Segregation of a Single Outboard Left-End Origin Is Essential for the Viability of Parvovirus Minute Virus of Mice
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| Published in | Journal of Virology Vol. 80; no. 21; pp. 10879 - 10883 |
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| Main Authors | , , |
| Format | Journal Article |
| Language | English |
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American Society for Microbiology
01.11.2006
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| ISSN | 0022-538X 1098-5514 |
| DOI | 10.1128/JVI.01501-06 |
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During DNA replication, the hairpin telomeres of Minute Virus of Mice (MVM) are extended and copied to create imperfectly palindromic duplex junction sequences that bridge adjacent genomes in concatameric replicative-form DNA. These are resolved by the viral initiator protein, NS1, but mechanisms employed at the two telomeres differ. Left-end:left-end junctions are resolved asymmetrically at a single site, OriL TC , by NS1 acting in concert with a host factor, parvovirus initiation factor (PIF). Replication segregates doublet and triplet sequences, initially present as unpaired nucleotides in the bubble region of the left-end hairpin stem, to either side of the junction. These act as spacers between the NS1 and PIF binding sites, and their asymmetric distribution sets up active (OriL TC ) and inactive (OriL GAA ) forms of OriL. We used a reverse genetic approach to disrupt this asymmetry and found that neither opposing doublets nor triplets in the hairpin bubble were tolerated. Viable mutants were isolated at low frequency and found to contain second-site mutations that either restored the asymmetry or crippled one PIF binding site. These mutations either inactivated the inboard or activated the outboard form of OriL, a polarity that strongly suggests that, in the genus Parvovirus , an active inboard OriL is lethal. During DNA replication, the hairpin telomeres of Minute Virus of Mice (MVM) are extended and copied to create imperfectly palindromic duplex junction sequences that bridge adjacent genomes in concatameric replicative-form DNA. These are resolved by the viral initiator protein, NS1, but mechanisms employed at the two telomeres differ. Left-end:left-end junctions are resolved asymmetrically at a single site, OriL sub(TC), by NS1 acting in concert with a host factor, parvovirus initiation factor (PIF). Replication segregates doublet and triplet sequences, initially present as unpaired nucleotides in the bubble region of the left-end hairpin stem, to either side of the junction. These act as spacers between the NS1 and PIF binding sites, and their asymmetric distribution sets up active (OriL sub(TC)) and inactive (OriL sub(GAA)) forms of OriL. We used a reverse genetic approach to disrupt this asymmetry and found that neither opposing doublets nor triplets in the hairpin bubble were tolerated. Viable mutants were isolated at low frequency and found to contain second-site mutations that either restored the asymmetry or crippled one PIF binding site. These mutations either inactivated the inboard or activated the outboard form of OriL, a polarity that strongly suggests that, in the genus Parvovirus, an active inboard OriL is lethal. During DNA replication, the hairpin telomeres of Minute Virus of Mice (MVM) are extended and copied to create imperfectly palindromic duplex junction sequences that bridge adjacent genomes in concatameric replicative-form DNA. These are resolved by the viral initiator protein, NS1, but mechanisms employed at the two telomeres differ. Left-end:left-end junctions are resolved asymmetrically at a single site, OriLTC, by NS1 acting in concert with a host factor, parvovirus initiation factor (PIF). Replication segregates doublet and triplet sequences, initially present as unpaired nucleotides in the bubble region of the left-end hairpin stem, to either side of the junction. These act as spacers between the NS1 and PIF binding sites, and their asymmetric distribution sets up active (OriLTC) and inactive (OriLGAA) forms of OriL. We used a reverse genetic approach to disrupt this asymmetry and found that neither opposing doublets nor triplets in the hairpin bubble were tolerated. Viable mutants were isolated at low frequency and found to contain second-site mutations that either restored the asymmetry or crippled one PIF binding site. These mutations either inactivated the inboard or activated the outboard form of OriL, a polarity that strongly suggests that, in the genus Parvovirus, an active inboard OriL is lethal.During DNA replication, the hairpin telomeres of Minute Virus of Mice (MVM) are extended and copied to create imperfectly palindromic duplex junction sequences that bridge adjacent genomes in concatameric replicative-form DNA. These are resolved by the viral initiator protein, NS1, but mechanisms employed at the two telomeres differ. Left-end:left-end junctions are resolved asymmetrically at a single site, OriLTC, by NS1 acting in concert with a host factor, parvovirus initiation factor (PIF). Replication segregates doublet and triplet sequences, initially present as unpaired nucleotides in the bubble region of the left-end hairpin stem, to either side of the junction. These act as spacers between the NS1 and PIF binding sites, and their asymmetric distribution sets up active (OriLTC) and inactive (OriLGAA) forms of OriL. We used a reverse genetic approach to disrupt this asymmetry and found that neither opposing doublets nor triplets in the hairpin bubble were tolerated. Viable mutants were isolated at low frequency and found to contain second-site mutations that either restored the asymmetry or crippled one PIF binding site. These mutations either inactivated the inboard or activated the outboard form of OriL, a polarity that strongly suggests that, in the genus Parvovirus, an active inboard OriL is lethal. During DNA replication, the hairpin telomeres of Minute Virus of Mice (MVM) are extended and copied to create imperfectly palindromic duplex junction sequences that bridge adjacent genomes in concatameric replicative-form DNA. These are resolved by the viral initiator protein, NS1, but mechanisms employed at the two telomeres differ. Left-end:left-end junctions are resolved asymmetrically at a single site, OriLTC, by NS1 acting in concert with a host factor, parvovirus initiation factor (PIF). Replication segregates doublet and triplet sequences, initially present as unpaired nucleotides in the bubble region of the left-end hairpin stem, to either side of the junction. These act as spacers between the NS1 and PIF binding sites, and their asymmetric distribution sets up active (OriLTC) and inactive (OriLGAA) forms of OriL. We used a reverse genetic approach to disrupt this asymmetry and found that neither opposing doublets nor triplets in the hairpin bubble were tolerated. Viable mutants were isolated at low frequency and found to contain second-site mutations that either restored the asymmetry or crippled one PIF binding site. These mutations either inactivated the inboard or activated the outboard form of OriL, a polarity that strongly suggests that, in the genus Parvovirus, an active inboard OriL is lethal. |
| Author | Peter Tattersall Erik Burnett Susan F. Cotmore |
| AuthorAffiliation | Departments of Laboratory Medicine, 1 Genetics, Yale University Medical School, 333 Cedar Street, New Haven, Connecticut 067510 2 |
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| CitedBy_id | crossref_primary_10_1016_j_virol_2006_11_006 crossref_primary_10_1016_j_jviromet_2015_11_022 crossref_primary_10_1371_journal_ppat_1000391 crossref_primary_10_1016_j_jviromet_2023_114870 crossref_primary_10_1128_JVI_01450_12 crossref_primary_10_1007_s00203_015_1093_4 crossref_primary_10_1016_j_virusres_2021_198574 crossref_primary_10_1016_j_virusres_2018_12_007 |
| Cites_doi | 10.1002/j.1460-2075.1994.tb06732.x 10.1128/JVI.74.3.1332-1341.2000 10.1128/jvi.69.1.239-246.1995 10.1128/JVI.72.10.8002-8012.1998 10.1128/JVI.77.16.8650-8660.2003 10.1128/MCB.19.11.7741 10.1128/JVI.75.15.7009-7017.2001 10.1128/JVI.72.11.8477-8484.1998 10.1128/jvi.69.9.5506-5515.1995 10.1074/jbc.273.28.17756 10.1038/sj.onc.1209080 10.1128/JVI.76.13.6518-6531.2002 10.1128/JVI.79.4.2287-2300.2005 10.1006/viro.1994.1363 10.1093/nar/23.21.4353 10.1006/jmbi.2000.5198 |
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| Keywords | Virus Origin Parvovirus Microbiology Parvoviridae Parvovirinae Virology Mouse minute virus |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Corresponding author. Mailing address: Departments of Laboratory Medicine and Genetics, Yale University Medical School, 333 Cedar St., CB408, New Haven, CT 067510. Phone: (203) 785-4586. Fax: (203) 688-7340. E-mail: peter.tattersall@yale.edu. Present address: Lawrence Livermore National Laboratory, Livermore, CA 94551. |
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| References | e_1_3_2_9_2 e_1_3_2_15_2 e_1_3_2_8_2 e_1_3_2_16_2 e_1_3_2_7_2 e_1_3_2_17_2 e_1_3_2_6_2 e_1_3_2_18_2 e_1_3_2_19_2 (e_1_3_2_12_2) 2006 e_1_3_2_20_2 e_1_3_2_5_2 e_1_3_2_11_2 e_1_3_2_4_2 e_1_3_2_3_2 (e_1_3_2_13_2) 2006 e_1_3_2_2_2 e_1_3_2_14_2 (e_1_3_2_10_2) 2006 10627544 - J Virol. 2000 Feb;74(3):1332-41 15681430 - J Virol. 2005 Feb;79(4):2287-300 7501456 - Nucleic Acids Res. 1995 Nov 11;23(21):4353-62 8009857 - Virology. 1994 Jul;202(1):466-70 9765384 - J Virol. 1998 Nov;72(11):8477-84 9651376 - J Biol Chem. 1998 Jul 10;273(28):17756-62 10523663 - Mol Cell Biol. 1999 Nov;19(11):7741-50 7983715 - J Virol. 1995 Jan;69(1):239-46 12050365 - J Virol. 2002 Jul;76(13):6518-31 16314846 - Oncogene. 2006 Feb 23;25(8):1125-42 9733839 - J Virol. 1998 Oct;72(10):8002-12 11743720 - J Mol Biol. 2001 Dec 14;314(5):1029-39 8076610 - EMBO J. 1994 Sep 1;13(17):4145-52 11435581 - J Virol. 2001 Aug;75(15):7009-17 12885883 - J Virol. 2003 Aug;77(16):8650-60 7636996 - J Virol. 1995 Sep;69(9):5506-15 |
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Mendeley... During DNA replication, the hairpin telomeres of Minute Virus of Mice (MVM) are extended and copied to create imperfectly palindromic duplex junction sequences... |
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| StartPage | 10879 |
| SubjectTerms | Animals Base Sequence Binding Sites - genetics Biological and medical sciences Cell Line DNA Replication - genetics DNA, Viral - biosynthesis DNA, Viral - chemistry DNA, Viral - genetics Fundamental and applied biological sciences. Psychology Genes, Lethal Genes, Viral Genome and Regulation of Viral Gene Expression Mice Microbiology Minute virus of mice Minute Virus of Mice - genetics Minute Virus of Mice - physiology Miscellaneous Molecular Sequence Data Mutation Nucleic Acid Conformation Parvovirus Phenotype Replication Origin Telomere - genetics Telomere - metabolism Virology |
| Title | Segregation of a Single Outboard Left-End Origin Is Essential for the Viability of Parvovirus Minute Virus of Mice |
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