Proximity mapping of the microtubule plus-end tracking protein SLAIN2 using the BioID approach
Proximity mapping of the microtubule plus-end tracking protein SLAIN2 using the BioID approach
The centrosome is the main microtubule-organizing center of animal cells, which plays key roles in critical cellular processesranging from cell division to cellular signaling. Accordingly, defects in the structure and function of centrosomes cause various humandiseases such as cancer and primary microcephaly. To elucidate the molecular defects underlying these diseases, the biogenesis andfunctions of the centrosomes have to be fully understood. An essential step towards addressing these questions is the identificationand functional dissection of the full repertoire of centrosome proteins. Here, we used high-resolution imaging and showed that themicrotubule plus-end tracking protein SLAIN2 localizes to the pericentriolar material at the proximal end of centrioles. To gain insightinto its cellular functions and mechanisms, we applied in vivo proximity-dependent biotin identification to SLAIN2 and generated itsproximity interaction map. Gene ontology analysis of the SLAIN2 interactome revealed extensive interactions with centriole duplication,ciliogenesis, and microtubule-associated proteins, including previously characterized and uncharacterized interactions. Collectively,our results define SLAIN2 as a component of pericentriolar material and provide an important resource for future studies aimed atelucidating SLAIN2 functions at the centrosome.
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- Akhmanova A, Steinmetz MO (2008). Tracking the ends: a dynamic
protein network controls the fate of microtubule tips. Nature
Reviews Molecular Cell Biology 9:309-322. doi: 10.1038/
nrm2369
- Akhmanova A, Steinmetz MO (2010). Microtubule +TIPs at a glance.
Journal of Cell Science 123:3415-3419. doi: 10.1242/jcs.062414
- Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, et al.
(2003). Proteomic characterization of the human centrosome
by protein correlation profiling. Nature 426:570-574. doi:
10.1038/nature02166
- Bagchi S, Fredriksson R, Wallen-Mackenzie A (2015). In Situ
Proximity Ligation Assay (PLA). Methods in Molecular
Biology 1318:149-159. doi: 10.1007/978-1-4939-2742-5_15
- Bettencourt-Dias M, Glover DM (2007). Centrosome biogenesis
and function: centrosomics brings new understanding. Nature
Reviews Molecular Cell Biology 8:451-463. doi: 10.1038/
nrm2180
- Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho
SA (2011). Centrosomes and cilia in human disease. Trends in
Genetics 27:307-315. doi: 10.1016/j.tig.2011.05.004
- Bouchet BP, Noordstra I, van Amersfoort M, Katrukha EA,
Ammon YC et al. (2016). Mesenchymal cell invasion requires
cooperative regulation of persistent microtubule Growth by
SLAIN2 and CLASP1. Developmental Cell 39:708-723. doi:
10.1016/j.devcel.2016.11.009
- Boveri T (2008). Concerning the origin of malignant tumours by
Theodor Boveri. Translated and annotated by Henry Harris.
Journal of Cell Science 121 Suppl 1:1-84. doi: 10.1242/
jcs.025742
- Braun DA, Hildebrandt F (2017). Ciliopathies. Cold Spring Harbor
Perspectives in Biology 9:doi: 10.1101/cshperspect.a028191
- Chavali PL, Putz M, Gergely F (2014). Small organelle, big
responsibility: the role of centrosomes in development and
disease. Philosophical Transactions of the Royal Society of B:
Biological Sciences 369. doi: 10.1098/rstb.2013.0468
- Dobbelaere J, Josue F, Suijkerbuijk S, Baum B, Tapon N, et al. (2008).
A genome-wide RNAi screen to dissect centriole duplication
and centrosome maturation in Drosophila. PLoS Biology
6:e224. doi: 10.1371/journal.pbio.0060224
- Firat-Karalar EN, Rauniyar N, Yates JR, 3rd, Stearns T (2014).
