FRINK Linked Data Fragments server

Matches in SemOpenAlex for { <https://semopenalex.org/work/W3000068919> ?p ?o ?g. }

• W3000068919 endingPage "283.e6" @default.
• W3000068919 startingPage "269" @default.
• W3000068919 abstract "•TACC3 regulates microtubule plus-end growth and HSV-1 infection in interphase cells•Loss of TACC3 functionality results in aberrant detyrosinated microtubule arrays•Effects of TACC3 on stable microtubule arrays affect cell shape and cargo sorting•Cargo sorting defects caused by TACC3 loss are rescued by impairing kinesin-1 activity End-binding proteins (EBs) are widely viewed as master regulators of microtubule dynamics and function. Here, we show that while EB1 mediates the dynamic microtubule capture of herpes simplex virus type 1 (HSV-1) in fibroblasts, in neuronal cells, infection occurs independently of EBs through stable microtubules. Prompted by this, we find that transforming acid coiled-coil protein 3 (TACC3), widely studied in mitotic spindle formation, regulates the cytoplasmic localization of the microtubule polymerizing factor chTOG and influences microtubule plus-end dynamics during interphase to control infection in distinct cell types. Furthermore, perturbing TACC3 function in neuronal cells resulted in the formation of disorganized stable, detyrosinated microtubule networks and changes in cellular morphology, as well as impaired trafficking of both HSV-1 and transferrin. These trafficking defects in TACC3-depleted cells were reversed by the depletion of kinesin-1 heavy chains. As such, TACC3 is a critical regulator of interphase microtubule dynamics and stability that influences kinesin-1-based cargo trafficking. End-binding proteins (EBs) are widely viewed as master regulators of microtubule dynamics and function. Here, we show that while EB1 mediates the dynamic microtubule capture of herpes simplex virus type 1 (HSV-1) in fibroblasts, in neuronal cells, infection occurs independently of EBs through stable microtubules. Prompted by this, we find that transforming acid coiled-coil protein 3 (TACC3), widely studied in mitotic spindle formation, regulates the cytoplasmic localization of the microtubule polymerizing factor chTOG and influences microtubule plus-end dynamics during interphase to control infection in distinct cell types. Furthermore, perturbing TACC3 function in neuronal cells resulted in the formation of disorganized stable, detyrosinated microtubule networks and changes in cellular morphology, as well as impaired trafficking of both HSV-1 and transferrin. These trafficking defects in TACC3-depleted cells were reversed by the depletion of kinesin-1 heavy chains. As such, TACC3 is a critical regulator of interphase microtubule dynamics and stability that influences kinesin-1-based cargo trafficking. The microtubule (MT) network regulates processes ranging from cell division and motility to cargo transport (Akhmanova and Steinmetz, 2008Akhmanova A. Steinmetz M.O. Tracking the ends: a dynamic protein network controls the fate of microtubule tips.Nat. Rev. Mol. Cell Biol. 2008; 9: 309-322Crossref PubMed Scopus (750) Google Scholar, Akhmanova and Steinmetz, 2015Akhmanova A. Steinmetz M.O. Control of microtubule organization and dynamics: two ends in the limelight.Nat. Rev. Mol. Cell Biol. 2015; 16: 711-726Crossref PubMed Scopus (490) Google Scholar, Stephens, 2012Stephens D.J. Functional coupling of microtubules to membranes - implications for membrane structure and dynamics.J. Cell Sci. 2012; 125: 2795-2804Crossref PubMed Scopus (22) Google Scholar). Filaments nucleate from an MT organizing center (MTOC) and explore the cytosol through phases of polymerization, pause, and catastrophe as tubulin heterodimer subunits are either added or removed from their more dynamic plus-end (Jánosi et al., 2002Jánosi I.M. Chrétien D. Flyvbjerg H. Structural microtubule cap: stability, catastrophe, rescue, and third state.Biophys. J. 2002; 83: 1317-1330Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar, Kristofferson et al., 1986Kristofferson D. Mitchison T. Kirschner M. Direct observation of steady-state microtubule dynamics.J. Cell Biol. 1986; 102: 1007-1019Crossref PubMed Scopus (82) Google Scholar). The MT plus-end transiently contains guanosine triphosphate (GTP)-bound tubulin before it is hydrolyzed to guanosine diphosphate (GDP)-tubulin within the filament lattice (Guesdon et al., 2016Guesdon A. Bazile F. Buey R.M. Mohan R. Monier S. García R.R. Angevin M. Heichette C. Wieneke R. Tampé R. et al.EB1 interacts with outwardly curved and straight regions of the microtubule lattice.Nat. Cell Biol. 2016; 18: 1102-1108Crossref PubMed Scopus (57) Google Scholar, Howard and Hyman, 2003Howard J. Hyman A.A. Dynamics and mechanics of the microtubule plus end.Nature. 