Retrovirus variation and reverse transcription: abnormal strand transfers result in retrovirus genetic variation

Temin, H M

doi:10.1073/pnas.90.15.6900

Cited by 310HIV Research and TreatmentHIV/AIDS drug development and treatmentEvolution and Genetic Dynamics

Retrovirus variation and reverse transcription: abnormal strand transfers result in retrovirus genetic variation

Open access

Temin, H M·1993·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.90.15.6900PMC PMC47042

Open this paper in CoChat — free account

Abstract

Human immunodeficiency virus variation is extensive and is based on numerous mistakes in reverse transcription. All retrovirus replication requires two strand transfers (growing point jumps) to synthesize the complete provirus. I propose that the numerous mistakes in reverse transcription are the result of this requirement for the two strand transfers needed to form the provirus.

Integrity signals

Registry

Crossref · 10.1073/pnas.90.15.6900

Cites

37 of 37 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Irrespective of whether the first strand transfer is intramolecular, intermolecular, or random, these mechanisms are likely to contribute to genetic variation among retroviruses during DNA synthesis because of errors during reverse transcription.
“Irrespective of the nature of the first strand transfer to be intramolecular, intermolecular, or random, they all are likely to contribute toward genetic variation among retroviruses during DNA synthesis, owing to the numerous errors occurring during reverse transcription (Temin 1993).”
From Beyond reverse transcription: molecular mechanisms and emerging paradigms in retroviral replication (2026) · cites this paper as Temin 1993

