The actin regulator profilin 1 is functionally associated with the mammalian centrosome
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33184056
PubMed Central
PMC7668531
DOI
10.26508/lsa.202000655
PII: 4/1/e202000655
Knihovny.cz E-zdroje
- MeSH
- aktiny metabolismus MeSH
- Caco-2 buňky MeSH
- centrozom metabolismus MeSH
- forminy metabolismus MeSH
- genový knockout MeSH
- lidé MeSH
- melanom experimentální metabolismus patologie MeSH
- mikrofilamentové proteiny metabolismus MeSH
- mikrotubuly metabolismus MeSH
- myši MeSH
- nádory kůže metabolismus patologie MeSH
- polymerizace MeSH
- profiliny genetika metabolismus MeSH
- signální transdukce genetika MeSH
- transfekce MeSH
- tubulin metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- aktiny MeSH
- forminy MeSH
- mikrofilamentové proteiny MeSH
- PFN1 protein, human MeSH Prohlížeč
- Pfn1 protein, mouse MeSH Prohlížeč
- profiliny MeSH
- tubulin MeSH
Profilin 1 is a crucial actin regulator, interacting with monomeric actin and several actin-binding proteins controlling actin polymerization. Recently, it has become evident that this profilin isoform associates with microtubules via formins and interferes with microtubule elongation at the cell periphery. Recruitment of microtubule-associated profilin upon extensive actin polymerizations, for example, at the cell edge, enhances microtubule growth, indicating that profilin contributes to the coordination of actin and microtubule organization. Here, we provide further evidence for the profilin-microtubule connection by demonstrating that it also functions in centrosomes where it impacts on microtubule nucleation.
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Conduit PT, Wainman A, Raff JW (2015) Centrosome function and assembly in animal cells. Nat Rev Mol Cell Biol 16: 611–624. 10.1038/nrm4062 PubMed DOI
Farina F, Gaillard J, Guerin C, Coute Y, Sillibourne J, Blanchoin L, Théry M (2016) The centrosome is an actin-organizing centre. Nat Cell Biol 18: 65–75. 10.1038/ncb3285 PubMed DOI PMC
Meiring JCM, Shneyer BI, Akhmanova A (2019) Generation and regulation of microtubule network asymmetry to drive cell polarity. Curr Opin Cell Biol 62: 86–95. 10.1016/j.ceb.2019.10.004 PubMed DOI
Sulimenko V, Hájková Z, Klebanovych A, Dráber P (2017) Regulation of microtubule nucleation mediated by γ-tubulin complexes. Protoplasma 254: 1187–1199. 10.1007/s00709-016-1070-z PubMed DOI
Au FK, Jia Y, Jiang K, Grigoriev I, Hau BK, Shen Y, Du S, Akhmanova A, Qi RZ (2017) GAS2L1 is a centriole-associated protein required for centrosome dynamics and disjunction. Dev Cell 40: 81–94. 10.1016/j.devcel.2016.11.019 PubMed DOI
Colin A, Singaravelu P, Thery M, Blanchoin L, Gueroui Z (2018) Actin-network architecture regulates microtubule dynamics. Curr Biol 28: 2647–2656. 10.1016/j.cub.2018.06.028 PubMed DOI
Hubert T, Vandekerckhove J, Gettemans J (2011) Actin and Arp2/3 localize at the centrosome of interphase cells. Biochem Biophys Res Commun 404: 153–158. 10.1016/j.bbrc.2010.11.084 PubMed DOI
Inoue D, Obino D, Pineau J, Farina F, Gaillard J, Guerin C, Blanchoin L, Lennon-Duménil AM, Théry M (2019) Actin filaments regulate microtubule growth at the centrosome. EMBO J 38: e99630 10.15252/embj.201899630 PubMed DOI PMC
Obino D, Farina F, Malbec O, Saez PJ, Maurin M, Gaillard J, Dingli F, Loew D, Gautreau A, Yuseff MI, et al. (2016) Actin nucleation at the centrosome controls lymphocyte polarity. Nat Commun 7: 10969 10.1038/ncomms10969 PubMed DOI PMC
van de Willige D, Hummel JJ, Alkemade C, Kahn OI, Au FK, Qi RZ, Dogterom M, Koenderink GH, Hoogenraad CC, Akhmanova A (2019) Cytolinker Gas2L1 regulates axon morphology through microtubule-modulated actin stabilization. EMBO Rep 20: e47732 10.15252/embr.201947732 PubMed DOI PMC
