Trafficking and/or division: Distinct roles of nucleoporins based on their location within the nuclear pore complex

. 2022 ; 19 (1) : 650-661. [epub] 20211231

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35491934

The nuclear pore complex (NPC) facilitates the trafficking of proteins and RNA between the nucleus and cytoplasm. The role of nucleoporins (Nups) in transport in the context of the NPC is well established, yet their function in tRNA export has not been fully explored. We selected several nucleoporins from different parts of the NPC to investigate their potential role in tRNA trafficking in Trypanosoma brucei. We show that while all of the nucleoporins studied are essential for cell viability, only TbNup62 and TbNup53a function in tRNA export. In contrast to homologs in yeast TbNup144 and TbNup158, which are part of the inner and outer ring of the NPC, have no role in nuclear tRNA trafficking. Instead, TbNup144 plays a critical role in nuclear division, highlighting the role of nucleoporins beyond nucleocytoplasmic transport. These results suggest that the location of nucleoporins within the NPC is crucial to maintaining various cellular processes.

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Rout MP, Aitchison JD, Suprapto A, et al. The yeast nuclear pore complex : composition, architecture, and transport mechanism. J Cell Biol. 2000;148(4):635–651. PubMed PMC

Alber F, Dokudovskaya S, Veenhoff LM, et al. The molecular architecture of the nuclear pore complex. Nature. 2007;450(7170):695–701. PubMed

Wente SR, Rout MP.. The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol. 2010;2(10):1–19.

Kabachinski G, Schwartz TU. The nuclear pore complex – structure and function at a glance. J Cell Sci. 2015;128(3):423–429. PubMed PMC

Grossman E, Medalia O, Zwerger M. Functional architecture of the nuclear pore complex. Annu Rev Biophys. 2012;41(1):557–584. PubMed

Devos D, Dokudovskaya S, Williams R, et al. Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci. 2006;103(7):2172–2177. PubMed PMC

Cronshaw JM, Krutchinsky AN, Zhang W, et al. Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol. 2002;158(5):915–927. PubMed PMC

Obado SO, Brillantes M, Uryu K, et al. Interactome mapping reveals the evolutionary history of the nuclear pore complex. PLoS Biol. 2016;14(2):1–30.

Kim SJ, Fernandez-martinez J, Nudelman I, et al. Integrative structure and functional anatomy of a nuclear pore complex. Nature. 2018;555(7697):475–482. PubMed PMC

Zeitler B, Weis K. The FG-repeat asymmetry of the nuclear pore complex is dispensable for bulk nucleocytoplasmic transport in vivo. J Cell Biol. 2004;167(4):583–590. PubMed PMC

DeGrasse JA, DuBois KN, Devos D, et al. Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol Cell Proteomics. 2009;8(9):2119–2130. PubMed PMC

Cordes VC, Reidenbach S, Rackwitz H, et al. Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex–attached intranuclear filaments. J Cell Biol. 1997;136(3):515–529. PubMed PMC

Xu XM, Rose A, Muthuswamy S, et al. NUCLEAR PORE ANCHOR, the arabidopsis homolog of Tpr/Mlp1/Mlp2/Megator, is involved in mRNA Export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell. 2007;19:1537–1548. PubMed PMC

Holden JM, Koreny L, Obado S, et al. Nuclear pore complex evolution : a trypanosome Mlp analogue functions in chromosomal segregation but lacks transcriptional barrier activity. Mol Biol Cell. 2014;25(9):1421–1436. PubMed PMC

Wente SR, Blobel G. A temperature-sensitive Nup116 null mutant forms a nuclear envelope seal over the yeast nuclear pore complex thereby blocking nucleocytoplasmic traffic. J Cell Biol. 1993;123(2):275–284. PubMed PMC

Fernandez-martinez J, Kim SJ, Shi Y, et al. Structure and function of the nuclear pore complex cytoplasmic mRNA export platform article structure and function of the nuclear pore complex cytoplasmic mRNA export platform. Cell. 2016;167(5):1215–1228. PubMed PMC

Lin DH, Correia AR, Cai SW, et al. Structural and functional analysis of mRNA export regulation by the nuclear pore complex. Nat Commun. 2018;9(1):1–19. PubMed PMC

Terry LJ, Wente SR. Nuclear mRNA export requires specifi c FG nucleoporins for translocation through the nuclear pore complex. J Cell Biol. 2007;178(7):1121–1132. PubMed PMC

Sharma K, Fabre E, Tekotte H, et al. Yeast nucleoporin mutants are defective in pre-tRNA splicing. Mol Cell Biol. 1996;16(1):294–301. PubMed PMC

Simos G, Tekottel H, Grosjean H, et al. Nuclear pore proteins of functional tRNA involved in the biogenesis of functional tRNA. EMBO J. 1996;15(9):2270–2284. PubMed PMC