Frameshift Mutations and the Genetic Code
Streisinger, G., Okada, Y., Emrich, J., Newton, J., Tsugita, A., Terzaghi, E., & Inouye, M. (1966) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1966.031.01.014 · Cited by 1,400 · see citing works
The accuracy of reverse transcriptase from HIV-1
Roberts, J. D., Bebenek, K., & Kunkel, T. A. (1988) · Science · doi:10.1126/science.2460925 · Cited by 997 · see citing works
Die Molekularbiologie der Tumorviren
Sauer, G. (1977) · Die Naturwissenschaften · doi:10.1007/bf00483548 · Cited by 943 · see citing works
Fidelity of HIV-1 reverse transcriptase
Preston, B. D., Poiesz, B. J., & Loeb, L. A. (1988) · Science · doi:10.1126/science.2460924 · Cited by 931 · see citing works
Structure, Replication, and Recombination of Retrovirus Genomes: Some Unifying Hypotheses
Coffin, J. M. (1979) · Journal of General Virology · doi:10.1099/0022-1317-42-1-1 · Cited by 522 · see citing works
Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination.
Hu, W. S., & Temin, H. M. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.4.1556 · Cited by 476 · see citing works
Self-citation
Rapid development of isolate-specific neutralizing antibodies after primary HIV-1 infection and consequent emergence of virus variants which resist neutralization by autologous sera
Albert, J., Abrahamsson, B., Nagy, K., Aurelius, E., Gaines, H., Nyström, G., & Fenyõ, É. M. (1990) · AIDS · doi:10.1097/00002030-199002000-00002 · Cited by 398 · see citing works
Mechanism of DNA Strand Transfer Reactions Catalyzed by HIV-1 Reverse Transcriptase
Peliska, J. A., & Benkovic, S. J. (1992) · Science · doi:10.1126/science.1279806 · Cited by 332 · see citing works
Specificity and Mechanism of Error-prone Replication by Human Immunodeficiency Virus-1 Reverse Transcriptase
Bębenek, K., Abbotts, J., Roberts, J. D., Wilson, S. H., & Kunkel, T. A. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84799-3 · Cited by 310 · see citing works
Base mispair extension kinetics. Comparison of DNA polymerase alpha and reverse transcriptase.
Mendelman, L. V., Petruska, J. A., & Goodman, M. F. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)39981-8 · Cited by 290 · see citing works
MECHANISMS OF SPONTANEOUS AND INDUCED FRAMESHIFT MUTATION IN BACTERIOPHAGE T4
Streisinger, G., & Owen, J. E. (1985) · Genetics · doi:10.1093/genetics/109.4.633 · Cited by 287 · see citing works
Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: substitutions, frameshifts, and hypermutations.
Pathak, V. K., & Temin, H. M. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6019 · Cited by 279 · see citing works
Self-citation
FRAMESHIFT MUTATION: DETERMINANTS OF SPECIFICITY
Ripley, L. S. (1990) · Annual Review of Genetics · doi:10.1146/annurev.ge.24.120190.001201 · Cited by 239 · see citing works
Template switching by reverse transcriptase during DNA synthesis
Luo, G. X., & Taylor, J. M. (1990) · Journal of Virology · doi:10.1128/jvi.64.9.4321-4328.1990 · Cited by 225 · see citing works
Ordered Interstrand and Intrastrand DNA Transfer During Reverse Transcription
Panganiban, A. T., & Fiore, D. (1988) · Science · doi:10.1126/science.2457948 · Cited by 221 · see citing works
Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: deletions and deletions with insertions.
Pathak, V. K., & Temin, H. M. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6024 · Cited by 214 · see citing works
Self-citation
Human immunodeficiency virus as a prototypic complex retrovirus
Cullen, B. R. (1991) · Journal of Virology · doi:10.1128/jvi.65.3.1053-1056.1991 · Cited by 194 · see citing works
Rate and Mechanism of Nonhomologous Recombination During a Single Cycle of Retroviral Replication
Zhang, J., & Temin, H. M. (1993) · Science · doi:10.1126/science.8421784 · Cited by 164 · see citing works
Self-citation
Molecular Matchmakers
Sancar, A., & Hearst, J. E. (1993) · Science · doi:10.1126/science.8451638 · Cited by 158 · see citing works
Reverse transcriptases and genomic variability: the accuracy of DNA replication is enzyme specific and sequence dependent.
Ricchetti, M., & BUC, H. C. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb08278.x · Cited by 142 · see citing works
Requirements for strand transfer between internal regions of heteropolymer templates by human immunodeficiency virus reverse transcriptase
DeStefano, J. J., Mallaber, L. M., Rodrı́guez-Rodrı́guez, L., Fay, P. J., & Bambara, R. A. (1992) · Journal of Virology · doi:10.1128/jvi.66.11.6370-6378.1992 · Cited by 130 · see citing works
Sex and recombination in retroviruses
Temin, H. M. (1991) · Trends in Genetics · doi:10.1016/0168-9525(91)90272-r · Cited by 130 · see citing works
Self-citation
Mechanism of Transduction by Retroviruses
Swain, A., & Coffin, J. M. (1992) · Science · doi:10.1126/science.1371365 · Cited by 123 · see citing works
Characterization of large deletions occurring during a single round of retrovirus vector replication: novel deletion mechanism involving errors in strand transfer
Pulsinelli, G. A., & Temin, H. M. (1991) · Journal of Virology · doi:10.1128/jvi.65.9.4786-4797.1991 · Cited by 107 · see citing works
Self-citation
High-frequency deletion between homologous sequences during retrotransposition of Ty elements in Saccharomyces cerevisiae.
Xu, H., & Boeke, J. D. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.23.8553 · Cited by 94 · see citing works
On the fidelity of DNA replication. Lack of exodeoxyribonuclease activity and error-correcting function in avian myeloblastosis virus DNA polymerase
Battula, N., & Loeb, L. A. (1976) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)33789-4 · Cited by 90 · see citing works
HIV mutation rate
