Kyushu University Academic Staff Educational and Research Activities Database
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Tsutomu Katayama Last modified date:2018.04.13



Undergraduate School


E-Mail
Homepage
http://bunsei.phar.kyushu-u.ac.jp/
Phone
092-642-6641
Fax
092-642-6646
Academic Degree
Ph.D.
Field of Specialization
Molecular Biology, Biochemistry, Molecular Genetics
Outline Activities
In E. coli, DnaA protein initiates chromosomal DNA replication. Our group revealed that this protein is inactivated by timely and direct interaction with DNA polymerase III holoenzyme, the chromosomal replicase, in a manner dependent on its conformational change concomitant with nucleotide-polymerizing activity. We named this regulatory system RIDA. In cell cycle, DnaA protein is most likely inactivated by RIDA after initiation, then reactivated before the next round of replication cycle. ADP-DnaA can be reactivated by DARS (DnaA-Reactivating Sequence), which promotes exchange of DnaA-bound nucleotide from ADP- to ATP. We investigate molecular mechanisms in this DnaA-activity cycle by applying molecular genetics, biochemistry, and structural biology.
Research
Research Interests
  • Structure and functional molecular mechanism in replicational initiation complexes
    keyword : Replication initiation, DnaA, oriC, Cell cycle, DNA unwinding
    2000.04Regulatory Mechanism for Chromosomal DNA Replication: Regulatory Inactivation of the Initiator Protein (RIDA).
  • Regulatory Inactivation of DnaA
    keyword : Replicational initiation, Feedback inhibition, DnaA, Hda, DNA polymerase (Clamp)
    1994.04Regulatory Mechanism for Chromosomal DNA Replication: Regulatory Inactivation of the Initiator Protein (RIDA).
  • Structure-function relationship in DnaA
    keyword : Replicational initiation, DnaA domain structures, AAA+, Protein-Protein interaction , Protein-DNA interaction
    1994.04Regulatory Mechanism for Chromosomal DNA Replication: Structure-Function Relashonship Analysis of the Initiator Protein.
  • Regulatory activation of DnaA
    keyword : Replicational initiation, transcription, Cell cycle, DiaA, DARS
    1995.04Regulatory Mechanism for Chromosomal DNA Replication:Regulation for the timely activation of replicational initiation.
  • Regulatory network in replicational initiation
    keyword : REplicational initiation, transcription, Cell cycle, Hda, DiaA, DARS, genome analysis
    1996.04Regulatory Mechanism for Chromosomal DNA Replicaton: Genome Netwarks and Interactions of Regulatory Systems.
Current and Past Project
  • Proteins 3000 Structual Biology Project
  • Post-Genome Project
  • Molecular Mechanisms that Monitor Chromosomal Replication
Academic Activities
Books
1. Tsutomu Katayama, DNA Replication: From Old Principles to New Discovery (Chapter: Initiation of DNA replication at the chromosomal origin of E. coli, oriC), Springer New York LLC, https://doi.org/10.1007/978-981-10-6955-0_4, 1042, 79-98, 2017.01.
2. Kirsten Skarstad, Tsutomu Katayama, DNA Replication , Cold Spring Harbor Press, pp343-359
Capter entitled "Replication Regulation in Bacteria", 2013.01, 細菌染色体の複製開始の制御システムにおける研究成果を体系的にまとめた.
3. Masayuki Su'etsugu, Tsutomu Katayama, Escherichia coli and Bacillus subtilis; The Frontiers of Molecular Microbiology Revisited, Research Signpost, pp29-43, Edited by Yoshito Sadaie and Kouji Matsumoto, Capter entitled "Chromosome replication in E. coli and B. subtilis", 2012.10.
4. Replication system in the E. coli genome. In "Advances in Genomics and Proteomics",, T. Imanaka (ed.), N.T.S., 2004.
5. Regulation of chromosome replication in prokayotes. In "Replication and Partition of the Genome", A. Matsukage and H. Masai (eds.), Springer-Verlag Tokyo, 2003.