Yoshihisa T, Yunoki-Esaki K, Ohshima C, et al. Possibility of cytoplasmic pre-tRNA splicing: the yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Mol Biol Cell. 2003;14(8):3266–3279. PubMed PMC

Yoshihisa T, Ohshima C, Yunoki-esaki K, et al. Cytoplasmic splicing of tRNA in Saccharomyces cerevisiae. Genes Cells. 2007;12(3):285–297. PubMed

Fabre E, Boelens WC, Wimmer C, et al. Nup145p is required for nuclear export of mRNA and binds homopolymeric RNA in vitro via a novel conserved motif. Cell. 1994;78(2):275–289. PubMed

Hegedűsová E, Kulkarni S, Burgman B, et al. The general mRNA exporters Mex67 and Mtr2 play distinct roles in nuclear export of tRNAs in Trypanosoma brucei. Nucleic Acids Res. 2019;1:1–12.

Derrer CP, Mancini R, Vallotton P, et al. The RNA export factor Mex67 functions as a mobile nucleoporin. J Cell Biol. 2019;218(12):3967–3976. PubMed PMC

Wu J, Bao A, Chatterjee K, et al. Genome-wide screen uncovers novel pathways for tRNA processing and nuclear–cytoplasmic dynamics. Genes Dev. 2015;29(24):2633–2644. PubMed PMC

Aitchison JD, Rout MP, Marelli M, et al. Two novel related yeast nucleoporins Nupl70p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p. J Cell Biol. 1995;131(5):1133–1148. PubMed PMC

Makio T, Stanton LH, Lin C, et al. The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J Cell Biol. 2009;185(3):459–473. PubMed PMC

Dean S, Sunter JD, Wheeler RJ. TrypTag.org: a trypanosome genome-wide protein localisation resource. Trends Parasitol. 2017;33(2):80–82. PubMed PMC

Lopes RRS, de O SG, Eitler R, et al. The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNATyr. RNA. 2016;22:1190–1199. PubMed PMC

Kessler AC, Kulkarni SS, Paulines MJ, et al. Retrograde nuclear transport from the cytoplasm is required for tRNATyr maturation in T. brucei. RNA Biol. 2017;15:1–9. PubMed PMC

Igloi GL, Kössel H. Affinity electrophoresis for monitoring terminal phosphorylation and the presence of queuosine in RNA. Application of polyacrylamide containing a covalently bound boronic acid. Nucleic Acids Res. 1985;13(19):6881–6898. PubMed PMC

Abeywickrema M, Vachova H, Farr H, et al. Non-equivalence in old- and new-flagellum daughter cells of a proliferative division in Trypanosoma brucei. Mol Microbiol. 2019;112:1024–1040. PubMed PMC

Zhou Q, Hu H, Li Z. New Insights into the Molecular Mechanisms of Mitosis and Cytokinesis in Trypanosomes. 1st ed. Elsevier Inc.; 2014.

Hammarton TC, Clark J, Douglas F, et al. Stage-specific differences in cell cycle control in Trypanosoma brucei revealed by RNA interference of a mitotic cyclin. J Biol Chem. 2003;278(25):22877–22886. PubMed

Hammarton TC, Engstler M, Mottram JC. The Trypanosoma brucei Cyclin, CYC2, is required for cell cycle progression through G1 phase and for maintenance of procyclic form cell morphology. J Biol Chem. 2004;279(23):24757–24764. PubMed

Li Z, Wang CC. A PHO80-like Cyclin and a B-type cyclin control the cell cycle of the procyclic form of Trypanosoma brucei. J Biol Chem. 2003;278(23):20652–20658. PubMed

Ploubidou A, Robinson DR, Docherty RC, et al. Evidence for novel cell cycle checkpoints in trypanosomes : kinetoplast segregation and cytokinesis in the absence of mitosis. J Cell Sci. 1999;112(24):4641–4650. PubMed

Zhou Q, Hu H, He CY, et al. Assembly and maintenance of the flagellum attachment zone filament in Trypanosoma brucei. J Cell Sci. 2015;128:2361–2372. PubMed PMC

Vickerman K. The evolutionary expansion of the Trypanosomatid Flagellates. Int J Parasitol. 1994;24(8):1317–1331. PubMed

Archivio SD, Wickstead B. Trypanosome outer kinetochore proteins suggest conservation of chromosome segregation machinery across eukaryotes. J Cell Biol. 2017;216(2):379–391. PubMed PMC

Zhou Q, Lee KJ, Kurasawa Y, et al. Faithful chromosome segregation in Trypanosoma brucei requires a cohort of divergent spindle-associated proteins with distinct functions. Nucleic Acids Res. 2018;1. DOI:10.1093/nar/gkx1156 PubMed DOI PMC

