SUMOylation regulates polo-like kinase 1-interacting Checkpoint Helicase (PICH) during mitosis

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3269-3276

  Sridharan, Vinidhra ^a   Park, Hyewon ^a   Ryu, Hyunju ^a   Azuma, Yoshiaki ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; PROTEINS; SUBSTRATES;

CHROMOSOME SEGREGATION; ENZYMATIC ACTIVITIES; MITOTIC CHROMOSOMES; POLO-LIKE KINASE; POLY(ADP RIBOSE) POLYMERASE 1; PROTEIN INHIBITORS; SMALL UBIQUITIN-LIKE MODIFIERS; SPECIFIC BINDING;

CHROMOSOMES;

ADENOSINE TRIPHOSPHATASE; COMPLEMENTARY DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN PICH; PROTEIN TOPOIIALPHA; STAT PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DNA HELICASE; DNA TOPOISOMERASE II ALPHA; ERCC6L2 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN; PROTEIN BINDING; SUMO2 PROTEIN, HUMAN; SUMO3 PROTEIN, HUMAN; TUMOR ANTIGEN; UBIQUITIN;

ANIMAL CELL; ARTICLE; CENTROMERE; CHROMOSOME ANALYSIS; DNA BINDING; EGG; IN VITRO STUDY; MITOSIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SPECIES CONSERVATION; SUMOYLATION; XENOPUS LAEVIS; ANIMAL; HUMAN; METABOLISM; PROTEIN TRANSPORT; XENOPUS;

EUKARYOTA;

ANIMALS; ANTIGENS, NEOPLASM; CENTROMERE; DNA HELICASES; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; HUMANS; MITOSIS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN TRANSPORT; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; UBIQUITINS; XENOPUS;

EID: 84922384292     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C114.601906     Document Type: Article

References (39)

