Binding and transport of SFPQ-RNA granules by KIF5A/KLC1 motors promotes axon survival

Fukuda et al. demonstrate that the RNA-binding protein SFPQ is preferentially transported by KIF5A rather than other motors of the kinesin-1 family. Defective axonal transport of SPFQ by KIF5A leads to axon degeneration and therefore provides a mechanistic understanding of specificity for neurologic diseases linked to the KIF5A gene.

[1]  Himanish Basu,et al.  Kymolyzer, a Semi‐Autonomous Kymography Tool to Analyze Intracellular Motility , 2020, Current protocols in cell biology.

[2]  T. Engber,et al.  Axons Matter: The Promise of Treating Neurodegenerative Disorders by Targeting SARM1-Mediated Axonal Degeneration. , 2020, Trends in pharmacological sciences.

[3]  C. S. Lai,et al.  Specific depletion of the motor protein KIF5B leads to deficits in dendritic transport, synaptic plasticity and memory , 2020, eLife.

[4]  S. Nakagawa,et al.  Molecular anatomy of the architectural NEAT1 noncoding RNA: The domains, interactors, and biogenesis pathway required to build phase‐separated nuclear paraspeckles , 2019, Wiley interdisciplinary reviews. RNA.

[5]  G. Schiavo,et al.  Axonal transport and neurological disease , 2019, Nature Reviews Neurology.

[6]  R. Singer,et al.  The travels of mRNAs in neurons: do they know where they are going? , 2019, Current Opinion in Neurobiology.

[7]  C. Holt,et al.  Local translation in neurons: visualization and function , 2019, Nature Structural & Molecular Biology.

[8]  S. Caria,et al.  A new crystal structure and small-angle X-ray scattering analysis of the homodimer of human SFPQ. , 2019, Acta crystallographica. Section F, Structural biology communications.

[9]  Gene W. Yeo,et al.  Disruption of RNA Metabolism in Neurological Diseases and Emerging Therapeutic Interventions , 2019, Neuron.

[10]  C. Holt,et al.  Late Endosomes Act as mRNA Translation Platforms and Sustain Mitochondria in Axons , 2019, Cell.

[11]  J. Onuchic,et al.  Structural consequences of hereditary spastic paraplegia disease-related mutations in kinesin , 2018, Proceedings of the National Academy of Sciences.

[12]  M. Aumont-Nicaise,et al.  Characterization of the binding mode of JNK-interacting protein 1 (JIP1) to kinesin-light chain 1 (KLC1) , 2018, The Journal of Biological Chemistry.

[13]  C. Bond,et al.  Functional Domains of NEAT1 Architectural lncRNA Induce Paraspeckle Assembly through Phase Separation. , 2018, Molecular cell.

[14]  J. Ule,et al.  Intron retention and nuclear loss of SFPQ are molecular hallmarks of ALS , 2018, Nature Communications.

[15]  R. Steiner,et al.  Structural basis for isoform-specific kinesin-1 recognition of Y-acidic cargo adaptors , 2018, bioRxiv.

[16]  N. Perrone-Bizzozero,et al.  Axonal mRNA transport and translation at a glance , 2018, Journal of Cell Science.

[17]  Timothy A. Miller,et al.  Genome-wide Analyses Identify KIF5A as a Novel ALS Gene in and for Therapeutic , 2018 .

[18]  H. Braak,et al.  Hot-spot KIF5A mutations cause familial ALS , 2018, Brain : a journal of neurology.

[19]  C. Hoogenraad,et al.  Differentiation between Oppositely Oriented Microtubules Controls Polarized Neuronal Transport , 2017, Neuron.

[20]  R. Segal,et al.  Paclitaxel Reduces Axonal Bclw to Initiate IP3R1-Dependent Axon Degeneration , 2017, Neuron.

[21]  P. Manque,et al.  Axonal Degeneration during Aging and Its Functional Role in Neurodegenerative Disorders , 2017, Front. Neurosci..

