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Reciprocal relationship between stem-loop potential and substitution density in retroviral quasispecies under positive Darwinian selection

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Abstract

Nucleic acids have the potential to form in trastrand stem-loops if complementary bases are suitably located. Computer analyses of poliovirus and retroviral RNAs have revealed a reciprocal relationship between “statistically significant” stem-loop potential and “sequence variability.” The statistically significant stem-loop potential of a nucleic acid segment has been defined as a function of the difference between the folding energy of the natural segment (FONS) and the mean folding energy of a set of randomized (shuffled) versions of the natural segment (FORS-M). Since FONS is dependent on both base composition and base order, whereas FORS-M is solely dependent on base composition (a genomic characteristic), it follows that statistically significant stem-loop potential (FORS-D) is a function of base order (a local characteristic). In retroviral genomes, as in all DNA genomes studied, positive FORS-D values are widely distributed. Thus there have been pressures on base order both to encode specific functions and to encode stem-loops. As in the case of DNA genomes under positive Darwinian selection pressure, in HIV-1 specific function appears to dominate in rapidly evolving regions. Here high sequence variability, expressed as substitution density (not indel density), is associated with negative FORS-D values (impaired base-order-dependent stem-loop potential). This suggests that in these regions HIV-1 genomes are under positive selection pressure by host defenses. The general function of stem-loops is recombination. This is a vital process if, from among members of viral “quasispecies,” functional genomes are to be salvaged. Thus, for rapidly evolving RNA genomes, it is as important to conserve base-order-dependent stem-loop potential as to conserve other functions.

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References

  • Berkhout B, van Hemert FJ (1994) The unusual nucleotide content of the HIV RNA genome results in a biased amino acid composition of HIV proteins. Nucleic Acids Res 22:1705–1711

    Google Scholar 

  • Bernardi G (1989) The isochore organization of the human genome. Annu Rev Genet 23:637–661

    Google Scholar 

  • Bernstein C, Bernstein H (1991) Aging, sex and DNA repair. Academic Press, San Diego

    Google Scholar 

  • Blum S, Forsdyke RE, Forsdyke DR (1990) Three human homologs of a murine gene encoding an inhibitor of stem cell proliferation. DNA Cell Biol 9:589–602

    Google Scholar 

  • Braun MJ, Clements JE, Gonda MA (1987) The visna virus genome: evidence for a hypervariable site in the env gene and sequence homology among lentivirus envelope proteins. J Virol 61: 4046–4054

    Google Scholar 

  • Bronson EC, Anderson JN (1994) Nucleotide composition as a driving force in the evolution of retroviruses. J Mol Evol 38:506–532

    Google Scholar 

  • Crick F (1971) General model for the chromosomes of higher organisms. Nature 234:25–27

    Google Scholar 

  • Coffin JM (1992) Genetic diversity and evolution of retroviruses. Carr Top Microbiol Immunol 176:143–163

    Google Scholar 

  • Cullen BR (1991) Regulation of HIV-1 gene expression. FASEB J 5:2361–2368

    Google Scholar 

  • Currey KM, Peterlin BM, Maizel JV (1986) Secondary structure prediction of poliovirus RNA: correlation of computer-predicted with electron microscopically observed structure. Virology 148:33–46

    Google Scholar 

  • Doolittle RF, Feng D-F, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Q Rev Biol 64:1–30

    Google Scholar 

  • Doyle GG (1978) A general theory of chromosome pairing based on the palindromic DNA model of Sobell with modifications and amplification. J Theor Biol 70:171–184

    Google Scholar 

  • Filipski J (1990) Evolution of DNA sequence. Contributions of mutational bias and selection to the origin of chromosomal compartments. Adv Mutagen Res 2:1–54

    Google Scholar 

  • Fitch WM (1983) Random sequences. J Mol Biol 163:171–176

    Google Scholar 

  • Forsdyke DR (1995a). Fine-tuning of intracellular protein concentrations, a collective protein function involved in aneuploid lethality, sex-determination and speciation? J Theor Biol 172:335–345

    Google Scholar 

  • Forsdyke DR (1995b) A stem-loop “kissing” model for the initiation of recombination and the origin of introns. Mol Biol Evol 12:949–958

    Google Scholar 

  • Forsdyke DR (1995c) Conservation of stem-loop potential in introns of snake venom phospholipase A2 genes. An application of FORS-D analysis. Mol Biol Evol 12:1157–1165

    Google Scholar 

  • Forsdyke DR (1995d) Relative roles of primary sequence and (G + C)% in determining the hierarchy of frequencies of complementary trinucleotide pairs in DNAs of different species. J Mol Evol 41:573–581

    Google Scholar 

  • Forsdyke DR (1996) Different biological species “broadcast” their DNAs at different (G + C)% “wavelengths.” J Theor Biol (in press)

  • Freter RR, Irminger JC, Porter JA, Jones SD, Stiles CD (1992) A novel 7-nucleotide motif located in 3′ untranslated sequences of the immediate-early gene set mediates platelet-derived growth factor induction of the JE gene. Mol Cell Biol 12:5288–5300

