RNA structures facilitate recombination-mediated gene swapping in HIV-1

Journal of Virology

Volumn 84, Issue 24, 2010, Pages 12675-12682

  Simon Loriere, Etienne ^a   Martin, Darren P ^b,c   Weeks, Kevin M ^d   Negroni, Matteo ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CENTRE FOR HIGH PERFORMANCE COMPUTING   (South Africa)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

^d The University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ARTICLE; CONTROLLED STUDY; ENVELOPE GENE; GENE LOCATION; GENE STRUCTURE; GENE SWITCHING; GENOME ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA SEQUENCE; RNA STRUCTURE; VIRUS GENE; VIRUS GENOME; VIRUS RECOMBINATION; VIRUS STRAIN;

COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENES, ENV; GENETIC VARIATION; GENOME, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; NUCLEIC ACID CONFORMATION; RECOMBINATION, GENETIC; RNA, VIRAL; SELECTION, GENETIC;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78649401437     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01302-10     Document Type: Article

References (52)

1. An, W., and A. Telesnitsky. 2002. Effects of varying sequence similarity on the frequency of repeat deletion during reverse transcription of a human immunodeficiency virus type 1 vector. J. Virol. 76:7897-7902. (Pubitemid 34761014)
2. An, W., and A. Telesnitsky. 2001. Frequency of direct repeat deletion in a human immunodeficiency virus type 1 vector during reverse transcription in human cells. Virology 286:475-482. (Pubitemid 32721823)
3. Baird, H. A., R. Galetto, Y. Gao, E. Simon-Loriere, M. Abreha, J. Archer, J. Fan, D. L. Robertson, E. J. Arts, and M. Negroni. 2006. Sequence determinants of breakpoint location during HIV-1 intersubtype recombination. Nucleic Acids Res. 34:5203-5216. (Pubitemid 44742485)
4. Chin, M. P., T. D. Rhodes, J. Chen, W. Fu, and W. S. Hu. 2005. Identification of a major restriction in HIV-1 intersubtype recombination. Proc. Natl. Acad. Sci. U. S. A. 102:9002-9007.
5. Cochrane, A. W., M. T. McNally, and A. J. Mouland. 2006. The retrovirus RNA trafficking granule: from birth to maturity. Retrovirology 3:18.
6. Cros, J. F., and P. Palese. 2003. Trafficking of viral genomic RNA into and out of the nucleus: influenza, Thogoto and Borna disease viruses. Virus Res. 95:3-12.
7. Drummond, D. A., J. J. Silberg, M. M. Meyer, C. O. Wilke, and F. H. Arnold. 2005. On the conservative nature of intragenic recombination. Proc. Natl. Acad. Sci. U. S. A. 102:5380-5385.
8. Duch, M., M. L. Carrasco, T. Jespersen, L. Aagaard, and F. S. Pedersen. 2004. An RNA secondary structure bias for non-homologous reverse transcriptase-mediated deletions in vivo. Nucleic Acids Res. 32:2039-2048.
9. Dykes, C., M. Balakrishnan, V. Planelles, Y. Zhu, R. A. Bambara, and L. M. Demeter. 2004. Identification of a preferred region for recombination and mutation in HIV-1 gag. Virology 326:262-279.
10. Flynn, J. A., W. An, S. R. King, and A. Telesnitsky. 2004. Nonrandom dimerization of murine leukemia virus genomic RNAs. J. Virol. 78:12129-12139.
11. Flynn, J. A., and A. Telesnitsky. 2006. Two distinct Moloney murine leukemia virus RNAs produced from a single locus dimerize at random. Virology 344:391-400.
12. Galetto, R., V. Giacomoni, M. Veron, and M. Negroni. 2006. Dissection of a circumscribed recombination hot spot in HIV-1 after a single infectious cycle. J. Biol. Chem. 281:2711-2720.
13. Galetto, R., A. Moumen, V. Giacomoni, M. Veron, P. Charneau, and M. Negroni. 2004. The structure of HIV-1 genomic RNA in the gp120 gene determines a recombination hot spot in vivo. J. Biol. Chem. 279:36625-36632.
14. Galli, A., M. Kearney, O. A. Nikolaitchik, S. Yu, M. P. Chin, F. Maldarelli, J. M. Coffin, V. K. Pathak, and W. S. Hu. 2010. Patterns of human immunodeficiency virus type 1 recombination ex vivo provide evidence for coadaptation of distant sites, resulting in purifying selection for intersubtype recombinants during replication. J. Virol. 84:7651-7661.