[22]  William M Alexander,et al.  multiplierz v2.0: A Python‐based ecosystem for shared access and analysis of native mass spectrometry data , 2017, Proteomics.

[23]  Madhusoodanan Mottamal,et al.  Characterization of kinesin switch I mutations that cause hereditary spastic paraplegia , 2017, PloS one.

[24]  W. Talbot,et al.  Erratum: Non-nuclear Pool of Splicing Factor SFPQ Regulates Axonal Transcripts Required for Normal Motor Development (Neuron (2017) 94(2) (322–336.e5)(S0896627317302386)(10.1016/j.neuron.2017.03.026)) , 2017 .

[25]  W. Talbot,et al.  Non-nuclear Pool of Splicing Factor SFPQ Regulates Axonal Transcripts Required for Normal Motor Development , 2017, Neuron.

[26]  Byung-Ok Choi,et al.  Wide phenotypic spectrum in axonal Charcot–Marie–Tooth neuropathy type 2 patients with KIF5A mutations , 2017, Genes & Genomics.

[27]  N. Hirokawa,et al.  The Molecular Motor KIF1A Transports the TrkA Neurotrophin Receptor and Is Essential for Sensory Neuron Survival and Function , 2016, Neuron.

[28]  Hunter L. Elliott,et al.  The RNA-binding protein SFPQ orchestrates an RNA regulon to promote axon viability , 2016, Nature Neuroscience.

[29]  C. Hoogenraad,et al.  Microtubule‐binding protein doublecortin‐like kinase 1 (DCLK1) guides kinesin‐3‐mediated cargo transport to dendrites , 2016, The EMBO journal.

[30]  Xu Zhang,et al.  FMRP-Mediated Axonal Delivery of miR-181d Regulates Axon Elongation by Locally Targeting Map1b and Calm1. , 2015, Cell reports.

[31]  L. Walensky,et al.  Inhibition of Pro-apoptotic BAX by a noncanonical interaction mechanism. , 2015, Molecular cell.

[32]  G. Morgan,et al.  Vaccinia Virus Protein Complex F12/E2 Interacts with Kinesin Light Chain Isoform 2 to Engage the Kinesin-1 Motor Complex , 2015, PLoS pathogens.

[33]  R. Segal,et al.  Campenot Cultures and Microfluidics Provide Complementary Platforms for Spatial Study of Dorsal Root Ganglia Neurons , 2015 .

[34]  Philip D. Campbell,et al.  Unique Function of Kinesin Kif5A in Localization of Mitochondria in Axons , 2014, The Journal of Neuroscience.

[35]  D. Hughes,et al.  Extended phenotypic spectrum of KIF5A mutations , 2014, Neurology.

[36]  J. Koepke,et al.  Endosomal transport of septin mRNA and protein indicates local translation on endosomes and is required for correct septin filamentation , 2014, EMBO reports.

[37]  C. Moores,et al.  Delineation of the TRAK binding regions of the kinesin-1 motor proteins , 2013, FEBS letters.

[38]  R. Segal,et al.  Target-Derived Neurotrophins Coordinate Transcription and Transport of Bclw to Prevent Axonal Degeneration , 2013, The Journal of Neuroscience.

[39]  N. Hirokawa,et al.  Molecular Motor KIF5A Is Essential for GABAA Receptor Transport, and KIF5A Deletion Causes Epilepsy , 2012, Neuron.

[40]  Tobias M. Rasse,et al.  Spastic Paraplegia Mutation N256S in the Neuronal Microtubule Motor KIF5A Disrupts Axonal Transport in a Drosophila HSP Model , 2012, PLoS genetics.

[41]  G. Banker,et al.  The Translocation Selectivity of the Kinesins that Mediate Neuronal Organelle Transport , 2012, Traffic.

[42]  F. Mackenzie,et al.  Crystal Structures of the Tetratricopeptide Repeat Domains of Kinesin Light Chains: Insight into Cargo Recognition Mechanisms , 2012, PloS one.

