Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

ChrII-Encoded DNA Helicase: A Preliminary Study

Author(s): Bailu Tang, Zhongyuan Chen, Hu Xia, Ronghua Wang and Xiaoyan Song*

Volume 30, Issue 1, 2023

Published on: 28 November, 2022

Page: [35 - 43] Pages: 9

DOI: 10.2174/0929866530666221104112210

Price: $65

Abstract

Background: DNA helicases are unwinding enzymes that are essential for many cellular processes. Research has suggested that both the model microorganisms of a single chromosome and the model microorganisms of multiple chromosomes adopt DNA helicases encoded by chromosome I. Therefore, studying DNA helicases encoded by chromosome II may lay some foundation for understanding nucleic acid metabolism processes.

Objective: To prove the existence of DNA helicase encoded by chromosome II and to reveal its difference compared to DNA helicase encoded by chromosome I.

Methods: The DNA helicases of Pseudoalteromonas spongiae JCM 12884T and Pseudoalteromonas tunicata DSM 14096T were analyzed by sequence alignment and phylogenetic relationships with other known DNA helicases. Then, proteins of P. spongiae JCM 12884T and P. tunicata DSM 14096T were obtained by heterologous expression. N-terminal sequencing and liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis were performed to confirm the form of proteins. A fluorescence resonance energy transfer (FRET) assay was used to measure the activity of helicases.

Results: DnaB-pspo and DnaB-ptun belong to the same family, the PRK08840 superfamily, and form a branch with helicases encoded by chromosome I. YwqA-pspo and YwqA-ptun have similar domains and form another branch with helicases encoded by chromosome II. All four helicases have DNA unwinding activity. YwqA is more efficient than DnaB for DNA unwinding, especially YwqA-pspo, which is encoded by bidirectional replication chromosome II.

Conclusion: This is the first study to show that the existence of a DNA helicase encoded by chromosome II, and DNA helicase encoded by chromosome II is more efficient than chromosome I for DNA unwinding.

Keywords: DNA helicase, DNA helicase encoded by chromosome II, DNA helicase encoded by chromosome I, helicase activity, DNA unwinding, Pseudoalteromonas.