15. Garcia-Andres, S., D. M. Tomas, S. Sanchez-Campos, J. Navas-Castillo, and E. Moriones. 2007. Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365:210-219. (Pubitemid 46907240)
16. Hanson, M. N., M. Balakrishnan, B. P. Roques, and R. A. Bambara. 2005. Effects of donor and acceptor RNA structures on the mechanism of strand transfer by HIV-1 reverse transcriptase. J. Mol. Biol. 353:772-787.
17. Harrington, P. R., J. A. Nelson, K. M. Kitrinos, and R. Swanstrom. 2007. Independent evolution of human immunodeficiency virus type 1 env V1/V2 and V4/V5 hypervariable regions during chronic infection. J. Virol. 81:5413-5417.
18. He, C. Q., Z. X. Xie, G. Z. Han, J. B. Dong, D. Wang, J. B. Liu, L. Y. Ma, X. F. Tang, X. P. Liu, Y. S. Pang, and G. R. Li. 2009. Homologous recombination as an evolutionary force in the avian influenza A virus. Mol. Biol. Evol. 26:177-187.
19. Heath, L., E. van der Walt, A. Varsani, and D. P. Martin. 2006. Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J. Virol. 80:11827-11832.
20. Holmes, E. C. 2001. On the origin and evolution of the human immunodeficiency virus (HIV). Biol. Rev. Camb. Philos. Soc. 76:239-254.
21. Hu, W. S., and H. M. Temin. 1990. Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proc. Natl. Acad. Sci. U. S. A. 87:1556-1560.
22. Jetzt, A. E., H. Yu, G. J. Klarmann, Y. Ron, B. D. Preston, and J. P. Dougherty. 2000. High rate of recombination throughout the human immunodeficiency virus type 1 genome. J. Virol. 74:1234-1240.
23. Kim, J. K., C. Palaniappan, W. Wu, P. J. Fay, and R. A. Bambara. 1997. Evidence for a unique mechanism of strand transfer from the transactivation response region of HIV-1. J. Biol. Chem. 272:16769-16777.
24. Klaver, B., and B. Berkhout. 1994. Premature strand transfer by the HIV-1 reverse transcriptase during strong-stop DNA synthesis. Nucleic Acids Res. 22:137-144. (Pubitemid 24160927)
25. Korber, B., B. Foley, C. Kuiken, S. Pillai, and J. Sodroski. December 1998, posting date. Numbering positions in HIV relative to HXB2CG. Los Alamos National Laboratory, Los Alamos, NM. http://www.hiv.lanl.gov/content/sequence/ HIV/COMPENDIUM/1998/III/HXB2.pdf.
26. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
27. Labrosse, B., L. Morand-Joubert, A. Goubard, S. Rochas, J. L. Labernardiere, J. Pacanowski, J. L. Meynard, A. J. Hance, F. Clavel, and F. Mammano. 2006. Role of the envelope genetic context in the development of enfuvirtide resistance in human immunodeficiency virus type 1-infected patients. J. Virol. 80:8807-8819. (Pubitemid 44384889)
28. Lefeuvre, P., J. M. Lett, B. Reynaud, and D. P. Martin. 2007. Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog. 3:e181.
29. Lefeuvre, P., J. M. Lett, A. Varsani, and D. P. Martin. 2009. Widely conserved recombination patterns among single-stranded DNA viruses. J. Virol. 83:2697-2707.
30. Liu, Y., E. Wimmer, and A. V. Paul. 2009. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim. Biophys. Acta 1789:495-517.
31. Magiorkinis, G., D. Paraskevis, A.-M. Vandamme, E. L. Magiorkinis, V. Sypsa, and A. Hatzakis. 2003. In vivo characteristics of human immunodeficiency virus type 1 intersubtype recombination: determination of hot spots and correlation with sequence similarity. J. Gen. Virol. 84:2715-2722.
32. Malim, M. H., J. Hauber, S. Y. Le, J. V. Maizel, and B. R. Cullen. 1989. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338:254-257.
33. Moumen, A., L. Polomack, T. Unge, M. Veron, H. Buc, and M. Negroni. 2003. Evidence for a mechanism of recombination during reverse transcription dependent on the structure of the acceptor RNA. J. Biol. Chem. 278:15973-15982.
34. Nora, T., C. Charpentier, O. Tenaillon, C. Hoede, F. Clavel, and A. J. Hance. 2007. Contribution of recombination to the evolution of human immunodeficiency viruses expressing resistance to antiretroviral treatment. J. Virol. 81:7620-7628.
35. Onafuwa, A., W. An, N. D. Robson, and A. Telesnitsky. 2003. Human immunodeficiency virus type 1 genetic recombination is more frequent than that of Moloney murine leukemia virus despite similar template switching rates. J. Virol. 77:4577-4587. (Pubitemid 36402807)
36. Paillart, J. C., M. Shehu-Xhilaga, R. Marquet, and J. Mak. 2004. Dimerization of retroviral RNA genomes: an inseparable pair. Nat. Rev. Microbiol. 2:461-472.
37. Rakoto-Andrianarivelo, M., N. Gumede, S. Jegouic, J. Balanant, S. N. Andriamamonjy, S. Rabemanantsoa, M. Birmingham, B. Randriamanalina, L. Nkolomoni, M. Venter, B. D. Schoub, F. Delpeyroux, and J. M. Reynes. 2008. Reemergence of recombinant vaccine-derived poliovirus outbreak in Madagascar. J. Infect. Dis. 197:1427-1435.
38. Ramirez, B. C., E. Simon-Loriere, R. Galetto, and M. Negroni. 2008. Implications of recombination for HIV diversity. Virus Res. 134:64-73.
39. Rasmussen, S. V., and F. S. Pedersen. 2006. Co-localization of gammaretroviral RNAs at their transcription site favours co-packaging. J. Gen. Virol. 87:2279-2289.
40. Roda, R. H., M. Balakrishnan, J. K. Kim, B. P. Roques, P. J. Fay, and R. A. Bambara. 2002. Strand transfer occurs in retroviruses by a pause-initiated two-step mechanism. J. Biol. Chem. 277:46900-46911.
41. Shen, W., L. Gao, M. Balakrishnan, and R. A. Bambara. 2009. A recombination hot spot in HIV-1 contains guanosine runs that can form a G-quartet structure and promote strand transfer in vitro. J. Biol. Chem. 284:33883-33893.
42. Simon, A. E., and L. Gehrke. 2009. RNA conformational changes in the life cycles of RNA viruses, viroids, and virus-associated RNAs. Biochim. Biophys. Acta 1789:571-583.
43. Simon-Loriere, E., R. Galetto, M. Hamoudi, J. Archer, P. Lefeuvre, D. P. Martin, D. L. Robertson, and M. Negroni. 2009. Molecular mechanisms of recombination restriction in the envelope gene of the human immunodeficiency virus. PLoS Pathog. 5:e1000418.
44. Song, R., J. Kafaie, L. Yang, and M. Laughrea. 2007. HIV-1 viral RNA is selected in the form of monomers that dimerize in a three-step protease-dependent process; the DIS of stem-loop 1 initiates viral RNA dimerization. J. Mol. Biol. 371:1084-1098.
45. Streeck, H., B. Li, A. F. Poon, A. Schneidewind, A. D. Gladden, K. A. Power, D. Daskalakis, S. Bazner, R. Zuniga, C. Brander, E. S. Rosenberg, S. D. Frost, M. Altfeld, and T. M. Allen. 2008. Immune-driven recombination and loss of control after HIV superinfection. J. Exp. Med. 205:1789-1796.
46. Voigt, C. A., C. Martinez, Z. G. Wang, S. L. Mayo, and F. H. Arnold. 2002. Protein building blocks preserved by recombination. Nat. Struct. Biol. 9:553-558.
47. Watts, J. M., K. K. Dang, R. J. Gorelick, C. W. Leonard, J. W. Bess, Jr., R. Swanstrom, C. L. Burch, and K. M. Weeks. 2009. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460:711-716.
48. White, K. A., and P. D. Nagy. 2004. Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Prog. Nucleic Acid Res. Mol. Biol. 78:187-226.
49. Worobey, M., and E. C. Holmes. 1999. Evolutionary aspects of recombination in RNA viruses. J. Gen. Virol. 80:2535-2543.
50. Zhang, J., L. Y. Tang, T. Li, Y. Ma, and C. M. Sapp. 2000. Most retroviral recombinations occur during minus-strand DNA synthesis. J. Virol. 74:2313-2322.
51. Zhang, J., and H. M. Temin. 1994. Retrovirus recombination depends on the length of sequence identity and is not error prone. J. Virol. 68:2409-2414.
52. Zhuang, J., S. Mukherjee, Y. Ron, and J. P. Dougherty. 2006. High rate of genetic recombination in murine leukemia virus: implications for influencing proviral ploidy. J. Virol. 80:6706-6711.