Multiple centrosomes enhance migration and immune cell effector functions of mature dendritic cells
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36214847
PubMed Central
PMC9555069
DOI
10.1083/jcb.202107134
PII: 213533
Knihovny.cz E-zdroje
- MeSH
- centrozom * metabolismus MeSH
- chemotaxe MeSH
- cytokiny metabolismus MeSH
- dendritické buňky * metabolismus MeSH
- kontrolní body buněčného cyklu MeSH
- lidé MeSH
- mitóza MeSH
- organizační centrum mikrotubulů MeSH
- pohyb buněk MeSH
- protein-serin-threoninkinasy metabolismus MeSH
- T-lymfocyty metabolismus MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cytokiny MeSH
- PLK2 protein, human MeSH Prohlížeč
- protein-serin-threoninkinasy MeSH
Centrosomes play a crucial role during immune cell interactions and initiation of the immune response. In proliferating cells, centrosome numbers are tightly controlled and generally limited to one in G1 and two prior to mitosis. Defects in regulating centrosome numbers have been associated with cell transformation and tumorigenesis. Here, we report the emergence of extra centrosomes in leukocytes during immune activation. Upon antigen encounter, dendritic cells pass through incomplete mitosis and arrest in the subsequent G1 phase leading to tetraploid cells with accumulated centrosomes. In addition, cell stimulation increases expression of polo-like kinase 2, resulting in diploid cells with two centrosomes in G1-arrested cells. During cell migration, centrosomes tightly cluster and act as functional microtubule-organizing centers allowing for increased persistent locomotion along gradients of chemotactic cues. Moreover, dendritic cells with extra centrosomes display enhanced secretion of inflammatory cytokines and optimized T cell responses. Together, these results demonstrate a previously unappreciated role of extra centrosomes for regular cell and tissue homeostasis.
BIOCEV 1st Faculty of Medicine Charles University Vestec Czech Republic
Institute of Genetics University of Bonn Bonn Germany
Institute of Science and Technology Austria Klosterneuburg Austria
Life and Medical Sciences Institute Cellular Immunology University of Bonn Bonn Germany
Life and Medical Sciences Institute Immune and Tumor Biology University of Bonn Bonn Germany
Life and Medical Sciences Institute Quantitative Systems Biology University of Bonn Bonn Germany
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Afzelius, B.A. 1976. A human syndrome caused by immotile cilia. Science. 193:317–319. 10.1126/science.1084576 PubMed DOI
Anderson, D.C., Wible L.J., Hughes B.J., Smith C.W., and Brinkley B.R.. 1982. Cytoplasmic microtubules in polymorphonuclear leukocytes: Effects of chemotactic stimulation and colchicine. Cell. 31:719–729. 10.1016/0092-8674(82)90326-9 PubMed DOI
Arnandis, T., Monteiro P., Adams S.D., Bridgeman V.L., Rajeeve V., Gadaleta E., Marzec J., Chelala C., Malanchi I., Cutillas P.R., and Godinho S.A.. 2018. Oxidative stress in cells with extra centrosomes drives non-cell-autonomous invasion. Dev. Cell. 47:409–424.e9. 10.1016/j.devcel.2018.10.026 PubMed DOI PMC
Ashley, D.M., Faiola B., Nair S., Hale L.P., Bigner D.D., and Gilboa E.. 1997. Bone marrow-generated dendritic cells pulsed with tumor extracts or tumor RNA induce antitumor immunity against central nervous system tumors. J. Exp. Med. 186:1177–1182. 10.1084/jem.186.7.1177 PubMed DOI PMC
Balashova, E.E., Lokhov P.G., and Bystrevskaya V.B.. 2009. Distribution of tyrosinated and acetylated tubulin in centrioles during mitosis of 3T3 and SV40-3T3 cells. Cell Tiss. Biol. 3:359–368. 10.1134/S1990519X09040087 PubMed DOI
Ballestrem, C., Wehrle-Haller B., Hinz B., and Imhof B.A.. 2000. Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration. Mol. Biol. Cell. 11:2999–3012. 10.1091/mbc.11.9.2999 PubMed DOI PMC
