808 16041373
  71. Smith B.N. Topp S.D. Fallini C. Shibata H. Chen H.-J. Troakes C. King A. Ticozzi N. Kenna K.P. Soragia-Gkazi A. Mutations in the vesicular trafficking protein annexin A11 are associated with amyotrophic lateral sclerosis Sci. Transl. Med. 9 2017 eaad9157 28469040 PMC6599403
  72. Sahoo P.K. Lee S.-J. Jaiswal P.B. Alber S. Kar A.N. Miller-Randolph S. Taylor E.E. Smith T. Singh B. Ho T.S. Axonal G3BP1 stress granule protein limits axonal mRNA translation and nerve regeneration Nat. Commun. 9 2018 3358 30135423 PMC6105716
  73. Tyanova S. Temu T. Cox J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics Nat. Protoc. 11 2016 2301 2319 27809316
  74. Tsai P.-C. Liao Y.-C. Jih K.-Y. Soong B.-W. Lin K.-P. Lee Y.-C. Genetic analysis of ANXA11 variants in a Han Chinese cohort with amyotrophic lateral sclerosis in Taiwan Neurobiol. Aging 72 2018 188.e1 188.e2 30054183
  75. Van Treeck B. Parker R. Emerging Roles for Intermolecular RNA-RNA Interactions in RNP Assemblies Cell 174 2018 791 802 30096311 PMC6200146
  76. Vance C. Rogelj B. Hortobágyi T. De Vos K.J. Nishimura A.L. Sreedharan J. Hu X. Smith B. Ruddy D. Wright P. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6 Science 323 2009 1208 1211 19251628 PMC4516382
  77. Van Deerlin V.M. Leverenz J.B. Bekris L.M. Bird T.D. Yuan W. Elman L.B. Clay D. Wood E.M. Chen-Plotkin A.S. Martinez-Lage M. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis Lancet Neurol. 7 2008 409 416 18396105 PMC3546119
  78. Ward M.E. Chen R. Huang H.-Y. Ludwig C. Telpoukhovskaia M. Taubes A. Boudin H. Minami S.S. Reichert M. Albrecht P. Individuals with progranulin haploinsufficiency exhibit features of neuronal ceroid lipofuscinosis Sci. Transl. Med. 9 2017 eaah5642 28404863 PMC5526610
  79. Weber S.C. Brangwynne C.P. Getting RNA and protein in phase Cell 149 2012 1188 1191 22682242
  80. Westerfield M. THE ZEBRAFISH BOOK A guide for the laboratory use of zebrafish Danio. Univ 2000 Oregon Press Eugene
  81. Wheeler J.R. Jain S. Khong A. Parker R. Isolation of yeast and mammalian stress granule cores Methods 126 2017 12 17 28457979 PMC5924690
  82. Wong H.H.W. Lin J.Q. Ströhl F. Roque C.G. Cioni J.M. Cagnetta R. Turner-Bridger B. Laine R.F. Harris W.A. Kaminski C.F. Holt C.E. RNA Docking and Local Translation Regulate Site-Specific Axon Remodeling In Vivo Neuron 95 2017 852 868.e8 28781168 PMC5563073
  83. Yao J. Sasaki Y. Wen Z. Bassell G.J. Zheng J.Q. An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance Nat. Neurosci. 9 2006 1265 1273 16980965
  84. Yoon Y.J. Wu B. Buxbaum A.R. Das S. Tsai A. English B.P. Grimm J.B. Lavis L.D. Singer R.H. Glutamate-induced RNA localization and translation in neurons Proc. Natl. Acad. Sci. USA 113 2016 E6877 E6886 27791158 PMC5098659
  85. Zhang K. Donnelly C.J. Haeusler A.R. Grima J.C. Machamer J.B. Steinwald P. Daley E.L. Miller S.J. Cunningham K.M. Vidensky S. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport Nature 525 2015 56 61 26308891 PMC4800742
  86. Zhang K. Liu Q. Liu K. Shen D. Tai H. Shu S. Ding Q. Fu H. Liu S. Wang Z. ANXA11 mutations prevail in Chinese ALS patients with and without cognitive dementia Neurol. Genet. 4 2018 e237 e239 29845112 PMC5963931
  87. Zhang P. Fan B. Yang P. Temirov J. Messing J. Kim H.J. Taylor J.P. OptoGranules reveal the evolution of stress granules to ALS-FTD pathology bioRxiv 2018 348870 PMC6426440 30893049
  88. Zheng J.-Q. Kelly T.K. Chang B. Ryazantsev S. Rajasekaran A.K. Martin K.C. Twiss J.L. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons J. Neurosci. 21 2001 9291 9303 11717363 PMC6763927

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Authors
Liao, Y.-C., Fernandopulle, M. S., Wang, G., Choi, H., Hao, L., Drerup, C. M., Patel, R., Qamar, S., Nixon-Abell, J., Shen, Y., Meadows, W., Vendruscolo, M., Knowles, T. P. J., Nelson, M., Czekalska, M. A., Musteikyte, G., Gachechiladze, M. A., Stephens, C. A., Pasolli, H. A., Forrest, L. R., St George-Hyslop, P., Lippincott-Schwartz, J., & Ward, M. E.
Affiliations
  • Howard Hughes Medical Institute (US)
  • National Institutes of Health (US)
  • University of Cambridge (GB)
Corresponding author
Ward, Michael E.
ORCID
Venue
Cell
Publisher
Elsevier BV
Published
2019-09
Volume
179
Issue
1
Pages
147-164.e20
ISSN
0092-8674 (ISSN-L)
DOI
10.1016/j.cell.2019.08.050
PMC
PMC6890474
OpenAlex
W2973356406
Cited by
550
References
3
Citations by year
2026: 64 · 2025: 91 · 2024: 86 · 2023: 78 · 2022: 72 · 2021: 74 · 2020: 73 · 2019: 12
FWCI
19.10
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell (publishedVersion, cc-by)
  • SSRN Electronic Journal (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
  • Apollo
Funders
  • National Institutes of Health
  • Canadian Institutes of Health Research
  • Wellcome Trust
  • ALS Society of Canada
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
Keywords
RNA granules, lysosomes, ANXA11, phase separation, biomolecular condensates, low-complexity domains, amyotrophic lateral sclerosis, ALS mutations, polarized cells, phosphoinositide binding
MeSH terms
Amyotrophic Lateral Sclerosis, Animals, Axons, Axonal Transport, Cytoplasmic Granules, Female, Humans, Lysosomes, Male, Mutation, Protein Binding, RNA, Transfection, Zebrafish, Rats, Sprague-Dawley, Annexins, Animals, Genetically Modified, Cell Line, Tumor, Rats, Induced Pluripotent Stem Cells

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