Dephosphorylation of barrier-to-autointegration factor by protein phosphatase 4 and its role in cell mitosis

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 1119-1127

  Zhuang, Xiaolei ^a,c   Semenova, Elena ^a   Maric, Dragan ^b   Craigie, Robert ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MITOSIS; CELL-CYCLE PROGRESSION; CELLULAR FUNCTION; DEPHOSPHORYLATIONS; ESSENTIAL PROTEINS; NUCLEAR ENVELOPE; NUCLEAR LAMINA; PROTEIN PHOSPHATASE;

BARIUM COMPOUNDS; PHOSPHORYLATION;

PROTEINS;

BARRIER TO AUTOINTEGRATION FACTOR; PHOSPHATASE; PHOSPHATASE 4; PHOSPHOPROTEIN; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CELLULAR DISTRIBUTION; CHROMOSOME; CONTROLLED STUDY; DNA INTEGRATION; HUMAN; HUMAN CELL; MITOSIS; MUTATION; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; TELOPHASE;

BAF; BAF BANF1; BAF BANF1 PP4C; CELL CYCLE; CHROMOSOMES; MITOSIS; NUCLEAR MEMBRANE; PHOSPHORYLATION;

BLOTTING, WESTERN; CELL CYCLE; DNA-BINDING PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, CONFOCAL; MITOSIS; MUTATION; NUCLEAR PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SERINE;

EID: 84891917410     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.492777     Document Type: Article

References (39)

1. Lee, M. S., and Craigie, R. (1998) A previously unidentified host protein protects retroviralDNAfrom autointegration. Proc. Natl. Acad. Sci. U.S.A. 95, 1528-1533
2. Umland, T. C., Wei, S. Q., Craigie, R., and Davies, D. R. (2000) Structural basis of DNA bridging by barrier-to-autointegration factor. Biochemistry 39, 9130-9138
3. Cai, M., Huang, Y., Zheng, R., Wei, S. Q., Ghirlando, R., Lee, M. S., Craigie, R., Gronenborn, A. M., and Clore, G. M. (1998) Solution structure of the cellular factor BAF responsible for protecting retroviral DNA from autointegration. Nat. Struct. Biol. 5, 903-909
4. Zheng, R., Ghirlando, R., Lee, M. S., Mizuuchi, K., Krause, M., and Craigie, R. (2000) Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc. Natl. Acad. Sci. U.S.A. 97, 8997-9002
5. Bradley, C. M., Ronning, D. R., Ghirlando, R., Craigie, R., and Dyda, F. (2005) Structural basis for DNA bridging by barrier-to-autointegration factor. Nat. Struct. Mol. Biol. 12, 935-936
6. Skoko, D., Li, M., Huang, Y., Mizuuchi, M., Cai, M., Bradley, C. M., Pease, P. J., Xiao, B., Marko, J. F., Craigie, R., and Mizuuchi, K. (2009) Barrier-toautointegration factor (BAF) condenses DNA by looping. Proc. Natl. Acad. Sci. U.S.A. 106, 16610-16615
7. Furukawa, K. (1999) LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J. Cell Sci. 112, 2485-2492
8. Lee, K. K., Haraguchi, T., Lee, R. S., Koujin, T., Hiraoka, Y., and Wilson, K. L. (2001) Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J. Cell Sci. 114, 4567-4573
9. Shumaker, D. K., Lee, K. K., Tanhehco, Y. C., Craigie, R., and Wilson, K. L. (2001) LAP2 binds to BAF center dot DNA complexes: requirement for the LEM domain and modulation by variable regions. EMBO J. 20, 1754-1764
10. Mansharamani, M., and Wilson, K. L. (2005) Direct binding of nuclear membrane protein MAN1 to emerin in vitro and two modes of binding to barrier-to-autointegration factor. J. Biol. Chem. 280, 13863-13870
11. Cai, M., Huang, Y., Suh, J. Y., Louis, J. M., Ghirlando, R., Craigie, R., and Clore, G. M. (2007) Solution NMR structure of the barrier-to- autointegration factor-emerin complex. J. Biol. Chem. 282, 14525-14535
12. Furukawa, K., Sugiyama, S., Osouda, S., Goto, H., Inagaki, M., Horigome, T., Omata, S., McConnell, M., Fisher, P. A., and Nishida, Y. (2003) Barrierto-autointegration factor plays crucial roles in cell cycle progression and nuclear organization in Drosophila. J. Cell Sci. 116, 3811-3823
13. Margalit, A., Segura-Totten, M., Gruenbaum, Y., and Wilson, K. L. (2005) Barrier-to-autointegration factor is required to segregate and enclose chromosomes within the nuclear envelope and assemble the nuclear lamina. Proc. Natl. Acad. Sci. U.S.A. 102, 3290-3295
14. Gorjánácz, M., Klerkx, E. P., Galy, V., Santarella, R., López-Iglesias, C., Askjaer, P., and Mattaj, I. W. (2007) Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. EMBO J. 26, 132-143
15. Haraguchi, T., Kojidani, T., Koujin, T., Shimi, T., Osakada, H., Mori, C., Yamamoto, A., and Hiraoka, Y. (2008) Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J. Cell Sci. 121, 2540-2554
16. Bengtsson, L., and Wilson, K. L. (2006) Barrier-to-autointegration factor phosphorylation on Ser-4 regulates emerin binding to laminAin vitro and emerin localization in vivo. Mol. Biol. Cell 17, 1154-1163
17. Nichols, R. J., Wiebe, M. S., and Traktman, P. (2006) The vaccinia-related kinases phosphorylate the N terminus of BAF, regulating its interaction with DNA and its retention in the nucleus. Mol. Biol. Cell 17, 2451-2464
18. Asencio, C., Davidson, I. F., Santarella-Mellwig, R., Ly-Hartig, T. B., Mall, M., Wallenfang, M. R., Mattaj, I. W., and Gorjánácz, M. (2012) Coordination of kinase and phosphatase activities by Lem4 enables nuclearenvelope reassembly during mitosis. Cell 150, 122-135
19. Nakada, S., Chen, G. I., Gingras, A. C., and Durocher, D. (2008) PP4 is a gamma H2AX phosphatase required for recovery from the DNA damage checkpoint. EMBO Rep. 9, 1019-1026
20. Dechat, T., Gajewski, A., Korbei, B., Gerlich, D., Daigle, N., Haraguchi, T., Furukawa, K., Ellenberg, J., and Foisner, R. (2004) LAP2-and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. J. Cell Sci. 117, 6117-6128
21. Cozzone, A. J. (1988) Protein-phosphorylation in prokaryotes. Ann. Rev. Microbiol. 42, 97-125
22. Barford, D., Das, A. K., and Egloff, M. P. (1998) The structure and mechanism of protein phosphatases: Insights into catalysis and regulation. Annu. Rev. Biophys. Biomol. Struct. 27, 133-164
23. Honkanen, R. E., and Golden, T. (2002) Regulators of serine/threonine protein phosphatases at the dawn of a clinical era? Curr. Med. Chem. 9, 2055-2075
24. Virshup, D. M., and Shenolikar, S. (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol. Cell 33, 537-545
25. Cohen, P. T. (2005) Protein phosphatase 4: a multifunctional protein serine/threonine phosphatase sensitive to antitumour drugs. FEBS J. 272, 303-303
26. Cohen, P. T., Philp, A., and Vázquez-Martin, C. (2005) Protein phosphatase 4-from obscurity to vital functions. FEBS Lett. 579, 3278-3286
27. 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., and López-Otín, C. (2011) Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am. J. Hum. Genet. 88, 650-656
28. Haraguchi, T., Koujin, T., Osakada, H., Kojidani, T., Mori, C., Masuda, H., and Hiraoka, Y. (2007) Nuclear localization of barrier-to-autointegration factor is correlated with progression of S phase in human cells. J. Cell Sci. 120, 1967-1977
29. Bollen, M., Gerlich, D. W., and Lesage, B. (2009) Mitotic phosphatases: from entry guards to exit guides. Trends Cell Biol. 19, 531-541
30. Carnegie, G. K., Sleeman, J. E., Morrice, N., Hastie, C. J., Peggie, M. W., Philp, A., Lamond, A. I., and Cohen, P. T. (2003) Protein phosphatase 4 interacts with the Survival of Motor Neurons complex and enhances the temporal localisation of snRNPs. J. Cell Sci. 116, 1905-1913
31. Chowdhury, D., Xu, X., Zhong, X., Ahmed, F., Zhong, J., Liao, J., Dykxhoorn, D. M., Weinstock, D. M., Pfeifer, G. P., and Lieberman, J. (2008) A PP4-phosphatase complex dephosphorylates-H2AX generated during DNA replication. Mol. Cell 31, 33-46
32. Montes de Oca, R., Shoemaker, C. J., Gucek, M., Cole, R. N., and Wilson, K. L. (2009) Barrier-to-autointegration factor proteome reveals chromatin-regulatory partners. PLoS One 4, e7050
33. Huang, Y., Cai, M., Clore, G. M., and Craigie, R. (2011) No interaction of barrier-to-autointegration factor (BAF) with HIV-1 MA, cone-rod homeobox (Crx) or MAN1-C in the absence of DNA. PLoS One 6, e25123
34. Haraguchi, T., Koujin, T., Hayakawa, T., Kaneda, T., Tsutsumi, C., Imamoto, N., Akazawa, C., Sukegawa, J., Yoneda, Y., and Hiraoka, Y. (2000) Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes. J. Cell Sci. 113, 779-794
35. Segura-Totten, M., Kowalski, A. K., Craigie, R., and Wilson, K. L. (2002) Barrier-to-autointegration factor: major roles in chromatin decondensation and nuclear assembly. J. Cell Biol. 158, 475-485
36. Brandt, A., Papagiannouli, F., Wagner, N., Wilsch-Bräuninger, M., Braun, M., Furlong, E. E., Loserth, S., Wenzl, C., Pilot, F., Vogt, N., Lecuit, T., Krohne, G., and Grosshans, J. (2006) Developmental control of nuclear size and shape by kugelkern and kurzkern. Curr. Biol. 16, 543-552
37. Gupton, S. L., Collings, D. A., and Allen, N. S. (2006) Endoplasmic reticulum targeted GFP reveals ER organization in tobacco NT-1 cells during cell division. Plant Physiol. Biochem. 44, 95-105
38. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K., and Wilson, K. L. (2005) The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31
39. Goldman, R. D., Shumaker, D. K., Erdos, M. R., Eriksson, M., Goldman, A. E., Gordon, L. B., Gruenbaum, Y., Khuon, S., Mendez, M., Varga, R., and Collins, F. S. (2004) Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. U.S.A. 101, 8963-8968