Reports
1. Tsutomu Katayama, Kazutoshi Kasho, Hironori Kawakami, The DnaA cycle in Escherichia coli: activation, function and inactivation of the initiator protein, Front. Microbiol., 8:2496. , 2017.12.
2. Katayama, T., Ozaki, S., Keyamura, K. and Fujimitsu, K, Regulation of the replication cycle: Conserved and diverse regulatory systems for DnaA and oriC, Nature Rev. Microbiol. 8(3):163-170, 2010.03.
3. Kawakami, H. and Katayama, T., DnaA, ORC, and Cdc6: Similarity beyond the domains of life and diversity, Biochem. Cell Biol. 88(22): 49-62, 2010.03.
4. Ozaki, S., and Katayama, T., DnaA structure, function, and dynamics in the initiation at the chromosomal origin, Plasmid, 2009.09.
5. Katayama. T., Roles for the AAA+ motifs of DnaA in the initiation of DNA replication, Biochem. Soc. Trans. 36(1), 78-82, 2008.02.
6. Regulatory mechanism of bacterail chromosome.
7. Katayama, T., Feedback controls restrain the initiation of Escherichia coli chromosomal replication, Mol. Microbiol., 41巻(1号), 9-18ページ, 2001.07.
8. A novel role for DNA polymerase: Negative regulation for initiation of chromosomal replication.
Papers
1. Yukari Sakiyama, Kazutoshi Kasho, Yasunori Noguchi, Hironori Kawakami, Tsutomu Katayama, Regulatory dynamics in the ternary DnaA complex for initiation of chromosomal replication in Escherichia coli, Nucleic Acids Res., doi/10.1093/nar/gkx914, 45(21): 12354-12373, 2017.12.
2. Kazutoshi Kasho, Hiroyuki Tanaka, Ryuji Sakai, Tsutomu Katayama, Cooperative DnaA binding to the negatively supercoiled datA locus stimulates DnaA-ATP hydrolysis, J. Biol. Chem., doi: 10.1074/jbc.M116.762815, 292(4), 1251-1266, 2017.01.
3. Masahiro Shimizu, Yasunori Noguchi, Yukari Sakiyama, Hironori Kawakami, Tsutomu Katayama, Shoji Takada, Near-atomic structural model for bacterial DNA replication initiation complex and its functional insights, Proc. Natl. Acad. Sci. USA, doi/10.1074/jbc.M115.662601, 113 (50) E8021–E8030., 2016.12.
4. Yasunori Noguchi, Tsutomu Katayama, The Escherichia coli cryptic prophage protein YfdR binds to DnaA and initiation of chromosomal replication is inhibited by overexpression of the gene cluster yfdQ-yfdR-yfdS-yfdT, Front. Microbiol. , doi: 10.3389/fmicb.2016.00239, 7; 239. (21 pages) , 2016.03.
5. Hironori Kawakami, Eiji Ohashi, Shota Kanamoto, Toshiki Tsurimoto, Tsutomu Katayama, Specific binding of eukaryotic ORC to DNA replication origins depends on highly conserved basic residues, Sci. Rep., 5; 14929 (14 pages), 2015.10.
6. Yasunori Noguchi, Yukari Sakiyama, Hironori Kawakami, Tsutomu Katayama, The Arg fingers of key DnaA protomers are oriented inward within the replication origin oriC and stimulate DnaA subcomplexes in the Initiation complex, J. Biol. Chem., doi/10.1074/jbc.M115.662601 , 290 (33) , 20295-20312, 2015.08.