[43]  Byung C. Yoon,et al.  Local Translation of Extranuclear Lamin B Promotes Axon Maintenance , 2012, Cell.

[44]  R. Segal,et al.  Sensory Neuropathy Attributable to Loss of Bcl-w , 2011, The Journal of Neuroscience.

[45]  Michal Linial,et al.  The complete peptide dictionary – A meta‐proteomics resource , 2010, Proteomics.

[46]  Joshua Barry,et al.  Kinesin I Transports Tetramerized Kv3 Channels through the Axon Initial Segment via Direct Binding , 2010, The Journal of Neuroscience.

[47]  Yosuke Tanaka,et al.  Molecular Motors in Neurons: Transport Mechanisms and Roles in Brain Function, Development, and Disease , 2010, Neuron.

[48]  Yi Zhang,et al.  multiplierz: an extensible API based desktop environment for proteomics data analysis , 2009, BMC Bioinformatics.

[49]  J. Milbrandt,et al.  Nicotinamide Mononucleotide Adenylyl Transferase-Mediated Axonal Protection Requires Enzymatic Activity But Not Increased Levels of Neuronal Nicotinamide Adenine Dinucleotide , 2009, The Journal of Neuroscience.

[50]  Jignesh R. Parikh,et al.  mzAPI: a new strategy for efficiently sharing mass spectrometry data , 2009, Nature Methods.

[51]  S. Ficarro,et al.  Improved electrospray ionization efficiency compensates for diminished chromatographic resolution and enables proteomics analysis of tyrosine signaling in embryonic stem cells. , 2009, Analytical chemistry.

[52]  Rebecca Schüle,et al.  Effect of spastic paraplegia mutations in KIF5A kinesin on transport activity. , 2008, Human molecular genetics.

[53]  É. Khandjian,et al.  The fragile X mental retardation protein is a molecular adaptor between the neurospecific KIF3C kinesin and dendritic RNA granules. , 2007, Human molecular genetics.

[54]  B. Schnapp,et al.  A Change in the Selective Translocation of the Kinesin-1 Motor Domain Marks the Initial Specification of the Axon , 2006, Neuron.

[55]  M. Gorenstein,et al.  Absolute Quantification of Proteins by LCMSE , 2006, Molecular & Cellular Proteomics.

[56]  Nobutaka Hirokawa,et al.  Kinesin Transports RNA Isolation and Characterization of an RNA-Transporting Granule , 2004, Neuron.

[57]  N. Hirokawa,et al.  Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head , 2003, The Journal of cell biology.

[58]  N. Hirokawa,et al.  Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites , 2002, Nature.

[59]  N. Hirokawa,et al.  All kinesin superfamily protein, KIF, genes in mouse and human , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[60]  J. Blenis,et al.  Cargo of Kinesin Identified as Jip Scaffolding Proteins and Associated Signaling Molecules , 2001, The Journal of cell biology.

[61]  E. Huang,et al.  Neurotrophins: roles in neuronal development and function. , 2001, Annual review of neuroscience.

[62]  N. Hirokawa,et al.  KIF5C, a Novel Neuronal Kinesin Enriched in Motor Neurons , 2000, The Journal of Neuroscience.

[63]  J. Mackay,et al.  The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. , 1998, Biochemistry.

[64]  L. Goldstein,et al.  Chromosomal localization reveals three kinesin heavy chain genes in mouse. , 1998, Genomics.

[65]  T. Deerinck,et al.  Translocation of RNA Granules in Living Neurons , 1996, The Journal of Neuroscience.

[66]  R. Winter.  Fragile X mental retardation. , 1989, Archives of disease in childhood.

[67]  Michael P. Sheetz,et al.  Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility , 1985, Cell.

[68]  Scott T. Brady,et al.  A novel brain ATPase with properties expected for the fast axonal transport motor , 1985, Nature.