Proximity interactions among centrosome components identify
regulators of centriole duplication. Current Biology 24:664-670.
doi: 10.1016/j.cub.2014.01.067
- Firat-Karalar EN, Sante J, Elliott S, Stearns T (2014). Proteomic
analysis of mammalian sperm cells identifies new components of
the centrosome. Journal of Cell Science doi: 10.1242/jcs.157008
- Firat-Karalar EN, Stearns T (2015). Probing mammalian centrosome
structure using BioID proximity-dependent biotinylation.
Methods in Cell Biology 129:153-170. doi: 10.1016/
bs.mcb.2015.03.016
- Firat-Karalar EN (2018). The ciliopathy gene product Cep290 is
required for primary cilium formation and microtubule
network organization. Turkish Journal of Biology 42:371-381.
doi: 10.3906/biy-1805-25
- Firat-Karalar EN (2018). The ciliopathy gene product Cep290 is
required for primary cilium formation and microtubule
network organization. Turkish Journal of Biology 42:371-381.
doi: 10.3906/biy-1805-25
- Godinho SA, Picone R, Burute M, Dagher R, Su Y et al. (2014).
Oncogene-like induction of cellular invasion from centrosome
amplification. Nature 510:167-171. doi: 10.1038/nature13277
- Gupta GD, Coyaud E, Goncalves J, Mojarad BA, Liu Y et al. (2015).
A dynamic protein interaction landscape of the human
centrosome-cilium interface. Cell 163:1484-1499. doi: 10.1016/j.
cell.2015.10.065
- Hatch EM, Kulukian A, Holland AJ, Cleveland DW, Stearns T (2010).
Cep152 interacts with Plk4 and is required for centriole
duplication. Journal of Cell Biology 191:721-729. doi: 10.1083/
jcb.201006049
- Hildebrandt F, Benzing T, Katsanis N (2011). Ciliopathies. New
England Journal of Medicine 364:1533-1543. doi: 10.1056/
NEJMra1010172
- Jakobsen L, Schroder JM, Larsen KM, Lundberg E, Andersen JS (2013).
Centrosome isolation and analysis by mass spectrometry-based
proteomics. Methods in Enzymology 525:371-393. doi: 10.1016/
B978-0-12-397944-5.00018-3
- Jiang K, Hua S, Mohan R, Grigoriev I, Yau KW et al. (2014).
Microtubule minus-end stabilization by polymerization-driven
CAMSAP deposition. Developmental Cell 28:295-309. doi:
10.1016/j.devcel.2014.01.001
- Kuleshov MV, Jones MR, Rouillard AD, Fernandez NF, Duan Q et al.
(2016). Enrichr: a comprehensive gene set enrichment analysis
web server 2016 update. Nucleic Acids Research 44:W90-97.
doi: 10.1093/nar/gkw377
- Lambert JP, Tucholska M, Go C, Knight JD, Gingras AC (2014).
Proximity biotinylation and affinity purification are
complementary approaches for the interactome mapping
of chromatin-associated protein complexes. Journal of
Proteomics doi: 10.1016/j.jprot.2014.09.011
- Luders J (2012). The amorphous pericentriolar cloud takes shape.
Nature Cell Biology 14:1126-1128. doi: 10.1038/ncb2617
Luders J, Stearns T (2007). Microtubule-organizing centres: a reevaluation. Nature Reviews Molecular Cell Biology 8:161-167.
doi: 0.1038/nrm2100
- Malicki JJ, Johnson CA (2017). The cilium: cellular antenna and
central processing unit. Trends in Cell Biology 27:126-140. doi:
10.1016/j.tcb.2016.08.002
- Marteil G, Guerrero A, Vieira AF, de Almeida BP, Machado P et
al. (2018). Over-elongation of centrioles in cancer promotes
centriole amplification and chromosome missegregation.
Nature Communications 9:1258. doi: 10.1038/s41467-018-
03641-x
- Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA et
al. (2013). The CRAPome: a contaminant repository for affinity
purification-mass spectrometry data. Nature Methods 10:730-
736. doi: 10.1038/nmeth.2557
- Mirvis M, Stearns T, James Nelson W (2018). Cilium structure,
assembly, and disassembly regulated by the cytoskeleton.