Nowak, M. A. (1990) · Nature · doi:10.1038/347522a0 · Cited by 85 · see citing works
Abortive reverse transcription by mutants of Moloney murine leukemia virus deficient in the reverse transcriptase-associated RNase H function
Tanese, N., Telesnitsky, A., & Goff, S. P. (1991) · Journal of Virology · doi:10.1128/jvi.65.8.4387-4397.1991 · Cited by 78 · see citing works
Reverse transcription of retroviral genomes: mutations in the terminal repeat sequences
Lobel, L. I., & Goff, S. P. (1985) · Journal of Virology · doi:10.1128/jvi.53.2.447-455.1985 · Cited by 70 · see citing works
Comparison of Moloney murine leukemia virus mutation rate with the fidelity of its reverse transcriptase in vitro.
Varela‐Echavarría, A., Garvey, N., Preston, B. D., & Dougherty, J. P. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)35818-6 · Cited by 68 · see citing works
Effect of gamma radiation on retroviral recombination
Hu, W.-S., & Temin, H. M. (1992) · Journal of Virology · doi:10.1128/jvi.66.7.4457-4463.1992 · Cited by 54 · see citing works
Self-citation
Instability of large direct repeats in retrovirus vectors
Rhode, B. W., Emerman, M., & Temin, H. M. (1987) · Journal of Virology · doi:10.1128/jvi.61.3.925-927.1987 · Cited by 50 · see citing works
Self-citation
Dilute passage promotes expression of genetic and phenotypic variants of human immunodeficiency virus type 1 in cell culture
Sánchez‐Palomino, S., Rojas, J. M., Martı́nez, M. Á., Fenyö, E. M., Nájera, R., Domingo, E., & López‐Galíndez, C. (1993) · Journal of Virology · doi:10.1128/jvi.67.5.2938-2943.1993 · Cited by 46 · see citing works
3' junctions of oncogene-virus sequences and the mechanisms for formation of highly oncogenic retroviruses
Zhang, J., & Temin, H. M. (1993) · Journal of Virology · doi:10.1128/jvi.67.4.1747-1751.1993 · Cited by 38 · see citing works
Self-citation
Replication of the retroviral terminal repeat sequence during in vivo reverse transcription
Ramsey, C. A., & Panganiban, A. T. (1993) · Journal of Virology · doi:10.1128/jvi.67.7.4114-4121.1993 · Cited by 36 · see citing works
Reverse transcriptase
Beard, W. A., & Wilson, S. H. (1995) · doi:10.1093/oso/9780199634996.003.0002 · Cited by 30 · see citing works
Alteration of location of dimer linkage sequence in retroviral RNA: little effect on replication or homologous recombination
Jones, J. S., Allan, R. W., & Temin, H. M. (1993) · Journal of Virology · doi:10.1128/jvi.67.6.3151-3158.1993 · Cited by 27 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure
Ho, Y.-C., Shan, L., Hosmane, N. N., Wang, J., Laskey, S. B., Rosenbloom, D. I. S., Lai, J., Blankson, J. N., Siliciano, J. D., & Siliciano, R. F. (2013) · Cell · doi:10.1016/j.cell.2013.09.020 · Cited by 1,405 · see citing works
Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase
Mansky, L. M., & Temin, H. M. (1995) · Journal of Virology · doi:10.1128/jvi.69.8.5087-5094.1995 · Cited by 1,154 · see citing works
Self-citation
Clustered Mutations in HIV-1 Gag Are Consistently Required for Escape from Hla-B27–Restricted Cytotoxic T Lymphocyte Responses
Kelleher, A. D., Long, C., Holmes, E. C., Allen, R. L., Wilson, J., Conlon, C. P., Workman, C., Shaunak, S., Olson, K., Goulder, P., et al. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.3.375 · Cited by 448 · see citing works
High Rate of Recombination throughout the Human Immunodeficiency Virus Type 1 Genome
Jetzt, A. E., Yu, H., Klarmann, G. J., Ron, Y., Preston, B. D., & Dougherty, J. P. (2000) · Journal of Virology · doi:10.1128/jvi.74.3.1234-1240.2000 · Cited by 379 · see citing works
Human Immunodeficiency Virus Type 1 Subtype Distribution in the Worldwide Epidemic: Pathogenetic and Therapeutic Implications
Buonaguro, L., Tornesello, M. L., & Buonaguro, L. (2007) · Journal of Virology · doi:10.1128/jvi.00872-07 · Cited by 359 · see citing works
Defective HIV-1 proviruses produce novel protein-coding RNA species in HIV-infected patients on combination antiretroviral therapy
Imamichi, H., Dewar, R. L., Adelsberger, J. W., Rehm, C. A., O’Doherty, U., Paxinos, E. E., Fauci, A. S., & Lane, H. C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1609057113 · Cited by 344 · see citing works
HIV-1 replication.
Freed, E. O. (2001) · Somatic Cell and Molecular Genetics · doi:10.1023/a:1021070512287 · Cited by 307 · see citing works
Tracking a century of global expansion and evolution of HIV to drive understanding and to combat disease
Tebit, D. M., & Arts, E. J. (2010) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(10)70186-9 · Cited by 279 · see citing works
Reverse transcriptase template switching and false alternative transcripts
Cocquet, J., Chong, A., Zhang, G., & Veitia, R. A. (2006) · Genomics · doi:10.1016/j.ygeno.2005.12.013 · Cited by 269 · see citing works
Human Immunodeficiency Virus Type 1 Recombination: Rate, Fidelity, and Putative Hot Spots
Zhuang, J., Jetzt, A. E., Sun, G., Yu, H. Y., Klarmann, G. J., Ron, Y., Preston, B. D., & Dougherty, J. P. (2002) · Journal of Virology · doi:10.1128/jvi.76.22.11273-11282.2002 · Cited by 262 · see citing works
A 19-nucleotide sequence upstream of the 5’ major splice donor is part of the dimerization domain of human immunodeficiency virus 1 genomic RNA
Laughrea, M., & Jette, L. (1994) · Biochemistry · doi:10.1021/bi00249a035 · Cited by 237 · see citing works
Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure.
Moutouh, L., Corbeil, J., & Richman, D. D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.12.6106 · Cited by 235 · see citing works
Evidence for Transcript Networks Composed of Chimeric RNAs in Human Cells