Banchereau, J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., Pulendran B., and Palucka K.. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767–811. 10.1146/annurev.immunol.18.1.767 PubMed DOI
Basto, R., Brunk K., Vinadogrova T., Peel N., Franz A., Khodjakov A., and Raff J.W.. 2008. Centrosome amplification can initiate tumorigenesis in flies. Cell. 133:1032–1042. 10.1016/j.cell.2008.05.039 PubMed DOI PMC
Bettencourt-Dias, M., Rodrigues-Martins A., Carpenter L., Riparbelli M., Lehmann L., Gatt M.K., Carmo N., Balloux F., Callaini G., and Glover D.M.. 2005. SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15:2199–2207. 10.1016/j.cub.2005.11.042 PubMed DOI
Blott, E.J., and Griffiths G.M.. 2002. Secretory lysosomes. Nat. Rev. Mol. Cell Biol. 3:122–131. 10.1038/nrm732 PubMed DOI
Bobinnec, Y., Khodjakov A., Mir L.M., Rieder C.L., Eddé B., and Bornens M.. 1998. Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J. Cell Biol. 143:1575–1589. 10.1083/jcb.143.6.1575 PubMed DOI PMC
Boes, M., Cerny J., Massol R., Op den Brouw M., Kirchhausen T., Chen J., and Ploegh H.L.. 2002. T cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature. 418:983–988. 10.1038/nature01004 PubMed DOI
Bornens, M. 2012. The centrosome in cells and organisms. Science. 335:422–426. 10.1126/science.1209037 PubMed DOI
Brandeis, M., Rosewell I., Carrington M., Crompton T., Jacobs M.A., Kirk J., Gannon J., and Hunt T.. 1998. Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc. Natl. Acad. Sci. USA. 95:4344–4349. 10.1073/pnas.95.8.4344 PubMed DOI PMC
Brooks, E.R., and Wallingford J.B.. 2014. Multiciliated cells. Curr. Biol. 24:R973–R982. 10.1016/j.cub.2014.08.047 PubMed DOI PMC
Cabeza-Cabrerizo, M., van Blijswijk J., Wienert S., Heim D., Jenkins R.P., Chakravarty P., Rogers N., Frederico B., Acton S., Beerling E., et al. . 2019. Tissue clonality of dendritic cell subsets and emergency DCpoiesis revealed by multicolor fate mapping of DC progenitors. Sci. Immunol. 4:eaaw1941. 10.1126/sciimmunol.aaw1941 PubMed DOI PMC
Carroll, P.E., Okuda M., Horn H.F., Biddinger P., Stambrook P.J., Gleich L.L., Li Y.-Q., Tarapore P., and Fukasawa K.. 1999. Centrosome hyperamplification in human cancer: Chromosome instability induced by p53 mutation and/or Mdm2 overexpression. Oncogene. 18:1935–1944. 10.1038/sj.onc.1202515 PubMed DOI
Castiel, A., Visochek L., Mittelman L., Dantzer F., Izraeli S., and Cohen-Armon M.. 2011. A phenanthrene derived PARP inhibitor is an extra-centrosomes de-clustering agent exclusively eradicating human cancer cells. BMC Cancer. 11:412. 10.1186/1471-2407-11-412 PubMed DOI PMC
Chan, J.Y. 2011. A clinical overview of centrosome amplification in human cancers. Int. J. Biol. Sci. 7:1122–1144. 10.7150/ijbs.7.1122 PubMed DOI PMC
Chevrier, N., Mertins P., Artyomov M.N., Shalek A.K., Iannacone M., Ciaccio M.F., Gat-Viks I., Tonti E., DeGrace M.M., Clauser K.R., et al. . 2011. Systematic discovery of TLR signaling components delineates viral-sensing circuits. Cell. 147:853–867. 10.1016/j.cell.2011.10.022 PubMed DOI PMC
Ching, K., and Stearns T.. 2020. Centrioles are amplified in cycling progenitors of olfactory sensory neurons. PLoS Biol. 18:e3000852. 10.1371/journal.pbio.3000852 PubMed DOI PMC
Cizmecioglu, O., Krause A., Bahtz R., Ehret L., Malek N., and Hoffmann I.. 2012. Plk2 regulates centriole duplication through phosphorylation-mediated degradation of Fbxw7 (human Cdc4). J. Cell Sci. 125:981–992. 10.1242/jcs.095075 PubMed DOI
Cizmecioglu, O., Warnke S., Arnold M., Duensing S., and Hoffmann I.. 2008. Plk2 regulated centriole duplication is dependent on its localization to the centrioles and a functional polo-box domain. Cell Cycle. 7:3548–3555. 10.4161/cc.7.22.7071 PubMed DOI
Davoli, T., and de Lange T.. 2011. The causes and consequences of polyploidy in normal development and cancer. Annu. Rev. Cell Dev. Biol. 27:585–610. 10.1146/annurev-cellbio-092910-154234 PubMed DOI