Nerusheva OO, Ludzia P, Akiyoshi B. Identification of four unconventional kinetoplastid kinetochore proteins KKT22 – 25 in Trypanosoma brucei. Open Biol. 2019;9:190236. PubMed PMC

Krull S, Dorries J, Boysen B, et al. Protein Tpr is required for establishing nuclear pore-associated zones of heterochromatin exclusion. EMBO J. 2010;29(10):1659–1673. PubMed PMC

Van De VDW, Wan Y, Lapetina DL, et al. A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell. 2013;152(5):969–983. PubMed PMC

Breuer M, Ohkura H. A negative loop within the nuclear pore complex controls global chromatin organization. Genes Dev. 2015;29(17):1789–1794. PubMed PMC

Kadota S, Ou J, Shi Y, et al. Nucleoporin 153 links nuclear pore complex to chromatin architecture by mediating CTCF abd cohesin binding. Nat Commun. 2020;11(1):1–17. PubMed PMC

Nakano H, Wang W, Hashizume C, et al. Unexpected role of nucleoporins in coordination of cell cycle progression. Cell Cycle. 2011;10(3):425–433. PubMed

Kalverda B, Pickersgill H, Shloma VV, et al. Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell. 2010;140(3):360–371. PubMed

Lussi YC, Shumaker DK, Shimi T, et al. The nucleoporin Nup153 affects spindle checkpoint activity due to an association with Mad1. Nucleus. 2010;1(1):71–84. PubMed PMC

Mackay DR, Elgort SW, Ullman KS. The Nucleoporin Nup153 has separable roles in both early mitotic progression and the resolution of mitosis. Mol Biol Cell. 2009;20(6):1652–1660. PubMed PMC

Iouk T, Kerscher O, Scott RJ, et al. The yeast nuclear pore complex functionally interacts with components of the spindle assembly checkpoint. J Cell Biol. 2002;159(5):807–819. PubMed PMC

Capelson M, Liang Y, Schulte R, et al. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell. 2010;140(3):372–383. PubMed PMC

Griffis ER, Altan N, Lippincott-Schwartz J, et al. Nup98 is a mobile nucleoporin with transcription- dependent dynamics. Mol Biol Cell. 2002;13(4):1282–1297. PubMed PMC

Chatel G, Fahrenkrog B. Nucleoporins : leaving the nuclear pore complex for a successful mitosis. Cell Signal. 2011;23(10):1555–1562. PubMed

Daigle N, Beaudouin J, Hartnell L, et al. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J Cell Biol. 2001;154(1):71–84. PubMed PMC

Ding R, McDonald KL, McIntosh JR. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J Cell Biol. 1993;120(1):141–151. PubMed PMC

Ogbadoyi E, Ersfeld K, Robinson D, et al. Architecture of the Trypanosoma brucei nucleus during interphase and mitosis. Chromosoma. 2000;108(8):501–513. PubMed

Roux KJ, Burke B. From pore to kinetochore and back : regulating envelope assembly. Dev Cell. 2006;11(3):276–278. PubMed

Morelle C, Sterkers Y, Crobu L, et al. The nucleoporin Mlp2 is involved in chromosomal distribution during mitosis in trypanosomatids. Nucleic Acids Res. 2015;43(8):4013–4027. PubMed PMC

Kerscher O, Hieter P, Winey M, et al. Novel Role for a Saccharomyces cerevisiae Nucleoporin, Nup170p, in Chromosome Segregation. Genetics. 2001;157:1543–1553. PubMed PMC

Seo H, Blus BJ, Jankovi NZ. Structure and nucleic acid binding activity of the nucleoporin Nup157. Proc Natl Acad Sci. 2013;110(41);16450–5. PubMed PMC

Rieder CL, Schultz A, Cole R, et al. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J Cell Biol. 1994;127(5):1301–1310. PubMed PMC

Hardwick KG, Weiss E, Luca FC, et al. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science. 1996;273(5277):953–955. PubMed

Kitagawa R, Rose AM. Components of the spindle-assembly checkpoint are essential in Caenorhabditis elegans. Nat Cell Biol. 1999;1(8):514–521. PubMed

Taylor SS, McKeon F. Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell. 1997;89(5):727–735. PubMed

Shah JV, Cleveland DW. Waiting for Anaphase: mad2 and the spindle assembly checkpoint. Cell. 2000;103(7):997–1000. PubMed

Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol. 2007;8(5):379–393. PubMed

Wickstead B, Ersfeld K, Gull K. Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol Biochem Parasitol. 2002;125(1–2):211–216. PubMed

Chomczynski P. Single-Step method of RNA isolation by acid guanidinium extraction. Anal Biochem. 1987;162(1):156–159. PubMed

Chatterjee K, Majumder S, Wan Y, et al. Sharing the load: mex67–Mtr2 cofunctions with Los1 in primary tRNA nuclear export. Genes Dev. 2017;31(21):2186–2198. PubMed PMC

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