Djebali, S., Lagarde, J., Kapranov, P., Lacroix, V., Borel, C., Mudge, J. M., Howald, C., Foissac, S., Ucla, C., Chrast, J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0028213 · Cited by 234 · see citing works
High-resolution human cytomegalovirus transcriptome
Gatherer, D., Seirafian, S., Cunningham, C., Holton, M., Dargan, D. J., Baluchova, K., Hector, R. D., Galbraith, J., Herzyk, P., Wilkinson, G. W. G., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115861108 · Cited by 229 · see citing works
HIV and T cell expansion in splenic white pulps is accompanied by infiltration of HIV-specific cytotoxic T lymphocytes
Cheynier, R., Henrichwark, S., Hadida, F., Pelletier, É., Oksenhendler, É., Autran, B., & Wain–Hobson, S. (1994) · Cell · doi:10.1016/0092-8674(94)90417-0 · Cited by 204 · see citing works
A dual role of the putative RNA dimerization initiation site of human immunodeficiency virus type 1 in genomic RNA packaging and proviral DNA synthesis
Paillart, J., Berthoux, L., Ottmann, M., Darlix, J., Marquet, R., Ehresmann, B., & Ehresmann, C. (1996) · Journal of Virology · doi:10.1128/jvi.70.12.8348-8354.1996 · Cited by 194 · see citing works
The puzzle of HIV-1 subtypes in Africa
Janssens, W., Buvé, A., & Nkengasong, J. N. (1997) · AIDS · doi:10.1097/00002030-199706000-00002 · Cited by 193 · see citing works
The Remarkable Frequency of Human Immunodeficiency Virus Type 1 Genetic Recombination
Onafuwa-Nuga, A., & Telesnitsky, A. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00012-09 · Cited by 174 · see citing works
Simplified Strategy for Detection of Recombinant Human Immunodeficiency Virus Type 1 Group M Isolates by gag/env Heteroduplex Mobility Assay
Heyndríckx, L., Janssens, W., Zekeng, L. A., Musonda, R. M., Anagonou, S., der Auwera, G. V., Coppens, S., Vereecken, K., Witte, K. D., Rampelbergh, R. V., et al. (2000) · Journal of Virology · doi:10.1128/jvi.74.1.363-370.2000 · Cited by 167 · see citing works
The Interaction of Vpr with Uracil DNA Glycosylase Modulates the Human Immunodeficiency Virus Type 1 In Vivo Mutation Rate
Mansky, L. M., Prévéral, S., Selig, L., Bénarous, R., & Bénichou, S. (2000) · Journal of Virology · doi:10.1128/jvi.74.15.7039-7047.2000 · Cited by 167 · see citing works
Drastic Fitness Loss in Human Immunodeficiency Virus Type 1 upon Serial Bottleneck Events
Yuste, E., Sánchez‐Palomino, S., Casado, C., Domingo, E., & López‐Galíndez, C. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.2745-2751.1999 · Cited by 156 · see citing works
Apparent Non-Canonical Trans-Splicing Is Generated by Reverse Transcriptase In Vitro
Houseley, J. M., & Tollervey, D. W. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012271 · Cited by 159 · see citing works
HIV DNA Is Frequently Present within Pathologic Tissues Evaluated at Autopsy from Combined Antiretroviral Therapy-Treated Patients with Undetectable Viral Loads
Lamers, S. L., Rose, R., Maidji, E., Agsalda‐Garcia, M., Nolan, D. J., Fogel, G. B., Salemi, M., Garcia, D. L., Bracci, P. M., Yong, W. H., et al. (2016) · Journal of Virology · doi:10.1128/jvi.00674-16 · Cited by 154 · see citing works
Ribavirin and lethal mutagenesis of poliovirus: molecular mechanisms, resistance and biological implications
Vignuzzi, M., Stone, J. K., & Andino, R. (2004) · Virus Research · doi:10.1016/j.virusres.2004.11.007 · Cited by 151 · see citing works
The origin of genetic diversity in HIV-1
Smyth, R. P., Davenport, M. P., & Mak, J. (2012) · Virus Research · doi:10.1016/j.virusres.2012.06.015 · Cited by 153 · see citing works
Non-canonical interactions in a kissing loop complex: the dimerization initiation site of HIV-1 genomic RNA
Paillart, J., Westhof, É., Ehresmann, C., Ehresmann, B., & Marquet, R. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.1096 · Cited by 151 · see citing works
Retroviral recombination can lead to linkage of reverse transcriptase mutations that confer increased zidovudine resistance
Kellam, P., & Larder, B. A. (1995) · Journal of Virology · doi:10.1128/jvi.69.2.669-674.1995 · Cited by 145 · see citing works
Mechanisms of Retroviral Recombination
Negroni, M., & BUC, H. C. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.090551 · Cited by 143 · see citing works
Molecular indetermination in the transition to error catastrophe: Systematic elimination of lymphocytic choriomeningitis virus through mutagenesis does not correlate linearly with large increases in mutant spectrum complexity
Grande-Pérez, A., Sierra, S., Castro, M. G., Domingo, E., & Lowenstein, P. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182426999 · Cited by 143 · see citing works
Retroelements and their impact on genome evolution and functioning
Gogvadze, E. V., & Buzdin, A. A. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0107-2 · Cited by 141 · see citing works
A Single Banana Streak Virus Integration Event in the Banana Genome as the Origin of Infectious Endogenous Pararetrovirus
Gayral, P., Noa-Carrazana, J. C., Lescot, M., Lheureux, F., Lockhart, B. E. L., Matsumoto, T., Piffanelli, P., & Iskra‐Caruana, M. (2008) · Journal of Virology · doi:10.1128/jvi.00212-08 · Cited by 139 · see citing works
The role of recombination in the emergence of a complex and dynamic HIV epidemic
Zhang, M., Foley, B. T., Schultz, A.-K., Macke, J. P., Bulla, I., Stanke, M., Morgenstern, B., Korber, B., & Leitner, T. (2010) · Retrovirology · doi:10.1186/1742-4690-7-25 · Cited by 132 · see citing works
Human immunodeficiency virus Type 1 nucleocapsid protein (NCp7) directs specific initiation of minus-strand DNA synthesis primed by human tRNA(Lys3) in vitro: studies of viral RNA molecules mutated in regions that flank the primer binding site