Dienz, O., and Rincon M.. 2009. The effects of IL-6 on CD4 T cell responses. Clin. Immunol. 130:27–33. 10.1016/j.clim.2008.08.018 PubMed DOI PMC
Durcan, T.M., Halpin E.S., Casaletti L., Vaughan K.T., Pierson M.R., Woods S., and Hinchcliffe E.H.. 2008. Centrosome duplication proceeds during mimosine-induced G1 cell cycle arrest. J. Cell. Physiol. 215:182–191. 10.1002/jcp.21298 PubMed DOI PMC
Eddy, R.J., Pierini L.M., and Maxfield F.R.. 2002. Microtubule asymmetry during neutrophil polarization and migration. Mol. Biol. Cell. 13:4470–4483. 10.1091/mbc.e02-04-0241 PubMed DOI PMC
Evans, T., Rosenthal E.T., Youngblom J., Distel D., and Hunt T.. 1983. Cyclin: A protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell. 33:389–396. 10.1016/0092-8674(83)90420-8 PubMed DOI
Farina, F., Gaillard J., Guérin C., Couté Y., Sillibourne J., Blanchoin L., and Théry M.. 2016. The centrosome is an actin-organizing centre. Nat. Cell Biol. 18:65–75. 10.1038/ncb3285 PubMed DOI PMC
Fourriere, L., Jimenez A.J., Perez F., and Boncompain G.. 2020. The role of microtubules in secretory protein transport. J. Cell Sci. 133:jcs237016. 10.1242/jcs.237016 PubMed DOI
Fox, D.T., and Duronio R.J.. 2013. Endoreplication and polyploidy: Insights into development and disease. Development. 140:3–12. 10.1242/dev.080531 PubMed DOI PMC
Fülle, L., Steiner N., Funke M., Gondorf F., Pfeiffer F., Siegl J., Opitz F.V., Haßel S.K., Erazo A.B., Schanz O., et al. . 2018. RNA aptamers recognizing murine CCL17 inhibit T cell chemotaxis and ReduceContact hypersensitivity in vivo. Mol. Thera. 26:95–104. 10.1016/j.ymthe.2017.10.005 PubMed DOI PMC
Ganem, N.J., Godinho S.A., and Pellman D.. 2009. A mechanism linking extra centrosomes to chromosomal instability. Nature. 460:278–282. 10.1038/nature08136 PubMed DOI PMC
Geiger, B., Rosen D., and Berke G.. 1982. Spatial relationships of microtubule-organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J. Cell Biol. 95:137–143. 10.1083/jcb.95.1.137 PubMed DOI PMC
Godinho, S.A., Picone R., Burute M., Dagher R., Su Y., Leung C.T., Polyak K., Brugge J.S., Théry M., and Pellman D.. 2014. Oncogene-like induction of cellular invasion from centrosome amplification. Nature. 510:167–171. 10.1038/nature13277 PubMed DOI PMC
Gorelik, R., and Gautreau A.. 2014. Quantitative and unbiased analysis of directional persistence in cell migration. Nat. Protoc. 9:1931–1943. 10.1038/nprot.2014.131 PubMed DOI
Griffith, J.W., Sokol C.L., and Luster A.D.. 2014. Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu. Rev. Immunol. 32:659–702. 10.1146/annurev-immunol-032713-120145 PubMed DOI
Guarguaglini, G., Duncan P.I., Stierhof Y.D., Holmström T., Duensing S., and Nigg E.A.. 2005. The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol. Biol. Cell. 16:1095–1107. 10.1091/mbc.E04-10-0939 PubMed DOI PMC
Guilliams, M., Ginhoux F., Jakubzick C., Naik S.H., Onai N., Schraml B.U., Segura E., Tussiwand R., and Yona S.. 2014. Dendritic cells, monocytes and macrophages: A unified nomenclature based on ontogeny. Nat. Rev. Immunol. 14:571–578. 10.1038/nri3712 PubMed DOI PMC
Habedanck, R., Stierhof Y.-D., Wilkinson C.J., and Nigg E.A.. 2005. The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7:1140–1146. 10.1038/ncb1320 PubMed DOI
He, J., Choe S., Walker R., Di Marzio P., Morgan D.O., and Landau N.R.. 1995. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69:6705–6711. 10.1128/JVI.69.11.6705-6711.1995 PubMed DOI PMC
Higginbotham, H., Bielas S., Tanaka T., and Gleeson J.G.. 2004. Transgenic mouse line with green-fluorescent protein-labeled Centrin 2 allows visualization of the centrosome in living cells. Transgenic Res. 13:155–164. 10.1023/b:trag.0000026071.41735.8e PubMed DOI
Hinchcliffe, E.H., Li C., Thompson E.A., Maller J.L., and Sluder G.. 1999. Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science. 283:851–854. 10.1126/science.283.5403.851 PubMed DOI
