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Protein & Cell

, Volume 1, Issue 11, pp 999–1010 | Cite as

The substrates of Plk1, beyond the functions in mitosis

  • X. Shawn Liu
  • Bing Song
  • Xiaoqi LiuEmail author
Review

Abstract

Polo-like kinase 1 (Plk1) is a key regulator of cell division in eukaryotic cells. In this short review, we briefly summarized the well-established functions modulated by Plk1 during mitosis. Beyond mitosis, we focused mainly on the unexpected processes in which Plk1 emerges as a critical player, including microtubule dynamics, DNA replication, chromosome dynamics, p53 regulation, and recovery from the G2 DNA-damage checkpoint. Our discussion is mainly based on the critical substrates targeted by Plk1 during these cellular events and the functional significance associated with each phosphorylation event.

Keywords

Polo-like kinase 1 phosphorylation substrates 

References

  1. Aggarwal, B.D., and Calvi, B.R. (2004). Chromatin regulates origin activity in Drosophila follicle cells. Nature 430, 372–376.CrossRefGoogle Scholar
  2. Alvarez-Fernández, M., Halim, V.A., Krenning, L., Aprelia, M., Mohammed, S., Heck, A.J., and Medema, R.H. (2010). Recovery from a DNA-damage-induced G2 arrest requires Cdk-dependent activation of FoxM1. EMBO Rep 11, 452–458.CrossRefGoogle Scholar
  3. Ando, K., Ozaki, T., Yamamoto, H., Furuya, K., Hosoda, M., Hayashi, S., Fukuzawa, M., and Nakagawara, A. (2004). Polo-like kinase 1 (Plk1) inhibits p53 function by physical interaction and phosphorylation. J Biol Chem 279, 25549–25561.CrossRefGoogle Scholar
  4. Bartek, J., and Lukas, J. (2007). DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19, 238–245.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. Baumann, P., and Cech, T.R. (2001). Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292, 1171–1175.CrossRefGoogle Scholar
  7. Brunner, D., and Nurse, P. (2000). CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell 102, 695–704.CrossRefGoogle Scholar
  8. Budde, P.P., Kumagai, A., Dunphy, W.G., and Heald, R. (2001). Regulation of Op18 during spindle assembly in Xenopus egg extracts. J Cell Biol 153, 149–158.CrossRefGoogle Scholar
  9. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J. P., Sedivy, J.M., Kinzler, K.W., and Vogelstein, B. (1998). Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497–1501.CrossRefGoogle Scholar
  10. Casenghi, M., Meraldi, P., Weinhart, U., Duncan, P.I., Körner, R., and Nigg, E.A. (2003). Polo-like kinase 1 regulates Nlp, a centrosome protein involved in microtubule nucleation. Dev Cell 5, 113–125.CrossRefGoogle Scholar
  11. Choi, J.H., Bertram, P.G., Drenan, R., Carvalho, J., Zhou, H.H., and Zheng, X.F. (2002). The FKBP12-rapamycin-associated protein (FRAP) is a CLIP-170 kinase. EMBO Rep 3, 988–994.CrossRefGoogle Scholar
  12. Chu, D., Kakazu, N., Gorrin-Rivas, M.J., Lu, H.P., Kawata, M., Abe, T., Ueda, K., and Adachi, Y. (2001). Cloning and characterization of LUN, a novel ring finger protein that is highly expressed in lung and specifically binds to a palindromic sequence. J Biol Chem 276, 14004–14013.Google Scholar
  13. Coquelle, F.M., Caspi, M., Cordelières, F.P., Dompierre, J.P., Dujardin, D.L., Koifman, C., Martin, P., Hoogenraad, C.C., Akhmanova, A., Galjart, N., et al. (2002). LIS1, CLIP-170’s key to the dynein/dynactin pathway. Mol Cell Biol 22, 3089–3102CrossRefGoogle Scholar
  14. Dhar, S.K., Delmolino, L., and Dutta, A. (2001). Architecture of the human origin recognition complex. J Biol Chem 276, 29067–29071.CrossRefGoogle Scholar