Li, X., Quan, Y., Arts, E. J., Li, Z., Preston, B. D., de ROCQUIGNY, H., Roques, B. P., Darlix, J., Kleiman, L., Parniak, M. A., et al. (1996) · Journal of Virology · doi:10.1128/jvi.70.8.4996-5004.1996 · Cited by 132 · see citing works
Dimerization of retroviral genomic RNAs: structural and functional implications
Paillart, J., Marquet, R., Skripkin, Е., Ehresmann, C., & Ehresmann, B. (1996) · Biochimie · doi:10.1016/s0300-9084(96)80010-1 · Cited by 131 · see citing works
Forward Mutation Rate of Human Immunodeficiency Virus Type 1 in a T Lymphoid Cell Line*
Mansky, L. M. (1996) · AIDS Research and Human Retroviruses · doi:10.1089/aid.1996.12.307 · Cited by 126 · see citing works
Tempo and mode of nucleotide substitutions in gag and env gene fragments in human immunodeficiency virus type 1 populations with a known transmission history
Leitner, T., Kumar, S., & Albert, J. (1997) · Journal of Virology · doi:10.1128/jvi.71.6.4761-4770.1997 · Cited by 125 · see citing works
Retrovirus mutation rates and their role in genetic variation.
Mansky, L. M. (1998) · Journal of General Virology · doi:10.1099/0022-1317-79-6-1337 · Cited by 118 · see citing works
Retroviral mutation rates and reverse transcriptase fidelity
Pathak, V. K. (2003) · Frontiers in bioscience · doi:10.2741/957 · Cited by 113 · see citing works
Mutation Patterns of the Reverse Transcriptase and Protease Genes in Human Immunodeficiency Virus Type 1-Infected Patients Undergoing Combination Therapy: Survey of 787 Sequences
Yahi, N., Tamalet, C., Tourrès, C., Tivoli, N., Ariasi, F., Volot, F., Gastaut, J., Gallais, H., Moreau, J., & Fantini, J. (1999) · Journal of Clinical Microbiology · doi:10.1128/jcm.37.12.4099-4106.1999 · Cited by 112 · see citing works
Retrovirus recombination depends on the length of sequence identity and is not error prone
Zhang, J., & Temin, H. M. (1994) · Journal of Virology · doi:10.1128/jvi.68.4.2409-2414.1994 · Cited by 110 · see citing works
Self-citation
Protein intrinsic disorder as a flexible armor and a weapon of HIV-1
Xue, B., Mizianty, M. J., Kurgan, L., & Uversky, V. N. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0859-3 · Cited by 107 · see citing works
Cytotoxic T Lymphocyte Lysis Inhibited by Viable HIV Mutants
Meier, U., Klenerman, P., Griffin, P. C., James, W., Köppe, B., Larder, B. A., McMichael, A. J., & Phillips, R. (1995) · Science · doi:10.1126/science.270.5240.1360 · Cited by 107 · see citing works
Determination of the site of first strand transfer during Moloney murine leukemia virus reverse transcription and identification of strand transfer‐associated reverse transcriptase errors
Kulpa, D. A., Topping, R. S., & Telesnitsky, A. (1997) · The EMBO Journal · doi:10.1093/emboj/16.4.856 · Cited by 104 · see citing works
Viral quasi-species and recombination
Boerlijst, M. C., Bonhoeffer, S., & Nowak, M. A. (1996) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1996.0231 · Cited by 101 · see citing works
Lower mutation rate of bovine leukemia virus relative to that of spleen necrosis virus
Mansky, L. M., & Temin, H. M. (1994) · Journal of Virology · doi:10.1128/jvi.68.1.494-499.1994 · Cited by 100 · see citing works
Self-citation
Management of chronic hepatitis C in HIV-infected patients
Soriano, V., Rodrı́guez-Rosado, R., & García‐Samaniego, J. (1999) · AIDS · doi:10.1097/00002030-199904010-00002 · Cited by 101 · see citing works
HIV diversity, recombination and disease progression: how does fitness "fit" into the puzzle?
Tebit, D. M., Nankya, I., Arts, E. J., & Gao, Y. (2007) · PubMed · Cited by 100 · see citing works
Copy-choice recombination by reverse transcriptases: Reshuffling of genetic markers mediated by RNA chaperones
Negroni, M., & BUC, H. C. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.120520497 · Cited by 96 · see citing works
Evolutionary Genetics of Life Cycles
Kondrashov, A. S. (1997) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.28.1.391 · Cited by 90 · see citing works
Evolutionary Potential and Requirements for Minimal Protocells
Szathmáry, E., Mauro Santos, A., & Fernando, C. (2005) · Springer eBooks · doi:10.1007/tcc001 · Cited by 86 · see citing works
Deoxyribonucleoside Triphosphate Pool Imbalances In Vivo Are Associated with an Increased Retroviral Mutation Rate
Julias, J. G., & Pathak, V. K. (1998) · Journal of Virology · doi:10.1128/jvi.72.10.7941-7949.1998 · Cited by 86 · see citing works
In Vivo Analysis of Human T-Cell Leukemia Virus Type 1 Reverse Transcription Accuracy
Mansky, L. M. (2000) · Journal of Virology · doi:10.1128/jvi.74.20.9525-9531.2000 · Cited by 85 · see citing works
The fastest genome evolution ever described: HIV variation in situ
Wain–Hobson, S. (1993) · Current Opinion in Genetics & Development · doi:10.1016/0959-437x(93)90008-d · Cited by 84 · see citing works
Longitudinal study reveals HIV-1–infected CD4+ T cell dynamics during long-term antiretroviral therapy
Antar, A. A. R., Jenike, K. M., Jang, S., Rigau, D. N., Reeves, D. B., Hoh, R., Krone, M., Keruly, J. C., Moore, R. D., Schiffer, J. T., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci135953 · Cited by 81 · see citing works
Incorporation of the Guanosine Triphosphate Analogs 8-Oxo-dGTP and 8-NH2-dGTP by Reverse Transcriptases and Mammalian DNA Polymerases
Kamath‐Loeb, A. S., Hizi, A., Kasai, H., & Loeb, L. A. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.9.5892 · Cited by 83 · see citing works
3′-Azido-3′-Deoxythymidine (AZT) and AZT-Resistant Reverse Transcriptase Can Increase the In Vivo Mutation Rate of Human Immunodeficiency Virus Type 1
Mansky, L. M., & Bernard, L. C. (2000) · Journal of Virology · doi:10.1128/jvi.74.20.9532-9539.2000 · Cited by 83 · see citing works
Replication infidelity during a single cycle of Ty1 retrotransposition.