    Google Scholar 

  • Grantham R, Gautier G, Gouy M, Mercier R, Pare A (1980) Codon catalog usage and the genome hypothesis. Nucleic Acids Res 8:r49-r62

    Google Scholar 

  • Gribskov M, Devereux J (1991) Sequence analysis primer. Stockton Press, New York

    Google Scholar 

  • Gurtler LG, Hauser PH, Eberle J, Brunn A von, Knapp S, Zekeng L, Tsague JM, Kaptue L (1994) A new type of human immunodeficiency virus type 1 from Cameroon. J Virol 68:1581–1585

    Google Scholar 

  • Hawley RS, Arbel T (1993) Yeast genetics and the fall of the classical view of meiosis. Cell 72:301–303

    Google Scholar 

  • Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S (1982) Rapid evolution of RNA genomes. Science 215:1577–1585

    Google Scholar 

  • Holland JJ, Torre JC de la, Steinhauer DA (1992) RNA virus populations as quasispecies. Curr Top Microbiol Immunol 176:1–20

    Google Scholar 

  • Huet T, Cheynier R, Meyerhans AR, Roelants G, Wain-Hobson S (1990) Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 345:356–358

    Google Scholar 

  • Hughes AL, Hughes MK, Howell CY, Nei M (1994) Natural selection at the class II major histocompatibility complex loci of mammals. Phil Trans R Soc Lond Biol 345:359–367

    Google Scholar 

  • Karlin S, Brendel V (1992) Chance and statistical significance in protein and DNA sequence analysis. Science 257:39–49

    Google Scholar 

  • Kleckner N, Padmore R, Bishop DK (1991) Meiotic chromosome metabolism: one view. Cold Spring Harbor Symp Quant Biol 56: 729–743

    Google Scholar 

  • Kleckner N, Weiner BM (1993) Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic and premeiotic cells. Cold Spring Harbor Symp Quant Biol 58:553–565

    Google Scholar 

  • Klein S (1994) Choose your partner: chromosome pairing in yeast meiosis. Bioessays 16:869–871

    Google Scholar 

  • Klein J, O'Huigin C (1994) MHC polymorphism and parasites. Philos Trans R Soc Lond Biol 346:351–358

    Google Scholar 

  • Lasky LA, Nakamura G, Smith DH, Fennie C, Shimasaki C, Patzer E, Berman P, Gregory T, Capon DJ (1987) Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell 50:975–985

    Google Scholar 

  • Le S-Y, Chen J-H, Braun MJ, Gonda MA, Maizel JV (1988) Stability of RNA stem-loop structure and distribution of non-random structure in the human immunodeficiency virus (HIV-I). Nucleic Acids Res 16:5153–5168

    Google Scholar 

  • Le S-Y, Chen J-H, Chatterjee D, Maizel JV (1989a) Sequence divergence and open regions of RNA secondary structures in the envelope regions of 17 human immunodeficiency virus isolates. Nucleic Acids Res 17:3275–3288

    Google Scholar 

  • Le S-Y, Chen J-H, Maizel JV (1989b) Thermodynamic stability and statistical significance of potential stem-loop structures situated at the frameshift sites of retroviruses. Nucleic Acids Res. 17:6143–6152

    Google Scholar 

  • Le S-Y, Chen J-H, Maizel JV (1991) Detection of unusual RNA folding regions in HIV and SIV sequences. Comput Appl Biosci 7:51–55

    Google Scholar 

  • Le S-Y, Maizel JV (1989) A method for assessing the statistical significance of RNA folding. J Theor Biol 138:495–510

    Google Scholar 

  • Le S-Y, Malim MH, Cullen BR, Maizel JV (1990) A highly conserved RNA folding region coincident with the Rev response element of primate immunodeficiency viruses. Nucleic Acids Res 18:1613–1623

    Google Scholar 

  • Leeds JM, Slabourgh MB, Mathews CK (1985) DNA precursor pools and ribonucleotide reductase activity: distribution between the nucleus and cytoplasm of mammalian cells. Mol Cell Biol 5:3443–3450

    Google Scholar 

  • Mann DA, Mikaelian I, Zemmel RW, Green SM, Lowe AD, Kimura T, Singh M, Butler JG, Gait MJ, Karn J (1994) A molecular rheostat. Cooperative Rev binding to stem I of the Rev-response element modulates human immunodeficiency virus type-1 late gene expression. J Mol Biol 241:193–207

    Google Scholar 

  • Martinez HM (1988) A flexible multiple sequence alignment program. Nucleic Acids Res 16:1683–1691

    Google Scholar 

  • Min Jou W, Fiers W (1976) Studies on the bacteriophage MS2. XXXIII. Comparison of the nucleotide sequences in related bacteriophage RNAs. J Mol Biol 106:1047–1060

    Google Scholar 

  • Murchie AIH, Bowater R, Aboul-Ela F, Lilley DMJ (1992) Helix opening transitions in supercoiled DNA. Biochem Biophys Acta 1131: 1–15

    Google Scholar 

  • Myers G, Korber B, Wain-Hobson S, Smith RF, Pavlakis GN (1993) Human retroviruses and AIDS I993. A compilation and analysis of nucleic acid and amino acid sequences. Los Alamos National Laboratory, Los Alamos, NM

    Google Scholar 

  • Nussinov R (1984) Strong doublet preferences in nucleotide sequences and DNA geometry. J Mol Evol 20:111–119

    Google Scholar 

  • Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single strand conformation polymorphisms. Proc Natl Acad Sci USA 86:2766–2770

    CAS  PubMed  Google Scholar 

  • Radman M, Wagner R, Kricker MC (1993) Homologous DNA interactions in the evolution of gene and chromosome structure. Genome Anal 7:139–154

    Google Scholar 

  • Ratner L, Haseltine W, Patarca R, Livak KJ, Starcich B, Josephs SF, Doran ER, Rafalski JA, Whitehorn EA, Baumeister K, Ivanoff L, Petteway SR, Pearson ML, Lautenberger JA, Papas TS, Ghrayeb J, Chang NT, Gallo RC, Wong-Staal F (1985) Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature 313:277–284

    Google Scholar 

  • Ratner L, Fisher A, Jagodzinski LL, Mitsuya H, Liou R-S, Gallo RC, Wong-Staal F (1987) Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res Hum Retrovir 3:57–69

    Google Scholar 

  • Robertson DL, Sharp PM, McCutchan FE, Hahn BH (1995) Recombination in HIV-1. Nature 374:124–126

    Google Scholar 

  • Romanova LI Blinov VM, Tolskaya EA, Viktorova EG, Kolesnikova MS, Guseva EA, Agol VI (1986) The primary structure of crossover regions of intertypic poliovirus recombinants: a model of recombination between RNA genomes. Virology 155:202–213

    Google Scholar 

  • Ryan BF, Joiner BL (1994) Minitab handbook, 3rd ed. Wadsworth Publishing, Belmont, CA

    Google Scholar 

  • Salser W (1977) Globin mRNA sequences: analysis of base pairing and evolutionary implications. Cold Spring Harb Symp Quant Biol 42: 985–1002

    Article  CAS  PubMed  Google Scholar 

  • Sepaer EG, Mullins JI (1993) Rates of amino acid change in the envelope protein correlates with pathogenicity of primate lentiviruses. J Mol Evol 37:57–65

    Google Scholar 

  • Sobell HM (1972) Molecular mechanism for genetic recombination. Proc Natl Acad Sci USA 69:2483–2487

    Google Scholar 

  • Spire B, Sire J, Zachar V, Rey F, Barre-Sinoussi B, Galibert F, Hampe A, Chermann J-C (1989) Nucleotide sequence of HIV1-NDK: a highly pathogenic strain of the human immunodeficiency virus. Gene 81:275–284

    Google Scholar 

  • Sueoka N (1961) Compositional correlation between deoxyribonucleic acid and protein. Cold Spring Harbor Symp Quant Biol 26:35–43

    Google Scholar 

  • Tolskaya EA, Romanova LI, Blinov VM, Viktorova EG, Sinyakov AN, Kolesnikova MS, Agol VI (1987) Studies on the recombination between RNA genomes of poliovirus: the primary structure and nonrandom distribution of crossover regions in the genomes of intertypic poliovirus recombinants. Virology 161:54–61

    Google Scholar 

  • Tomizawa J (1984) Control of ColEl plasmid replication: the process of binding of RNA I to the primer transcript. Cell 38:861–870

    Google Scholar 

  • Turner DH, Sugimoto N, Freier SM (1988) RNA structure prediction. Annu Rev Biophys Chem 17:167–192

    Google Scholar 

  • Vartanian JP, Meyerhans A, Asjo B, Wain-Hobson S (1991) Selection, recombination and G → A hypermutation of human immunodeficiency virus type 1 genomes. J Virol 65:1779–1788

    Google Scholar 

  • Wagner RE, Radman M (1975) A mechanism for initiation of genetic recombination. Proc Natl Acad Sci USA 72:3619–3622

    Google Scholar 

  • Zoubak S, Richardson JH, Rynditch A, Hollsberg P, Hafler DA, Boeri E, Lever AML, Bernardi G (1994) Regional specificity of HTLV-1 proviral integration in the human genome. Gene 143:155–163

    Google Scholar 

  • Zuker M (1989) Computer prediction of RNA secondary structure. Methods Enzym 180:262–289

    Google Scholar 

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  1. Department of Biochemistry, Queen's University, K7L3N6, Kingston, Ontario, Canada

    D. R. Forsdyke

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Forsdyke, D.R. Reciprocal relationship between stem-loop potential and substitution density in retroviral quasispecies under positive Darwinian selection. J Mol Evol 41, 1022–1037 (1995). https://doi.org/10.1007/BF00173184

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