1. Goodson, M.L., Hong, Y., Rogers, R., Matunis, M.J., Park-Sarge, O. K., and Sarge, K. D. (2001) SUMO-1 modification regulates the DNA binding activity of heat shock transcription factor 2, a promyelocytic leukemia nuclear body associated transcription factor. J. Biol. Chem. 276, 18513-18518
2. Hong, Y., Rogers, R., Matunis, M. J., Mayhew, C. N., Goodson, M. L., Park-Sarge, O. K., and Sarge, K. D. (2001) Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J. Biol. Chem. 276, 40263-40267
3. Matunis, M. J., Wu, J., and Blobel, G. (1998) SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 140, 499-509
4. Pichler, A., and Melchior, F. (2002) Ubiquitin-related modifier SUMO1 and nucleocytoplasmic transport. Traffic 3, 381-387
5. Hardeland, U., Steinacher, R., Jiricny, J., and Schär, P. (2002) Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21, 1456-1464
6. Geiss-Friedlander, R., and Melchior, F. (2007) Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell. Biol. 8, 947-956
7. Dasso, M. (2008) Emerging roles of the SUMO pathway in mitosis. Cell Div. 3, 5
8. Watts, F. Z. (2007) The role of SUMO in chromosome segregation. Chromosoma 116, 15-20
9. Azuma, Y., Arnaoutov, A., Anan, T., and Dasso, M. (2005) PIASy mediates SUMO-2 conjugation of Topoisomerase-II on mitotic chromosomes. EMBOJ. 24, 2172-2182
10. Cubeñas-Potts, C, Goeres, J. D., and Matunis, M. J. (2013) SENP1 and SENP2 affect spatial and temporal control of sumoylation in mitosis. Mol. Biol. Cell 24, 3483-3495
11. Azuma, Y., Arnaoutov, A., and Dasso, M. (2003) SUMO-2/3 regulates topoisomerase II in mitosis. J. Cell Biol. 163, 477-487
12. Ryu, H., Al-Ani, G., Deckert, K., Kirkpatrick, D., Gygi, S. P., Dasso, M., and Azuma, Y. (2010) PIASy mediates SUMO-2/3 conjugation of poly(ADP-ribose) polymerase 1 (PARP1) on mitotic chromosomes. J. Biol. Chem. 285, 14415-14423
13. Bachant, J., Alcasabas, A., Blat, Y., Kleckner, N, and Elledge, S. J. (2002) The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. cell 9, 1169-1182
14. Ryu, H., Furuta, M., Kirkpatrick, D., Gygi, S. P., and Azuma, Y. (2010) PIASy-dependent SUMOylation regulates DNA topoisomerase IIa activity. J. Cell Biol. 191, 783-794
15. Porter, A. C., and Farr, C. J. (2004) Topoisomerase II: untangling its contribution at the centromere. Chromosome Res. 12, 569-583
16. Hassa, P. O., and Hottiger, M. O. (2008) The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci. 13, 3046-3082
17. Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G., and Chen, Y. (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 14373-14378
18. Kerscher, O. (2007) SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 8, 550-555
19. Minty, A., Dumont, X., Kaghad, M., and Caput, D. (2000) Covalent modification of p73α by SUMO-1: two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J. Biol. Chem. 275, 36316-36323
20. Lin, D. Y., Huang, Y. S., Jeng, J. C, Kuo, H. Y., Chang, C. C, Chao, T. T., Ho, C. C, Chen, Y. C, Lin, T. P., Fang, H. I., Hung, C. C, Suen, C. S., Hwang, M. J., Chang, K. S., Maul, G. G., and Shih, H. M. (2006) Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 24, 341-354
21. Steinacher, R., and Schär, P. (2005) Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 15, 616-623
22. Hoege, C, Pfander, B., Moldovan, G. L., Pyrowolakis, G., and Jentsch, S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141
23. Baumann, C, Körner, R., Hofmann, K., and Nigg, E. A. (2007) PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 128, 101-114
24. Kurasawa, Y., and Yu-Lee, L. Y. (2010) PICH and cotargeted Plk1 coordinately maintain prometaphase chromosome arm architecture. Mol. Biol. Cell 21, 1188-1199
25. Leng, M., Bessuso, D., Jung, S. Y., Wang, Y., and Qin, J. (2008) Targeting Plk1 to chromosome arms and regulating chromosome compaction by the PICH ATPase. Cell Cycle 7, 1480-1489
26. Kelly, A. E., Ghenoiu, C, Xue, J. Z., Zierhut, C, Kimura, H., and Funabiki, H. (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330, 235-239
27. Kornbluth, S., Yang, J., and Powers, M. (2006) Analysis of the cell cycle using Xenopus egg extracts. Curr. Protoc. Cell Biol. Chapter 11, Unit 11.11 10.1002/0471143030.cb1111s29
28. Ryu, H., and Azuma, Y. (2010) Rod/Zw10 complex is required for PIASγ-dependent centromeric SUMOylation. J. Biol. Chem. 285, 32576-32585
29. Gareau, J. R., and Lima, C. D. (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell. Biol. 11, 861-871
30. Ke, Y., Huh, J. W., Warrington, R., Li, B., Wu, N., Leng, M., Zhang, J., Ball, H. L., Li, B., and Yu, H. (2011) PICH and BLM limit histone association with anaphase centromeric DNA threads and promote their resolution. EMBO J. 30, 3309-3321
31. Chan, K. L., North, P. S., and Hickson, I. D. (2007) BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 26, 3397-3409
32. Ying, S., and Hickson, I. D. (2011) Fanconi anaemia proteins are associated with sister chromatid bridging in mitosis. Int. J. Hematol. 93, 440-445
33. Kaulich, M., Cubizolles, F., and Nigg, E. A. (2012) On the regulation, function, and localization of the DNA-dependent AT Pase PICH. Chromosoma 121, 395-408
34. Sampson, D. A., Wang, M., and Matunis, M. J. (2001) The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276, 21664-21669
35. Eladad, S., Ye, T. Z., Hu, P., Leversha, M., Beresten, S., Matunis, M. J., and Ellis, N. A. (2005) Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum. Mol. Genet. 14, 1351-1365
36. Wang, L. H., Schwarzbraun, T., Speicher, M. R., and Nigg, E. A. (2008) Persistence of DNA threads in human anaphase cells suggests late completion of sister chromatid decatenation. Chromosoma 117, 123-135
37. Agostinho, M., Santos, V., Ferreira, F., Costa, R., Cardoso, J., Pinheiro, I., Rino, J., Jaffray, E., Hay, R. T., and Ferreira, J. (2008) Conjugation of human topoisomerase 2α with small ubiquitin-like modifiers 2/3 in response to topoisomerase inhibitors: cell cycle stage and chromosome domain specificity. Cancer Res. 68, 2409-2418
38. Biebricher, A., Hirano, S., Enzlin, J. H, Wiechens, N, Streicher, W. W., Huttner, D., Wang, L. H, Nigg, E. A., Owen-Hughes, T., Liu, Y., Peterman, E., Wuite, G. J., and Hickson, I. D. (2013) PICH: a DNA translocase specially adapted for processing anaphase bridge DNA. Mol. Cell 51, 691-701
39. Nathan, D., Ingvarsdottir, K., Sterner, D. E., Bylebyl, G. R., Dokmanovic, M., Dorsey, J. A., Whelan, K. A., Krsmanovic, M., Lane, W. S., Meluh, P. B., Johnson, E. S., and Berger, S. L. (2006) Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev. 20, 966-976