Dynamics and mechanisms of interactions between ring-shaped heterohexameric TIP49a/b protein complexes and double-stranded DNA

详细信息    查看全文

• 作者：A. S. Afanasyeva ; A. P. Yakimov ; M. Yu. Grigoriev…
• 关键词：molecular dynamics ; TIP49 ; structural changes ; double ; stranded DNA ; hexamer complex
• 刊名：Cell and Tissue Biology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：10
• 期：1
• 页码：47-54
• 全文大小：1,424 KB
• 参考文献：Afanasyeva, A., Hirtreiter, A., Schreiber, A., Grohmann, D., Pobegalov, G., McKay, A.R., Tsaneva, I., Petukhov, M., Kas, E., Grigoriev, M., and Werner, F., Lytic water dynamics reveal evolutionarily conserved mechanisms of ATP hydrolysis by TIP49 AAA+ ATPases, Structure, 2014, vol. 22, pp. 549–4.PubMedCentral CrossRef PubMed
  Ammelburg, M., Frickey, T., Lupas, A.N. Classification of AAA+ proteins, J. Struct. Biol., 2006, vol. 156, pp. 2–4.CrossRef PubMed
  Bussi, G., Donadio, D., Parrinello. M. Canonical sampling through velocity rescaling, J. Chem. Physics, 2007, vol. 126, pp. 014101.CrossRef
  Chen, Z., Yang, H., and Pavletich, N.P., Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures, Nature, 2008, vol. 453, pp. 489–4.CrossRef PubMed
  Cheung, K.L., Huen, J., Houry, W.A., and Ortega. J., Comparison of the multiple oligomeric structures observed for the Rvb1 and Rvb2 proteins, Biochem. Cell Biol., 2010, vol. 88, pp. 77–4.PubMedCentral CrossRef PubMed
  Gribun, A., Cheung, K.L., Huen, J., Ortega, J., and Houry, W.A., Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex, J. Mol. Biol., 2008, vol. 376, pp. 1320–4.CrossRef PubMed
  Hishida, T., Han, Y.-W., Fujimoto, S., Iwasaki, H., and Shinagawa, H., Direct evidence that a conserved arginine in RuvB AAA+ ATPase acts as an allosteric effector for the ATPase activity of the adjacent subunit in a hexamer, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 9573–4.PubMedCentral CrossRef PubMed
  Huber, O., Menard, L., Haurie, V., Nicou, A., Taras, D., and Rosenbaum, J., Pontin and reptin, two related ATPases with multiple roles in cancer, Cancer Res., 2008, vol. 68, pp. 6873–4.CrossRef PubMed
  Huen, J., Kakihara, Y., Ugwu, F., Cheung, K.L., Ortega, J., and Houry, W.A., Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes, Biochem. Cell Biol., 2010, vol. 88, pp. 29–4.CrossRef PubMed
  Ikura, T., Ogryzko, V.V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., Scully, R., Qin, J., and Nakatani, Y., Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis, Cell, 2000, vol. 102, pp. 463–4.CrossRef PubMed
  Jha, S. and Dutta, A., RVB1/RVB2: running rings around molecular biology, Mol. Cell, 2009, vol. 34, pp. 521–4.PubMedCentral CrossRef PubMed
  Lebrun, A. and Lavery, R., Modelling extreme stretching of DNA, Nucleic Acids Res., 1996, vol. 24, pp. 2260–4.PubMedCentral CrossRef PubMed
  Li, D., Zhao, R., Lilyestrom, W., Gai, D., Zhang, R., DeCaprio, J.A., Fanning, E., Jochimiak, A., Szakonyi, G., and Chen, X.S., Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen, Nature, 2003, vol. 423, pp. 512–4.CrossRef PubMed
  Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J.L., Dror, R.O., and Shaw, D.E., Improved sidechain torsion potentials for the Amber ff99SB protein force field, Proteins, 2010, vol. 78, pp. 1950–4.PubMedCentral PubMed
  Matias, P.M., Gorynia, S., Donner, P., and Carrondo, M.A., Crystal structure of the human AAA+ protein RuvBL1, J. Biol. Chem., 2006, vol. 281, pp. 38918–4.CrossRef PubMed
  Nishinaka, T., Shinohara, A., Ito, Y., Yokoyama, S., and Shibata, T., Base pair switching by interconversion of sugar puckers in DNA extended by proteins of RecA-family, pp. a model for homology search in homologous genetic recombination, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 11071–4.PubMedCentral CrossRef PubMed
  Nosé, S. and Klein, M. L., Constant pressure molecular dynamics for molecular systems, Mol. Physics, 2006, vol. 50, pp. 1055–4.CrossRef
  Lu, X.J. and Olson, W.K., 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures, Nucleic Acids Res., 2003, vol. 31, pp. 5108–4.PubMedCentral CrossRef PubMed
  Papin, C., Humbert, O., Kalashnikova, A., Eckert, K., Morera, S., Kas, E., and Grigoriev, M., 3′- to 5′ DNA unwinding by TIP49b proteins, FEBS J., 2010, vol. 277, pp. 2705–4.CrossRef PubMed
  Parrinello, M., Polymorphic transitions in single crystals, pp. A new molecular dynamics method, J. Appl. Physics, 1981, vol. 52, pp. 7182.CrossRef
  Petukhov, M., Dagkessamanskaja, A., Bommer, M., Barrett, T., Tsaneva, I., Yakimov, A., Queval, R., Shvetsov, A., Khodorkovskiy, M., Kas, E., and Grigorie, M., Large-Scale Conformational Flexibility Determines the Properties of AAA+TIP49 ATPases, Structure, 2012, vol. 20, pp. 1321–4.CrossRef PubMed
  Petukhov, M., Ilatovskiy, A., Artamonova, T., Afanasieva, A., Yakimov, A., Khodorkovski, M., Kas, E., and Grigoriev, M., Dynamics of the dsDNA/TIP49a hexameric complexes, FEBS J., 2013, vol. 280, pp. 156–4.
  Putnam, C.D., Clancy, S.B., Tsuruta, H., Gonzalez, S., Wetmur, J.G., and Tainer, J.A., Structure and mechanism of the RuvB Holliday junction branch migration motor, J. Mol. Biol., 2001, vol. 311, pp. 297–4.CrossRef PubMed
  
