Functional Interactions of BAF and LEM Proteins in the Formation of Germ Cells
- Authors: Bogolyubova I.O.1, Bogolyubov D.S.1
-
Affiliations:
- Institute of Cytology, Russian Academy of Sciences
- Issue: Vol 65, No 5 (2023)
- Pages: 407-419
- Section: Articles
- URL: https://journals.rcsi.science/0041-3771/article/view/140088
- DOI: https://doi.org/10.31857/S0041377123050036
- EDN: https://elibrary.ru/PISDQF
- ID: 140088
Cite item
Abstract
Recovery of the nuclear structure after cell division requires special interactions between the integral proteins of the inner nuclear membrane having a special LEM domain (LEMD), nuclear lamina proteins (lamins) and the conserved BAF protein that serves as a central link in these interactions, providing topological relationships between chromatin and nuclear envelope. The dynamic transformations of these protein ensembles in the mitotic cycle are characterized in detail at the molecular level, however, less attention is paid to the developing germ cells undergoing meiotic divisions, despite of their nuclei, especially in diplotene oocytes, differ significantly in structure from the somatic nucleus. This review summarizes the still relatively scarce experimental data proving the significance of functional interactions between BAF and LEMD proteins for gamete formation, from the selection of germline cells to the transformation of haploid spermatids into morphologically mature spermatozoa.
Keywords
About the authors
I. O. Bogolyubova
Institute of Cytology, Russian Academy of Sciences
Email: dbogol@mail.ru
Russia, 194064, St. Petersburg
D. S. Bogolyubov
Institute of Cytology, Russian Academy of Sciences
Author for correspondence.
Email: dbogol@mail.ru
Russia, 194064, St. Petersburg
References
- Богданов Ю.Ф., Гришаева Т.М. 2020. Консерватизм, изменчивость и эволюция мейоза. М.: Товарищество научных изданий КМК. 345 с. (Bogdanov Yu.F., Grishaeva T.M. 2020. Conservation, variation an evolution of meiosis. Moscow: KMK Scientific Press. 345 p.)
- Дондуа А.К. 2018. Биология развития. СПб.: Изд-во С.-Петерб. ун-та. 812 с. (Dondua A.K. 2018. Developmental biology. Saint Petersburg: Saint Petersburg University Publishing House. 812 p.)
- Alsheimer M., Fecher E., Benavente R. 1998. Nuclear envelope remodelling during rat spermiogenesis: distribution and expression pattern of LAP2/thymopoietins. J. Cell Sci. V. 111. P. 2227. https://doi.org/10.1242/jcs.111.15.2227
- Asencio C., Davidson I.F., Santarella-Mellwig R., Ly-Hartig T.B.N., Mall M., Wallenfang M.R., Mattaj I.W., Gorjánácz M. 2012. Coordination of kinase and phosphatase activities by Lem4 enables nuclear envelope reassembly during mitosis. Cell. V. 150. P. 122. https://doi.org/10.1016/j.cell.2012.04.043
- Bailly C., Vergoten G. 2021. Interaction of obtusilactone B and related butanolide lactones with the barrier-to-autointegration factor 1 (BAF1). A computational study. Curr. Res. Pharmacol. Drug Discov. V. 2: 100059. https://doi.org/10.1016/j.crphar.2021.100059
- Barrales R.R., Forn M., Georgescu P.R., Sarkadi Z., Braun S. 2016. Control of heterochromatin localization and silencing by the nuclear membrane protein Lem2. Genes Dev. V. 30. P. 133. https://doi.org/10.1101/gad.271288.115
- Barton L.J., Lovander K.E., Pinto B.S., Geyer P.K. 2016. Drosophila male and female germline stem cell niches require the nuclear lamina protein Otefin. Dev. Biol. V. 415. P. 75. https://doi.org/10.1016/j.ydbio.2016.05.001