Imai, T., Yoshida T., Baba M., Nishimura M., Kakizaki M., and Yoshie O.. 1996. Molecular cloning of a novel T cell-directed CC chemokine expressed in thymus by signal sequence trap using epstein-barr virus vector. J. Biol. Chem. 271:21514–21521. 10.1074/jbc.271.35.21514 PubMed DOI
Inaba, K., Turley S., Iyoda T., Yamaide F., Shimoyama S., Reis e Sousa C., Germain R.N., Mellman I., and Steinman R.M.. 2000. The formation of immunogenic major histocompatibility complex class II-peptide ligands in lysosomal compartments of dendritic cells is regulated by inflammatory stimuli. J. Exp. Med. 191:927–936. 10.1084/jem.191.6.927 PubMed DOI PMC
Inoue, D., Obino D., Pineau J., Farina F., Gaillard J., Guérin C., Blanchoin L., Lennon-Dumenil A.-M., and Théry M.. 2019. Actin filaments regulate microtubule growth at the centrosome. EMBO J. 38:e99630. 10.15252/embj.201899630 PubMed DOI PMC
Kohlmaier, G., Lončarek J., Meng X., McEwen B.F., Mogensen M.M., Spektor A., Dynlacht B.D., Khodjakov A., and Gönczy P.. 2009. Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr. Biol. 19:1012–1018. 10.1016/j.cub.2009.05.018 PubMed DOI PMC
Kong, D., Sahabandu N., Sullenberger C., Vásquez-Limeta A., Luvsanjav D., Lukasik K., and Lončarek J.. 2020. Prolonged mitosis results in structurally aberrant and over-elongated centrioles. J. Cell Biol. 219:e201910019. 10.1083/jcb.201910019 PubMed DOI PMC
Kopf, A., and Kiermaier E.. 2021. Dynamic microtubule arrays in leukocytes and their role in cell migration and immune synapse formation. Front. Cell Dev. Biol. 9:635511. 10.3389/fcell.2021.635511 PubMed DOI PMC
Kopf, A., Renkawitz J., Hauschild R., Girkontaite I., Tedford K., Merrin J., Thorn-Seshold O., Trauner D., Häcker H., Fischer K.-D., et al. . 2020. Microtubules control cellular shape and coherence in amoeboid migrating cells. J. Cell Biol. 219:e201907154. 10.1083/jcb.201907154 PubMed DOI PMC
Kushner, E.J., Ferro L.S., Liu J.-Y., Durrant J.R., Rogers S.L., Dudley A.C., and Bautch V.L.. 2014. Excess centrosomes disrupt endothelial cell migration via centrosome scattering. J. Cell Biol. 206:257–272. 10.1083/jcb.201311013 PubMed DOI PMC
Kwon, M., Godinho S.A., Chandhok N.S., Ganem N.J., Azioune A., Théry M., and Pellman D.. 2008. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 22:2189–2203. 10.1101/gad.1700908 PubMed DOI PMC
Lacey, K.R., Jackson P.K., and Stearns T.. 1999. Cyclin-dependent kinase control of centrosome duplication. Proc. Natl. Acad. Sci. USA. 96:2817–2822. 10.1073/pnas.96.6.2817 PubMed DOI PMC
Lawo, S., Hasegan M., Gupta G.D., and Pelletier L.. 2012. Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat. Cell Biol. 14:1148–1158. 10.1038/ncb2591 PubMed DOI
Lämmermann, T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Söldner R., Hirsch K., Keller M., Förster R., Critchley D.R., Fässler R., and Sixt M.. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature. 453:51–55. 10.1038/nature06887 PubMed DOI
Leithner, A., Renkawitz J., de Vries I., Hauschild R., Häcker H., and Sixt M.. 2018. Fast and efficient genetic engineering of hematopoietic precursor cells for the study of dendritic cell migration. Eur. J. Immunol. 48:1074–1077. 10.1002/eji.201747358 PubMed DOI
Levine, M.S., Bakker B., Boeckx B., Moyett J., Lu J., Vitre B., Spierings D.C., Lansdorp P.M., Cleveland D.W., Lambrechts D., et al. . 2017. Centrosome amplification is sufficient to promote spontaneous tumorigenesis in mammals. Dev. Cell. 40:313–322.e5. 10.1016/j.devcel.2016.12.022 PubMed DOI PMC
Li, X., Zhao Q., Liao R., Sun P., and Wu X.. 2003. The SCF(Skp2) ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation. J. Biol. Chem. 278:30854–30858. 10.1074/jbc.C300251200 PubMed DOI
Lingle, W.L., Lutz W.H., Ingle J.N., Maihle N.J., and Salisbury J.L.. 1998. Centrosome hypertrophy in human breast tumors: Implications for genomic stability and cell polarity. Proc. Natl. Acad. Sci. USA. 95:2950–2955. 10.1073/pnas.95.6.2950 PubMed DOI PMC