  15. Doyon, Y., Cayrou, C., Ullah, M., Landry, A.J., Côté, V., Selleck, W., Lane, W.S., Tan, S., Yang, X.J., and Côté, J. (2006). ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 21, 51–64.CrossRefGoogle Scholar
  16. Eckerdt, F., Yuan, J., and Strebhardt, K. (2005). Polo-like kinases and oncogenesis. Oncogene 24, 267–276.CrossRefGoogle Scholar
  17. Elia, A.E., Cantley, L.C., and Yaffe, M.B. (2003). Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299, 1228–1231.CrossRefGoogle Scholar
  18. Elowe, S., Hümmer, S., Uldschmid, A., Li, X., and Nigg, E.A. (2007). Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 21, 2205–2219.CrossRefGoogle Scholar
  19. Fu, Z., Malureanu, L., Huang, J., Wang, W., Li, H., van Deursen, J.M., Tindall, D.J., and Chen, J. (2008). Plk1-dependent phosphorylation of FoxM1 regulates a transcriptional programme required for mitotic progression. Nat Cell Biol 10, 1076–1082.CrossRefGoogle Scholar
  20. Fukata, M., Watanabe, T., Noritake, J., Nakagawa, M., Yamaga, M., Kuroda, S., Matsuura, Y., Iwamatsu, A., Perez, F., and Kaibuchi, K. (2002). Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109, 873–885.CrossRefGoogle Scholar
  21. Griffith, J.D., Comeau, L., Rosenfield, S., Stansel, R.M., Bianchi, A., Moss, H., and de Lange, T. (1999). Mammalian telomeres end in a large duplex loop. Cell 97, 503–514.CrossRefGoogle Scholar
  22. Guan, B., Pungaliya, P., Li, X., Uquillas, C., Mutton, L.N., Rubin, E.H., and Bieberich, C.J. (2008). Ubiquitination by TOPORS regulates the prostate tumor suppressor NKX3.1. J Biol Chem 283, 4834–4840.CrossRefGoogle Scholar
  23. Haluska, P. Jr, Saleem, A., Rasheed, Z., Ahmed, F., Su, E.W., Liu, L. F., and Rubin, E.H. (1999). Interaction between human topoisomerase I and a novel RING finger/arginine-serine protein. Nucleic Acids Res 27, 2538–2544.CrossRefGoogle Scholar
  24. Hammer, E., Heilbronn, R., and Weger, S. (2007). The E3 ligase Topors induces the accumulation of polysumoylated forms of DNA topoisomerase I in vitro and in vivo. FEBS Lett 581, 5418–5424.CrossRefGoogle Scholar
  25. Iizuka, M., Matsui, T., Takisawa, H., and Smith, M.M. (2006). Regulation of replication licensing by acetyltransferase Hbo1. Mol Cell Biol 26, 1098–1108.CrossRefGoogle Scholar
  26. Iizuka, M., Sarmento, O.F., Sekiya, T., Scrable, H., Allis, C.D., and Smith, M.M. (2007). Hbo1 Links p53-Dependent Stress Signaling to DNA Replication Licensing. Mol Cell Biol.Google Scholar
  27. Iizuka, M., and Stillman, B. (1999). Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J Biol Chem 274, 23027–23034.CrossRefGoogle Scholar
  28. Iwano, T., Tachibana, M., Reth, M., and Shinkai, Y. (2004). Importance of TRF1 for functional telomere structure. J Biol Chem 279, 1442–1448.CrossRefGoogle Scholar
  29. Kang, Y.H., Park, J.E., Yu, L.R., Soung, N.K., Yun, S.M., Bang, J.K., Seong, Y.S., Yu, H., Garfield, S., Veenstra, T.D., et al. (2006). Selfregulated Plk1 recruitment to kinetochores by the Plk1-PBIP1 interaction is critical for proper chromosome segregation. Mol Cell 24, 409–422.CrossRefGoogle Scholar
  30. Kim, S.H., Kaminker, P., and Campisi, J. (1999). TIN2, a new regulator of telomere length in human cells. Nat Genet 23, 405–412.CrossRefGoogle Scholar
  31. Kishi, S., Zhou, X.Z., Ziv, Y., Khoo, C., Hill, D.E., Shiloh, Y., and Lu, K. P. (2001). Telomeric protein Pin2/TRF1 as an important ATM target in response to double strand DNA breaks. J Biol Chem 276, 29282–29291.CrossRefGoogle Scholar
  32. Knecht, R., Elez, R., Oechler, M., Solbach, C., von Ilberg, C., and Strebhardt, K. (1999). Prognostic significance of polo-like kinase (PLK) expression in squamous cell carcinomas of the head and neck. Cancer Res 59, 2794–2797.Google Scholar