Gabriel, A., Willems, M., Mules, E. H., & Boeke, J. D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.7767 · Cited by 83 · see citing works
Hypervariable 3′ UTR region of plant LTR-retrotransposons as a source of novel satellite repeats
Macas, J., Koblížková, A., Navrátilová, A., & Neumann, P. (2009) · Gene · doi:10.1016/j.gene.2009.06.014 · Cited by 82 · see citing works
Structural Determinants of Murine Leukemia Virus Reverse Transcriptase That Affect the Frequency of Template Switching
Svarovskaia, E. S., Delviks‐Frankenberry, K. A., Hwang, C. K., & Pathak, V. K. (2000) · Journal of Virology · doi:10.1128/jvi.74.15.7171-7178.2000 · Cited by 82 · see citing works
Sequence variability within the tobacco retrotransposon Tnt1 population.
Casacuberta, J., Vernhettes, S., & Grandbastien, M. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07265.x · Cited by 81 · see citing works
Genetic rearrangements occurring during a single cycle of murine leukemia virus vector replication: characterization and implications
Parthasarathi, S., Varela‐Echavarría, A., Ron, Y., Preston, B. D., & Dougherty, J. P. (1995) · Journal of Virology · doi:10.1128/jvi.69.12.7991-8000.1995 · Cited by 79 · see citing works
Dynamic copy choice: Steady state between murine leukemia virus polymerase and polymerase-dependent RNase H activity determines frequency of in vivo template switching
Hwang, C. K., Svarovskaia, E. S., & Pathak, V. K. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221289898 · Cited by 80 · see citing works
One retroviral RNA is sufficient for synthesis of viral DNA
Jones, J. S., Allan, R. W., & Temin, H. M. (1994) · Journal of Virology · doi:10.1128/jvi.68.1.207-216.1994 · Cited by 79 · see citing works
Self-citation
Retroviral mutation rates and A-to-G hypermutations during different stages of retroviral replication
Kim, T., Mudry, R., Rexrode, C. A., & Pathak, V. K. (1996) · Journal of Virology · doi:10.1128/jvi.70.11.7594-7602.1996 · Cited by 77 · see citing works
Homologous recombination occurs in a distinct retroviral subpopulation and exhibits high negative interference
Hu, W., Bowman, E. H., Delviks‐Frankenberry, K. A., & Pathak, V. K. (1997) · Journal of Virology · doi:10.1128/jvi.71.8.6028-6036.1997 · Cited by 78 · see citing works
The Drosophila micropia retrotransposon encodes a testis-specific antisense RNA complementary to reverse transcriptase.
Lankenau, S., Corces, V. G., & Lankenau, D. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.3.1764 · Cited by 76 · see citing works
Human Immunodeficiency Virus Type 1 Genetic Recombination Is More Frequent Than That of Moloney Murine Leukemia Virus despite Similar Template Switching Rates
Onafuwa-Nuga, A., An, W., Robson, N. D., & Telesnitsky, A. (2003) · Journal of Virology · doi:10.1128/jvi.77.8.4577-4587.2003 · Cited by 73 · see citing works
Identifying the Important HIV-1 Recombination Breakpoints
Archer, J. P., Pinney, J. W., Fan, J., Simon‐Lorière, E., Arts, E. J., Negroni, M., & Robertson, D. L. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000178 · Cited by 70 · see citing works
Role of the Reverse Transcriptase, Nucleocapsid Protein, and Template Structure in the Two-step Transfer Mechanism in Retroviral Recombination
Roda, R. H., Balakrishnan, M., Hanson, M. N., Wöhrl, B. M., Grice, S. F. J. L., Roques, B. P., Gorelick, R. J., & Bambara, R. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304608200 · Cited by 70 · see citing works
Infectious Molecular Clones with the Nonhomologous Dimer Initiation Sequences Found in Different Subtypes of Human Immunodeficiency Virus Type 1 Can Recombine and Initiate a Spreading Infection In Vitro
Louis, D. C. S., Gotte, D., Sanders‐Buell, E., Ritchey, D. W., Salminen, M. O., Carr, J. K., & McCutchan, F. E. (1998) · Journal of Virology · doi:10.1128/jvi.72.5.3991-3998.1998 · Cited by 70 · see citing works
Evidence for a Mechanism of Recombination during Reverse Transcription Dependent on the Structure of the Acceptor RNA
Moumen, A., Polomack, L., Unge, T., Véron, M., BUC, H. C., & Negroni, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212306200 · Cited by 70 · see citing works
Mystery of intron gain: new data and new models
Roy, S. W., & Irimia, M. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.11.004 · Cited by 69 · see citing works
Genetic variability: The key problem in the prevention and therapy of RNA‐based virus infections
Figlerowicz, M., Alejska, M., Kurzyńska‐Kokorniak, A., & Figlerowicz, M. (2003) · Medicinal Research Reviews · doi:10.1002/med.10045 · Cited by 68 · see citing works
Genomic Stability of Murine Leukemia Viruses Containing Insertions at the Env-3′ Untranslated Region Boundary
Logg, C. R., Logg, A., Tai, C.-K., Cannon, P. M., & Kasahara, N. (2001) · Journal of Virology · doi:10.1128/jvi.75.15.6989-6998.2001 · Cited by 67 · see citing works
The chaperoning and assistance roles of the HIV-1 nucleocapsid protein in proviral DNA synthesis and maintenance
Bampi, C., Jacquenet, S., Lener, D., Décimo, D., & Darlix, J. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.02.024 · Cited by 66 · see citing works
Origins of Life: The Primal Self-Organisation
Egel, H., Lankenau, D., & Mulkidjanian, A. (2011) · Springer eBooks · doi:10.1007/978-3-642-21625-1 · Cited by 39 · see citing works
E- vectors: development of novel self-inactivating and self-activating retroviral vectors for safer gene therapy
Julias, J. G., Hash, D. C., & Pathak, V. K. (1995) · Journal of Virology · doi:10.1128/jvi.69.11.6839-6846.1995 · Cited by 65 · see citing works
Autonomous Targeting of Infectious Superspreaders Using Engineered Transmissible Therapies