Liu, K., Victora G.D., Schwickert T.A., Guermonprez P., Meredith M.M., Yao K., Chu F.-F., Randolph G.J., Rudensky A.Y., and Nussenzweig M.. 2009. In Vivo Analysis of Dendritic Cell Development and Homeostasis. Science. 324:392–397. 10.1126/science.1170540 PubMed DOI PMC
Liu, Z., Gu Y., Shin A., Zhang S., and Ginhoux F.. 2020. Analysis of myeloid cells in mouse tissues with flow cytometry. STAR Protoc. 1:100029. 10.1016/j.xpro.2020.100029 PubMed DOI PMC
Lončarek, J., Hergert P., and Khodjakov A.. 2010. Centriole reduplication during prolonged interphase requires procentriole maturation governed by Plk1. Curr. Biol. 20:1277–1282. 10.1016/j.cub.2010.05.050 PubMed DOI PMC
Lutz, M.B., Kukutsch N., Ogilvie A.L., Rössner S., Koch F., Romani N., and Schuler G.. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods. 223:77–92. 10.1016/s0022-1759(98)00204-x PubMed DOI
Madaan, A., Verma R., Singh A.T., Jain S.K., and Jaggi M.. 2014. A stepwise procedure for isolation of murine bone marrow and generation of dendritic cells. J. Biol. Methods. 1:e1. 10.14440/jbm.2014.12 DOI
Maiuri, P., Rupprecht J.-F., Wieser S., Ruprecht V., Bénichou O., Carpi N., Coppey M., De Beco S., Gov N., Heisenberg C.-P., et al. . 2015. Actin flows mediate a universal coupling between cell speed and cell persistence. Cell. 161:374–386. 10.1016/j.cell.2015.01.056 PubMed DOI
Malech, H.L., Root R.K., and Gallin J.I.. 1977. Structural-analysis of human neutrophil migration - centriole, microtubule, and microfilament orientation and function during chemotaxis. J. Cell Biol. 75:666–693. 10.1083/jcb.75.3.666 PubMed DOI PMC
McGarry, T.J., and Kirschner M.W.. 1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell. 93:1043–1053. 10.1016/s0092-8674(00)81209-x PubMed DOI
Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135–145. 10.1038/35100529 PubMed DOI
Mellman, I., and Steinman R.M.. 2001. Dendritic cells: Specialized and regulated antigen processing machines. Cell. 106:255–258. 10.1016/s0092-8674(01)00449-4 PubMed DOI
Mennella, V., Keszthelyi B., McDonald K.L., Chhun B., Kan F., Rogers G.C., Huang B., and Agard D.A.. 2012. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat. Cell Biol. 14:1159–1168. 10.1038/ncb2597 PubMed DOI PMC
Merad, M., Sathe P., Helft J., Miller J., and Mortha A.. 2013. The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31:563–604. 10.1146/annurev-immunol-020711-074950 PubMed DOI PMC
Meraldi, P., Lukas J., Fry A.M., Bartek J., and Nigg E.A.. 1999. Centrosome duplication in mammalian somatic cells requires E2F and Cdk2-cyclin A. Nat. Cell Biol. 1:88–93. 10.1038/10054 PubMed DOI
Moritz, M., Braunfeld M.B., Sedat J.W., Alberts B., and Agard D.A.. 1995. Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature. 378:638–640. 10.1038/378638a0 PubMed DOI
Müller, A., Schmidt D., Xu C.S., Pang S., D'Costa J.V., Kretschmar S., Münster C., Kurth T., Jug F., Weigert M., et al. . 2021. 3D FIB-SEM reconstruction of microtubule-organelle interaction in whole primary mouse β cells. J. Cell Biol. 220:e202010039. 10.1083/jcb.202010039 PubMed DOI PMC
Nagele, R., Freeman T., McMorrow L., and Lee H.Y.. 1995. Precise spatial positioning of chromosomes during prometaphase: Evidence for chromosomal order. Science. 270:1831–1835. 10.1126/science.270.5243.1831 PubMed DOI
Neefjes, J., Jongsma M.L.M., Paul P., and Bakke O.. 2011. Towards a systems understanding ofMHC class I and MHC class II antigenpresentation. Nat. Rev. Immunol. 11:823–836. 10.1038/nri3084 PubMed DOI
Nigg, E.A. 2007. Centrosome duplication: Of rules and licenses. Trends Cell Biol. 17:215–221. 10.1016/j.tcb.2007.03.003 PubMed DOI
Nigg, E.A. 2002. Centrosome aberrations: Cause or consequence of cancer progression? Nat. Rev. Cancer. 2:815–825. 10.1038/nrc924 PubMed DOI
Nurse, P. 2000. A long twentieth century of the cell cycle and beyond. Cell. 100:71–78. 10.1016/s0092-8674(00)81684-0 PubMed DOI