  33. Knecht, R., Oberhauser, C., and Strebhardt, K. (2000). PLK (polo-like kinase), a new prognostic marker for oropharyngeal carcinomas. Int J Cancer 89, 535–536.CrossRefGoogle Scholar
  34. Komarova, Y.A., Akhmanova, A.S., Kojima, S., Galjart, N., and Borisy, G.G. (2002). Cytoplasmic linker proteins promote microtubule rescue in vivo. J Cell Biol 159, 589–599.CrossRefGoogle Scholar
  35. Kurasawa, Y., and Yu-Lee, L.Y. (2010). PICH and cotargeted Plk1 coordinately maintain prometaphase chromosome arm architecture. Mol Biol Cell 21, 1188–1199.CrossRefGoogle Scholar
  36. Lam, M.H., and Rosen, J.M. (2004). Chk1 versus Cdc25: chking one’s levels of cellular proliferation. Cell Cycle 3, 1355–1357.CrossRefGoogle Scholar
  37. Lansbergen, G., Komarova, Y., Modesti, M., Wyman, C., Hoogenraad, C.C., Goodson, H.V., Lemaitre, R.P., Drechsel, D.N., van Munster, E., Gadella, T.W. Jr, et al. (2004). Conformational changes in CLIP-170 regulate its binding to microtubules and dynactin localization. J Cell Biol 166, 1003–1014.CrossRefGoogle Scholar
  38. Li, H., Liu, X.S., Yang, X., Song, B., Wang, Y., and Liu, X. (2010b). Polo-like kinase 1 phosphorylation of p150Glued facilitates nuclear envelope breakdown during prophase. Proc Natl Acad Sci U S A 107, 14633–14638.CrossRefGoogle Scholar
  39. Li, H., Liu, X.S., Yang, X., Wang, Y., Wang, Y., Turner, J.R., and Liu, X. (2010a). Phosphorylation of CLIP-170 by Plk1 and CK2 promotes timely formation of kinetochore-microtubule attachments. EMBO J 29, 2953–2965.CrossRefGoogle Scholar
  40. Li, H., Wang, Y., and Liu, X. (2008). Plk1-dependent phosphorylation regulates functions of DNA topoisomerase IIalpha in cell cycle progression. J Biol Chem 283, 6209–6221.CrossRefGoogle Scholar
  41. Liang, C., Weinreich, M., and Stillman, B. (1995). ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell 81, 667–676.CrossRefGoogle Scholar
  42. Lin, L., Ozaki, T., Takada, Y., Kageyama, H., Nakamura, Y., Hata, A., Zhang, J.H., Simonds, W.F., Nakagawara, A., and Koseki, H. (2005). topors, a p53 and topoisomerase I-binding RING finger protein, is a coactivator of p53 in growth suppression induced by DNA damage. Oncogene 24, 3385–3396.CrossRefGoogle Scholar
  43. Lingner, J., and Cech, T.R. (1996). Purification of telomerase from Euplotes aediculatus: requirement of a primer 3′ overhang. Proc Natl Acad Sci U S A 93, 10712–10717.CrossRefGoogle Scholar
  44. Liu, X., and Erikson, R.L. (2003). Polo-like kinase (Plk)1 depletion induces apoptosis in cancer cells. Proc Natl Acad Sci U S A 100, 5789–5794.CrossRefGoogle Scholar
  45. Liu, X., Lin, C.Y., Lei, M., Yan, S., Zhou, T., and Erikson, R.L. (2005). CCT chaperonin complex is required for the biogenesis of functional Plk1. Mol Cell Biol 25, 4993–5010.CrossRefGoogle Scholar
  46. Liu, X.S., Li, H., Song, B., and Liu, X. (2010). Polo-like kinase 1 phosphorylation of G2 and S-phase-expressed 1 protein is essential for p53 inactivation during G2 checkpoint recovery. EMBO Rep 11, 626–632.CrossRefGoogle Scholar
  47. Llamazares, S., Moreira, A., Tavares, A., Girdham, C., Spruce, B.A., Gonzalez, C., Karess, R.E., Glover, D.M., and Sunkel, C.E. (1991). polo encodes a protein kinase homolog required for mitosis in Drosophila. Genes Dev 5, 2153–2165.CrossRefGoogle Scholar
  48. Loayza, D., and De Lange, T. (2003). POT1 as a terminal transducer of TRF1 telomere length control. Nature 423, 1013–1018.CrossRefGoogle Scholar
  49. Loayza, D., Parsons, H., Donigian, J., Hoke, K., and de Lange, T. (2004). DNA binding features of human POT1: a nonamer 5′-TAGGGTTAG-3′ minimal binding site, sequence specificity, and internal binding to multimeric sites. J Biol Chem 279, 13241–13248CrossRefGoogle Scholar
  50. Lowery, D.M., Clauser, K.R., Hjerrild, M., Lim, D., Alexander, J., Kishi, K., Ong, S.E., Gammeltoft, S., Carr, S.A., and Yaffe, M.B. (2007). Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate. EMBO J 26, 2262–2273.CrossRefGoogle Scholar
  51. Macůrek, L., Lindqvist, A., Lim, D., Lampson, M.A., Klompmaker, R., Freire, R., Clouin, C., Taylor, S.S., Yaffe, M.B., and Medema, R.H. (2008). Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455, 119–123.CrossRefGoogle Scholar
  52. Mamely, I., van Vugt, M.A., Smits, V.A., Semple, J.I., Lemmens, B., Perrakis, A., Medema, R.H., and Freire, R. (2006). Polo-like kinase-1 controls proteasome-dependent degradation of Claspin during checkpoint recovery. Curr Biol 16, 1950–1955.CrossRefGoogle Scholar
  53. Miotto, B., and Struhl, K. (2008). HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Genes Dev 22, 2633–2638.CrossRefGoogle Scholar
  54. Miotto, B., and Struhl, K. (2010). HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol Cell 37, 57–66.CrossRefGoogle Scholar
  55. Mitchison, T., and Kirschner, M. (1984). Dynamic instability of microtubule growth. Nature 312, 237–242.CrossRefGoogle Scholar
  56. Monte, M., Benetti, R., Buscemi, G., Sandy, P., Del Sal, G., and Schneider, C. (2003). The cell cycle-regulated protein human GTSE-1 controls DNA damage-induced apoptosis by affecting p53 function. J Biol Chem 278, 30356–30364.CrossRefGoogle Scholar
  57. Monte, M., Benetti, R., Collavin, L., Marchionni, L., Del Sal, G., and Schneider, C. (2004). hGTSE-1 expression stimulates cytoplasmic localization of p53. J Biol Chem 279, 11744–11752.CrossRefGoogle Scholar
  58. Nakamura, M., Zhou, X.Z., Kishi, S., Kosugi, I., Tsutsui, Y., and Lu, K. P. (2001). A specific interaction between the telomeric protein Pin2/TRF1 and the mitotic spindle. Curr Biol 11, 1512–1516.CrossRefGoogle Scholar
  59. Nakamura, M., Zhou, X.Z., Kishi, S., and Lu, K.P. (2002). Involvement of the telomeric protein Pin2/TRF1 in the regulation of the mitotic spindle. FEBS Lett 514, 193–198.CrossRefGoogle Scholar
  60. Pacek, M., Tutter, A.V., Kubota, Y., Takisawa, H., and Walter, J.C. (2006). Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol Cell 21, 581–587.CrossRefGoogle Scholar
  61. Perez, F., Diamantopoulos, G.S., Stalder, R., and Kreis, T.E. (1999). CLIP-170 highlights growing microtubule ends in vivo. Cell 96, 517–527.CrossRefGoogle Scholar
  62. Peschiaroli, A., Dorrello, N.V., Guardavaccaro, D., Venere, M., Halazonetis, T., Sherman, N.E., and Pagano, M. (2006). SCFbetaTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol Cell 23, 319–329.CrossRefGoogle Scholar
  63. Rajendra, R., Malegaonkar, D., Pungaliya, P., Marshall, H., Rasheed, Z., Brownell, J., Liu, L.F., Lutzker, S., Saleem, A., and Rubin, E.H. (2004). Topors functions as an E3 ubiquitin ligase with specific E2 enzymes and ubiquitinates p53. J Biol Chem 279, 36440–36444.CrossRefGoogle Scholar
  64. Rasheed, Z.A., Saleem, A., Ravee, Y., Pandolfi, P.P., and Rubin, E.H. (2002). The topoisomerase I-binding RING protein, topors, is associated with promyelocytic leukemia nuclear bodies. Exp Cell Res 277, 152–160.CrossRefGoogle Scholar
  65. Rickard, J.E., and Kreis, T.E. (1991). Binding of pp170 to microtubules is regulated by phosphorylation. J Biol Chem 266, 17597–17605.Google Scholar
  66. Saleem, A., Dutta, J., Malegaonkar, D., Rasheed, F., Rasheed, Z., Rajendra, R., Marshall, H., Luo, M., Li, H., and Rubin, E.H. (2004). The topoisomerase I- and p53-binding protein topors is differentially expressed in normal and malignant human tissues and may function as a tumor suppressor. Oncogene 23, 5293–5300.CrossRefGoogle Scholar
  67. Sanchez, Y., Wong, C., Thoma, R.S., Richman, R., Wu, Z., Piwnica-Worms, H., and Elledge, S.J. (1997). Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277, 1497–1501.CrossRefGoogle Scholar
  68. Santamaria, A., Wang, B., Elowe, S., Malik, R., Zhang, F., Bauer, M., Schmidt, A., Sillje, H.H., Koerner, R., and Nigg, E.A. (2010). The Plk1-dependent phosphoproteome of the early mitotic spindle. Mol Cell Proteomics. In press.Google Scholar
  69. Smith, M.R., Wilson, M.L., Hamanaka, R., Chase, D., Kung, H., Longo, D.L., and Ferris, D.K. (1997). Malignant transformation of mammalian cells initiated by constitutive expression of the pololike kinase. Biochem Biophys Res Commun 234, 397–405.CrossRefGoogle Scholar
  70. Smith, S., and de Lange, T. (2000). Tankyrase promotes telomere elongation in human cells. Curr Biol 10, 1299–1302.CrossRefGoogle Scholar
  71. Smogorzewska, A., and de Lange, T. (2004). Regulation of telomerase by telomeric proteins. Annu Rev Biochem 73, 177–208.CrossRefGoogle Scholar
  72. Spänkuch, B., Matthess, Y., Knecht, R., Zimmer, B., Kaufmann, M., and Strebhardt, K. (2004). Cancer inhibition in nude mice after systemic application of U6 promoter-driven short hairpin RNAs against PLK1. J Natl Cancer Inst 96, 862–872.CrossRefGoogle Scholar
  73. St-Pierre, J., Douziech, M., Bazile, F., Pascariu, M., Bonneil, E., Sauvé, V., Ratsima, H., and D’Amours, D. (2009). Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol Cell 34, 416–426.CrossRefGoogle Scholar
  74. Strebhardt, K. (2010). Multifaceted polo-like kinases: drug targets and antitargets for cancer therapy. Nat Rev Drug Discov 9, 643–660.CrossRefGoogle Scholar
  75. Strebhardt, K., Kneisel, L., Linhart, C., Bernd, A., and Kaufmann, R. (2000). Prognostic value of pololike kinase expression in melanomas. JAMA 283, 479–480.CrossRefGoogle Scholar
  76. Stuermer, A., Hoehn, K., Faul, T., Auth, T., Brand, N., Kneissl, M., Pütter, V., and Grummt, F. (2007). Mouse pre-replicative complex proteins colocalise and interact with the centrosome. Eur J Cell Biol 86, 37–50.CrossRefGoogle Scholar
  77. Sunkel, C.E., and Glover, D.M. (1988). polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J Cell Sci 89, 25–38.Google Scholar
  78. Tai, C.Y., Dujardin, D.L., Faulkner, N.E., and Vallee, R.B. (2002). Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. J Cell Biol 156, 959–968.CrossRefGoogle Scholar
  79. Takai, N., Hamanaka, R., Yoshimatsu, J., and Miyakawa, I. (2005). Polo-like kinases (Plks) and cancer. Oncogene 24, 287–291.CrossRefGoogle Scholar
  80. Takeda, D.Y., and Dutta, A. (2005). DNA replication and progression through S phase. Oncogene 24, 2827–2843.CrossRefGoogle Scholar
  81. Tanenbaum, M.E., Galjart, N., van Vugt, M.A., and Medema, R.H. (2006). CLIP-170 facilitates the formation of kinetochore-microtubule attachments. EMBO J 25, 45–57.CrossRefGoogle Scholar
  82. Tsou, M.F., Wang, W.J., George, K.A., Uryu, K., Stearns, T., and Jallepalli, P.V. (2009). Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev Cell 17, 344–354.CrossRefGoogle Scholar
  83. Tsvetkov, L., and Stern, D.F. (2005). Interaction of chromatin-associated Plk1 and Mcm7. J Biol Chem 280, 11943–11947.CrossRefGoogle Scholar
  84. Utrera, R., Collavin, L., Lazarević, D., Delia, D., and Schneider, C. (1998). A novel p53-inducible gene coding for a microtubule-localized protein with G2-phase-specific expression. EMBO J 17, 5015–5025.CrossRefGoogle Scholar
  85. van Steensel, B., and de Lange, T. (1997). Control of telomere length by the human telomeric protein TRF1. Nature 385, 740–743.CrossRefGoogle Scholar