Antoniades I, Stylianou P, Skourides PA (2014) Making the connection: Ciliary adhesion complexes anchor basal bodies to the actin cytoskeleton. Dev Cell 28: 70–80. 10.1016/j.devcel.2013.12.003 PubMed DOI
Dogterom M, Koenderink GH (2019) Actin-microtubule crosstalk in cell biology. Nat Rev Mol Cell Biol 20: 38–54. 10.1038/s41580-018-0067-1 PubMed DOI
Tang N, Marshall WF (2012) Centrosome positioning in vertebrate development. J Cell Sci 125: 4951–4961. 10.1242/jcs.038083 PubMed DOI PMC
Gomez TS, Kumar K, Medeiros RB, Shimizu Y, Leibson PJ, Billadeau DD (2007) Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 26: 177–190. 10.1016/j.immuni.2007.01.008 PubMed DOI PMC
Plessner M, Knerr J, Grosse R (2019) Centrosomal actin assembly is required for proper mitotic spindle formation and chromosome congression. iScience 15: 274–281. 10.1016/j.isci.2019.04.022 PubMed DOI PMC
Luo Y, Barrios-Rodiles M, Gupta GD, Zhang YY, Ogunjimi AA, Bashkurov M, Tkach JM, Underhill AQ, Zhang L, Bourmoum M, et al. (2019) Atypical function of a centrosomal module in WNT signalling drives contextual cancer cell motility. Nat Commun 10: 2356–2374. 10.1038/s41467-019-10241-w PubMed DOI PMC
Zheng Y, Wong ML, Alberts B, Mitchison T (1995) Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 378: 578–583. 10.1038/378578a0 PubMed DOI
Oakley CE, Oakley BR (1989) Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338: 662–664. 10.1038/338662a0 PubMed DOI
Murphy SM, Preble AM, Patel UK, O’Connell KL, Dias DP, Moritz M, Agard D, Stults JT, Stearns T (2001) GCP5 and GCP6: Two new members of the human γ-tubulin complex. Mol Biol Cell 12: 3340–3352. 10.1091/mbc.12.11.3340 PubMed DOI PMC
Kollman JM, Greenberg CH, Li S, Moritz M, Zelter A, Fong KK, Fernandez JJ, Sali A, Kilmartin J, Davis TN, et al. (2015) Ring closure activates yeast γ-TuRC for species-specific microtubule nucleation. Nat Struct Mol Biol 22: 132–137. 10.1038/nsmb.2953 PubMed DOI PMC
Peng Y, Moritz M, Han X, Giddings TH, Lyon A, Kollman J, Winey M, Yates J 3rd, Agard DA, Drubin DG, et al. (2015) Interaction of CK1δ with γ-TuSC ensures proper microtubule assembly and spindle positioning. Mol Biol Cell 26: 2505–2518. 10.1091/mbc.e14-12-1627 PubMed DOI PMC
Consolati T, Locke J, Roostalu J, Chen ZA, Gannon J, Asthana J, Lim WM, Martino F, Cvetkovic MA, Rappsilber J, et al. (2020) Microtubule nucleation properties of single human γTuRCs explained by their Cryo-EM structure. Dev Cell 53: 603–617.e8. 10.1016/j.devcel.2020.04.019 PubMed DOI PMC
Liu P, Zupa E, Neuner A, Bohler A, Loerke J, Flemming D, Ruppert T, Rudack T, Peter C, Spahn C, et al. (2019) Insights into the assembly and activation of the microtubule nucleator γ-TuRC. Nature 578: 467–471. 10.1038/s41586-019-1896-6 PubMed DOI
Wieczorek M, Urnavicius L, Ti SC, Molloy KR, Chait BT, Kapoor TM (2020) Asymmetric molecular architecture of the human γ-tubulin ring complex. Cell 180: 165–175. 10.1016/j.cell.2019.12.007 PubMed DOI PMC
Hubert T, Perdu S, Vandekerckhove J, Gettemans J (2011) γ-tubulin localizes at actin-based membrane protrusions and inhibits formation of stress-fibers. Biochem Biophys Res Commun 408: 248–252. 10.1016/j.bbrc.2011.04.007 PubMed DOI
Carlier MF, Shekhar S (2017) Global treadmilling coordinates actin turnover and controls the size of actin networks. Nat Rev Mol Cell Biol 18: 389–401. 10.1038/nrm.2016.172 PubMed DOI
Karlsson R, Lindberg U (2007) Profilin, an essential control element for actin polymerization In Actin Monomer-Binding Proteins. Lappalainen P. (ed), pp 29–44. Austin, TX/New York, NY: Landes Bioscience/Springer.
Mullins RD, Bieling P, Fletcher DA (2018) From solution to surface to filament: Actin flux into branched networks. Biophys Rev 10: 1537–1551. 10.1007/s12551-018-0469-5 PubMed DOI PMC
Witke W. (2004) The role of profilin complexes in cell motility and other cellular processes. Trends Cell Biol 14: 461–469. 10.1016/j.tcb.2004.07.003 PubMed DOI
Nejedlá M, Sadi S, Sulimenko V, de Almeida FN, Blom H, Dráber P, Aspenstrom P, Karlsson R (2016) Profilin connects actin assembly with microtubule dynamics. Mol Biol Cell 27: 2381–2393. 10.1091/mbc.e15-11-0799 PubMed DOI PMC
Nejedlá M, Li Z, Masser AE, Biancospino M, Spiess M, Mackowiak SD, Friedländer MR, Karlsson R (2017) A fluorophore fusion-construct of human profilin I with non-compromized poly(L-Proline) binding capacity suitable for imaging. J Mol Biol 429: 964–976. 10.1016/j.jmb.2017.01.004 PubMed DOI
Connolly JA, Kalnins VI (1978) Visualization of centrioles and basal bodies by fluorescent staining with nonimmune rabbit sera. J Cell Biol 79: 526–532. 10.1083/jcb.79.2.526 PubMed DOI PMC
Jockusch BM, Murk K, Rothkegel M (2007) The profile of profilins. Rev Physiol Biochem Pharmacol 159: 131–149. 10.1007/112_2007_704 PubMed DOI
Bjorkegren C, Rozycki M, Schutt CE, Lindberg U, Karlsson R (1993) Mutagenesis of human profilin locates its poly(L-proline)-binding site to a hydrophobic patch of aromatic amino acids. FEBS Lett 333: 123–126. 10.1016/0014-5793(93)80388-b PubMed DOI
Colello D, Reverte CG, Ward R, Jones CW, Magidson V, Khodjakov A, LaFlamme SE (2010) Androgen and Src signaling regulate centrosome activity. J Cell Sci 123: 2094–2102. 10.1242/jcs.057505 PubMed DOI PMC
Sulimenko V, Hájková Z, Černohorská M, Sulimenko T, Sládková V, Dráberová L, Vinopal S, Dráberová E, Dráber P (2015) Microtubule nucleation in mouse bone marrow-derived mast cells is regulated by the concerted action of GIT1/βPIX proteins and calcium. J Immunol 194: 4099–4111. 10.4049/jimmunol.1402459 PubMed DOI
Akhmanova A, Steinmetz MO (2008) Tracking the ends: A dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9: 309–322. 10.1038/nrm2369 PubMed DOI
Henty-Ridilla JL, Juanes MA, Goode BL (2017) Profilin directly promotes microtubule growth through residues mutated in amyotrophic lateral sclerosis. Curr Biol 27: 3535–3543. 10.1016/j.cub.2017.10.002 PubMed DOI PMC
Pimm ML, Hotaling J, Henty-Ridilla JL (2020) Profilin choreographs actin and microtubules in cells and cancer. Int Rev Cell Mol Biol 355: 155–204. 10.1016/bs.ircmb.2020.05.005 PubMed DOI PMC
Grantham J, Lassing I, Karlsson R (2012) Controlling the cortical actin motor. Protoplasma 249: 1001–1015. 10.1007/s00709-012-0403-9 PubMed DOI PMC
Skruber K, Warp PV, Shklyarov R, Thomas JD, Swanson MS, Henty-Ridilla JL, Read TA, Vitriol EA (2020) Arp2/3 and Mena/VASP require profilin 1 for actin network assembly at the leading edge. Curr Biol 30: 2651–2664.e5. 10.1016/j.cub.2020.04.085 PubMed DOI PMC
Farina F, Ramkumar N, Brown L, Samandar Eweis D, Anstatt J, Waring T, Bithell J, Scita G, Thery M, Blanchoin L, et al. (2019) Local actin nucleation tunes centrosomal microtubule nucleation during passage through mitosis. EMBO J 38: e99843 10.15252/embj.201899843 PubMed DOI PMC
Dráberová E, D’Agostino L, Caracciolo V, Sládková V, Sulimenko T, Sulimenko V, Sobol M, Maounis NF, Tzelepis E, Mahera E, et al. (2015) Overexpression and nucleolar localization of γ-tubulin small complex proteins GCP2 and GCP3 in glioblastoma. J Neuropathol Exp Neurol 74: 723–742. 10.1097/nen.0000000000000212 PubMed DOI
Dráberová E, Sulimenko V, Vinopal S, Sulimenko T, Sládková V, D’Agostino L, Sobol M, Hozák P, Křen L, Katsetos CD, et al. (2017) Differential expression of human γ-tubulin isotypes during neuronal development and oxidative stress points to a γ-tubulin-2 prosurvival function. FASEB J 31: 1828–1846. 10.1096/fj.201600846rr PubMed DOI
Nováková M, Dráberová E, Schürmann W, Czihak G, Viklický V, Dráber P (1996) γ-Tubulin redistribution in taxol-treated mitotic cells probed by monoclonal antibodies. Cell Motil Cytoskeleton 33: 38–51. 10.1002/(sici)1097-0169(1996)33:1<38::aid-cm5>3.0.co;2-e PubMed DOI
Dráberová E, Sulimenko V, Kukharskyy V, Dráber P (1999) Monoclonal antibody NF-09 specific for neurofilament protein NF-M. Folia Biol (Praha) 45: 163–165. https://fb.cuni.cz/volume-45-1999-no-4 PubMed
Blume Y, Yemets A, Sulimenko V, Sulimenko T, Chan J, Lloyd C, Dráber P (2008) Tyrosine phosphorylation of plant tubulin. Planta 229: 143–150. 10.1007/s00425-008-0816-z PubMed DOI
Kukharskyy V, Sulimenko V, Macurek L, Sulimenko T, Dráberová E, Dráber P (2004) Complexes of γ-tubulin with nonreceptor protein tyrosine kinases Src and Fyn in differentiating P19 embryonal carcinoma cells. Exp Cell Res 298: 218–228. 10.1016/j.yexcr.2004.04.016 PubMed DOI
Dráber P, Lagunowich LA, Dráberová E, Viklický V, Damjanov I (1988) Heterogeneity of tubulin epitopes in mouse fetal tissues. Histochemistry 89: 485–492. 10.1007/BF00492606 PubMed DOI
Dráberová E, Dráber P (1993) A microtubule-interacting protein involved in coalignment of vimentin intermediate filaments with microtubules. J Cell Sci 106: 1263–1273. https://jcs.biologists.org/content/106/4/1263 PubMed
Klebanovych A, Sládková V, Sulimenko T, Vosecká V, Rubiková Z, Čapek M, Dráberová E, Dráber P, Sulimenko V (2019) Regulation of microtubule nucleation in mouse bone marrow-derived mast cells by protein tyrosine phosphatase SHP-1. Cells 8: 345–368. 10.3390/cells8040345 PubMed DOI PMC
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. (2012) Fiji: An open-source platform for biological-image analysis. Nat Methods 9: 676–682. 10.1038/nmeth.2019 PubMed DOI PMC
Cui XA, Palazzo AF (2012) Visualization of endoplasmic reticulum localized mRNAs in mammalian cells. J Vis Exp 70: e50066 10.3791/50066 PubMed DOI PMC
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