Ogden, A., Rida P.C.G., and Aneja R.. 2013. Heading off with the herd: How cancer cells might maneuver supernumerary centrosomes for directional migration. Cancer Metastasis Rev. 32:269–287. 10.1007/s10555-012-9413-5 PubMed DOI PMC
Ohtsubo, M., Theodoras A.M., Schumacher J., Roberts J.M., and Pagano M.. 1995. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell Biol. 15:2612–2624. 10.1128/mcb.15.5.2612 PubMed DOI PMC
Oliver, G., Kipnis J., Randolph G.J., and Harvey N.L.. 2020. The lymphatic vasculature in the 21st century: Novel functional roles in homeostasis and disease. Cell. 182:270–296. 10.1016/j.cell.2020.06.039 PubMed DOI PMC
Paintrand, M., Moudjou M., Delacroix H., and Bornens M.. 1992. Centrosome organization and centriole architecture: Their sensitivity to divalent cations. J. Struct. Biol. 108:107–128. 10.1016/1047-8477(92)90011-x PubMed DOI
Pannu, V., Rida P.C.G., Celik B., Turaga R.C., Ogden A., Cantuaria G., Gopalakrishnan J., and Aneja R.. 2014. Centrosome-declustering drugs mediatea two-pronged attack on interphase and mitosis in supercentrosomal cancer cells. Cell Death Dis. 5:e15388. 10.1038/cddis.2014.505 PubMed DOI PMC
Piel, M., Meyer P., Khodjakov A., Rieder C.L., and Bornens M.. 2000. The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149:317–330. 10.1083/jcb.149.2.317 PubMed DOI PMC
Pihan, G.A., Purohit A., Wallace J., Knecht H., Woda B., Quesenberry P., and Doxsey S.J.. 1998. Centrosome defects and genetic instability in malignant tumors. Cancer Res. 58:3974–3985 PubMed
Planelles, V., Jowett J.B., Li Q.X., Xie Y., Hahn B., and Chen I.S.. 1996. Vpr-induced cell cycle arrest is conserved among primate lentiviruses. J. Virol. 70:2516–2524. 10.1128/JVI.70.4.2516-2524.1996 PubMed DOI PMC
Pulecio, J., Petrovic J., Prete F., Chiaruttini G., Lennon-Dumenil A.-M., Desdouets C., Gasman S., Burrone O.R., and Benvenuti F.. 2010. Cdc42-mediated MTOC polarization in dendritic cells controls targeted delivery of cytokines at the immune synapse. J. Exp. Med. 207:2719–2732. 10.1084/jem.20100007 PubMed DOI PMC
Quah, B.J.C., Warren H.S., and Parish C.R.. 2007. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fluorescent dye carboxyfluorescein diacetate succinimidyl ester. Nat. Protoc. 2:2049–2056. 10.1038/nprot.2007.296 PubMed DOI
Quintyne, N.J., Reing J.E., Hoffelder D.R., Gollin S.M., and Saunders W.S.. 2005. Spindle multipolarity is prevented by centrosomal clustering. Science. 307:127–129. 10.1126/science.1104905 PubMed DOI
Raab, M.S., Breitkreutz I., Anderhub S., Rønnest M.H., Leber B., Larsen T.O., Weiz L., Konotop G., Hayden P.J., Podar K., et al. . 2012. GF-15, a novel inhibitor of centrosomal clustering, suppresses tumor cell growth in vitro and in vivo. Cancer Res. 72:5374–5385. 10.1158/0008-5472.CAN-12-2026 PubMed DOI
Ratner, S., Sherrod W.S., and Lichlyter D.. 1997. Microtubule retraction into the uropod and its role in T cell polarization and motility. J. Immunol. 159:1063–1067 PubMed
Redecke, V., Wu R., Zhou J., Finkelstein D., Chaturvedi V., High A.A., and Häcker H.. 2013. Hematopoietic progenitor cell lines with myeloid and lymphoid potential. Nat. Methods. 10:795–803. 10.1038/nmeth.2510 PubMed DOI PMC
Renkawitz, J., Kopf A., Stopp J., de Vries I., Driscoll M.K., Merrin J., Hauschild R., Welf E.S., Danuser G., Fiolka R., and Sixt M.. 2019. Nuclear positioning facilitates amoeboid migration along the path of least resistance. Nature. 568:546–550. 10.1038/s41586-019-1087-5 PubMed DOI PMC
Renkawitz, J., Schumann K., Weber M., Lämmermann T., Pflicke H., Piel M., Polleux J., Spatz J.P., and Sixt M.. 2009. Adaptive force transmission in amoeboid cell migration. Nat. Cell Biol. 11:1438–1443. 10.1038/ncb1992 PubMed DOI
Ritter, A.T., Asano Y., Stinchcombe J.C., Dieckmann N.M.G., Chen B.-C., Gawden-Bone C., van Engelenburg S., Legant W., Gao L., Davidson M.W., et al. . 2015. Actin depletion initiates events leading to granule secretion at the immunological synapse. Immunity. 42:864–876. 10.1016/j.immuni.2015.04.013 PubMed DOI PMC
Ritzman, A.M., Hughes-Hanks J.M., Blaho V.A., Wax L.E., Mitchell W.J., and Brown C.R.. 2010. The chemokine receptor CXCR2 ligand KC (CXCL1) mediates neutrophil recruitment and is critical for development of experimental Lyme arthritis and carditis. Infect. Immun. 78:4593–4600. 10.1128/IAI.00798-10 PubMed DOI PMC
Sabino, D., Gogendeau D., Gambarotto D., Nano M., Pennetier C., Dingli F., Arras G., Loew D., and Basto R.. 2015. Moesin is a major regulator of centrosome behavior in epithelial cells with extra centrosomes. Curr. Biol. 25:879–889. 10.1016/j.cub.2015.01.066 PubMed DOI PMC
Sakaue-Sawano, A., Kurokawa H., Morimura T., Hanyu A., Hama H., Osawa H., Kashiwagi S., Fukami K., Miyata T., Miyoshi H., et al. . 2008. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell. 132:487–498. 10.1016/j.cell.2007.12.033 PubMed DOI
Salisbury, J.L., Suino K.M., Busby R., and Springett M.. 2002. Centrin-2 is required for centriole duplication in mammalian cells. Curr. Biol. 12:1287–1292. 10.1016/s0960-9822(02)01019-9 PubMed DOI
Sanjana, N.E., Shalem O., and Zhang F.. 2014. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods. 11:783–784. 10.1038/nmeth.3047 PubMed DOI PMC
Schmidt, T.I., Kleylein-Sohn J., Westendorf J., Le Clech M., Lavoie S.B., Stierhof Y.-D., and Nigg E.A.. 2009. Control of centriole length by CPAP and CP110. Curr. Biol. 19:1005–1011. 10.1016/j.cub.2009.05.016 PubMed DOI
Semino, C., Angelini G., Poggi A., and Rubartelli A.. 2005. NK/iDC interaction results in IL-18 secretion by DCs at the synaptic cleft followed by NK cell activation and release of the DC maturation factor HMGB1. Blood. 106:609–616. 10.1182/blood-2004-10-3906 PubMed DOI
Shalem, O., Sanjana N.E., Hartenian E., Shi X., Scott D.A., Mikkelsen T., Heckl D., Ebert B.L., Root D.E., Doench J.G., and Zhang F.. 2014. Genome-scale CRISPR-cas9 knockout screening in human cells. Science. 343:84–87. 10.1126/science.1247005 PubMed DOI PMC
Steinman, R.M., Pack M., and Inaba K.. 1997. Dendritic cells in the T cell areas of lymphoid organs. Immunol. Rev. 156:25–37. 10.1111/j.1600-065x.1997.tb00956.x PubMed DOI
Stiess, M., Maghelli N., Kapitein L.C., Gomis-Rüth S., Wilsch-Bräuninger M., Hoogenraad C.C., Tolić-Nørrelykke I.M., and Bradke F.. 2010. Axon extension occurs independently of centrosomal microtubule nucleation. Science. 327:704–707. 10.1126/science.1182179 PubMed DOI
Stinchcombe, J.C., and Griffiths G.M.. 2014. Communication, the centrosome and the immunological synapse. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 369:20130463. 10.1098/rstb.2013.0463 PubMed DOI PMC
Stinchcombe, J.C., Majorovits E., Bossi G., Fuller S., and Griffiths G.M.. 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature. 443:462–465. 10.1038/nature05071 PubMed DOI
Stoitzner, P., Romani N., McLellan A.D., Tripp C.H., and Ebner S., 2009. Isolation of skin dendritic cells from mouse and man. Antigen Processing, Methods in Molecular Biology. Humana Press, Totowa, NJ, 235–248. 10.1007/978-1-60761-421-0_16 PubMed DOI
Tang, C.-J.C., Fu R.-H., Wu K.-S., Hsu W.-B., and Tang T.K.. 2009. CPAP is a cell-cycle regulated protein that controls centriole length. Nat. Cell Biol. 11:825–831. 10.1038/ncb1889 PubMed DOI
Toettcher, J.E., Loewer A., Ostheimer G.J., Yaffe M.B., Tidor B., and Lahav G.. 2009. Distinct mechanisms act in concert to mediate cell cycle arrest. Proc. Natl. Acad. Sci. USA. 106:785–790. 10.1073/pnas.0806196106 PubMed DOI PMC
Tsou, M.-F.B., and Stearns T.. 2006a. Mechanism limiting centrosome duplication to once per cell cycle. Nature. 442:947–951. 10.1038/nature04985 PubMed DOI
Tsou, M.-F.B., and Stearns T.. 2006b. Controlling centrosome number: Licenses and blocks. Curr. Opin. Cell Biol. 18:74–78. 10.1016/j.ceb.2005.12.008 PubMed DOI
Turley, S.J., Inaba K., Garrett W.S., Ebersold M., Unternaehrer J., Steinman R.M., and Mellman I.. 2000. Transport of peptide-MHC class II complexes in developing dendritic cells. Science. 288:522–527. 10.1126/science.288.5465.522 PubMed DOI
Ueda, M., Gräf R., MacWilliams H.K., Schliwa M., and Euteneuer U.. 1997. Centrosome positioning and directionality of cell movements. Proc. Natl. Acad. Sci. USA. 94:9674–9678. 10.1073/pnas.94.18.9674 PubMed DOI PMC
Uetake, Y., Lončarek J., Nordberg J.J., English C.N., La Terra S., Khodjakov A., and Sluder G.. 2007. Cell cycle progression and de novo centriole assembly after centrosomal removal in untransformed human cells. J. Cell Biol. 176:173–182. 10.1083/jcb.200607073 PubMed DOI PMC
Verboogen, D.R.J., Revelo N.H., Ter Beest M., and van den Bogaart G.. 2019. Interleukin-6 secretion is limited by self-signaling in endosomes. J. Mol. Cell Biol. 11:144–157. 10.1093/jmcb/mjy038 PubMed DOI PMC
Vertii, A., Ivshina M., Zimmerman W., Hehnly H., Kant S., and Doxsey S.. 2016. The centrosome undergoes plk1-independent interphase maturation during inflammation and mediates cytokine release. Dev. Cell. 37:377–386. 10.1016/j.devcel.2016.04.023 PubMed DOI
Vicente-Manzanares, M., and Sánchez-Madrid F.. 2004. Role of the cytoskeleton during leukocyte responses. Nat. Rev. Immunol. 4:110–122. 10.1038/nri1268 PubMed DOI
Vyas, J.M., Kim Y.-M., Artavanis-Tsakonas K., Love J.C., Van der Veen A.G., and Ploegh H.L.. 2007. Tubulation of class II MHC compartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells. J. Immunol. 178:7199–7210. 10.4049/jimmunol.178.11.7199 PubMed DOI PMC
Weber, R.G., Bridger J.M., Benner A., Weisenberger D., Ehemann V., Reifenberger G., and Lichter P.. 1998. Centrosome amplification as a possible mechanism for numerical chromosome aberrations in cerebral primitive neuroectodermal tumors with TP53 mutations. Cytogenet. Cell Genet. 83:266–269. 10.1159/000015168 PubMed DOI
Wieser, S., and Schutz G.J.. 2008. Tracking single molecules in the live cell plasma membrane-Do's and Don't's. Methods. 46:131–140. 10.1016/j.ymeth.2008.06.010 PubMed DOI
Wong, Y.L., Anzola J.V., Davis R.L., Yoon M., Motamedi A., Kroll A., Seo C.P., Hsia J.E., Kim S.K., Mitchell J.W., et al. . 2015. Cell biology. Reversible centriole depletion with an inhibitor of Polo-like kinase 4. Science. 348:1155–1160. 10.1126/science.aaa5111 PubMed DOI PMC
Wubbolts, R., Fernandez-Borja M., Oomen L., Verwoerd D., Janssen H., Calafat J., Tulp A., Dusseljee S., and Neefjes J.. 1996. Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135:611–622. 10.1083/jcb.135.3.611 PubMed DOI PMC
Wubbolts, R., Fernandez-Borja M., Jordens I., Reits E., Dusseljee S., Echeverri C., Vallee R.B., and Neefjes J.. 1999. Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J. Cell Sci. 112:785–795. 10.1242/jcs.112.6.785 PubMed DOI
Xu, J., Wang F., Van Keymeulen A., Rentel M., and Bourne H.R.. 2005. Neutrophil microtubules suppress polarity and enhance directional migration. Proc. Natl. Acad. Sci. USA. 102:6884–6889. 10.1073/pnas.0502106102 PubMed DOI PMC
Yi, J., Wu X., Chung A.H., Chen J.K., Kapoor T.M., and Hammer J.A.. 2013. Centrosome repositioning in T cells is biphasic and driven by microtubule end-on capture-shrinkage. J. Cell Biol. 202:779–792. 10.1083/jcb.201301004 PubMed DOI PMC
Yuseff, M.-I., Reversat A., Lankar D., Diaz J., Fanget I., Pierobon P., Randrian V., Larochette N., Vascotto F., Desdouets C., et al. . 2011. Polarized secretion of lysosomesat the B cell synapse couples antigen extraction to processing and presentation. Immunity. 35:361–374. 10.1016/j.immuni.2011.07.008 PubMed DOI
Zebrowski, D.C., Vergarajauregui S., Wu C.-C., Piatkowski T., Becker R., Leone M., Hirth S., Ricciardi F., Falk N., Giessl A., et al. . 2015. Developmental alterations in centrosome integrity contribute to the post-mitotic state of mammalian cardiomyocytes. Elife. 4:e05563. 10.7554/eLife.05563 PubMed DOI PMC