7. Kazutoshi Kasho, Fujimitsu Kazuyuki, Toshihiro Matoba, Taku Oshima, Tsutomu Katayama, Timely binding of IHF and Fis to DARS2 regulates ATP–DnaA production and replication initiation
, Nucleic Acids Res., 10.1093/nar/gku1051, 42(21):13134-13149, 2014.12, 大腸菌の細胞周期において複製開始が正しい時期に起こるためには、複製開始蛋白質DnaAが不活性なADP型から、活性のあるATP結合型にタイミングよく変換される必要があります。これまでの同分野の研究により、ADP-DnaAが染色体上の非コード型DNA因子DARS2と相互作用すると、ヌクレオチド交換が促進されATP-DnaAに変換することが見出されておりました(Fujimitsu et al., Genes Dev., 2009)。しかしながら、細胞周期においてDARS2がどのようにタイミングよく活性化されるかという制御機構は不明でした。同分野は今回の研究において、DARS2に結合する2種の蛋白質IHFおよびFisを同定しました。これらは細菌型ヒストン様因子とも呼ばれるDNA結合因子です。DARS2の活性化には両者の結合が必要でした。さらに、IHFは複製開始前の時間帯のみでDARS2と結合しました。Fisは増殖が活発な細胞のみでDARS2に結合していました。このようにIHFとFisの時期特異的な結合によって、DARS2が増殖中の細胞でタイミングよく活性化されることがわかりました。このことが正しいタイミングで複製開始を起こすための基盤となっていたのです。.
8. Ozaki Shogo, Yusaku Matsuda, Kenji Keyamura, Hironori Kawakami, Yasunori Noguchi, Kazutoshi Kasho, Komomo Nagata, Tamami Masuda, Yukari Sakiyama, Tsutomu Katayama, A replicase clamp-binding protein with a dynamin motif promotes colocalization of the nascent DNA strands and equipartitioning of chromosomes in Escherichia coli
, Cell Reports, 4, 985-995, 2013.09, DNA複製と均等分配は細胞増殖に必須であり、その破綻は発ガン、発生異常、不妊などにも結びつく。複製後のDNA 分子を正常に姉妹細胞へ分配するには、複製直後のDNA分子どおしを接着させ、その後、規則的に折りたたんでゆくという高次構造形成が必要と考えられていいる。しかしながら、このような構造形成を担う因子はまだわずかしか見出されておらず、その分子機構はほとんど不明である。本研究では、大腸菌で複製直後のDNA鎖を接着させる新規なキー因子CrfCタンパク質を見出し、その基盤となる分子機構を解明した。CrfCタンパク質は、複製直後のDNA上に「足あと」のように残る「クランプ・タンパク質」と結合する。そして、「かすがい」のような働きによって、複製直後のDNA分子同士をつなぎ留める。変異CrfCタンパク質をもつ細胞では、複製されたDNAどおしの接着と均等分配が阻害された。このようにCrfCタンパク質は、新たな分子機構により、DNA複製と共役してDNAの接着と均等分配に働く重要な因子であることがわかった。.
9. Kazutoshi Kasho, Tsutomu Katayama, DnaA-binding locus datA promotes DnaA-ATP hydrolysis to enable cell cycle-coordinated replication initiation
, Proc. Natl. Acad. Sci. USA , 110, 946-941, 2013.01, 大腸菌染色体の複製開始を起こす活性型のATP-DnaAを制御的に不活化する新たな分子機構を解明し、DDAH (datA-dependent DnaA-ATP hydrolysis)と命名した。DDAH系では、datAと呼ばれる染色体DNA領域でATP-DnaAが集合し、DnaA-ATP加水分解を促進し、不活性なADP-DnaAを産生する。また、DDAH系は、染色体構築因子IHFがdatAに結合することにより、複製開始後に適時的に活性化される。この制御系は、細胞周期における染色体複製開始タイミングの制御と染色体コピー数の適正維持に必須である。.
10. Ozaki Shogo, Yasuhisa Hayashi, Yasunori Noguchi, Erika Miyazaki, Tsutomu Katayama, Novel functional substructures of DnaA specifically promote ATP-dependent activation of the DNA unwinding subcomplex within a replication initiation complex, J. Biol. Chem., 287(44), 37458-37471, 2012.10.
11. Ozaki, S., and Katayama, T., Highly organized DnaA-oriC complexes recruit the single-stranded DNA for replication initiation, Nucleic Acids Res., 10.1093/nar/gkr832, 40(4), 1648-1665, 2012.02.
12. Nakamura, K. and Katayama, T., Novel essential residues of Hda for interaction with DnaA in the regulatory inactivation of DnaA: Unique roles for Hda AAA+ Box VI and VII motifs, Mol. Microbiol. , 76(2): 302-317, 2010.04.
13. Keyamura, K., Abe, Y., Higashi, M., Ueda, T., and Katayama, T., DiaA dynamics are coupled with changes in initial origin complexes leading to helicase loading, J. Biol. Chem. , 284: 25038-25050, 2009.09.
14. Fujimitsu, K., Senriuchi, T., and Katayama, T. , Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA, Genes Dev., 23, 1221-1233, 2009.05.
15. Su’etsugu, M., Nakamura, K., Keyamura, K., Kudo, Y. and Katayama, T., Hda monomerization by ADP binding promotes replicase clamp-mediated DnaA-ATP hydrolysis., J. Biol. Chem, 283(52); 36118-36131, 2008.12.
16. Ozaki, S., Kawakami,H., Nakamura, K., Fujikawa, N., Kagawa, W., Park, S.-Y., Yokoyama, S., Kurumizaka, H., and Katayama, T., A common mechanism for the ATP-DnaA-dependent formation of open complexes at the replication origin, J. Biol. Chem. , 283(13), 8351-8362, 2008.03.
17. Keyamura, K., Fujikawa, N., Ishida, T., Ozaki, S., Su'etsugu, M., Fujimitsu, K., Kagawa, W., Yokoyama, S., Kurumizaka, H., and Katayama, T., The interaction of DiaA and DnaA regulates the replication cycle in E. coli by directly promoting ATP-DnaA-specific initiation complexes, Genes Dev., 21, 2083-2099, 2007.10.
18. Abe, Y., Jo, T., Matsuda, Y., Matsunaga, C., Katayama, T.* and Ueda, T* (*Co-corresponding authors), Structure and function of DnaA N-terminal domains: Specific sites and mechanisms in inter-DnaA interaction and in DnaB helicase loading on oriC, J. Biol. Chem., 282(24), 17816-17827 [JBC Paper of the Week; Cited for the Journal Cover], 2007.06.
19. Kawakami, H., Ozaki, S., Suzuki, S., Nakamura, K., Senriuchi, T., Su'etsugu, M., Fujimitsu, K., and Katayama, T. , The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif, Mol. Microbiol. , 62(5), 1310-1324, 2006.10.
20. Ozaki, S., Fujimitsu, K., Kurumizaka, H., and Katayama, T., The DnaA homolog of the hyperthermophilic eubacterium Thermotoga maritima forms an open complex with a minimal 149-bp origin region in an ATP-dependent manner, Genes Cells, 11, 425-438, 2006.04.
21. Kawakami, H., Keyamura, K., and Katayama, T., Formation of an ATP-DnaA-specific initiation complex requires DnaA arginine-285, a conserved motif in the AAA+ protein family, J. Biol. Chem., 10.1074/jbc.M502764200, 280, 29, 27420-27430, 280(29),27420-27430, 2005.07.
22. Su'etsugu, M, Shimuta, T., Ishida, T., Kawakami, H. and Katayama, T., Protein associations in DnaA-ATP hydrolysis mediated by the replicase clamp-Hda complex, J. Biol. Chem., 10.1074/jbc.M412060200, 280, 8, 6528-6536, 280(8), 6528-6536, 2005.03.
23. Shimuta, T., Nakano, K., Yamaguchi, Y., Ozaki, S., Fujimitsu, K., Matsunaga, C., Noguchi, K., Emoto, A., and Katayama, T., Novel heat-shock protein HspQ stimulates the degradation of mutant DnaA protein in Escherichia coli, Genes Cells, 10.1111/j.1365-2443.2004.00800.x, 9, 12, 1151-1166, 9, 1151-1166, 2004.11.
24. Ishida, T., Akimitsu, N., Kashioka, T., Hatano, M., Kubota, T., Ogata, Y., Sekimizu, K., and Katayama, T, DiaA, a novel DnaA-binding protein, ensures the initiation timing of Escherichia coli chromosome replication, J. Biol. Chem., 10.1074/jbc.M402762200, 279, 44, 45546-45555, 279, 45546-45555, 2004.10.
25. Su'etsugu, M., Takata, M., Kubota, T., Matsuda, Y. and Katayama, T, Molecular mechanism of DNA replication-coupled inactivation of the initiator protein in Escherichia coli: Interaction of DnaA with the sliding clamp-loaded DNA and the sliding clamp-Hda complex, Genes Cells, 10.1111/j.1365-2443.2004.00741.x, 9, 6, 509-522, 9 (6), 509-522, 2004.06.
26. Su'etsugu, M., Emoto, A., Fujimitsu, K.,Keyamura, K., and Katayama, T., Transcriptional control for initiation of chromosomal replication in Escherichia coli: fluctuation of the level of origin transcription ensures timely initiation, Genes Cells, 10.1046/j.1365-2443.2003.00671.x, 8, 9, 731-745, 8(9), 731-745, 2003.09.
27. Fujikawa, N., Kurumizaka, H., Nureki, O., Terada, T., Shirouzu, M., Katayama, T., and Yokoyama, S., Structural basis of replication origin recognition by the DnaA protein., Nucleic Acids Res., 10.1093/nar/gkg309, 31, 8, 2077-2086, 31(8), 2077-2086, 2003.04.
28. Nishida, S., Fujimitsu, K., Sekimizu, K., Ohmura, T., Ueda, T., and Katayama, T., A nucleotide switch in E. coli DnaA protein initiates chromosomal replication: Evidence from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo., J. Biol. Chem., 10.1074/jbc.M108303200, 277, 17, 14986-14995, 277(17), 14986-14995, 2002.04.
29. Kato, J. and Katayama, T., Hda, a novel dnaA-related protein, regulates the replication cycle in Escherichia coli., EMBO J., 10.1093/emboj/20.15.4253, 20, 15, 4253-4262, 20(15), 4253-4262, 2001.08.
30. Su'etsugu, M., Kawakami, H., Kurokawa, K., Kubota, T., Takata, M., and Katayama, T., DNA replication-coupled inactivation of DnaA protein in vitro: a role for DnaA arginine-334 of the AAA+ Box VIII motif in ATP hydrolysis., Mol. Microbiol., 10.1046/j.1365-2958.2001.02378.x, 40, 2, 376-386, 40(2), 376-386, 2001.04.
31. Kurokawa, K., Nishida, S., Emoto, A., Sekimizu, K., and Katayama, T., Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli., EMBO J., 10.1093/emboj/18.23.6642, 18, 23, 6642-6652, 18(23), 6642-6652, 1999.12.
32. Katayama, T. (Corresponding author), Kubota, T., Kurokawa, K., Crooke, E., and Sekimizu, K., The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase., Cell, 10.1016/S0092-8674(00)81222-2, 94, 1, 61-71, 94 (1), 61-71, 1998.06.
33. Katayama, T., Takata, M., and Sekimizu, K., CedA is a novel Escherichia coli protein that activates the cell division inhibited by chromosomal DNA overreplication., Mol. Microbiol., 10.1046/j.1365-2958.1997.5941967.x, 26, 4, 687-697, 26 (4), 687-697, 1997.10.
34. Katayama, T., Akimitsu, N., Miki, T., and Sekimizu, K., Overinitiation of chromosome replication in the Escherichia coli dnaAcos mutant depends on activation of oriC function by the dam gene product., Mol. Microbiol., 10.1046/j.1365-2958.1997.5001872.x, 25, 4, 661-670, 25 (4), 661-670., 1997.08.
35. Katayama, T. (Corresponding author), and Crooke, E., DnaA protein is sensitive to a soluble factor and is specifically inactivated for initiation of in vitro replication of the Escherichia coli minichromosome., J. Biol. Chem., 270 (16), 9265-9271, 1995.04.
36. Katayama, T., The mutant DnaAcos protein which overinitiates replication of the Escherichia coli chromosome is inert to negative regulation for initiation., J. Biol. Chem., 269 (35), 22075-22079, 1994.09.
37. Katayama, T., and Kornberg, A, Hyperactive initiation of chromosomal replication in vivo and in vitro by a mutant DnaA protein, DnaAcos, of Escherichia coli., J. Biol. Chem., 269 (17), 12698-12703, 1994.04.
Presentations
1. 片山 勉, 﨑山友香里, 野口泰徳, 川上広宣, Structure, Mechanism and Regulation of Escherichia coli Replication Initiation Complexes in DNA Unwinding, The 10th 3R (Replication, Recombination and Repair) Symposium, 2016.11.
2. Tsutomu Katayama, Ozaki Shogo, Kenji Keyamura, Yasunori Noguchi, Saki Taniguchi, Komomo Nagata, Yukari Sakiyama, Hironori Kawakami, Kazutoshi Kasho, The E. coli dynamin-like protein CrfC binds the replicase clamp and sustains colocalization of sister replication forks, The 9th 3R Symposium , 2014.11, 大腸菌の染色体の接着と均等分配に必須となる新規因子を見出し、その分子機構を解明した。主なる内容はCell誌の姉妹誌でオンラインジャーナルであるCell Reports誌で論文発表した(Cell Reports 4(5):985-995, 2013)。.
3. 片山 勉, 赤間勇介, 野口泰徳, 西村昌洋, 宮崎恵里加, 尾﨑 省吾, Analysis on regulation and mechanism in DnaB helicase interaction with the initiation complex of the Escherichia coli chromosome replication, 第87回日本生化学会シンポジウム「New development in exploring structures and functions of DNA helicases sustaining genome integrity」(オーガナイザー;片山 勉、 正井久雄), 2014.10.
4. 片山 勉, 加生 和寿, 野口泰徳, 崎山友香里, 的場俊大, 田中宏幸, 谷口夢顯, 尾﨑 省吾, 藤光 和之, 川上 広宣, DnaA assemblies on the replication origin oriC, DARS and the datA locus for the replication initiation and regulation of the initiation in E. coli, 第86回日本生化学会大会International Session: Assembly and architecture of protein complexes regulating inheritance and stable maintenance of genome (organizers: Hosao Masai, Tsutomu Katayama) , 2013.09.
5. Yasunori Noguchi, Ozaki Shogo, Erika Miyazaki, Tsutomu Katayama, Specific inter-DnaA interaction for construction of functionally-distinct DnaA sub-complexes on the E. coli replication origin, 2013 Keystone Symposia X5/X6 DNA Replication and Recombination, 2013.03.
6. Kazutoshi Kasho, Tsutomu Katayama, A novel mechanism of a specific DnaA-binding locus datA for regulation of the replication initiator DnaA, 2013 Keystone Symposia X5/X6 DNA Replication and Recombination, 2013.03.
7. Tsutomu Katayama, A novel model for overall structure of a replication initiation complex and duplex unwinding mechanism in E. coli, The 8th 3R Symposium together with National Institute of Genetics 2012 International Symposium: Molecular mechanism and pathology of the 3R , 2012.11.
8. Ozaki Shogo, Yasunori Noguchi, Erika Miyazaki, Tsutomu Katayama, Reconstitution and molecular anatomy of oriC initiation complexes in E. coli chromosomal replication: ssDNA recruitment and roles for IHF and distinct DnaA oligomers formed on oriC., EMBO Workshop: Reconstructing the essential bacterial cell cycle machinery , 2012.09.
9. DNA Replication-Dependent Feedback Against DnaA Initiator Activity in E. coli.
10. Regulatory inactivation of the E. coli DnaA initiator: Molecular mechanisms in interactions of DnaA, Hda, and the replicase sliding clamp.
11. Regulatory Inactivation of The Initiator Protein in E. coli: Roles of The AAA+ Motifs of DnaA and Hda Proteins.
Awards
  • Functional mechanism and regulation for the E. coli chromosomal replication initiator DnaA