Graphical Abstract
[1]
Prozorov, A.A. Additional chromosomes in bacteria: Properties and origin. Microbiology, 2008, 77(4), 385-394.
[http://dx.doi.org/10.1134/S0026261708040012] [PMID: 18825968]
[2]
Harrison, P.W.; Lower, R.P.J.; Kim, N.K.D.; Young, J.P.W. Introducing the bacterial ‘chromid’: Not a chromosome, not a plasmid. Trends Microbiol., 2010, 18(4), 141-148.
[http://dx.doi.org/10.1016/j.tim.2009.12.010] [PMID: 20080407]
[3]
Gangloff, S.; McDonald, J.P.; Bendixen, C.; Arthur, L.; Rothstein, R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: A potential eukaryotic reverse gyrase. Mol. Cell. Biol., 1994, 14(12), 8391-8398.
[http://dx.doi.org/10.1128/MCB.14.12.8391] [PMID: 7969174]
[4]
Stewart, E.; Chapman, C.R.; Al-Khodairy, F.; Carr, A.M.; Enoch, T. rqh1+, a fission yeast gene related to the Bloom’s and Werner’s syndrome genes, is required for reversible S phase arrest. EMBO J., 1997, 16(10), 2682-2692.
[http://dx.doi.org/10.1093/emboj/16.10.2682] [PMID: 9184215]
[5]
Cogoni, C.; Macino, G. Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science, 1999, 286(5448), 2342-2344.
[http://dx.doi.org/10.1126/science.286.5448.2342] [PMID: 10600745]
[6]
Kusano, K.; Berres, M.E.; Engels, W.R. Evolution of the RECQ family of helicases: A drosophila homolog, Dmblm, is similar to the human bloom syndrome gene. Genetics, 1999, 151(3), 1027-1039.
[http://dx.doi.org/10.1093/genetics/151.3.1027] [PMID: 10049920]
[7]
Puranam, K.L.; Blackshear, P.J. Cloning and characterization of RECQL, a potential human homologue of the Escherichia coli DNA helicase RecQ. J. Biol. Chem., 1994, 269(47), 29838-29845.
[http://dx.doi.org/10.1016/S0021-9258(18)43957-9] [PMID: 7961977]
[8]
Kitao, S.; Shimamoto, A.; Goto, M.; Miller, R.W.; Smithson, W.A.; Lindor, N.M.; Furuichi, Y. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet., 1999, 22(1), 82-84.
[http://dx.doi.org/10.1038/8788] [PMID: 10319867]
[9]
Matson, S.W.; Richardson, C.C. DNA-dependent nucleoside 5′-triphosphatase activity of the gene 4 protein of bacteriophage T7. J. Biol. Chem., 1983, 258(22), 14009-14016.
[http://dx.doi.org/10.1016/S0021-9258(17)44017-8] [PMID: 6139375]
[10]
Hall, M.C.; Matson, S.W. Helicase motifs: The engine that powers DNA unwinding. Mol. Microbiol., 1999, 34(5), 867-877.
[http://dx.doi.org/10.1046/j.1365-2958.1999.01659.x] [PMID: 10594814]
[11]
Xu, H.Q.; Deprez, E.; Zhang, A.H.; Tauc, P.; Ladjimi, M.M.; Brochon, J.C.; Auclair, C.; Xi, X.G. The Escherichia coli RecQ helicase functions as a monomer. J. Biol. Chem., 2003, 278(37), 34925-34933.
[http://dx.doi.org/10.1074/jbc.M303581200] [PMID: 12805371]
[12]
Matson, S.W.; Bean, D.W.; George, J.W. DNA helicases: Enzymes with essential roles in all aspects of DNA metabolism. BioEssays, 1994, 16(1), 13-22.
[http://dx.doi.org/10.1002/bies.950160103] [PMID: 8141804]
[13]
Lohman, T.M.; Bjornson, K.P. Mechanisms of helicase-catalyzed DNA unwinding. Annu. Rev. Biochem., 1996, 65(1), 169-214.
[http://dx.doi.org/10.1146/annurev.bi.65.070196.001125] [PMID: 8811178]
[14]
Abdel-Monem, M.; Dürwald, H.; Hoffmann-Berling, H. Enzymic unwinding of DNA. 2. Chain separation by an ATP-dependent DNA unwinding enzyme. Eur. J. Biochem., 1976, 65(2), 441-449.
[http://dx.doi.org/10.1111/j.1432-1033.1976.tb10359.x] [PMID: 133023]
[15]
Matson, S.W.; Kaiser-Rogers, K.A. DNA helicases. Annu. Rev. Biochem., 1990, 59(1), 289-329.
[http://dx.doi.org/10.1146/annurev.bi.59.070190.001445] [PMID: 2165383]
[16]
Blattner, F.R.; Plunkett, G., III; Bloch, C.A.; Perna, N.T.; Burland, V.; Riley, M.; Collado-Vides, J.; Glasner, J.D.; Rode, C.K.; Mayhew, G.F.; Gregor, J.; Davis, N.W.; Kirkpatrick, H.A.; Goeden, M.A.; Rose, D.J.; Mau, B.; Shao, Y. The complete genome sequence of Escherichia coli K-12. Science, 1997, 277(5331), 1453-1462.
[http://dx.doi.org/10.1126/science.277.5331.1453] [PMID: 9278503]
[17]
Kunst, F.; Ogasawara, N.; Moszer, I.; Albertini, A.M.; Alloni, G.; Azevedo, V.; Bertero, M.G.; Bessières, P.; Bolotin, A.; Borchert, S.; Borriss, R.; Boursier, L.; Brans, A.; Braun, M.; Brignell, S.C.; Bron, S.; Brouillet, S.; Bruschi, C.V.; Caldwell, B.; Capuano, V.; Carter, N.M.; Choi, S.K.; Codani, J-J.; Connerton, I.F.; Cummings, N.J.; Daniel, R.A.; Denizot, F.; Devine, K.M.; Düsterhöft, A.; Ehrlich, S.D.; Emmerson, P.T.; Entian, K.D.; Errington, J.; Fabret, C.; Ferrari, E.; Foulger, D.; Fritz, C.; Fujita, M.; Fujita, Y.; Fuma, S.; Galizzi, A.; Galleron, N.; Ghim, S.Y.; Glaser, P.; Goffeau, A.; Golightly, E.J.; Grandi, G.; Guiseppi, G.; Guy, B.J.; Haga, K.; Haiech, J.; Harwood, C.R.; Hénaut, A.; Hilbert, H.; Holsappel, S.; Hosono, S.; Hullo, M.F.; Itaya, M.; Jones, L.; Joris, B.; Karamata, D.; Kasahara, Y.; Klaerr-Blanchard, M.; Klein, C.; Kobayashi, Y.; Koetter, P.; Koningstein, G.; Krogh, S.; Kumano, M.; Kurita, K.; Lapidus, A.; Lardinois, S.; Lauber, J.; Lazarevic, V.; Lee, S.M.; Levine, A.; Liu, H.; Masuda, S.; Mauël, C.; Médigue, C.; Medina, N.; Mellado, R.P.; Mizuno, M.; Moestl, D.; Nakai, S.; Noback, M.; Noone, D.; O’Reilly, M.; Ogawa, K.; Ogiwara, A.; Oudega, B.; Park, S.H.; Parro, V.; Pohl, T.M.; Portetelle, D.; Porwollik, S.; Prescott, A.M.; Presecan, E.; Pujic, P.; Purnelle, B.; Rapoport, G.; Rey, M.; Reynolds, S.; Rieger, M.; Rivolta, C.; Rocha, E.; Roche, B.; Rose, M.; Sadaie, Y.; Sato, T.; Scanlan, E.; Schleich, S.; Schroeter, R.; Scoffone, F.; Sekiguchi, J.; Sekowska, A.; Seror, S.J.; Serror, P.; Shin, B.S.; Soldo, B.; Sorokin, A.; Tacconi, E.; Takagi, T.; Takahashi, H.; Takemaru, K.; Takeuchi, M.; Tamakoshi, A.; Tanaka, T.; Terpstra, P.; Tognoni, A.; Tosato, V.; Uchiyama, S.; Vandenbol, M.; Vannier, F.; Vassarotti, A.; Viari, A.; Wambutt, R.; Wedler, E.; Wedler, H.; Weitzenegger, T.; Winters, P.; Wipat, A.; Yamamoto, H.; Yamane, K.; Yasumoto, K.; Yata, K.; Yoshida, K.; Yoshikawa, H-F.; Zumstein, E.; Yoshikawa, H.; Danchin, A. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature, 1997, 390(6657), 249-256.
[http://dx.doi.org/10.1038/36786] [PMID: 9384377]
[18]
Heidelberg, J.F.; Eisen, J.A.; Nelson, W.C.; Clayton, R.A.; Gwinn, M.L.; Dodson, R.J.; Haft, D.H.; Hickey, E.K.; Peterson, J.D.; Umayam, L.; Gill, S.R.; Nelson, K.E.; Read, T.D.; Tettelin, H.; Richardson, D.; Ermolaeva, M.D.; Vamathevan, J.; Bass, S.; Qin, H.; Dragoi, I.; Sellers, P.; McDonald, L.; Utterback, T.; Fleishmann, R.D.; Nierman, W.C.; White, O.; Salzberg, S.L.; Smith, H.O.; Colwell, R.R.; Mekalanos, J.J.; Venter, J.C.; Fraser, C.M. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature, 2000, 406(6795), 477-483.
[http://dx.doi.org/10.1038/35020000] [PMID: 10952301]
[19]
Egan, E.S.; Waldor, M.K. Distinct replication requirements for the two Vibrio cholerae chromosomes. Cell, 2003, 114(4), 521-530.
[http://dx.doi.org/10.1016/S0092-8674(03)00611-1] [PMID: 12941279]
[20]
Médigue, C.; Krin, E.; Pascal, G.; Barbe, V.; Bernsel, A.; Bertin, P.N.; Cheung, F.; Cruveiller, S.; D’Amico, S.; Duilio, A.; Fang, G.; Feller, G.; Ho, C.; Mangenot, S.; Marino, G.; Nilsson, J.; Parrilli, E.; Rocha, E.P.C.; Rouy, Z.; Sekowska, A.; Tutino, M.L.; Vallenet, D.; von Heijne, G.; Danchin, A. Coping with cold: The genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res., 2005, 15(10), 1325-1335.
[http://dx.doi.org/10.1101/gr.4126905] [PMID: 16169927]
[21]
Xie, B.B.; Rong, J.C.; Tang, B.L.; Wang, S.; Liu, G.; Qin, Q.L.; Zhang, X.Y.; Zhang, W.; She, Q.; Chen, Y.; Li, F.; Li, S.; Chen, X.L.; Luo, H.; Zhang, Y.Z. Evolutionary trajectory of the replication mode of bacterial replicons. MBio, 2021, 12(1), e02745-e20.
[http://dx.doi.org/10.1128/mBio.02745-20] [PMID: 33500342]
[22]
Zhao, H.L.; Yang, J.; Chen, X.L.; Su, H.N.; Zhang, X.Y.; Huang, F.; Zhou, B.C.; Xie, B.B. Optimization of fermentation conditions for the production of the M23 protease Pseudoalterin by deep-sea Pseudoalteromonas sp. CF6-2 with artery powder as an inducer. Molecules, 2014, 19(4), 4779-4790.
[http://dx.doi.org/10.3390/molecules19044779] [PMID: 24743935]
[23]
Manthei, K.A.; Hill, M.C.; Burke, J.E.; Butcher, S.E.; Keck, J.L. Structural mechanisms of DNA binding and unwinding in bacterial RecQ helicases. Proc. Natl. Acad. Sci. USA, 2015, 112(14), 4292-4297.
[http://dx.doi.org/10.1073/pnas.1416746112] [PMID: 25831501]
[24]
Sutherland, H.G.E.; Mumford, G.K.; Newton, K.; Ford, L.V.; Farrall, R.; Dellaire, G.; Cáceres, J.F.; Bickmore, W.A. Large-scale identification of mammalian proteins localized to nuclear sub-compartments. Hum. Mol. Genet., 2001, 10(18), 1995-2011.
[http://dx.doi.org/10.1093/hmg/10.18.1995] [PMID: 11555636]
[25]
Martín, V.; Chahwan, C.; Gao, H.; Blais, V.; Wohlschlegel, J.; Yates, J.R., III; McGowan, C.H.; Russell, P. Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. EMBO J., 2006, 25(11), 2564-2574.
[http://dx.doi.org/10.1038/sj.emboj.7601141] [PMID: 16710300]
[26]
Awad, S.; Ryan, D.; Prochasson, P.; Owen-Hughes, T.; Hassan, A.H. The Snf2 homolog Fun30 acts as a homodimeric ATP-dependent chromatin-remodeling enzyme. J. Biol. Chem., 2010, 285(13), 9477-9484.
[http://dx.doi.org/10.1074/jbc.M109.082149] [PMID: 20075079]
[27]
Shaked, H.; Avivi-Ragolsky, N.; Levy, A.A. Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics, 2006, 173(2), 985-994.
[http://dx.doi.org/10.1534/genetics.105.051664] [PMID: 16547115]
[28]
Liu, T.; Wan, L.; Wu, Y.; Chen, J.; Huang, J. hSWS1·SWSAP1 is an evolutionarily conserved complex required for efficient homologous recombination repair. J. Biol. Chem., 2011, 286(48), 41758-41766.
[http://dx.doi.org/10.1074/jbc.M111.271080] [PMID: 21965664]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy