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Journal of Virology, February 2000, p. 1332-1341, Vol. 74, No. 3
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Two Widely Spaced Initiator Binding Sites Create an HMG1-Dependent Parvovirus Rolling-Hairpin Replication Origin

Susan F. Cotmore,1 Jesper Christensen,2 and Peter Tattersall1,3,*

Departments of Laboratory Medicine1 and Genetics,3 Yale University School of Medicine, New Haven, Connecticut 06510, and Department for Virology and Immunology, The Royal Veterinary and Agricultural University of Copenhagen, 1870 Frederiksberg C, Denmark2

Received 4 August 1999/Accepted 4 November 1999

Minute virus of mice (MVM) replicates via a linearized form of rolling-circle replication in which the viral nickase, NS1, initiates DNA synthesis by introducing a site-specific nick into either of two distinct origin sequences. In vitro nicking and replication assays with substrates that had deletions or mutations were used to explore the sequences and structural elements essential for activity of one of these origins, located in the right-end (5') viral telomere. This structure contains 248 nucleotides, most-favorably arranged as a simple hairpin with six unpaired bases. However, a pair of opposing NS1 binding sites, located near its outboard end, create a 33-bp palindrome that could potentially assume an alternate cruciform configuration and hence directly bind HMG1, the essential cofactor for this origin. The palindromic nature of this sequence, and thus its ability to fold into a cruciform, was dispensable for origin function, as was the NS1 binding site occupying the inboard arm of the palindrome. In contrast, the NS1 site in the outboard arm was essential for initiation, even though positioned 120 bp from the nick site. The specific sequence of the nick site and an additional NS1 binding site which directly orients NS1 over the initiation site were also essential and delimited the inboard border of the minimal right-end origin. DNase I and hydroxyl radical footprints defined sequences protected by NS1 and suggest that HMG1 allows the NS1 molecules positioned at each end of the origin to interact, creating a distortion characteristic of a double helical loop.

* Corresponding author. Mailing address: Department of Laboratory Medicine, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510. Phone: (203) 785-4586. Fax: (203) 688-7340. E-mail: peter.tattersall{at}yale.edu.

Journal of Virology, February 2000, p. 1332-1341, Vol. 74, No. 3
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Cotmore, S. F., Gottlieb, R. L., Tattersall, P. (2007). Replication Initiator Protein NS1 of the Parvovirus Minute Virus of Mice Binds to Modular Divergent Sites Distributed throughout Duplex Viral DNA. J. Virol. 81: 13015-13027 [Abstract] [Full Text]  
  • Burnett, E., Cotmore, S. F., Tattersall, P. (2006). Segregation of a Single Outboard Left-End Origin Is Essential for the Viability of Parvovirus Minute Virus of Mice. J. Virol. 80: 10879-10883 [Abstract] [Full Text]  
  • Cotmore, S. F., Tattersall, P. (2005). Genome Packaging Sense Is Controlled by the Efficiency of the Nick Site in the Right-End Replication Origin of Parvoviruses Minute Virus of Mice and LuIII. J. Virol. 79: 2287-2300 [Abstract] [Full Text]  
  • Ravin, N. V., Kuprianov, V. V., Gilcrease, E. B., Casjens, S. R. (2003). Bidirectional replication from an internal ori site of the linear N15 plasmid prophage. Nucleic Acids Res 31: 6552-6560 [Abstract] [Full Text]  
  • Willwand, K., Moroianu, A., Horlein, R., Stremmel, W., Rommelaere, J. (2002). Specific interaction of the nonstructural protein NS1 of minute virus of mice (MVM) with [ACCA]2 motifs in the centre of the right-end MVM DNA palindrome induces hairpin-primed viral DNA replication. J. Gen. Virol. 83: 1659-1664 [Abstract] [Full Text]  
  • Christensen, J., Cotmore, S. F., Tattersall, P. (2001). Minute Virus of Mice Initiator Protein NS1 and a Host KDWK Family Transcription Factor Must Form a Precise Ternary Complex with Origin DNA for Nicking To Occur. J. Virol. 75: 7009-7017 [Abstract] [Full Text]  
  • Nuesch, J. P. F., Christensen, J., Rommelaere, J. (2001). Initiation of Minute Virus of Mice DNA Replication Is Regulated at the Level of Origin Unwinding by Atypical Protein Kinase C Phosphorylation of NS1. J. Virol. 75: 5730-5739 [Abstract] [Full Text]  


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