2003; 422: 753-758Crossref PubMed Scopus (584) Google Scholar, Jánosi et al., 2002Jánosi I.M. Chrétien D. Flyvbjerg H. Structural microtubule cap: stability, catastrophe, rescue, and third state.Biophys. J. 2002; 83: 1317-1330Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar). This GTP-tubulin cap enables the growing MT plus-end to be recognized by members of the end-binding (EB) family of proteins, EB1–EB3 (Guesdon et al., 2016Guesdon A. Bazile F. Buey R.M. Mohan R. Monier S. García R.R. Angevin M. Heichette C. Wieneke R. Tampé R. et al.EB1 interacts with outwardly curved and straight regions of the microtubule lattice.Nat. Cell Biol. 2016; 18: 1102-1108Crossref PubMed Scopus (57) Google Scholar, Komarova et al., 2009Komarova Y. De Groot C.O. Grigoriev I. Gouveia S.M. Munteanu E.L. Schober J.M. Honnappa S. Buey R.M. Hoogenraad C.C. Dogterom M. et al.Mammalian end binding proteins control persistent microtubule growth.J. Cell Biol. 2009; 184: 691-706Crossref PubMed Scopus (271) Google Scholar, Maurer et al., 2012Maurer S.P. Fourniol F.J. Bohner G. Moores C.A. Surrey T. EBs recognize a nucleotide-dependent structural cap at growing microtubule ends.Cell. 2012; 149: 371-382Abstract Full Text Full Text PDF PubMed Scopus (255) Google Scholar). At the plus-end, EBs can directly suppress catastrophe events, leading to enhanced MT growth (Komarova et al., 2009Komarova Y. De Groot C.O. Grigoriev I. Gouveia S.M. Munteanu E.L. Schober J.M. Honnappa S. Buey R.M. Hoogenraad C.C. Dogterom M. et al.Mammalian end binding proteins control persistent microtubule growth.J. Cell Biol. 2009; 184: 691-706Crossref PubMed Scopus (271) Google Scholar). EBs also bind and recruit other plus-end tracking proteins (+TIPs) to form functional nodes that control filament growth, stability, spatial organization, and interactions with targets such as cortical actin or cellular cargoes (Akhmanova and Steinmetz, 2015Akhmanova A. Steinmetz M.O. Control of microtubule organization and dynamics: two ends in the limelight.Nat. Rev. Mol. Cell Biol. 2015; 16: 711-726Crossref PubMed Scopus (490) Google Scholar, Honnappa et al., 2009Honnappa S. Gouveia S.M. Weisbrich A. Damberger F.F. Bhavesh N.S. Jawhari H. Grigoriev I. van Rijssel F.J. Buey R.M. Lawera A. et al.An EB1-binding motif acts as a microtubule tip localization signal.Cell. 2009; 138: 366-376Abstract Full Text Full Text PDF PubMed Scopus (475) Google Scholar, Komarova et al., 2005Komarova Y. Lansbergen G. Galjart N. Grosveld F. Borisy G.G. Akhmanova A. EB1 and EB3 control CLIP dissociation from the ends of growing microtubules.Mol. Biol. Cell. 2005; 16: 5334-5345Crossref PubMed Scopus (160) Google Scholar, Lansbergen et al., 2006Lansbergen G. Grigoriev I. Mimori-Kiyosue Y. Ohtsuka T. Higa S. Kitajima I. Demmers J. Galjart N. Houtsmuller A.B. Grosveld F. Akhmanova A. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta.Dev. Cell. 2006; 11: 21-32Abstract Full Text Full Text PDF PubMed Scopus (223) Google Scholar, Zhang et al., 2015Zhang R. Alushin G.M. Brown A. Nogales E. Mechanistic Origin of Microtubule Dynamic Instability and Its Modulation by EB Proteins.Cell. 2015; 162: 849-859Abstract Full Text Full Text PDF PubMed Scopus (244) Google Scholar). While several +TIPs have been identified in recent years, many of which can bind MT filaments independently, most require EB proteins to mediate their specific accumulation at MT plus-ends. For this reason, EBs are widely considered to be master regulators of MT function (Akhmanova and Steinmetz, 2015Akhmanova A. Steinmetz M.O. Control of microtubule organization and dynamics: two ends in the limelight.Nat. Rev. Mol. Cell Biol. 2015; 16: 711-726Crossref PubMed Scopus (490) Google Scholar). Other proteins do operate at the MT plus-end independently of EB proteins, yet their functions are less well defined. chTOG (colonic and hepatic tumor-overexpressed gene) is a microtubule polymerase that binds soluble tubulin dimers and catalyzes their addition to MT plus-ends (Brouhard et al., 2008Brouhard G.J. Stear J.H. Noetzel T.L. Al-Bassam J. Kinoshita K. Harrison S.C. Howard J. Hyman A.A. XMAP215 is a processive microtubule polymerase.Cell. 2008; 132: 79-88Abstract Full Text Full Text PDF PubMed Scopus (366) Google Scholar, Gard and Kirschner, 1987Gard D.L. Kirschner M.W. A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end.J. Cell Biol. 1987; 105: 2203-2215Crossref PubMed Scopus (270) Google Scholar, Slep and Vale, 2007Slep K.C. Vale R.D. Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1.Mol. Cell. 2007; 27: 976-991Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar). chTOG binds MT plus-ends autonomously, but its optimal plus-end localization depends upon recruitment by transforming acidic coiled-coil-containing (TACC) proteins (Hussmann et al., 2016Hussmann F. Drummond D.R. Peet D.R. Martin D.S. Cross R.A. Alp7/TACC-Alp14/TOG generates long-lived, fast-growing MTs by an unconventional mechanism.Sci. Rep. 2016; 6: 20653Crossref PubMed Scopus (21) Google Scholar, Mortuza et al., 2014Mortuza G.B. Cavazza T. Garcia-Mayoral M.F. Hermida D. Peset I. Pedrero J.G. Merino N. Blanco F.J. Lyngsø J. Bruix M. et al.XTACC3-XMAP215 association reveals an asymmetric interaction promoting microtubule elongation.Nat. Commun. 2014; 5: 5072Crossref PubMed Scopus (15) Google Scholar). Homologs of both chTOG and TACCs are widely conserved across eukaryotes (Gard et al., 2004Gard D.L. Becker B.E. Josh Romney S. MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins.Int. Rev. Cytol. 2004; 239: 179-272Crossref PubMed Scopus (69) Google Scholar, Still et al., 2004Still I.H. Vettaikkorumakankauv A.K. DiMatteo A. Liang P. Structure-function evolution of the transforming acidic coiled coil genes revealed by analysis of phylogenetically diverse organisms.BMC Evol. Biol. 2004; 4: 16Crossref PubMed Google Scholar). Humans express three TACC proteins (TACC1–TACC3) and along with chTOG, TACCs have been extensively studied in the context of mitotic spindle organization during cell division and in cancer (Ding et al., 2017Ding Z.M. Huang C.J. Jiao X.F. Wu D. Huo L.J. The role of TACC3 in mitotic spindle organization.Cytoskeleton (Hoboken). 2017; 74: 369-378Crossref PubMed Scopus (9) Google Scholar, Gard et al., 2004Gard D.L. Becker B.E. Josh Romney S. MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins.Int. Rev. Cytol. 2004; 239: 179-272Crossref PubMed Scopus (69) Google Scholar, Mortuza et al., 2014Mortuza G.B. Cavazza T. Garcia-Mayoral M.F. Hermida D. Peset I. Pedrero J.G. Merino N. Blanco F.J. Lyngsø J. Bruix M. et al.XTACC3-XMAP215 association reveals an asymmetric interaction promoting microtubule elongation.Nat. Commun. 2014; 5: 5072Crossref PubMed Scopus (15) Google Scholar, Peset and Vernos, 2008Peset I. Vernos I. The TACC proteins: TACC-ling microtubule dynamics and centrosome function.Trends Cell Biol. 2008; 18: 379-388Abstract Full Text Full Text PDF PubMed Scopus (119) Google Scholar, Raff, 2002Raff J.W. Centrosomes and cancer: lessons from a TACC.Trends Cell Biol. 2002; 12: 222-225Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar, Still et al., 1999Still I.H. Vince P. Cowell J.K. The third member of the transforming acidic coiled coil-containing gene family, TACC3, maps in 4p16, close to translocation breakpoints in multiple myeloma, and is upregulated in various cancer cell lines.Genomics. 1999; 58: 165-170Crossref PubMed Scopus (113) Google Scholar, Still et al., 2004Still I.H. Vettaikkorumakankauv A.K. DiMatteo A. Liang P. Structure-function evolution of the transforming acidic coiled coil genes revealed by analysis of phylogenetically diverse organisms.BMC Evol. Biol. 2004; 4: 16Crossref PubMed Google Scholar, Thakur et al., 2014Thakur H.C. Singh M. Nagel-Steger L. Kremer J. Prumbaum D. Fansa E.K. Ezzahoini H. Nouri K. Gremer L. Abts A. et al.The centrosomal adaptor TACC3 and the microtubule polymerase chTOG interact via defined C-terminal subdomains in an Aurora-A kinase-independent manner.J. Biol. Chem. 2014; 289: 74-88Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar), although TACC3 is the most widely studied and best-characterized family member. By recruiting chTOG, TACC3 functions at the centrosome to regulate MT nucleation, along the MT lattice to stabilize the spindle apparatus, and at the MT plus-end to promote mitotic spindle elongation (Gergely et al., 2000Gergely F. Karlsson C. Still I. Cowell J. Kilmartin J. Raff J.W. The TACC domain identifies a family of centrosomal proteins that can interact with microtubules.Proc. Natl. Acad. Sci. USA. 2000; 97: 14352-14357Crossref PubMed Scopus (205) Google Scholar, Gergely et al., 2003Gergely F. Draviam V.M. Raff J.W. The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells.Genes Dev. 2003; 17: 336-341Crossref PubMed Scopus (218) Google Scholar, Kinoshita et al., 2005Kinoshita K. Noetzel T.L. Pelletier L. Mechtler K. Drechsel D.N. Schwager A. Lee M. Raff J.W. Hyman A.A. Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis.J. Cell Biol. 2005; 170: 1047-1055Crossref PubMed Scopus (206) Google Scholar, Lee et al., 2001Lee M.J. Gergely F. Jeffers K. Peak-Chew S.Y. Raff J.W. Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour.Nat. Cell Biol. 2001; 3: 643-649Crossref PubMed Scopus (219) Google Scholar, Lin et al., 2010Lin C.-H. Hu C.-K. Shih H.-M. Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability.J. Cell Biol. 2010; 189: 1097-1105Crossref PubMed Scopus (64) Google Scholar, Mortuza et al., 2014Mortuza G.B. Cavazza T. Garcia-Mayoral M.F. Hermida D. Peset I. Pedrero J.G. Merino N. Blanco F.J. Lyngsø J. Bruix M. et al.XTACC3-XMAP215 association reveals an asymmetric interaction promoting microtubule elongation.Nat. Commun. 2014; 5: 5072Crossref PubMed Scopus (15) Google Scholar). However, our understanding of the potential functions of TACC3 in interphase remains limited (Chanez et al., 2015Chanez B. Gonçalves A. Badache A. Verdier-Pinard P. Eribulin targets a ch-TOG-dependent directed migration of cancer cells.Oncotarget. 2015; 6: 41667-41678Crossref PubMed Scopus (18) Google Scholar, Gunzelmann et al., 2018Gunzelmann J. Rüthnick D. Lin T.-C. Zhang W. Neuner A. Jäkle U. Schiebel E. The microtubule polymerase Stu2 promotes oligomerization of the γ-TuSC for cytoplasmic microtubule nucleation.eLife. 2018; 7: e39932Crossref PubMed Scopus (23) Google Scholar, Kume et al., 2018Kume K. Kaneko S. Nishikawa K. Mizunuma M. Hirata D. Role of nucleocytoplasmic transport in interphase microtubule organization in fission yeast.Biochem. Biophys. Res. Commun. 2018; 503: 1160-1167Crossref PubMed Scopus (2) Google Scholar, Nakamura et al., 2012Nakamura S. Grigoriev I. Nogi T. Hamaji T. Cassimeris L. Mimori-Kiyosue Y. Dissecting the nanoscale distributions and functions of microtubule-end-binding proteins EB1 and ch-TOG in interphase HeLa cells.PLoS One. 2012; 7: e51442Crossref PubMed Scopus (44) Google Scholar, Nakaseko et al., 2001Nakaseko Y. Goshima G. Morishita J. Yanagida M. M phase-specific kinetochore proteins in fission yeast: microtubule-associating Dis1 and Mtc1 display rapid separation and segregation during anaphase.Curr. Biol. 2001; 11: 537-549Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar, Trogden and Rogers, 2015Trogden K.P. Rogers S.L. TOG Proteins Are Spatially Regulated by Rac-GSK3β to Control Interphase Microtubule Dynamics.PLoS One. 2015; 10: e0138966Crossref PubMed Scopus (6) Google Scholar). In yeast, the homolog of TACC3, Alp7, recruits Alp14/TOG to the nucleus during cell division or to the cytoplasm during interphase. The absence of Alp7 results in short spindles during mitosis or defects in MT growth and organization in interphase (Hussmann et al., 2016Hussmann F. Drummond D.R. Peet D.R. Martin D.S. Cross R.A. Alp7/TACC-Alp14/TOG generates long-lived, fast-growing MTs by an unconventional mechanism.Sci. Rep. 2016; 6: 20653Crossref PubMed Scopus (21) Google Scholar, Ling et al., 2009Ling Y.C. Vjestica A. Oliferenko S. Nucleocytoplasmic shuttling of the TACC protein Mia1p/Alp7p is required for remodeling of microtubule arrays during the cell cycle.PLoS One. 2009; 4: e6255Crossref PubMed Scopus (16) Google Scholar, Sato et al., 2004Sato M. Vardy L. Angel Garcia M. Koonrugsa N. Toda T. Interdependency of fission yeast Alp14/TOG and coiled coil protein Alp7 in microtubule localization and bipolar spindle formation.Mol. Biol. Cell. 2004; 15: 1609-1622Crossref PubMed Scopus (68) Google Scholar, Sato et al., 2009Sato M. Okada N. Kakui Y. Yamamoto M. Yoshida M. Toda T. Nucleocytoplasmic transport of Alp7/TACC organizes spatiotemporal microtubule formation in fission yeast.EMBO Rep. 2009; 10: 1161-1167Crossref PubMed Scopus (24) Google Scholar, Sato and Toda, 2007Sato M. Toda T. Alp7/TACC is a crucial target in Ran-GTPase-dependent spindle formation in fission yeast.Nature. 2007; 447: 334-337Crossref PubMed Scopus (56) Google Scholar, Zheng et al., 2006Zheng L. Schwartz C. Wee L. Oliferenko S. The fission yeast transforming acidic coiled coil-related protein Mia1p/Alp7p is required for formation and maintenance of persistent microtubule-organizing centers at the nuclear envelope.Mol. Biol. Cell. 2006; 17: 2212-2222Crossref PubMed Scopus (22) Google Scholar). Moreover, yeast Alp7 mediates the recruitment of Alp14/TOG to MT plus-ends in vitro (Hussmann et al., 2016Hussmann F. Drummond D.R. Peet D.R. Martin D.S. Cross R.A. Alp7/TACC-Alp14/TOG generates long-lived, fast-growing MTs by an unconventional mechanism.Sci. Rep. 2016; 6: 20653Crossref PubMed Scopus (21) Google Scholar). Evidence for similar interphase functions of TACC3 is also emerging in higher organisms. TACC3 has been shown to recognize interphase MT plus-ends in Drosophila and Xenopus embryonic cells, as well as in human HeLa and RpeI cells (Gutiérrez-Caballero et al., 2015Gutiérrez-Caballero C. Burgess S.G. Bayliss R. Royle S.J. TACC3-ch-TOG track the growing tips of microtubules independently of clathrin and Aurora-A phosphorylation.Biol. Open. 2015; 4: 170-179Crossref PubMed Scopus (29) Google Scholar, Lee et al., 2001Lee M.J. Gergely F. Jeffers K. Peak-Chew S.Y. Raff J.W. Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour.Nat. Cell Biol. 2001; 3: 643-649Crossref PubMed Scopus (219) Google Scholar, Nwagbara et al., 2014Nwagbara B.U. Faris A.E. Bearce E.A. Erdogan B. Ebbert P.T. Evans M.F. Rutherford E.L. Enzenbacher T.B. Lowery L.A. TACC3 is a microtubule plus end-tracking protein that promotes axon elongation and also regulates microtubule plus end dynamics in multiple embryonic cell types.Mol. Biol. Cell. 2014; 25: 3350-3362Crossref PubMed Google Scholar). However, while TACC3 homologs promote interphase MT dynamics in both Drosophila and Xenopus systems, modulating TACC3 levels has been reported to have no effect in HeLa cells (Erdogan et al., 2017Erdogan B. Cammarata G.M. Lee E.J. Pratt B.C. Francl A.F. Rutherford E.L. Lowery L.A. The microtubule plus-end-tracking protein TACC3 promotes persistent axon outgrowth and mediates responses to axon guidance signals during development.Neural Dev. 2017; 12: 3Crossref PubMed Scopus (13) Google Scholar, Gutiérrez-Caballero et al., 2015Gutiérrez-Caballero C. Burgess S.G. Bayliss R. Royle S.J. TACC3-ch-TOG track the growing tips of microtubules independently of clathrin and Aurora-A phosphorylation.Biol. Open. 2015; 4: 170-179Crossref PubMed Scopus (29) Google Scholar, Long et al., 2013Long J.B. Bagonis M. Lowery L.A. Lee H. Danuser G. Van Vactor D. Multiparametric analysis of CLASP-interacting protein functions during interphase microtubule dynamics.Mol. Cell. Biol. 2013; 33: 1528-1545Crossref PubMed Scopus (19) Google Scholar, Nwagbara et al., 2014Nwagbara B.U. Faris A.E. Bearce E.A. Erdogan B. Ebbert P.T. Evans M.F. Rutherford E.L. Enzenbacher T.B. Lowery L.A. TACC3 is a microtubule plus end-tracking protein that promotes axon elongation and also regulates microtubule plus end dynamics in multiple embryonic cell types.Mol. Biol. Cell. 2014; 25: 3350-3362Crossref PubMed Google Scholar). Thus, the potential role of TACC3 in regulating MT dynamics and its broader functionality during interphase remains poorly understood, particularly in human cells. As intracellular pathogens, viruses are dependent upon MTs to facilitate their replication (Naghavi and Walsh, 2017Naghavi M.H. Walsh D. Microtubule Regulation and Function during Virus Infection.J. Virol. 2017; 91: e00538-17Crossref PubMed Scopus (65) Google Scholar). However, the importance of +TIPs during infection has only recently begun to emerge (Delaney et al., 2017Delaney M.K. Malikov V. Chai Q. Zhao G. Naghavi M.H. Distinct functions of diaphanous-related formins regulate HIV-1 uncoating and transport.Proc. Natl. Acad. Sci. USA. 2017; 114: E6932-E6941Crossref PubMed Scopus (31) Google Scholar, Jovasevic et al., 2015Jovasevic V. Naghavi M.H. Walsh D. Microtubule plus end-associated CLIP-170 initiates HSV-1 retrograde transport in primary human cells.J. Cell Biol. 2015; 211: 323-337Crossref PubMed Scopus (34) Google Scholar, Naghavi et al., 2013Naghavi M.H. Gundersen G.G. Walsh D. Plus-end tracking proteins, CLASPs, and a viral Akt mimic regulate herpesvirus-induced stable microtubule formation and virus spread.Proc. Natl. Acad. Sci. USA. 2013; 110: 18268-18273Crossref PubMed Scopus (36) Google Scholar, Procter et al., 2018Procter D.J. Banerjee A. Nukui M. Kruse K. Gaponenko V. Murphy E.A. Komarova Y. Walsh D. The HCMV Assembly Compartment Is a Dynamic Golgi-Derived MTOC that Controls Nuclear Rotation and Virus Spread.Dev. Cell. 2018; 45: 83-100.e7Abstract Full Text Full Text PDF PubMed Scopus (39) Google Scholar, Sabo et al., 2013Sabo Y. Walsh D. Barry D.S. Tinaztepe S. de Los Santos K. Goff S.P. Gundersen G.G. Naghavi M.H. HIV-1 induces the formation of stable microtubules to enhance early infection.Cell Host Microbe. 2013; 14: 535-546Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar). Of particular relevance to this study, we previously showed that EB1 and the +TIP, cytoplasmic linker-associated protein 170 (CLIP170), are required for herpes simplex virus type 1 (HSV-1) particles to load onto dynamic MTs for subsequent motor-mediated transport to the nucleus in dermal fibroblasts (Jovasevic et al., 2015Jovasevic V. Naghavi M.H. Walsh D. Microtubule plus end-associated CLIP-170 initiates HSV-1 retrograde transport in primary human cells.J. Cell Biol. 2015; 211: 323-337Crossref PubMed Scopus (34) Google Scholar). However, in vivo HSV-1 infects a variety of cell types, which include epithelial, dermal, and neuronal cells (Roizman et al., 2013Roizman B. Knipe D.M. Whitley R. Herpes simplex viruses.in: Knipe D.M. Howley P.M. Fields Virology. Wolters Kluwer/Lippincott Williams & Wilkins Health, 2013: 1823-1897Google Scholar). Many cell types contain mixtures of both dynamic and stable MT arrays, but neuronal cells contain a particularly high proportion of stabilized filaments (Baas and Black, 1990Baas P.W. Black M.M. Individual microtubules in the axon consist of domains that differ in both composition and stability.J. Cell Biol. 1990; 111: 495-509Crossref PubMed Scopus (280) Google Scholar, Brady, 1993Brady S. Axonal Dynamics and Regeneration.in: Gorio A. Neuroregeneration. Raven Press, 1993: 7-36Google Scholar, Sahenk and Brady, 1987Sahenk Z. Brady S.T. Axonal tubulin and microtubules: morphologic evidence for stable regions on axonal microtubules.Cell Motil. Cytoskeleton. 1987; 8: 155-164Crossref PubMed Scopus (45) Google Scholar, Song et al., 2013Song Y. Kirkpatrick L.L. Schilling A.B. Helseth D.L. Chabot N. Keillor J.W. Johnson G.V. Brady S.T. Transglutaminase and polyamination of tubulin: posttranslational modification for stabilizing axonal microtubules.Neuron. 2013; 78: 109-123Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). While dynamic MTs have a relatively short half-life, stable MTs are long-lived and therefore accumulate higher levels of several tubulin post-translational modifications (PTMs) (Janke and Bulinski, 2011Janke C. Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions.Nat. Rev. Mol. Cell Biol. 2011; 12: 773-786Crossref PubMed Scopus (593) Google Scholar). Tubulin PTMs include acetylation at lysine 40, which resides within the lumen of the filament and confers mechanical strength against breakage (Portran et al., 2017Portran D. Schaedel L. Xu Z. Théry M. Nachury M.V. Tubulin acetylation protects long-lived microtubules against mechanical ageing.Nat. Cell Biol. 2017; 19: 391-398Crossref PubMed Scopus (226) Google Scholar, Xu et al., 2017Xu Z. Schaedel L. Portran D. Aguilar A. Gaillard J. Marinkovich M.P. Théry M. Nachury M.V. Microtubules acquire resistance from mechanical breakage through intralumenal acetylation.Science. 2017; 356: 328-332Crossref PubMed Scopus (209) Google Scholar). While acetylation can occur quite rapidly, another PTM, tubulin detyrosination, appears to occur more gradually and accumulates largely on stable MTs. Tubulin detyrosination occurs on the cytosolic side of the MT filament (Hallak et al., 1977Hallak M.E. Rodriguez J.A. Barra H.S. Caputto R. Release of tyrosine from tyrosinated tubulin. Some common factors that affect this process and the assembly of tubulin.FEBS Lett. 1977; 73: 147-150Crossref PubMed Scopus (113) Google Scholar, Rodrĭguez et al., 1973Rodrĭguez J.A. Arce C.A. Barra H.S. Caputto R. Release of tyrosine incorporated as a single unit into rat brain protein.Biochem. Biophys. Res. Commun. 1973; 54: 335-340Crossref PubMed Scopus (31) Google Scholar) and alters interactions with motors to favor kinesin-1 activity (Cai et al., 2009Cai D. McEwen D.P. Martens J.R. Meyhofer E. Verhey K.J. Single molecule imaging reveals differences in microtubule track selection between Kinesin motors.PLoS Biol. 2009; 7: e1000216Crossref PubMed Scopus (202) Google Scholar, Dunn et al., 2008Dunn S. Morrison E.E. Liverpool T.B. Molina-París C. Cross R.A. Alonso M.C. Peckham M. Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells.J. Cell Sci. 2008; 121: 1085-1095Crossref PubMed Scopus (161) Google Scholar, Liao and Gundersen, 1998Liao G. Gundersen G.G. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin.J. Biol. Chem. 1998; 273: 9797-9803Abstract Full Text Full Text PDF PubMed Scopus (229) Google Scholar). As such, distinct properties conferred by different tubulin PTMs enable stable MTs to serve as long-lived, specialized tracks for cargo sorting (Janke and Bulinski, 2011Janke C. Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions.Nat. Rev. Mol. Cell Biol. 2011; 12: 773-786Crossref PubMed Scopus (593) Google Scholar). Here, in examining the role of +TIPs during HSV-1 infection of different human cell types, we unexpectedly reveal that EB1 and CLIP170 are required for the infection of fibroblasts but not neuronal cells. In neuronal cells, infection was largely mediated by stable, detyrosinated MT networks that formed independently of EB1. Stemming from this, we find that TACC3 regulates interphase MT dynamics and in neuronal cells, by regulating the organization of detyrosinated MT arrays, influences kinesin-1-based sorting of both pathogenic and cellular cargoes. EB1 and CLIP170 are required for HSV-1 infection in normal human dermal fibroblasts (NHDFs) (Jovasevic et al., 2015Jovasevic V. Naghavi M.H. Walsh D. Microtubule plus end-associated CLIP-170 initiates HSV-1 retrograde transport in primary human cells.J. Cell Biol. 2015; 211: 323-337Crossref PubMed Scopus (34) Google Scholar). This prompted us to test whether these +TIPs also functioned during the infection of neuronal cells. To do this, we compared the effects of EB1 or CLIP170 depletion on infection in NHDFs versus SK-N-SH cells, a human neuroblastoma cell line used to model neuronal infection (Biedler et al., 1973Biedler J.L. Helson L. Spengler B.A. Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture.Cancer Res. 1973; 33: 2643-2652PubMed Google Scholar, Gordon et al., 2013Gordon J. Amini S. White M.K. General overview of neuronal cell culture.Methods Mol. Biol. 2013; 1078: 1-8Crossref PubMed Scopus (102) Google Scholar) (Figures S1A and S1B). Western blot (WB) analysis revealed that while knockdown of either EB1 or CLIP170 suppressed early infection in NHDFs, as detected by the reduced abundance of the viral immediate early infected cell protein 4 (ICP4), depletion of either factor had no effect on infection in SK-N-SHs (Figure 1A). While EB1 is the dominant EB family member in many cell types (Akhmanova and Steinmetz, 2015Akhmanova A. Steinmetz M.O. Control of microtubule organization and d" @default.
• W3000068919 created "2020-01-23" @default.
• W3000068919 creator A5048434095 @default.
• W3000068919 creator A5050062709 @default.
• W3000068919 creator A5059794447 @default.
• W3000068919 date "2020-01-01" @default.
• W3000068919 modified "2023-09-24" @default.
• W3000068919 title "TACC3 Regulates Microtubule Plus-End Dynamics and Cargo Transport in Interphase Cells" @default.
• W3000068919 cites W1566284745 @default.
• W3000068919 cites W1573751470 @default.
• W3000068919 cites W1785817244 @default.
• W3000068919 cites W1831209917 @default.
• W3000068919 cites W1890814105 @default.
• W3000068919 cites W1964865474 @default.
• W3000068919 cites W1985501881 @default.
• W3000068919 cites W1993764616 @default.
• W3000068919 cites W1996184123 @default.
• W3000068919 cites W2007040549 @default.
• W3000068919 cites W2021919254 @default.
• W3000068919 cites W2024641153 @default.
• W3000068919 cites W2028375545 @default.
• W3000068919 cites W2029059762 @default.
• W3000068919 cites W2034498504 @default.
• W3000068919 cites W2035773876 @default.
• W3000068919 cites W2036016893 @default.
• W3000068919 cites W2036760996 @default.
• W3000068919 cites W2041158925 @default.
• W3000068919 cites W2042921949 @default.
• W3000068919 cites W2044237166 @default.
• W3000068919 cites W2044820159 @default.
• W3000068919 cites W2049973173 @default.
• W3000068919 cites W2053691011 @default.
• W3000068919 cites W2054099226 @default.
• W3000068919 cites W2064194614 @default.
• W3000068919 cites W2066290070 @default.
• W3000068919 cites W2072342354 @default.
• W3000068919 cites W2097179914 @default.
• W3000068919 cites W2099220194 @default.
• W3000068919 cites W2100813299 @default.
• W3000068919 cites W2101799851 @default.
• W3000068919 cites W2117121945 @default.
• W3000068919 cites W2121439080 @default.
• W3000068919 cites W2125474168 @default.
• W3000068919 cites W2130589938 @default.
• W3000068919 cites W2130771394 @default.
• W3000068919 cites W2130867962 @default.
• W3000068919 cites W2132438476 @default.
• W3000068919 cites W2134812384 @default.
• W3000068919 cites W2135645995 @default.
• W3000068919 cites W2136242594 @default.
• W3000068919 cites W2140098146 @default.
• W3000068919 cites W2140306229 @default.
• W3000068919 cites W2140995916 @default.
• W3000068919 cites W2141960374 @default.
• W3000068919 cites W2143214705 @default.
• W3000068919 cites W2147332958 @default.
• W3000068919 cites W2148327308 @default.
• W3000068919 cites W2158232840 @default.
• W3000068919 cites W2159447001 @default.
• W3000068919 cites W2160496335 @default.
• W3000068919 cites W2162894558 @default.
• W3000068919 cites W2165909436 @default.
• W3000068919 cites W2167998440 @default.
• W3000068919 cites W2169987970 @default.
• W3000068919 cites W2220211909 @default.
• W3000068919 cites W2237971187 @default.
• W3000068919 cites W2244332011 @default.
• W3000068919 cites W2262783978 @default.
• W3000068919 cites W2294993303 @default.
• W3000068919 cites W2298933030 @default.
• W3000068919 cites W2519303614 @default.
• W3000068919 cites W2588057128 @default.
• W3000068919 cites W2591669685 @default.
• W3000068919 cites W2606253816 @default.
• W3000068919 cites W2736348964 @default.
• W3000068919 cites W2741584110 @default.
• W3000068919 cites W2741618452 @default.
• W3000068919 cites W2797371808 @default.
• W3000068919 cites W2809836575 @default.
• W3000068919 cites W2890996727 @default.
• W3000068919 cites W2951848464 @default.
• W3000068919 doi "https://doi.org/10.1016/j.celrep.2019.12.025" @default.
• W3000068919 hasPubMedCentralId "https://www.ncbi.nlm.nih.gov/pmc/articles/6980831" @default.
• W3000068919 hasPubMedId "https://pubmed.ncbi.nlm.nih.gov/31914393" @default.
• W3000068919 hasPublicationYear "2020" @default.
• W3000068919 type Work @default.
• W3000068919 sameAs 3000068919 @default.
• W3000068919 citedByCount "9" @default.
• W3000068919 countsByYear W30000689192020 @default.
• W3000068919 countsByYear W30000689192021 @default.
• W3000068919 countsByYear W30000689192022 @default.
• W3000068919 countsByYear W30000689192023 @default.
• W3000068919 crossrefType "journal-article" @default.
• W3000068919 hasAuthorship W3000068919A5048434095 @default.
• W3000068919 hasAuthorship W3000068919A5050062709 @default.
• W3000068919 hasAuthorship W3000068919A5059794447 @default.
• W3000068919 hasBestOaLocation W30000689191 @default.
• W3000068919 hasConcept C121332964 @default.

• next