Biochemical Journal 475:2329-2353. doi: 10.1042/
BCJ20170453
- Muller EG, Snydsman BE, Novik I, Hailey DW, Gestaut DR, et al.
(2005). The organization of the core proteins of the yeast
spindle pole body. Molecular Biology of the Cell 16:3341-3352.
doi: 10.1091/mbc.E05-03-0214
- Nigg EA, Cajanek L, Arquint C (2014). The centrosome duplication
cycle in health and disease. FEBS Letters 588:2366-2372. doi:
10.1016/j.febslet.2014.06.030
- Nigg EA, Holland AJ (2018). Once and only once: mechanisms of
centriole duplication and their deregulation in disease. Nature
Reviews Molecular Cell Biology 19:297-312. doi: 10.1038/
nrm.2017.127
- Nigg EA, Raff JW (2009). Centrioles, centrosomes, and cilia in health
and disease. Cell 139:663-678. doi: 10.1016/j.cell.2009.10.036
- Odabasi E, Gul S, Kavakli IH, Firat-Karalar EN (2019). Centriolar
satellites are required for efficient ciliogenesis and ciliary
content regulation. EMBO Reports pii: e47723. doi: 10.15252/
embr.201947723
- Prosser SL, Pelletier L (2020). Centriolar satellite biogenesis and
function in vertebrate cells. Journal of Cell Science 133:doi:
10.1242/jcs.239566
- Roux KJ, Kim DI, Burke B (2013). BioID: a screen for protein-protein
interactions. Current Protocols in Protein Science 74:Unit 19
23. doi: 10.1002/0471140864.ps1923s74
- Schmidt TI, Kleylein-Sohn J, Westendorf J, Le Clech M, Lavoie SB
et al. (2009). Control of centriole length by CPAP and CP110.
Current Biology 19:1005-1011. doi: 10.1016/j.cub.2009.05.016
- Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. (2003).
Cytoscape: a software environment for integrated models
of biomolecular interaction networks. Genome Research
13:2498-2504. doi: 10.1101/gr.1239303
- Sonnen KF, Schermelleh L, Leonhardt H, Nigg EA (2012).
3D-structured illumination microscopy provides novel insight
into architecture of human centrosomes. Biology Open 1:965-
976. doi: 10.1242/bio.20122337
- Spektor A, Tsang WY, Khoo D, Dynlacht BD (2007). Cep97 and
CP110 suppress a cilia assembly program. Cell 130:678-690.
doi: 10.1016/j.cell.2007.06.027
- Stark C, Breitkreutz BJ, Reguly T, Boucher L, Breitkreutz A et al.
(2006). BioGRID: a general repository for interaction datasets.
Nucleic Acids Research 34:D535-539. doi: 10.1093/nar/gkj109
- Uzbekov R, Alieva I (2018). Who are you, subdistal appendages of
centriole? Open Biology 8:doi: 10.1098/rsob.180062
- van der Vaart B, Franker MA, Kuijpers M, Hua S, Bouchet BP et al.
(2012). Microtubule plus-end tracking proteins SLAIN1/2 and
ch-TOG promote axonal development. Journal of Neuroscience
32:14722-14728. doi: 10.1523/JNEUROSCI.1240-12.2012
- van der Vaart B, Manatschal C, Grigoriev I, Olieric V, Gouveia SM et
al. (2011). SLAIN2 links microtubule plus end-tracking proteins
and controls microtubule growth in interphase. Journal of Cell
Biology 193:1083-1099. doi: 10.1083/jcb.201012179
- Zhuang M, Zhao S, Jiang Z, Wang S, Sun P et al. (2019). MALAT1
sponges miR-106b-5p to promote the invasion and metastasis of
colorectal cancer via SLAIN2 enhanced microtubules mobility.
EBioMedicine 41:286-298. doi: 10.1016/j.ebiom.2018.12.049
- Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L et al.
(2006). Statistical analysis of membrane proteome expression
changes in Saccharomyces cerevisiae. Journal of Proteome
Research 5:2339-2347. doi: 10.1021/pr060161n