• 作者单位：A. S. Afanasyeva (1) (2) (3)
  A. P. Yakimov (2) (3)
  M. Yu. Grigoriev (4)
  M. G. Petukhov (2) (3)
  
  1. Department of Biophysics, Peter the Great St. Petersburg State Polytechnic University, St. Petersburg, 195251, Russia
  2. Konstantinov Institute of Nuclear Physics, Russian Research Centre Kurchatov Institute, Gatchina, 188300, Russia
  3. Institute of Nanobiotechnology, Peter the Great St. Petersburg State Polytechnic University, St. Petersburg, 195251, Russia
  4. Laboratoire de Biologie Moléculaire Eucaryote, Paul Sabatier University, Toulouse, F-31062, France
  
• 刊物主题：Cell Biology;
• 出版者：Springer US
• ISSN：1990-5203

文摘

TIP49a and TIP49b, highly conserved proteins belonging to the AAA+ superfamily of DNA-dependent ATPases, participate in numerous cell processes, such as chromatin remodeling, regulation of gene transcription and mitotic cell division, maintenance of genome stability, and snoRNP biogenesis, as well as in the formation of active DNA–telomerase complexes. It has been shown that they are involved in complex networks of protein–protein interactions and, in spite of their structural similarity, sometimes perform opposite functions. Although these proteins exhibit a wide range of activities, the mechanisms of their actions are still poorly understood. In this work, ring-shaped heterohexameric TIP49a/b complexes containing in their central channel short fragments of double-stranded DNA (dsDNA, 20 base pairs of different GC composition) were obtained for the first time using the molecular docking technique, while methods of molecular dynamics in a periodic water box were applied to investigate the conformational dynamics of these proteins and the mechanisms of their helicase activity. It was found that (1) interaction of a DNA helix with positively charged protein loops inside the central channel of the ring-shaped hexameric complex caused unwinding of the helix; (2) the unwinding occurred only inside the hexameric ring, whereas the tails of the helix, which lie outside, retained the initial classical B-form conformation throughout the 50 ns of molecular dynamics; and (3) the presence of ATP in TIP49a/b complexes affected the dynamics and the final structure of dsDNA, causing partial breaking of complementary bonds in GC-poor DNA sequences.