  86. van Vugt, M.A., Brás, A., and Medema, R.H. (2004). Polo-like kinase-1 controls recovery from a G2 DNA damage-induced arrest in mammalian cells. Mol Cell 15, 799–811.CrossRefGoogle Scholar
  87. van Vugt, M.A., Gardino, A.K., Linding, R., Ostheimer, G.J., Reinhardt, H.C., Ong, S.E., Tan, C.S., Miao, H., Keezer, S.M., Li, J., et al. (2010). A mitotic phosphorylation feedback network connects Cdk1, Plk1, 53BP1, and Chk2 to inactivate the G(2)/M DNA damage checkpoint. PLoS Biol 8, e1000287.CrossRefGoogle Scholar
  88. Vaughan, P.S., Miura, P., Henderson, M., Byrne, B., and Vaughan, K. T. (2002). A role for regulated binding of p150(Glued) to microtubule plus ends in organelle transport. J Cell Biol 158, 305–319.CrossRefGoogle Scholar
  89. Weger, S., Hammer, E., and Heilbronn, R. (2005). Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett 579, 5007–5012.CrossRefGoogle Scholar
  90. Wolf, G., Elez, R., Doermer, A., Holtrich, U., Ackermann, H., Stutte, H. J., Altmannsberger, H.M., Rübsamen-Waigmann, H., and Strebhardt, K. (1997). Prognostic significance of polo-like kinase (PLK) expression in non-small cell lung cancer. Oncogene 14, 543–549.CrossRefGoogle Scholar
  91. Wu, Y., Xiao, S., and Zhu, X.D. (2007). MRE11-RAD50-NBS1 and ATM function as co-mediators of TRF1 in telomere length control. Nat Struct Mol Biol 14, 832–840.CrossRefGoogle Scholar
  92. Wu, Z.Q., and Liu, X. (2008). Role for Plk1 phosphorylation of Hbo1 in regulation of replication licensing. Proc Natl Acad Sci U S A 105, 1919–1924.CrossRefGoogle Scholar
  93. Wu, Z.Q., Yang, X., Weber, G., and Liu, X. (2008). Plk1 phosphorylation of TRF1 is essential for its binding to telomeres. J Biol Chem 283, 25503–25513.CrossRefGoogle Scholar
  94. Xie, S., Wu, H., Wang, Q., Cogswell, J.P., Husain, I., Conn, C., Stambrook, P., Jhanwar-Uniyal, M., and Dai, W. (2001). Plk3 functionally links DNA damage to cell cycle arrest and apoptosis at least in part via the p53 pathway. J Biol Chem 276, 43305–43312.CrossRefGoogle Scholar
  95. Yang, X., Li, H., Liu, X.S., Deng, A., and Liu, X. (2009a). Cdc2-mediated phosphorylation of CLIP-170 is essential for its inhibition of centrosome reduplication. J Biol Chem 284, 28775–28782.CrossRefGoogle Scholar
  96. Yang, X., Li, H., Zhou, Z., Wang, W.H., Deng, A., Andrisani, O., and Liu, X. (2009b). Plk1-mediated phosphorylation of Topors regulates p53 stability. J Biol Chem 284, 18588–18592.CrossRefGoogle Scholar
  97. Yarm, F.R. (2002). Plk phosphorylation regulates the microtubule-stabilizing protein TCTP. Mol Cell Biol 22, 6209–6221.CrossRefGoogle Scholar
  98. Ye, J.Z., Donigian, J.R., van Overbeek, M., Loayza, D., Luo, Y., Krutchinsky, A.N., Chait, B.T., and de Lange, T. (2004). TIN2 binds TRF1 and TRF2 simultaneously and stabilizes the TRF2 complex on telomeres. J Biol Chem 279, 47264–47271.CrossRefGoogle Scholar
  99. Yim, H., and Erikson, R.L. (2009). Polo-like kinase 1 depletion induces DNA damage in early S prior to caspase activation. Mol Cell Biol 29, 2609–2621.CrossRefGoogle Scholar
  100. Zhou, R., Wen, H., and Ao, S.Z. (1999). Identification of a novel gene encoding a p53-associated protein. Gene 235, 93–101.CrossRefGoogle Scholar

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© Higher Education Press and Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Department of BiochemistryPurdue UniversityWest LafayetteUSA
  2. 2.Department of Biological SciencesPurdue UniversityWest LafayetteUSA
  3. 3.Center for Cancer ResearchPurdue UniversityWest LafayetteUSA

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