Structure-Based Genetic Analysis of Hel308a in the Hyperthermophilic Archaeon Sulfolobus islandicus

Xueguo Song; Jinfeng Ni; Yulong Shen

doi:10.1016/j.jgg.2016.03.003

Volume 43 Issue 6

Jun. 2016

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2016 > 43(6): 405-413

PDF( 1468 KB)

Structure-Based Genetic Analysis of Hel308a in the Hyperthermophilic Archaeon Sulfolobus islandicus

doi: 10.1016/j.jgg.2016.03.003

State Key Laboratory of Microbial Technology, Shandong University, Jinan 250100, China

More Information

Corresponding author: E-mail address: yulgshen@sdu.edu.cn (Yulong Shen)
Received Date: 2015-10-22
Accepted Date: 2016-03-07
Rev Recd Date: 2016-03-06

Available Online: 2016-03-17

Publish Date: 2016-06-20

Abstract

Abstract

In archaea, the HEL308 homolog Hel308a (or Hjm) is implicated in stalled replication fork repair. The biochemical properties and structures of Hjm homologs are well documented, but in vivo mechanistic information is limited. Herein, a structure-based functional analysis of Hjm was performed in the genetically tractable hyperthermophilic archaeon, Sulfolobus islandicus. Results showed that domain V and residues within it, which affect Hjm activity and regulation, are essential and that the domain V-truncated mutants and site-directed mutants within domain V cannot complement hjm chromosomal deletion. Chromosomal hjm deletion can be complemented by ectopic expression of hjm under the control of its native promoter but not an artificial arabinose promoter. Cellular Hjm levels are kept constant under ultraviolet (UV) and methyl methanesulfonate (MMS) treatment conditions in a strain carrying a plasmid to induce Hjm overexpression. These results suggest that Hjm expression and activity are tightly controlled, probably at the translational level.
- Archaea,
- Hel308a,
- Replication fork regression,
- Genetic complementation

FullText(HTML)

References(41)

References

[1]	Atkinson, J., McGlynn, P. Replication fork reversal and the maintenance of genome stability Nucleic Acids Res., 37 (2009),pp. 3475-3492
[2]	Büttner, K., Nehring, S., Hopfner, K.P. Structural basis for DNA duplex separation by a superfamily-2 helicase Nat. Struct. Mol. Biol., 14 (2007),pp. 647-652
[3]	Barry, E.R., Bell, S.D. DNA replication in the archaea Microbiol. Mol. Biol. Rev., 70 (2006),pp. 876-887
[4]	Brennan, R.G. The winged-helix DNA-binding motif: another helix-turn-helix takeoff Cell, 74 (1993),pp. 773-776
[5]	Bugreev, D.V., Rossi, M.J., Mazin, A.V. Cooperation of RAD51 and RAD54 in regression of a model replication fork Nucleic Acids Res., 39 (2011),pp. 2153-2164
[6]	Deng, L., Zhu, H., Chen, Z. et al. Extremophiles, 13 (2009),pp. 735-746
[7]	Doherty, A.J., Serpell, L.C., Ponting, C.P. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA Nucleic Acids Res., 24 (1996),pp. 2488-2497
[8]	Fujikane, R., Komori, K., Shinagawa, H. et al. J. Biol. Chem., 280 (2005),pp. 12351-12358
[9]	Fujikane, R., Shinagawa, H., Ishino, Y. The archaeal Hjm helicase has recQ-like functions, and may be involved in repair of stalled replication fork Genes Cells, 11 (2006),pp. 99-110
[10]	Gajiwala, K.S., Burley, S.K. Winged helix proteins Curr. Opin. Struc. Biol., 10 (2000),pp. 110-116
[11]	Grompone, G., Ehrlich, D., Michel, B. Cells defective for replication restart undergo replication fork reversal EMBO Rep., 5 (2004),pp. 607-612
[12]	Guy, C.P., Bolt, E.L. Nucleic Acids Res., 33 (2005),pp. 3678-3690
[13]	Hong, Y., Chu, M., Li, Y. et al. Dissection of the functional domains of an archaeal Holliday junction helicase DNA Repair, 11 (2012),pp. 102-111
[14]	Huffman, J.L., Brennan, R.G. Prokaryotic transcription regulators: more than just the helix-turn-helix motif Curr. Opin. Struc. Biol., 12 (2002),pp. 98-106
[15]	Kelman, Z., White, M.F. Archaeal DNA replication and repair Curr. Opin. Microbiol., 8 (2005),pp. 669-676
[16]	Kitano, K., Kim, S.-Y., Hakoshima, T. Structural basis for DNA strand separation by the unconventional winged-helix domain of RecQ helicase WRN Structure, 18 (2010),pp. 177-187
[17]	Li, Z., Lu, S., Hou, G. et al. J. Bacteriol., 190 (2008),pp. 3006-3017
[18]	Liu, Y., West, S.C. Happy Hollidays: 40th anniversary of the Holliday junction Nat. Rev. Mol. Cell Biol., 5 (2004),pp. 937-944
[19]	Machwe, A., Xiao, L., Groden, J. et al. The Werner and Bloom syndrome proteins catalyze regression of a model replication fork Biochemistry, 45 (2006),pp. 13939-13946
[20]	Machwe, A., Xiao, L., Lloyd, R.G. et al. Nucleic Acids Res., 35 (2007),pp. 5729-5747
[21]	Marini, F., Wood, R.D. A human DNA helicase homologous to the DNA cross-link sensitivity protein Mus308 J. Biol. Chem., 277 (2002),pp. 8716-8723
[22]	McGlynn, P., Lloyd, R.G. Rescue of stalled replication forks by RecG: simultaneous translocation on the leading and lagging strand templates supports an active DNA unwinding model of fork reversal and Holliday junction formation Proc. Natl. Acad. Sci. USA, 98 (2001),pp. 8227-8234
[23]	Michel, B., Grompone, G., Florès, M.-J. et al. Multiple pathways process stalled replication forks Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 12783-12788
[24]	Moldovan, G.-L., Madhavan, M.V., Mirchandani, K.D. et al. DNA polymerase POLN participates in cross-link repair and homologous recombination Mol. Cell. Biol., 30 (2010),pp. 1088-1096
[25]	Oyama, T., Oka, H., Mayanagi, K. et al. Atomic structures and functional implications of the archaeal RecQ-like helicase Hjm BMC Struct. Biol., 9 (2009),p. 2
[26]	Peng, N., Xia, Q., Chen, Z. et al. An upstream activation element exerting differential transcriptional activation on an archaeal promoter Mol. Microbiol., 74 (2009),pp. 928-939
[27]	Ralf, C., Hickson, I.D., Wu, L. The Bloom's syndrome helicase can promote the regression of a model replication fork J. Biol. Chem., 281 (2006),pp. 22839-22846
[28]	Richards, J.D., Johnson, K.A., Liu, H. et al. Structure of the DNA repair helicase hel308 reveals DNA binding and autoinhibitory domains J. Biol. Chem., 283 (2008),pp. 5118-5126
[29]	Shen, Y., Musti, K., Hiramoto, M. et al. J. Biol. Chem., 276 (2001),pp. 27376-27383
[30]	Shinagawa, H., Iwasaki, H. Processing the Holliday junction in homologous recombination Trends Biochem. Sci., 21 (1996),pp. 107-111
[31]	Snider, J., Thibault, G., Houry, W.A. The AAA+ superfamily of functionally diverse proteins Genome Biol., 9 (2008),p. 216
[32]	Tafel, A.A., Wu, L., McHugh, P.J. Human HEL308 localizes to damaged replication forks and unwinds lagging strand structures J. Biol. Chem., 286 (2011),pp. 15832-15840
[33]	Takata, K., Reh, S., Tomida, J. et al. Human DNA helicase HELQ participates in DNA interstrand crosslink tolerance with ATR and RAD51 paralogs Nat. Commun., 4 (2013),p. 2338
[34]	Tubbs, J.L., Pegg, A.E., Tainer, J.A. DNA binding, nucleotide flipping, and the helix-turn-helix motif in base repair by O 6-alkylguanine-DNA alkyltransferase and its implications for cancer chemotherapy DNA Repair, 6 (2007),pp. 1100-1115
[35]	Woodman, I., Bolt, E. Molecular biology of Hel308 helicase in archaea Biochem. Soc. Trans., 37 (2009),p. 74
[36]	Woodman, I., Bolt, E. Winged helix domains with unknown function in Hel308 and related helicases Biochem. Soc. Trans., 39 (2011),pp. 140-144
[37]	Woodman, I.L., Brammer, K., Bolt, E.L. Physical interaction between archaeal DNA repair helicase Hel308 and replication protein A (RPA) DNA Repair, 10 (2011),pp. 306-313
[38]	Woodman, I.L., Briggs, G.S., Bolt, E.L. Archaeal Hel308 domain V couples DNA binding to ATP hydrolysis and positions DNA for unwinding over the helicase ratchet J. Mol. Biol., 374 (2007),pp. 1139-1144
[39]	Zhang, C., Cooper, T.E., Krause, D.J. et al. Appl. Environ. Microb., 79 (2013),pp. 5539-5549
[40]	Zhang, C., Guo, L., Deng, L. et al. Revealing the essentiality of multiple archaeal pcna genes using a mutant propagation assay based on an improved knockout method Microbiology, 156 (2010),pp. 3386-3397
[41]	Zheng, T., Huang, Q., Zhang, C. et al. Appl. Environ. Microb., 78 (2012),pp. 568-574