- Barton L.J., Soshnev A.A., Geyer P.K. 2015. Networking in the nucleus: a spotlight on LEM-domain proteins. Curr. Opin. Cell Biol. V. 34. P. 1. https://doi.org/10.1016/j.ceb.2015.03.005
- Bogolyubov D. 2018. Karyosphere (karyosome): a peculiar structure of the oocyte nucleus. Int. Rev. Cell Mol. Biol. V. 337. P. 1. https://doi.org/10.1016/bs.ircmb.2017.12.001
- Brachner A., Foisner R. 2011. Evolvement of LEM proteins as chromatin tethers at the nuclear periphery. Biochem. Soc. Trans. V. 39. P. 1735. https://doi.org/10.1042/BST20110724
- Brachner A., Braun J., Ghodgaonkar M., Castor D., Zlopasa L., Ehrlich V., Jiricny J., Gotzmann J., Knasmüller S., Foisner R. 2012. The endonuclease Ankle-1 requires its LEM and GIY-YIG motifs for DNA cleavage in vivo. J. Cell Sci. V. 125. P. 1048. https://doi.org/10.1242/jcs.098392
- Bradley C.M., Ronning D.R., Ghirlando R., Craigie R., Dyda F. 2005. Structural basis for DNA bridging by barrier-to-autointegration factor. Nat. Struct. Mol. Biol. V. 12. P. 935. https://doi.org/10.1038/nsmb989
- Burla R., La Torre M., Maccaroni K., Verni F., Giunta S., Saggio I. 2020. Interplay of the nuclear envelope with chromatin in physiology and pathology. Nucleus. V. 11. P. 205. https://doi.org/10.1080/19491034.2020.1806661
- Cabanillas R., Cadinanos J., Villameytide J.A., Perez M., Longo J., Richard J.M., Alvarez R., Duran N.S., Illan R., Gonzalez D.J., López-Otín C. 2011. Nestor-Guillermo progeria syndrome: a novel premature aging condition with early onset and chronic development caused by BANF1 mutations. Am. J. Med. Genet. A. V. 155A. P. 2617. https://doi.org/10.1002/ajmg.a.34249
- Cai M., Huang Y., Ghirlando R., Wilson K.L., Craigie R., Clore G.M. 2001. Solution structure of the constant region of nuclear envelope protein LAP2 reveals two LEM-domain structures: one binds BAF and the other binds DNA. EMBO J. V. 20. P. 4399. https://doi.org/10.1093/emboj/20.16.4399
- Cai M., Huang Y., Zheng R., Wei S.-Q., Ghirlando R., Lee M.S., Craigie R., Gronenborn A.M., Clore G.M. 1998. Solution structure of the cellular factor BAF responsible for protecting retroviral DNA from autointegration. Nature Struct. Biol. V. 5. P. 903. https://doi.org/10.1038/2345
- Caputo S., Couprie J., Duband-Goulet I., Kondé E., Lin F., Braud S., Gondry M., Gilquin B., Worman H.J., Zinn-Justin S. 2006. The carboxyl-terminal nucleoplasmic region of MAN1 exhibits a DNA binding winged helix domain. J. Biol. Chem. V. 281. P. 18 208. https://doi.org/10.1074/jbc.M601980200
- Cohen M., Lee K.K., Wilson K.L., Gruenbaum Y. 2001. Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem. Sci. V. 26. P. 41. https://doi.org/10.1016/s0968-0004(00)01727-8
- Correia Soeiro M.N., Vergoten G., Bailly C. 2022. Molecular docking of brazilin and its analogs to barrier-to-autointegration factor 1 (BAF1). Ann. N. Y. Acad. Sci. V. 1511. P. 154. https://doi.org/10.1111/nyas.14742
- Dechat T., Vlcek S., Foisner R. 2000. Review: lamina-associated polypeptide 2 isoforms and related proteins in cell cycle-dependent nuclear structure dynamics. J. Struct. Biol. V. 129. P. 335. https://doi.org/10.1006/jsbi.2000.4212
- Duan T., Cupp R., Geyer P.K. 2021. Drosophila female germline stem cells undergo mitosis without nuclear breakdown. Curr. Biol. V. 31. P. 1450–1462.e3. https://doi.org/10.1016/j.cub.2021.01.033
- Duan T., Green N., Tootle T.L., Geyer P.K. 2020a. Nuclear architecture as an intrinsic regulator of Drosophila female germline stem cell maintenance. Curr. Opin. Insect. Sci. V. 37. P. 30–38. https://doi.org/10.1016/j.cois.2019.11.007
- Duan T., Kitzman S.C., Geyer P.K. 2020b. Survival of Drosophila germline stem cells requires the chromatin-binding protein Barrier-to-autointegration factor. Development. V. 147: dev186171. https://doi.org/10.1242/dev.186171
- Elkhatib R.A., Paci M., Boissier R., Longepied G., Auguste Y., Achard V., Bourgeois P., Levy N., Branger N., Mitchell M.J., Metzler-Guillemain C. 2017. LEM-domain proteins are lost during human spermiogenesis but BAF and BAF-L persist. Reproduction. V. 154. P. 387. https://doi.org/10.1530/REP-17-0358
- Foisner R. 2003. Cell cycle dynamics of the nuclear envelope. Scientific World J. V. 3. P. 1. https://doi.org/10.1100/tsw.2003.06
- Furukawa K. 1999. LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J. Cell Sci. V. 112. P. 2485. https://doi.org/10.1242/jcs.112.15.2485
- Furukawa K., Sugiyama S., Osouda S., Goto H., Inagaki M., Horigome T., Omata S., McConnell M., Fisher P.A., Nishida Y. 2003. Barrier-to-autointegration factor plays crucial roles in cell cycle progression and nuclear organization in Drosophila. J. Cell Sci. V. 116. P. 3811. https://doi.org/10.1242/jcs.00682
- Gant T.M., Harris C.A., Wilson K.L. 1999. Roles of LAP2 proteins in nuclear assembly and DNA replication: truncated LAP2β proteins alter lamina assembly, envelope formation, nuclear size, and DNA replication efficiency in Xenopus laevis extracts. J. Cell Biol. V. 144. P. 1083. https://doi.org/10.1083/jcb.144.6.1083
- Gorjánácz M., Klerkx E.P., Galy V., Santarella R., López-Iglesias C., Askjaer P., Mattaj I.W. 2007. Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. EMBO J. V. 26. P. 132. https://doi.org/10.1038/sj.emboj.7601470
- Göb E., Schmitt J., Benavente R., Alsheimer M. 2010. Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS One. V. 5: e12072. https://doi.org/10.1371/journal.pone.0012072
- Haraguchi T., Koujin T., Segura-Totten M., Lee K.K., Matsuoka Y., Yoneda Y., Wilson K.L., Hiraoka Y. 2001. BAF is required for emerin assembly into the reforming nuclear envelope. J. Cell Sci. V. 114. P. 4575. https://doi.org/10.1242/jcs.114.24.4575
- Hirano Y., Segawa M., Ouchi F.S., Yamakawa Y., Furukawa K., Takeyasu K., Horigome T. 2005. Dissociation of emerin from barrier-to-autointegration factor is regulated through mitotic phosphorylation of emerin in a Xenopus egg cell-free system. J. Biol. Chem. V. 280. P. 39925. https://doi.org/10.1074/jbc.m503214200
- Holaska J.M., Lee K.K., Kowalski A.K., Wilson K.L. 2003. Transcriptional repressor germ cell-less (GCL) and barrier-to-autointegration factor (BAF) compete for binding to emerin in vitro. J. Biol. Chem. V. 278. P. 6969. https://doi.org/10.1074/jbc.M208811200
- Huber M.D., Guan T., Gerace L. 2009. Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in regulation of extracellular signal-regulated kinase signaling in myoblast differentiation. Mol. Cell Biol. V. 29. P. 5718. https://doi.org/10.1128/MCB.00270-09
- Jamin A., Wiebe M.S. 2015. Barrier to autointegration factor (BANF1): interwoven roles in nuclear structure, genome integrity, innate immunity, stress responses and progeria. Curr. Opin. Cell Biol. V. 34. P. 61. https://doi.org/10.1016/j.ceb.2015.05.006
- Jiang X., Xia L., Chen D., Yang Y., Huang H., Yang L., Zhao Q., Shen L., Wang J., Chen D. 2008. Otefin, a nuclear membrane protein, determines the fate of germline stem cells in Drosophila via interaction with Smad complexes. Dev. Cell. V. 14. P. 494. https://doi.org/10.1016/j.devcel.2008.02.018
- Lancaster O.M., Cullen C.F., Ohkura H. 2007. NHK-1 phosphorylates BAF to allow karyosome formation in the Drosophila oocyte nucleus. J. Cell Biol. V. 179. P. 817. https://doi.org/10.1083/jcb.200706067
- Leatherman J.L., Levin L., Boero J., Jongens T.A. 2002. germ cell-less Acts to repress transcription during the establishment of the Drosophila germ cell lineage. Curr. Biol. V. 12. P. 1681. https://doi.org/10.1016/S0960-9822(02)01182-X
- Lee K.K., Gruenbaum Y., Spann P., Liu J., Wilson K.L. 2000. C. elegans nuclear envelope proteins emerin, MAN1, lamin, and nucleoporins reveal unique timing of nuclear envelope breakdown during mitosis. Mol. Biol. Cell. V. 11. P. 3089. https://doi.org/10.1091/mbc.11.9.3089
- Lee M.S., Craigie R. 1998. A previously unidentified host protein protects retroviral DNA from autointegration. Proc. Natl. Acad. Sci. USA. V. 95. P. 1528. https://doi.org/10.1073/pnas.95.4.1528
- Li J., Hu B., Fang L., Gao Y., Shi S., He H., Liu X., Yuan C. 2018. Barrier-to-autointegration factor 1: A novel biomarker for gastric cancer. Oncol. Lett. V. 16. P. 6488. https://doi.org/10.3892/ol.2018.9432
- Li J., Wang T., Pei L., Jing J., Hu W., Sun T., Liu H. 2017. Expression of VRK1 and the downstream gene BANF1 in esophageal cancer. Biomed. Pharmacother. V. 89. P. 1086. https://doi.org/10.1016/j.biopha.2017.02.095
- Liu J., Rolef-Ben Shahar T., Riemer D., Treinin M., Spann P., Weber K., Fire A., Gruenbaum Y. 2000. Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell. V. 11. P. 3937. https://doi.org/10.1091/mbc.11.11.3937
- Marcelot A., Petitalot A., Ropars V., Le Du M.H., Samson C., Dubois S., Hoffmann G., Miron S., Cuniasse P., Marquez J.A., Thai R., Theillet F.X., Zinn-Justin S. 2021a. Di-phosphorylated BAF shows altered structural dynamics and binding to DNA, but interacts with its nuclear envelope partners. Nucleic Acids Res. V. 49. P. 3841. https://doi.org/10.1093/nar/gkab184
- Marcelot A., Worman H.J., Zinn-Justin S. 2021b. Protein structural and mechanistic basis of progeroid laminopathies. FEBS J. V. 288. P. 2757.
- https://doi.org/10.1111/febs.15526
- Marcelot A., Zinn-Justin S., Cuniasse P. 2022. The conformation of the intrinsically disordered N-terminal region of Barrier-to-autointegration factor (BAF) is regulated by pH and phosphorylation. J. Mol. Biol. V. 435: 167888. https://doi.org/10.1016/j.jmb.2022.167888
- Martins S., Eikvar S., Furukawa K., Collas P. 2003. HA95 and LAP2β mediate a novel chromatin–nuclear envelope interaction implicated in initiation of DNA replication. J. Cell Biol. V. 160. P. 177. https://doi.org/10.1083/jcb.200210026
- Mattout-Drubezki A., Gruenbaum Y. 2003. Dynamic interactions of nuclear lamina proteins with chromatin and transcriptional machinery. Cell Mol. Life Sci. V. 60. P. 2053. https://doi.org/10.1007/s00018-003-3038-3
- Molitor T.P., Traktman P. 2014. Depletion of the protein kinase VRK1 disrupts nuclear envelope morphology and leads to BAF retention on mitotic chromosomes. Mol. Biol. Cell. V. 25. P. 891. https://doi.org/10.1091/mbc.E13-10-0603
- Naetar N., Ferraioli S., Foisner R. 2017. Lamins in the nuclear interior – life outside the lamina. J. Cell Sci. V. 130. P. 2087. https://doi.org/10.1242/jcs.203430
- Nili E., Cojocaru G.S., Kalma Y., Ginsberg D., Copeland N.G., Gilbert D.J., Jenkins N.A., Berger R., Shaklai S., Amariglio N., Brok-Simoni F., Simon A.J., Rechavi G. 2001. Nuclear membrane protein, LAP2β, mediates transcriptional repression alone and together with its binding partner GCL (germ-cell-less). J. Cell Sci. V. 114. P. 3297. https://doi.org/10.1242/jcs.114.18.3297
- Paquet N., Box J.K., Ashton N.W., Suraweera A., Croft L.V., Urquhart A.J., Bolderson E., Zhang S.D., O’Byrne K.J., Richard D.J. 2014. Néstor-Guillermo Progeria Syndrome: A biochemical insight into Barrier-to-autointegration factor 1, alanine 12 threonine mutation. BMC Mol. Biol. V. 15: 27. https://doi.org/10.1186/s12867-014-0027-z
- Pereira C.D., Serrano J.B., Martins F., da Cruz E. Silva O.A.B., Rebelo S. 2019. Nuclear envelope dynamics during mammalian spermatogenesis: new insights on male fertility. Biol. Rev. Camb. Philos. Soc. V. 94. P. 1195. https://doi.org/10.1111/brv.12498
- Pekovic V., Harborth J., Broers J.L., Ramaekers F.C., van Engelen B., Lammens M., von Zglinicki T., Foisner R., Hutchison C., Markiewicz E. 2007. Nucleoplasmic LAP2α–lamin A complexes are required to maintain a proliferative state in human fibroblasts. J. Cell Biol. V. 176. P. 163. https://doi.org/10.1083/jcb.200606139
- Puente X.S., Quesada V., Osorio F.G., Cabanillas R., Cadiñanos J., Fraile J.M., Ordóñez G.R., Puente D.A., Gutiérrez-Fernández A., Fanjul-Fernández M., Lévy N., Freije J.M.P., López-Otín C. 2011. Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am. J. Hum. Genet. V. 88. P. 650. https://doi.org/10.1016/j.ajhg.2011.04.010
- Qi R., Xu N., Wang G., Ren H., Li S., Lei J., Lin Q., Wang L., Gu X., Zhang H., Jiang Q., Zhang C. 2015. The laminA/C-LAP2α-BAF1 protein complex regulates mitotic spindle assembly and positioning. J. Cell Sci. V. 128. P. 2830. https://doi.org/10.1242/jcs.164566
- Rose M., Bai B., Tang M., Cheong C.M., Beard S., Burgess J.T., Adams M.N., O’Byrne K.J., Richard D.J., Gandhi N.S., Bolderson E. 2021. The impact of rare human variants on barrier-to-auto-integration factor 1 (Banf1) structure and function. Front. Cell Dev. Biol. V. 9: 775441. https://doi.org/10.3389/fcell.2021.775441
- Samson C., Petitalot A., Celli F., Herrada I., Ropars V., Le Du M.H., Nhiri N., Jacquet E., Arteni A.-A., Buendia B., Zinn-Justin S. 2018. Structural analysis of the ternary complex between lamin A/C, BAF and emerin identifies an interface disrupted in autosomal recessive progeroid diseases. Nucleic Acids Res. V. 46. P. 10460. https://doi.org/10.1093/nar/gky736
- Samwer M., Schneider M.W.G., Hoefler R., Schmalhorst P.S., Jude J.G., Zuber J., Gerlich D.W. 2017. DNA cross-bridging shapes a single nucleus from a set of mitotic chromosomes. Cell. V. 170. P. 956–972.e923. https://doi.org/10.1016/j.cell.2017.07.038
- Segura-Totten M., Kowalski A.K., Craigie R., Wilson K.L. 2002. Barrier-to-autointegration factor: major roles in chromatin decondensation and nuclear assembly. J. Cell Biol. V. 158. P. 475. https://doi.org/10.1083/jcb.200202019
- Segura-Totten M., Wilson K.L. 2004. BAF: roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol. V. 14. P. 261. https://doi.org/10.1016/j.tcb.2004.03.004
- Serrano J.B., Martins F., Sousa J.C., Pereira C.D., van Pelt A.M., Rebelo S., da Cruz E., Silva O.A. 2017. Descriptive analysis of LAP1 distribution and that of associated proteins throughout spermatogenesis. Membranes (Basel). V. 7: 22. https://doi.org/10.3390/membranes7020022
- Shen Q., Eun J.W., Lee K., Kim H.S., Yang H.D., Kim S.Y., Lee E.K., Kim T., Kang K., Kim S., Min D.H., Oh S.N., Lee Y.J., Moon H., Ro S.W. et al. 2018. Barrier to autointegration factor 1, procollagen-lysine, 2-oxoglutarate 5-dioxygenase 3, and splicing factor 3b subunit 4 as early-stage cancer decision markers and drivers of hepatocellular carcinoma. Hepatology. V. 67. P. 1360. https://doi.org/10.1002/hep.29606
- Snyers L., Erhart R., Laffer S., Pusch O., Weipoltshammer K., Schöfer C. 2018. LEM4/ANKLE-2 deficiency impairs post-mitotic re-localization of BAF, LAP2α and LaminA to the nucleus, causes nuclear envelope instability in telophase and leads to hyperploidy in HeLa cells. Eur. J. Cell Biol. V. 97. P. 63. https://doi.org/10.1016/j.ejcb.2017.12.001
- Snyers L., Löhnert R., Weipoltshammer K., Schöfer C. 2022. Emerin prevents BAF-mediated aggregation of lamin A on chromosomes in telophase to allow nuclear membrane expansion and nuclear lamina formation. Mol. Biol Cell. V. 33: ar137. https://doi.org/10.1091/mbc.E22-01-0007
- Torras-Llort M., Medina-Giró S., Escudero-Ferruz P., Lipinszki Z., Moreno-Moreno O., Karman Z., Przewloka M.R., Azorín F. 2020. A fraction of barrier-to-autointegration factor (BAF) associates with centromeres and controls mitosis progression. Commun. Biol. V. 3: 454. https://doi.org/10.1038/s42003-020-01182-y
- Vivante A., Brozgol E., Bronshtein I., Levi V., Garini Y. 2019. Chromatin dynamics governed by a set of nuclear structural proteins. Genes Chromosomes Cancer. V. 58. P. 437. https://doi.org/10.1002/gcc.22719
- Wagner N., Kagermeier B., Loserth S., Krohne G. 2006. The Drosophila melanogaster LEM-domain protein MAN1. Eur. J. Cell Biol. V. 85. P. 91. https://doi.org/10.1016/j.ejcb.2005.10.002
- Wagner N., Krohne G. 2007. LEM-domain proteins: new insights into lamin-interacting proteins. Int. Rev. Cytol. V. 261. P. 1. https://doi.org/10.1016/S0074-7696(07)61001-8
- Wang X., Xu S., Rivolta C., Li L.Y., Peng G.-H., Swain P.K., Sung C.-H., Swaroop A., Berson E.L., Dryja T.P., Chen S. 2002. Barrier to autointegration factor interacts with the cone-rod homeobox and represses its transactivation function. J. Biol. Chem. V. 277. P. 43288. https://doi.org/10.1074/jbc.M207952200
- Wong X., Melendez-Perez A.J., Reddy K.L. 2022. The nuclear lamina. Cold Spring Harb. Perspect. Biol. V. 14: a040113. https://doi.org/10.1101/cshperspect.a040113
- Zetka M., Paouneskou D., Jantsch V. 2020. The nuclear envelope, a meiotic jack-of-all-trades. Curr. Opin. Cell Biol. V. 64. P. 34. https://doi.org/10.1016/j.ceb.2019.12.010
- Zhang G. 2020. Expression and prognostic significance of BANF1 in triple-negative breast cancer. Cancer Manag. Res. V. 12. P. 145. https://doi.org/10.2147/CMAR.S229022
- Zheng R., Ghirlando R., Lee M.S., Mizuuchi K., Krause M., Craigie R. 2000. Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc. Natl. Acad. Sci. USA. V. 97. P. 8997. https://doi.org/10.1073/pnas.150240197
- Zhuang X., Semenova E., Maric D., Craigie R. 2014. Dephosphorylation of barrier-to-autointegration factor by protein phosphatase 4 and its role in cell mitosis. J. Biol. Chem. V. 289. P. 1119. https://doi.org/10.1074/jbc.M113.492777