Metzger, V. T., Lloyd‐Smith, J. O., & Weinberger, L. S. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002015 · Cited by 64 · see citing works
The first strand transfer during HIV-1 reverse transcription can occur either intramolecularly or intermolecularly
van Wamel, J. L. B., & Berkhout, B. (1998) · Virology · doi:10.1006/viro.1998.9096 · Cited by 63 · see citing works
The HIV-1 repeated sequence R as a robust hot-spot for copy-choice recombination
Moumen, A. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.18.3814 · Cited by 63 · see citing works
The public health significance of HIV-1 subtypes
Tatt, I. D., Barlow, K. L., Nicoll, A., & Clewley, J. P. (2001) · AIDS · doi:10.1097/00002030-200100005-00009 · Cited by 63 · see citing works
In vivo selection of protease cleavage sites from retrovirus display libraries
Buchholz, C. J., Peng, K.-W., Morling, F. J., Zhang, J., Cosset, F., & Russell, S. J. (1998) · Nature Biotechnology · doi:10.1038/nbt1098-951 · Cited by 63 · see citing works
Retroelements and formation of chimeric retrogenes
Buzdin, A. A. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-4041-z · Cited by 62 · see citing works
Altering the Intracellular Environment Increases the Frequency of Tandem Repeat Deletion during Moloney Murine Leukemia Virus Reverse Transcription
Pfeiffer, J. K., Topping, R. S., Shin, N.-H., & Telesnitsky, A. (1999) · Journal of Virology · doi:10.1128/jvi.73.10.8441-8447.1999 · Cited by 62 · see citing works
Template Dimerization Promotes an Acceptor Invasion-Induced Transfer Mechanism during Human Immunodeficiency Virus Type 1 Minus-Strand Synthesis
Balakrishnan, M., Roques, B. P., Fay, P. J., & Bambara, R. A. (2003) · Journal of Virology · doi:10.1128/jvi.77.8.4710-4721.2003 · Cited by 62 · see citing works
Nucleocapsid protein of human immunodeficiency virus as a model protein with chaperoning functions and as a target for antiviral drugs
Darlix, J., Cristofari, G., Rau, M., Péchoux, C., Berthoux, L., & Roques, B. P. (2000) · Advances in pharmacology · doi:10.1016/s1054-3589(00)48011-7 · Cited by 61 · see citing works
Dominant Role of Host Selective Pressure in Driving Hepatitis C Virus Evolution in Perinatal Infection
Manzin, A., Solforosi, L., Debiaggi, M., Zara, F., Tanzi, E., Romanò, L., Zanetti, A. R., & Clementi, M. (2000) · Journal of Virology · doi:10.1128/jvi.74.9.4327-4334.2000 · Cited by 60 · see citing works
Comparison of three different crystal forms shows HIV-1 reverse transcriptase displays an internal swivel motion
Jäger, J., Smerdon, S. J., Wang, J., Boisvert, D. C., & Steitz, T. A. (1994) · Structure · doi:10.1016/s0969-2126(94)00087-5 · Cited by 60 · see citing works
Turnover of env Variable Region 1 and 2 Genotypes in Subjects with Late-Stage Human Immunodeficiency Virus Type 1 Infection
Kitrinos, K. M., Hoffman, N. G., Nelson, J. A. E., & Swanstrom, R. I. (2003) · Journal of Virology · doi:10.1128/jvi.77.12.6811-6822.2003 · Cited by 58 · see citing works
Dimer Initiation Sequence of HIV-1LaiGenomic RNA: NMR Solution Structure of the Extended Duplex
Girard, F. C., Barbault, F., Gouyette, C., Huynh‐Dinh, T., Paoletti, J., & Lancelot, G. (1999) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.1999.10508323 · Cited by 58 · see citing works
Unique Functions of Repetitive Transcriptomes
Schumann, G. G., Gogvadze, E. V., Osanai-Futahashi, M., Kuroki, A., Münk, C., Fujiwara, H., Ivics, Z., & Buzdin, A. A. (2010) · International review of cytology · doi:10.1016/b978-0-12-381047-2.00003-7 · Cited by 57 · see citing works
Effect of Distance between Homologous Sequences and 3′ Homology on the Frequency of Retroviral Reverse Transcriptase Template Switching
Delviks‐Frankenberry, K. A., & Pathak, V. K. (1999) · Journal of Virology · doi:10.1128/jvi.73.10.7923-7932.1999 · Cited by 57 · see citing works
Genetic Reassortment and Patch Repair by Recombination in Retroviruses
Mikkelsen, J. G., & Pedersen, F. S. (2000) · Journal of Biomedical Science · doi:10.1007/bf02256615 · Cited by 56 · see citing works
The Retroviral Vector: Replication Cycle and Safety Considerations for Retrovirus‐Mediated Gene Therapy
Boris‐Lawrie, K., & Temin, H. M. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb21703.x · Cited by 55 · see citing works
Self-citation
Detection of Avian Leukosis Virus Subgroup J Using the Polymerase Chain Reaction
Smith, E. J., Williams, S. M., & Fadly, A. M. (1998) · Avian Diseases · doi:10.2307/1592488 · Cited by 54 · see citing works
Recombination during reverse transcription: an evaluation of the role of the nucleocapsid protein
Negroni, M., & BUC, H. C. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2460 · Cited by 54 · see citing works
A new NMR solution structure of the SL1 HIV-1Lai loop-loop dimer
Kieken, F. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj427 · Cited by 53 · see citing works
In Vitro Intersubtype Recombinants of Human Immunodeficiency Virus Type 1: Comparison to Recent and Circulating In Vivo Recombinant Forms
Quiñones‐Mateu, M. E., Gao, Y., Ball, S. C., Marozsan, A. J., Abraha, A., & Arts, E. J. (2002) · Journal of Virology · doi:10.1128/jvi.76.19.9600-9613.2002 · Cited by 53 · see citing works
Extreme Structural Heterogeneity Among the Members of a Maize Retrotransposon Family
Marillonnet, S., & Wessler, S. R. (1998) · Genetics · doi:10.1093/genetics/150.3.1245 · Cited by 53 · see citing works
A New Glycan-Dependent CD4-Binding Site Neutralizing Antibody Exerts Pressure on HIV-1 In Vivo
Freund, N. T., Horwitz, J. A., Nogueira, L., Sievers, S. A., Scharf, L., Scheid, J. F., Gazumyan, A., Liu, C., Velinzon, K., Goldenthal, A. R., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005238 · Cited by 51 · see citing works

High-Frequency Illegitimate Strand Transfers of Nascent DNA Fragments During Reverse Transcription Result in Defective Retrovirus Genomes
Li, X., Fan, P., Jiang, C., Ma, T., Yu, X., Kong, W., & Gao, F. (2016) · JAIDS Journal of Acquired Immune Deficiency Syndromes · doi:10.1097/qai.0000000000000952 · Cited by 2 · see citing works
Accessory replication proteins and the accuracy of reverse transcription: implications for retroviral genetic diversity
Mansky, L. M. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01062-7 · Cited by 9 · see citing works
GENETIC VARIABILITY AND MOLECULAR EPIDEMIOLOGY OF HUMAN IMMUNODEFICIENCY VIRUS
Chin-Yih, & Ou (1991) · Carcinogenesis,Teratogenesis and Mutagenesis
Misincorporation by HIV-1 Reverse Transcriptase Promotes Recombination via Strand Transfer Synthesis
Palaniappan, C., Wisniewski, M., Wu, W., Fay, P. J., & Bambara, R. A. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.37.22331 · Cited by 32 · see citing works
Reprint of Temin's 1993 Paper on the Inherent Contributions of Reverse Transcription to Retroviral Variation
Sugden, B. (2014) · ASM Press eBooks · doi:10.1128/9781555818302.ch15

Authors: Temin, H. M.
Affiliations: University of Wisconsin–Madison (US)
Corresponding author: Temin, H M
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 1993-08
Volume: 90
Issue: 15
Pages: 6900-6903
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.90.15.6900
PMC: PMC47042
OpenAlex: W2087946368
Cited by: 309
References: 37
Citations by year: 2026: 2 · 2025: 3 · 2022: 1 · 2021: 1 · 2020: 4 · 2019: 4 · 2018: 1 · 2017: 7 · 2016: 6 · 2015: 3 · 2014: 4 · 2013: 7 · 2012: 7
FWCI: 6.91
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5p30ca007175-36)
U.S. Public Health Service (CA-07175)
National Cancer Institute (CA-22443, CA-07175, P01CA022443)
Topics: Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
Health Sciences › Medicine › Infectious Diseases › HIV/AIDS drug development and treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords: strand transfer, human immunodeficiency virus, growing points, retroviral replication
MeSH terms: Mutation, Recombination, Genetic, Retroviridae, RNA-Directed DNA Polymerase, RNA, Viral, Templates, Genetic, Genetic Variation, Virus Replication, Sequence Deletion

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Retrovirus variation and reverse transcription: abnormal strand transfers result in retrovirus genetic variation

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks